Proteomics of Seed Development, Desiccation Tolerance, Germination

PLAPHY4085_proof 5 November 2014 1/15
Plant Physiology and Biochemistry xxx (2014) 1e15
55
Contents lists available at ScienceDirect 56
57
58
Plant Physiology and Biochemistry 59
60
journal homepage: www.elsevier.com/locate/plaphy 61
62
63
Review 64
65
1 Proteomics of seed development, desiccation tolerance, germination 66
2 67
3 and vigor 68
4 69
5 Q9,1 Wei-Qing Wang a, Shu-Jun Liu a, Song-Quan Song a, **, Ian Max Mller b, * 70
6 a 71
Key Laboratory of Plant Resources and Beijing Botanical Garden, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China
7 b 72
Department of Molecular Biology and Genetics, Aarhus University, Flakkebjerg, DK-4200 Slagelse, Denmark
8 73
9 74
10 75
a r t i c l e i n f o a b s t r a c t
11 76
12 Article history: 77
Proteomics, the large-scale study of the total complement of proteins in a given sample, has been applied
13 Received 2 September 2014 to all aspects of seed biology mainly using model species such as Arabidopsis or important agricultural 78
14 Accepted 3 November 2014 crops such as corn and rice. Proteins extracted from the sample have typically been separated and 79
15 Available online xxx
quantied by 2-dimensional polyacrylamide gel electrophoresis followed by liquid chromatography and 80
16 mass spectrometry to identify the proteins in the gel spots. In this way, qualitative and quantitative 81
Keywords:
17 changes in the proteome during seed development, desiccation tolerance, germination, dormancy 82
Proteome
18 release, vigor alteration and responses to environmental factors have all been studied. Many proteins or 83
Seed development
19 biological processes potentially important for each seed process have been highlighted by these studies,
Desiccation tolerance 84
20 Seed germination which greatly expands our knowledge of seed biology. Proteins that have been identied to be partic-
85
Seed vigor ularly important for at least two of the seed processes are involved in detoxication of reactive oxygen
21 86
species, the cytoskeleton, glycolysis, protein biosynthesis, post-translational modications, methionine
22 87
metabolism, and late embryogenesis-abundant (LEA) proteins. It will be useful for molecular biologists
23 88
and molecular plant breeders to identify and study genes encoding particularly interesting target pro-
24 teins with the aim to improve the yield, stress tolerance or other critical properties of our crop species. 89
25 2014 Published by Elsevier Masson SAS. 90
26 91
27 92
28 93
29 94
30 Q2 1. Introduction potential in plant breeding. This requires that we understand the
95
31 fundamental processes taking place in the seeds during their
96
32 Almost all plant cultivation in agriculture and horticulture is development, storage, germination and growth. An excellent
97
33 based on seeds. The vast majority of our domesticated plants are overview of all aspects of seed biology is found in Bewley et al.
98
34 propagated via seeds and seeds provide most of our caloric intake (2013).
99
35 either directly as food or indirectly as feed for our domestic animals. Seed development. The seed develops from a single fertilized
100
36 To feed the ever-growing human population we need to increase zygote into an embryo and endosperm in association with the
101
37 the productivity of our crop species by exploiting their full genetic surrounding maternal tissues. Most seeds contain large quantities
102
38 of nutrient reserves, mainly carbohydrates, oils, and/or proteins,
103
39 which are biosynthesized and deposited during seed development.
104
40 These reserves are not only important for seed germination and
Abbreviations: ABA, abscisic acid; ADH, aldehyde dehydrogenase; APX, ascor- 105
41 bate peroxidase; CAT, catalases; Cys, cysteine; DAF, days after owering; DAP, days seedling growth, but are also vital components of human and an-
106
42 after pollination; GA, gibberellic acid; GC, green carbohydrate abundant; GO, green imal diets. Their production in crops is the basis of agriculture.
107
43 oil abundant; GPX, glutathione peroxidase; HSP, heat shock proteins; LEA, late Before reaching maturity, the seed develops other important
embryogenesis abundant; LHC, light harvesting complex; MDHR, mono- 108
44 properties, including desiccation tolerance, germination/dormancy
dehydroascorbate reductase; Met, methionine; MV, methylviologen; NGO, 109
45 nongreen oil abundant; PDC, pyruvate dehydrogenase complex; PEG, polyethylene
and vigor (Bewley et al., 2013).
110
46 glycol; Prx, peroxiredoxin; PSII, photosystem II; PTM, post-translational modica- Seed desiccation tolerance. Considered only in terms of tolerance
111
47 tion; ROS, reactive oxygen species; Rubisco, ribulose bisphosphate carboxylase/ of, or sensitivity to, desiccation, seeds can be categorized as or-
oxygenase; SAM, S-adenosylmethionine; Ser, serine; SOD, superoxide dismutase;
112
48 thodox or recalcitrant (Berjak and Pammenter, 2008). The orthodox
TCA, tricarboxylic acid; TPX, thioredoxin peroxidase; Tyr, tyrosine. 113
49 seed acquires desiccation tolerance during seed development
* Corresponding author. 114
50 ** Corresponding author.
approximately halfway through development. This trait ensures
115
51 E-mail addresses: sqsong@ibcas.ac.cn (S.-Q. Song), ian.max.moller@agrsci.dk that the seeds passes unharmed through maturation drying and
116
(I.M. Mller).
52 117
53 118
http://dx.doi.org/10.1016/j.plaphy.2014.11.003
54 0981-9428/ 2014 Published by Elsevier Masson SAS. 119
Please cite this article in press as: Wang, W.-Q., et al., Proteomics of seed development, desiccation tolerance, germination and vigor, Plant
Physiology and Biochemistry (2014), http://dx.doi.org/10.1016/j.plaphy.2014.11.003
2 W.-Q. Wang et al. / Plant Physiology and Biochemistry xxx (2014) 1e15
1 retains viability in the dry state for long periods of time (up to essential to ensure the physiological (developmental stage) and 66
2 hundreds of years in some case) under natural or articial condi- genetic uniformity of the seeds sampled. 67
3 tions (Kermode and Finch-Savage, 2002). In contrast, the recalci- The dynamic range for protein amount may be as high as 68
4 trant seed is desiccation sensitive and can not survive drying during 1010e1012 whereas the dynamic range for the analytical methods 69
5 ex situ conservation (Berjak and Pammenter, 2008). This creates a are much lower perhaps only 103e104 (Hortin and Sviridov, 2010; 70
6 serious problem in the conservation of recalcitrant species. Many Miernyk, 2014). It can therefore be an advantage to remove the 71
7 species with recalcitrant seeds are economically important, such as superabundant storage proteins during protein extraction or during 72
8 avocado, mango, lychee, cocoa, coffee, citrus, and rubber. the early stages of separation in order to improve the chances of 73
9 Seed germination. Seed germination is the most critical phase in detecting lower-abundance proteins (Miernyk and Hajduch, 2011). 74
10 the seed plant life cycle. It determines when the plant enters nat- Gel-based methods for separation e particularly two- 75
11 ural or agricultural ecosystems. Cultivation of most crop species is dimensional polyacrylamide gel electrophoresis (2D-PAGE) e 76
12 dependent on seed germination. Seeds of most species acquire the have dominated and will probably continue to dominate because, 77
13 ability to germinate during development. This is important for crop in addition to being reasonably quantitative, they provide a lot of 78
14 production, because it ensures that the untreated seed quickly information about the proteins not provided by the gel-free 79
15 germinates after sowing. However, in a few species, such as maize, shotgun methods, such as changes in protein size, pI, and post- 80
16 wheat and rice, it can result in precocious germination, which translational modications (PTMs) (Rogowska-Wrzesinska et al., 81
17 typically occurs when developing seeds with a low degree of 2013). This is always useful information, and particularly so for 82
18 dormancy experience rainfall or humid conditions (Bewley et al., species where the genome has not yet been fully sequenced. 83
19 2013). Precocious germination can decrease the grain quality and Mass spectrometer-based methods for protein identication 84
20 cause great economic losses. In some species, seeds are dormant at have dominated completely in recent years also in seed proteomics, 85
21 the end of development. Seed dormancy is dened as the failure of but the methods have been extensively reviewed recently (e.g. Pan 86
22 an intact viable seed to complete germination under favorable et al., 2009; Walther and Mann, 2010; Bantscheff et al., 2012; 87
23 conditions (Bewley, 1997). It is an adaptive strategy for seed to Rogers and Overall, 2013) and since they are essentially indepen- 88
24 survive under adverse natural conditions, but it also creates an dent of species (except for the question of access to a full genome 89
25 obstacle for agricultural production, where rapid germination and sequence), they will not be reviewed here. Q3 90
26 growth are required. 91
27 Seed vigor. Seed deterioration occurs always during storage of 1.2. Pitfalls in the use of 2D-PAGE and other quantitative proteomic 92
28 orthodox seeds, resulting in the gradually loss of vigor and even methods 93
29 death. For crop species, preventing or minimizing the loss of vigor 94
30 during storage is critical for the production in the subsequent Although 2D-PAGE is reasonably quantitative, a note of caution 95
31 seasons. Seed longevity is dependent on storage temperature and is in order concerning the way it is routinely used. The standard 96
32 moisture (Walters et al., 2005). Seed priming, imbibing seeds in procedure is to extract all proteins from a series of samples, for 97
33 water or chemicals, such as PEG, for a period of times followed by instance a time series during seed development. The same xed 98
34 dehydration, is utilized commercially to increase seed vigor amount of protein (typically 100e500 mg protein) from each sam- 99
35 (Heydecker et al. 1973; McDonald, 2000). ple is then separated by 2D-PAGE and, when the gels are stained 100
36 Seed proteomics. The great biological and economic importance typically using Coomassie Brilliant Blue or silver nitrate, the total 101
37 of seeds has led to a vast number of studies of all the above aspects staining on all the gels is very similar. A total of 500e1000 discrete 102
38 of seed biology. One type of study is proteomics, the study of all the spots are typically discernable, where each spots normally repre- 103
39 expressed proteins. Since proteins are responsible for most meta- sents one dominant unique protein. When a change in the number 104
40 bolic processes in the seed, in addition to being important struc- of pixels in a given spot is observed between different samples, it is 105
41 tural components in the cytoskeleton, membranes, the cell wall, then concluded that the amount of that protein has changed. 106
42 etc., it makes excellent sense to describe the proteome of a seed, a Contrariwise, if no signicant change in the number of pixels in a 107
43 seed tissue, a specic cell type or a subcellular compartment. given spot is observed between different samples, it is concluded 108
44 However, proteomics are also a powerful tool for detecting changes that the amount of that protein has not changed. Both of these 109
45 in the protein composition in response to developmental or envi- conclusions can actually be wrong! 110
46 ronmental stimuli, so-called differential proteomics. In other The problem is that the standard procedure for sampling and 111
47 words, proteomics can be used analytically rather than descrip- loading outlined above ensures that the number of pixels in a spot 112
48 tively to identify proteins associated with, and therefore probably represents not the absolute amount of protein in the sample, but 113
49 important for, specic processes and specic responses. This will be the fraction of the sample protein contributed by that protein. 114
50 the focus in the present review e qualitative and quantitative To appreciate this point, let us consider two extreme cases in 115
51 changes in the seed proteome during the life cycle of the seed. seed biology: 116
52 We will start by giving a very brief overview of the methods 117
53 used to study seed proteomics. We will then review the proteomics (1) The composition of the proteome changes strongly, e.g. due 118
54 of seed development, desiccation tolerance, germination and to biosynthesis of storage proteins. This happens during the 119
55 dormancy release and vigor. Finally, we will attempt to give some reserve deposition stage. Let us assume that the storage 120
56 perspectives. proteins go from constituting 10% of the total protein in the 121
57 seed to 40% between two samples, while all the rest of the 122
58 1.1. Proteomic methods proteins in the seed are present in unchanged amounts. This 123
59 means that the non-storage proteins will make up 90% in the 124
60 The seed proteome can be analyzed like any other proteome rst sample, but only 60% in the second. As a result all their 125
61 using the standard general procedure of protein extraction, sepa- spots will therefore decrease in size to 60%/90% 0.67 of 126
62 ration and identication. The sampling is, as always, the basis for their original size (a decrease by a factor 1.5). The relative 127
63 obtaining meaningful results. As discussed by Miernyk (2014) this amounts of the non-storage proteins have changed, in spite 128
64 is not a trivial point: The seed part to be analyzed needs to be of the fact that there was no change in the absolute amounts 129
65 considered carefully in relation to the question asked. It is also of those proteins! 130
W.-Q. Wang et al. / Plant Physiology and Biochemistry xxx (2014) 1e15 3
1 (2) The total amount of protein per seed changes strongly be- 2. Proteomic studies of seed development 66
2 tween samples, e.g. due to general growth and protein 67
3 biosynthesis. This might happen during the early stages of Seed development can be divided into three sequential, tem- 68
4 seed development. In this case the amount of many of the poral phases: histodifferentiation, reserve deposition and matura- 69
5 proteins increase similarly, but on the gel their spot size will tion drying (Kermode and Finch-Savage, 2002; Black et al., 2006; 70
6 remain unchanged. Their relative amounts are constant, but Bewley et al., 2013). During the histodifferentiation stage, the 71
7 their absolute amounts are not. fertilized egg cells undergoes rapid cell division and develops into 72
8 different seed tissues; thereafter, little cell division occurs and cell 73
9 The way to avoid such misinterpretations is to quantify the total expansion and deposition of seed reserves (normally proteins, 74
10 amount of protein extracted per unit sample (per seed, per leaf, etc) along with lipids or carbohydrates) occurs primarily in the storage 75
11 and to take major shifts in protein pattern into account when tissue (i.e., cotyledons or endosperm); nally, seed development 76
12 interpreting spot volume changes. Similar words of caution are also ends by a maturation drying, which slows down and stops the dry 77
13 relevant for non-gel-based proteomic methods such as iTRAQ, matter accumulation and leads the seed into a metabolically 78
14 where several samples are labeled separately and then mixed quiescent state (Kermode and Finch-Savage, 2002; Black et al., 79
15 before MS analysis. If the same amount of protein from each sample 2006; Bewley et al., 2013). 80
16 is mixed, it corresponds precisely to comparing several 2D-gels Seed development has been studied by proteomics in many 81
17 with the same loading. species, such as Medicago truncatula (Gallardo et al., 2003, 2007; 82
18 83
19 84
20 Table 1 85
Recent proteomic studies on seed development. Q8
21 86
22 Species Development stage Tissue Reference 87
23 Histodifferentiation Reserve Maturation 88
24 deposition drying 89
25 Arabidopsis 5,7 DAFb 9,11,13 DAF Whole seed Hajduch et al., 2010; Meyer et al., 2012 90
26 thaliana 91
27 Brassica 10, 16, 20, 25 DAF 35 DAF Whole seed Li et al., 2012 92
28 campestri 93
Brassica napus 2 WAFc 3, 4, 5 WAF 6 WAF Whole seed Hajduch et al., 2006; Meyer et al., 2012
29 (rapeseed)
94
30 Cunninghamia Cleavage polyembryony, dominant embryo, columnar Whole seed Shi et al., 2010 95
31 lanceolata embryo, and early cotyledonary 96
32 Glycine max 2, 3 WAF 4, 5, 6 WAF Whole seed Hajduch et al., 2005; Agrawal et al., 97
(soybean) 2008; Meyer et al., 2012
33 98
S2 S4, S6 S8, S9 Coat Miernyk and Johnston, 2013
34 Hordeum vulgare Stage 80, 82 Stage 85, 86, Whole seed Finnie et al., 2002 99
35 (barley) 87 100
36 Jatropha curcas 5, 10, 15 DAF 20, 25, 30 DAF Endosperm Liu et al., 2013 101
37 Lotus japonicus 16e25 DAF 43 DAF Whole seed Dam et al., 2009 102
7, 13 DAF 19, 22, 31 DAF Whole seed and Nautrup-Pedersen et al., 2010
38 103
pod
39 Medicago 12, 14, 16, 18, 20 Whole seed Gallardo et al., 2003 104
40 truncatula DAF 105
41 12, 14, 16, 20, Embryo, Gallardo et al., 2007 106
24, 36 DAF endosperm, seed
42 107
coat
43 Oryza sativa (rice) 5, 7 DAF 13 DAF 21, 30 DAF Embryo Xu et al., 2012 108
44 6, 8 DAF 10, 12, 14, 16, Whole seed Xu et al., 2008 109
45 18, 20 DAF 110
46 10, 20 DAF 30, 40 DAF Whole seed Lee and Koh, 2011; Sano et al., 2013a,b 111
12, 15, 18 DAF Endosperm Xu et al., 2010
47 112
Oryza sativa (rice, Deng et al., 2013
48 othersa) 113
49 Pinus massoniana Cleavage polyembryony, dominant embryo, columnar Whole seed Zhen et al., 2012 114
50 embryo, and early cotyledonary 115
Ricinus communis 2, 3 WAF 4, 5, 6 WAF Whole seed Houston et al., 2009
51 116
(castor)
52 Stage III, IV Nucellus Nogueira et al., 2012
117
53 Stage IV Stages VI Stages X whole seed Nogueira et al., 2013 118
54 Triticum aestivum Stage I, II Stage III Stage IV,V Whole seed Guo et al., 2012 119
55 (wheat) 120
35, 88, 125, 195, 227 and 280 -days Whole seed Nadaud et al., 2010
56 121
10, 36 DAF Endosperm Vensel et al., 2005
57 Zea mays (maize) 17, 22, 25, 28 Embryo and Jin et al., 2013 122
58 DAF endosperm 123
59 4, 7, 10 DAF 14, 21, 30 DAF 40 DAF Whole kernel or chin et al., 2007
Me 124
endosperm
60 125
40, 65 AF Embryo and Wang et al., 2014
61 endosperm
126
62 28 DAF 52 AF Embryo Huang et al., 2012 127
63 a 128
See Deng et al. (2013).
64 b
DAF: days after owering. 129
65 c
WAF: weeks after owering. 130
1 Cha^telain et al., 2012), soybean (Hajduch et al., 2005; Agrawal et al., suggest that protein turnover and rearrangements during or at the 66
2 2008; Miernyk and Johnston, 2013), rice (Xu et al., 2008, 2012; Lee end of histodifferentiation is important. Protein degradation would 67
3 and Koh, 2011; Sano et al., 2013a, 2013b), Arabidopsis (Hajduch allow a reallocation of amino acids to pathways involved in syn- 68
4 et al., 2010), and castor bean (Houston et al., 2009; Nogueira thesis of storage products. Proteolysis will occur across all the 69
5 et al., 2012, 2013) (Table 1). The proteomic studies on rice seed development stages. Some proteolytic proteins such as the ubiq- 70
6 development were reviewed recently (Deng et al., 2013). uitin carboxyl-terminal hydrolase-related in rapeseed (Hajduch 71
7 Most of the proteomic studies of seed development have used et al., 2006), putative aminopeptidase N in rice (Xu et al., 2008), 72
8 whole seeds as the experimental material and only in a few cases 20S proteasome a subunit E2 and 20S proteasome b subunit C1 in 73
9 has the proteome of embryo, endosperm and/or seed coat been Arabidopsis (Hajduch et al., 2010) were found to accumulate 74
10 studied separately (Table 1). Therefore, this section will focus abundantly during the reserve deposition, while others, such as 26S 75
11 mainly on proteomic changes occurring in the whole seeds during protease regulatory subunit proteins in rice (Xu et al., 2008) and 76
12 seed development. Seed lling has been the main developmental cystatin in maize (Wang et al., 2014), had high accumulation at the 77
13 stage to be investigated in most proteomic studies. This stage starts stage of maturation drying. The proteases accumulating during 78
14 during the late histodifferentiation and continues during reserve seed development have been proposed to play a key role in nitro- 79
15 deposition. Some important events occurring during maturation gen remobilization by releasing the free amino acids in the endo- 80
16 drying are also covered in the present review although this process sperm and seed coat for storage protein synthesis in the embryo 81
17 has only been investigated in a few species (Table 1). (Gallardo et al., 2007). In addition, some of proteases may act as 82
18 storage proteins in mature dry seed and function in the degradation 83
19 2.1. Protein synthesis of other storage proteins during seed germination (Tan-Wilson and 84
20 Wilson, 2012). 85
21 Cell division and enlargement occurring during seed develop- 86
22 ment require proteins involved in processes such as DNA replica- 2.2. Reserve accumulation 87
23 tion, transcription, cytoskeleton and cell wall formation. In many 88
24 species, such as castor (Houston et al., 2009; Nogueira et al., 2013), Most mature seeds contain two or more reserve compounds 89
25 soybean (Hajduch et al., 2005; Agrawal et al., 2008) and rice (Xu including carbohydrates, oils and proteins, and to a large extent 90
26 et al., 2008), most of the proteins involved in protein synthesis they are synthesized during seed development, especially during 91
27 including ribosomal proteins, translation factors and tRNA syn- the stage of reserve deposition. Sucrose and amino acids, imported 92
28 thases, in protein folding and stability, such as chaperones and heat from the parent plant, are the major carbon and nitrogen sources 93
29 shock proteins, and in biosynthesis of amino acids accumulated for the synthesis of reserve compounds (Bewley et al., 2013). 94
30 most abundantly at the stage of histodifferentiation and/or the Enzymes involved in carbohydrate synthesis showed the high- 95
31 early stage of reserve deposition. Their accumulation would help est abundance at the early stage of reserve deposition. For instance, 96
32 produce the various proteins used for cell division and expansion UDP-glucose pyrophosphorylase 2 reached its peak abundance at 97
33 during these stages. During reserve deposition when cell division 11 days after owering (DAF) in Arabidopsis (Hajduch et al., 2010); 98
34 ceases, protein synthesis slows down, and the above proteins in rice, starch synthase showed the highest abundance at 14 DAF 99
35 therefore decrease in abundance. However, storage proteins and (Xu et al., 2012). In developing maize seed, sorbitol dehydrogenase 100
36 proteins involved in cell defense and rescue are synthesized at high had reached its maximal abundance at 25 DAF and it was suggested 101
37 rates during this stage. The accumulation of storage proteins is that sorbitol dehydrogenase is an important regulator of maize 102
38 important for nutrition during seed germination and seedling grain lling, especially for hybrid Zhengdan 958 (Jin et al., 2013). 103
39 growth (Rajjou et al., 2012; Tan-Wilson and Wilson, 2012), while Proteins involved in oil synthesis showed different accumula- 104
40 the proteins involved in cell defence and rescue are associated with tion proles in non-oilseed and oilseed species. Enoyl-CoA- 105
41 increased seed desiccation tolerance and vigor (Cha ^telain et al., hydratase reached the peak level at the stage of histodiffer- 106
42 2012; Rajjou et al., 2012; Wang et al., 2014). In Arabidopsis, some entiation in the non-oilseed species rice (Xu et al., 2008). In oilseed 107
43 proteins related to protein synthesis, such as cytosolic ribosomal species, these proteins can be divided into two groups according to 108
44 protein S15, 60S acidic ribosomal protein P2 and elongation factor the trend of change. One group including ATP-citrate lyase B-1 in 109
45 EF-2 increased in abundance during reserve deposition (Hajduch Arabidopsis (Hajduch et al., 2010) and rapeseed (Hajduch et al., 110
46 et al., 2010). In addition, proteins related to protein folding and 2006), has a similar accumulation pattern as in non-oilseed 111
47 stability in some species, such as protein disulde isomerase in plants; the other group shows the maximal accumulation at the 112
48 developing seeds of Arabidopsis (Hajduch et al., 2010), middle and/or late stage of reserve deposition. Change in abun- 113
49 M. truncatula (Gallardo et al., 2003) and rice (Xu et al., 2008) and dance of pyruvate dehydrogenase E1 b subunit, enoyl-ACP reduc- 114
50 BiP proteins in soybean (Hajduch et al., 2005) and rice (Xu et al., tase and malonyl-CoA ACP transacylase in Arabidopsis (Hajduch 115
51 2008) showed a high accumulation at this stage. Protein disulde et al., 2010), b-ketoacyl-ACP synthetase 1, enoyl acyl carrier pro- 116
52 isomerase, an abundant 57-kDa protein, is a chaperone in eukary- tein reductase and pyruvate dehydrogenase E1 a subunit in rape- 117
53 otes, including yeast, mammals, and plants and it may participate in seed (Hajduch et al., 2006) belongs to the latter group. 118
54 the synthesis and deposition of storage proteins (Kim et al., 2012). 119
55 BiP, an ER-localized member of the heat shock 70 family, has been 2.3. Energy production 120
56 proposed to play a role in protein body assembly and retention of 121
57 zeins within the ER (Boston et al., 1991; Vitale and Ceriotti, 2004). The central metabolism (glycolysis and tricarboxylic acid (TCA) 122
58 Therefore, it is not surprising to nd that these proteins have an cycle) provides most of the energy for processes in the seed. In 123
59 accumulation prole similar to storage proteins. developing seeds, most of the glycolytic enzymes in the cytosol and 124
60 High proteolytic activity occurs simultaneously with protein a few in plastids have been identied in many species by prote- 125
61 biosynthesis during histodifferentiation. Most of the proteolytic omics (Fig. 1). In castor seeds nearly all the glycolytic enzymes in 126
62 proteins such as proteasome family proteins, ubiquitin protease both cytosol and plastids, with the exception of plastidic phos- 127
63 family proteins, and amino acid peptidases showed a high accu- phoglyceromutase, were identied and shown to change in abun- 128
64 mulation at the stage of histodifferentiation, and then decreased dance during seed development (Nogueira et al., 2013). These data 129
65 gradually in abundance during the following stage. These results gave what appeared to be a relatively clear picture of the 130
1 66
2 67
3 68
4 69
5 70
6 71
7 72
8 73
9 74
10 75
11 76
12 77
13 78
14 79
15 80
16 81
17 82
18 83
19 84
20 85
21 86
22 87
23 88
24 89
25 90
26 91
27 92
28 93
29 94
30 95
31 96
32 97
33 98
34 99
35 100
36 101
37 102
38 103
39 104
40 105
41 106
42 107
43 108
44 109
45 110
46 Fig. 1. Changes in the amounts of identied proteins involved in glycolysis and the TCA cycle during seed development. The gure was plotted using data reported for soybean
111
47 (Glycine max, Gm) (Hajduch et al., 2006), rapeseed (Brassica napus, Bn) (Agrawal et al., 2008), rice (Oryza sative, Os) (Xu et al., 2008; Lee and Koh, 2011), castor (Ricinus communis, Rc) 112
48 (Houston et al., 2009) and Arabidopsis (Arabidopsis thaliana, At) (Hajduch et al., 2010) and modied from Houston et al. (2009). The relative abundance of each enzyme was 113
49 extracted for each species and plotted against the developmental time (horizontal axis) to show the trend of the change. Only the plastidial glycolytic pathway enzymes identied in 114
these species are shown. In rice seed, the TCA cycle, PDC, CST and ODC were identied by Lee and Koh (2011), while MDH was identied by Xu et al. (2008). In each part gure, the
50 115
left gray part shows the developmental stage of histodifferentiation and the following white part is the reserve deposition. In some part gures, maturation drying is depicted by the
51 light gray area on the right. Abbreviations: CST, citrate synthase; FBA, fructose bisphosphate adolase; FK, fructose kinase; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; IDH, 116
52 isocitrate dehydrogenase; MDH, malate dehydrogenase; PDC, pyruvate dehydrogenase complex; PFK, phosphofructose kinase; PGM, phosphoglucomutase; PGI, phosphoglucose 117
53 isomerase; PK, pyruvate kinase; PGK, phosphoglycerate kinase; PGAM, phosphoglycerate mutase; ODC, 2-oxoglutarate dehydrogenase complex; SuSy, Sucrose synthase; SCST, 118
54 succinyl-CoA synthetase; SDH, succinate dehydrogenase; TPI, triose phosphate isomerase; UDP, UDP-glucose pyrophosphorylase. 119
55 120
56 121
involvement of glycolysis during seed development. However, accumulated most abundantly at the stage of histodifferentiation
57 122
when similar studies were performed in other species, it became and decreased gradually during reserve deposition, while in Ara-
58 123
clear that the identied glycolytic enzymes vary greatly not only in bidopsis, various trends of change were observed (Fig. 1). A varia-
59 124
number, but also in accumulation pattern, among different species tion in the number and accumulation pattern was also observed for
60 125
(Fig. 1). For example, using the same 2-D PAGE proteomic approach, the enzymes of the TCA cycle (Fig. 1).
61 126
a total of 63 protein spots involved in glycolysis were identied in The above results imply that the participation of glycolysis and
62 127
developing castor seeds (Houston et al., 2009), while this number the TCA cycle in seed development is not entirely straightforward
63 128
was only 19 in Arabidopsis seeds (Hajduch et al., 2010). In castor and possibly regulated by different mechanisms in different plant
64 129
seeds, the identied glycolytic proteins in both cytosol and plastids species. In addition to providing energy in the form of ATP,
65 130
1 glycolysis and the TCA cycle also provide many intermediates for during biosynthesis of oil (Schwender et al., 2004; Allen et al., 66
2 the biosynthesis of storage reserves, secondary metabolites, nu- 2009). In developing rape seeds, Rubisco participated in an alter- 67
3 cleotides, etc. (Mller et al., in press), where the need differs among native pathway in conversion of carbohydrate to oil that provided 68
4 different plant species. Therefore, the various accumulation pat- 20% more acetyl-CoA for oil synthesis and resulted in 40% smaller 69
5 terns of proteins involved in glycolysis and the TCA cycle may loss of carbon as CO2 (Schwender et al., 2004). The role of Rubisco in 70
6 reect different requirement for glycolytic and/or TCA cycle in- NGO and GO seeds is still unclear. 71
7 termediates in biosynthesis. 72
8 In many species, it was interesting to nd that proteins of the 2.4. Formation of cytoskeleton and cell wall 73
9 pyruvate dehydrogenase complex (PDC) had a consistent accu- 74
10 mulation pattern during seed development. They accumulated Cell division and expansion during seed development is ex- 75
11 abundantly at the stage of histodifferentiation and decreased dur- pected to rely largely on the biosynthesis of proteins involved in the 76
12 ing reserve deposition (Fig. 1). The PDC catalyzing the conversion of formation of the cytoskeleton and the cell wall. The microtubules 77
13 pyruvate to acetyl-CoA is a step linking the glycolytic pathway to and actin laments, assembled from tubulin and actin molecules, 78
14 the TCA cycle. When the accumulation of PDC decreased, the car- respectively, are the two key components of the cytoskeleton 79
15 bon ux through the TCA cycle would be expected to decline. The (Mayer and Jrgens, 2002). Proteomic analysis of seed development 80
16 time at which the PDC declines coincides with the time that storage revealed that tubulins accumulated at high abundance during 81
17 reserves start to be deposed (Fig. 1). Therefore, it is possible that the histodifferentiation, and then decreased during the following 82
18 decrease in PDC plays a role in switching carbon ux through the developmental stage. In most species, actin also accumulated 83
19 energy production to the deposition of storage reserve. In addition, abundantly during histodifferentiation, but decreased later than 84
20 a decrease in the ux through the TCA cycle would decrease the the tubulins, normally at the mid or late stage of reserve deposition. 85
21 production of NADH and therefore limit the oxygen consumption. These results imply that tubulins may play more roles in cell divi- 86
22 Because the internal oxygen level is low inside developing seeds sion, while actin may be essential for both cell division and 87
23 (Geigenberger, 2003; Borisjuk and Rolletschek, 2009), this will expansion during seed development. The actin cytoskeleton seems 88
24 limit the occurrence of anoxia inside the seeds, which is a damaging to be a dynamic structure, which undergoes dramatic reorganiza- 89
25 to the cells (Geigenberger, 2003). tion during seed development. Prolin in rice (Xu et al., 2008) and 90
26 Proteins involved in photosynthesis accumulated during seed castor (Nogueira et al., 2013) seeds and actin depolymerizing factor 91
27 development in almost all the species, but the pattern differed in Arabidopsis (Hajduch et al., 2010), rice (Xu et al., 2008) and castor 92
28 between green oil abundant (GO) seeds and nongreen oil abundant (Houston et al., 2009) seeds accumulated to high levels at the stage 93
29 (NGO) and green carbohydrate abundant (GC) seeds. of histodifferentiation and early stage of reserve deposition and 94
30 In general, photosynthetic proteins in NGO, e.g. castor (Nogueira then decreased in abundance during the following stage. These two 95
31 et al., 2013) and maize (Me chin et al., 2007) seeds and GC seeds, proteins are both thought to play a role in reorganizing the actin 96
32 such as barley (Finnie et al., 2002), rice (Xu et al., 2008) and wheat cytoskeleton (Staiger et al., 1997; Henty-Ridilla et al., 2013). 97
33 (Guo et al., 2012) seeds, accumulated to high abundance at the The polysaccharides, cellulose, hemicelluloses and pectin, are 98
34 stage of histodifferentiation and/or the early stage of reserve the main components of the plant cell wall. Proteomic studies 99
35 deposition and then decreased during the following development, identied many proteins involved in the biosynthesis of these 100
36 while in GO seeds, such as soybean (Agrawal et al., 2008), polysaccharides in developing seeds. The identied proteins vary 101
37 M. truncatula (Gallardo et al., 2003, 2007), Arabidopsis (Hajduch greatly among different plant species and are involved in various 102
38 et al., 2010) and rape (Hajduch et al., 2006) seeds, those proteins processes of cell wall formation. The a-1,4-glucan-protein synthase, 103
39 accumulated most abundantly at the stage of reserve deposition. identied in developing M. truncatula (Gallardo et al., 2007) and 104
40 In GO seeds, light is known to provide the energy for oil castor (Houston et al., 2009; Nogueira et al., 2013) and cellulose 105
41 biosynthesis (Ruuska and Ohlrogge, 2004; Goffman et al., 2005; synthase catalytic subunit in rape (Hajduch et al., 2006) seeds are 106
42 Allen et al., 2009; Borisjuk et al., 2013), and a number of studies involved in biosynthesis of cellulose. Rhamnose synthase found in 107
43 have shown that the accumulation of photosystem components Arabidopsis (Hajduch et al., 2010) and UDP-D-apiose/xylose syn- 108
44 coincides with oil accumulation in GO seeds. The components were thase in Jatropha curcas (Liu et al., 2013) seeds are related to the 109
45 photosystem (PS) II oxygen-evolving complex 1, PSII subunit P-1 biosynthesis of pectin. Pectin methylesterase, involved in cell wall 110
46 and 2, chlorophyll a/b binding protein/light harvesting complex modication, was found in rice (Xu et al., 2008) and castor 111
47 (LHC) II type I and PSI LHC gene 3 in Arabidopsis (Hajduch et al., (Nogueira et al., 2013) seeds. Reversibly glycosylated polypeptide, 112
48 2010), chlorophyll a/b binding protein and oxygen-evolving possibly participating in the synthesis of xyloglucan, one of the 113
49 enhancer protein in M. truncatula (Gallardo et al., 2003, 2007), hemicelluloses (Dhugga et al., 1997) differentially accumulated in 114
50 oxygen-evolving enhancer protein and water-soluble chlorophyll M. truncatula (Gallardo et al., 2003) and Arabidopsis (Hajduch et al., 115
51 protein in rape (Hajduch et al., 2006), and chlorophyll a/b binding 2010) seeds. In addition, glycoside hydrolases, such as b-D-xylosi- 116
52 protein in soybean (Agrawal et al., 2008) seeds. dase, b-galactosidase and xyloglucan endotransglycosylases/hy- 117
53 Photosystem components have also been identied in GC seeds, drolases, involved in the biosynthesis and remodeling of glycans 118
54 such as wheat (Guo et al., 2012) and rice (Xu et al., 2008) seeds. This (Minic, 2008), were found in developing seeds of many species. The 119
55 indicates that photosynthesis occurs also in the GC seeds where it dynamic changes in the cytoskeleton and cell wall would assist cell 120
56 may support starch biosynthesis. In barley seeds, pericarp photo- expansion and reserve nutrition deposition. 121
57 synthesis supplied oxygen to the growing lateral and peripheral The accumulation of the cell wall-related proteins fall into two 122
58 regions of the endosperm, and the accumulation of oxygen corre- groups: (1) Proteins whose abundance increases transiently during 123
59 lated well with the accumulation of ATP and starch (Rolletschek histodifferentiation, e.g. rhamnose synthase in Arabidopsis, a-1,4- 124
60 et al., 2004). glucan-protein synthase in M. truncatula, rice and castor, cellulose 125
61 Ribulose bisphosphate carboxylase/oxygenase (Rubisco) has synthase catalytic subunit in rape and xyloglucan endo- 126
62 been found in the above seed types. In GO seeds, Rubisco may play transglycosylases/hydrolases in soybean (Agrawal et al., 2008) 127
63 also an important role in the biosynthesis of oil. It has been re- seeds; (2) Proteins whose abundance increases strongly during 128
64 ported that carbon ux through Rubisco without the Calvin cycle reserve deposition, e.g. reversibly glycosylated polypeptide in rice 129
65 improved the efciency of carbon use in the developing green seeds and M. truncatula, UDP-D-apiose/xylose synthase in J. curcas (Liu 130
1 et al., 2013) and b-D-xylosidase in rice (Xu et al., 2008) and wheat in maize (Wang et al., 2014) seeds. This enzyme is involved in the 66
2 (Guo et al., 2012). These results suggest that cell wall formation detoxication of methylglyoxal, a highly reactive aldehyde derived 67
3 differs between species and even within species between different from glycolysis (Thornalley, 2003). The important role of aldehyde 68
4 developmental stages. detoxication for seed developments is underlined by the obser- 69
5 vation that aldehyde dehydrogenase (ADH) accumulated highly 70
6 2.5. Removal of reactive oxygen species during reserve deposition but also during maturation drying in 71
7 several species, such as rice (Xu et al., 2008; Lee and Koh, 2011) and 72
8 The production of reactive oxygen species (ROS), such as su- maize seeds (Wang et al., 2014). 73
9 peroxide radical (O 2 ) and hydrogen peroxide (H2O2), is an un- 74
10 avoidable consequence of aerobic metabolism (Mller et al., 2001). 2.6. Protein modications 75
11 ROS can act as signal molecules to regulate biological processes, but 76
12 can also damage cellular components (Mller, 2001; Mller et al., Few studies have looked for protein modications during seed 77
13 2007). The amount of ROS must be tightly controlled in the cell. development. Meyer et al. (2012) analyzed the phosphoproteome 78
14 At the stage of histodifferentiation, production of ROS is high due to of Arabidopsis, rapeseed and soybean at ve sequential stages 79
15 the high metabolic and respiratory activity in the developing seeds during seed development. During seed development, 459, 325 and 80
16 (Bailly, 2004; Bailly et al., 2008). It appears that the enzymes of 172 phosphoproteins accumulated differentially in soybean, rape- 81
17 ascorbateeglutathione cycle play a major role in removal of ROS at seed and Arabidopsis, respectively. In soybean and Arabidopsis 82
18 this stage. In Arabidopsis, six of ten proteins accumulating abun- seeds, protein phosphorylation occurs mainly during the stage of 83
19 dantly during histodifferentiation belonged to antioxidant enzymes histodifferentiation and early stage of reserve deposition; while in 84
20 of the ascorbateeglutathione cycle. They were three ascorbate rapeseed, a majority of the phosphoproteins were identied during 85
21 peroxidases (APX) and three monodehydroascorbate reductases maturation drying (Meyer et al. 2012). Protein phosphorylation 86
22 (MDHR) as well as one glutathione synthetase (Hajduch et al., varied greatly among species and only few phosphopeptides and 87
23 2010). In addition, two catalases (CAT) accumulated in high abun- phosphoproteins were identied in all three species (Meyer et al. 88
24 dance during this stage (Hajduch et al., 2010). In rice, ve antioxi- 2012). Tyrosine (Tyr) phosphorylation was thought to be more 89
25 dant enzymes of the ascorbateeglutathione cycle, including three prevalent in crop oilseeds, since the occurrence rate of Tyr phos- 90
26 APXs, one MDHR and one superoxide dismutase (SOD) and one phorylation was 7.1, 7.2 and 3.5% for soybean, rapeseed and Arabi- 91
27 protein involved in the detoxication of aldehydes, lactoylgluta- dopsis, respectively. This should be compared to an overall 92
28 thione lyase accumulated abundantly during histodifferentiation frequency of 5.5% phospho-Tyr out of a reported 100,000 phos- 93
29 (Xu et al., 2008). The antioxidant enzymes of the ascorbateeglu- phorylation sites in all proteins and all species, but only 1.3% in 94
30 tathione cycle were also observed to accumulate abundantly during Arabidopsis (out of 1057 sites) (Rao and Mller, 2012). Two protein 95
31 histodifferentiation in many other species, such as M. truncatula phosphorylation motifs found by Meyer et al. (2012), the Pro- 96
32 (Gallardo et al., 2003, 2007), soybean (Agrawal et al., 2008), castor targeted motif E-X-X-X-X-S-P and the Thr motif X-T-D-X, may 97
33 (Houston et al., 2009; Nogueira et al., 2013), J. curcas (Liu et al., turn out to be unique for the developing seed. The former can be 98
34 2013), and wheat (Guo et al., 2012). recognized by protein kinases that are involved in the regulation of 99
35 As the metabolic and respiratory activity decreases during transcription (Meyer et al., 2012). 100
36 reserve deposition and maturation drying, the production of ROS 101
37 will be reduced. However, the internal hypoxic condition of the 3. Desiccation tolerance 102
38 developing seeds (Borisjuk and Rolletschek, 2009) and the meta- 103
39 bolic imbalance resulting from the desiccation at these stages could Desiccation tolerance refers to the ability of an organism to 104
40 well cause ROS production to increase (Bailly, 2004; Bailly et al., endure loss of all or almost all of its cellular water without irre- 105
41 2008). The antioxidant enzymes of the ascorbateeglutathione cy- versible damage (Leprince and Buitink, 2010). This phenomenon is 106
42 cle were constant or increased at the early stage of reserve depo- widely observed in the plant kingdom, including ferns, mosses, 107
43 sition, but decreased during later development. However, many pollen and seeds of higher plants and resurrection plants (Hoekstra 108
44 thiol-dependent antioxidant enzymes increased in abundance et al., 2001; Oliver et al., 2005). In higher plant, only orthodox seeds 109
45 during reserve deposition and even during maturation drying. For are desiccation tolerant. This property gives the orthodox seeds the 110
46 example, in castor seeds, glutaredoxin, glutathione peroxidase ability to survive under extreme environmental conditions. In the 111
47 (GPX), glutathione reductase, thioredoxin and one peroxiredoxin dry state, the orthodox seeds can be stored for long periods of time, 112
48 (Prx), increased in abundance during reserve deposition (Nogueira depending on species and storage temperature and humidity 113
49 et al., 2013). In rice seeds, one proteomic study observed that thi- (Walters et al., 2005; Berjak and Pammenter, 2008). A number of 114
50 oredoxin peroxidase (TPX) and GPX increased in abundance during protective mechanisms have been proposed for seed desiccation 115
51 reserve deposition (Xu et al., 2008), while another study found that tolerance, including metabolic switch off, structural stabilization, 116
52 glutathione S-transferase accumulated abundantly not only during accumulation of protective molecules and removal of ROS 117
53 reserve deposition, but also in the fully mature seeds (Lee and Koh, (Pammenter and Berjak, 1999; Berjak and Pammenter, 2008). De- 118
54 2011). This would suggest that thiol-dependent antioxidant pro- tails of some of these protective mechanisms have been identied 119
55 teins play a major role in the removal of ROS during reserve by proteomic studies as outlined in the following sections. 120
56 deposition and maturation drying. 121
57 It appears that detoxication of aldehydes is also a necessary 3.1. Experimental approaches 122
58 process for seed development, especially in the late stages. During 123
59 rice seed development, it was striking to observe that glyoxalase Orthodox seeds acquire desiccation tolerance during develop- 124
60 was the most abundant protein accounting for more than 1.6% of ment, and lose it during germination (Kermode and Finch-Savage, 125
61 the total protein (Xu et al., 2008). This protein not only increased in 2002). Thus, comparing the dehydration response of seeds during 126
62 abundance at the stage of reserve deposition, but also during development and/or germination is a common approach for the 127
63 maturation drying (Lee and Koh, 2011). Glyoxalase was also study of desiccation tolerance. In proteomic studies, this approach 128
64 observed to increase in abundance during reserve deposition in has been applied to rice (Sano et al., 2013a, 2013b) and maize 129
65 M. truncatula (Gallardo et al., 2007) and during maturation drying (Huang et al., 2012) seeds. However, it is not easy to differentiate 130
1 the events related to seed desiccation tolerance from those of seed coinciding with the loss of desiccation tolerance (Wang et al., 66
2 development or germination (Leprince and Buitink, 2010). Some 2012b). At the same imbibition time, seeds imbibed in CaCl2 were 67
3 physiological models have been developed to overcome this dif- more tolerant to dehydration than seeds imbibed in distilled water, 68
4 culty. Re-establishment of desiccation tolerance in germinating while the SBP65 protein accumulated to a higher level in the former 69
5 seeds by application of a mild osmotic stress with polyethylene seeds (Wang et al., 2012b). In rice, a proteomic investigation of the 70
6 glycol (PEG) solution is one such model (Bruggink and van der change in the amount of stress-related proteins during seed 71
7 Toorn, 1995) and has been used in the proteomic analysis of development showed that several LEA proteins accumulated after 72
8 M. truncatula seed desiccation tolerance (Boudet et al., 2006). In maturation drying and remained at high levels in the mature seeds 73
9 pea, application of the chemical reagents, CaCl2 and methylviol- (Sano et al., 2013a). In maize seeds, one LEA protein, EMB564 74
10 ogen (MV), can increase and decrease desiccation tolerance of accumulated abundantly in desiccation-tolerant seeds and 75
11 germinated seeds, respectively (Wang et al., 2012a). In this way, decreased in amount during germination when the seed lost its 76
12 seed desiccation tolerance and germination are uncoupled. This desiccation tolerance (Huang et al., 2012). 77
13 approach was used to identify the potential proteins related to 78
14 desiccation tolerance in pea (Wang et al., 2012b). 3.3. Removal of ROS 79
15 It is difcult to establish a comparable model in recalcitrant 80
16 seeds during their development and germination. However, their Dehydration will disrupt the metabolism of seeds and lead to 81
production of ROS, such as H2O2, O2, singlet oxygen (1O2) and the

17 tolerance to desiccation can be altered by application of chemical 82

18 reagents, like NO (Bai et al., 2011), and H2O2 scavengers (Chen et al., hydroxyl radical (HO ) (Bailly, 2004; Kranner and Birtic, 2005; 83
19 2011). The mechanism of the effect of NO on seed desiccation Berjak and Pammenter, 2008). At lower concentration, ROS can 84
20 tolerance was investigated by the proteomic analysis of recalcitrant act as a messenger to regulate biological process, while they can 85
21 Antiaris toxicaria seeds (Bai et al., 2011). In view of the contrasting damage cellular components, like lipids, proteins and DNA at 86
22 dehydration properties between orthodox and recalcitrant seeds, a higher concentration (Mller, 2001; Bailly, 2004; Mller et al., 87
23 comparison between the seeds of these two types of species, 2007). It is also possible that breakdown products, e.g. oxidized 88
24 especially the closely related ones is a useful model to identify the peptides deriving from oxidized proteins, can act as signals (Mller 89
25 mechanisms related to desiccation tolerance (Kermode, 1997; and Sweetlove, 2010). Thus, ROS and the various oxidation products 90
26 Oliver et al., 2011). This has been applied in the proteomic study must be strictly controlled in seeds during dehydration (Bailly, 91
27 of seeds of two Papilionaceae species with different desiccation 2004; Kranner and Birtic, 2005; Berjak and Pammenter, 2008). 92
28 tolerance (Delahaie et al., 2013). In the rice seed proteome, Prx and a putative aldose reductase 93
29 were observed to accumulate at the beginning of the dehydration 94
30 3.2. Accumulation of LEA proteins phase, and continuously increased their abundance with seed 95
31 dehydration, while glyoxalase I accumulated during the later stages 96
32 Late embryogenesis abundant (LEA) proteins are well charac- of dehydration (Sano et al., 2013a). These proteins may play a role in 97
33 terized as protective molecules against desiccation stress (Cuming, protecting seeds against ROS damage during desiccation (Sano 98
34 1999). They are thought to act by replacing water, sequestering et al., 2013a). Protein carbonylation is one of the most commonly 99
35 ions, removing ROS and/or stabilizing protein and membrane occurring protein modications by ROS (Mller et al., 2007). 100
36 structure (Cuming, 1999; Tunnacliffe and Wise, 2007; Battaglia Analysis of protein carbonylation in recalcitrant A. toxicaria seeds 101
37 et al., 2008). LEA proteins are commonly found in proteomic ana- using 2-D PAGE showed that the number of carbonylated proteins 102
38 lyses of desiccation tolerance. increased during dehydration, but was reduced by pretreating the 103
39 Boudet et al. (2006) investigated the change of the heat-stable seeds with NO, which decreased the desiccation sensitivity of 104
40 proteome during germination and after re-establishment of A. toxicaria seeds (Bai et al., 2011). It has been proposed that NO 105
41 desiccation tolerance in M. truncatula seeds. Six LEA proteins from promotes seed desiccation tolerance by decreasing and increasing 106
42 four gene groups, including Em6, MP2, an isoform of PM18, six carbonylation and S-nitrosylation of antioxidant enzymes, respec- 107
43 isoforms of SBP65, PM25, and one isoform of DHN3 were identied tively, which increases the ability of antioxidant enzymes to 108
44 to be associated with desiccation tolerance (Boudet et al., 2006). In remove ROS (Bai et al., 2011). 109
45 this species, LEA proteins of Em6, PM18 and PM25 were also 110
46 observed to accumulate abundantly during late seed development 3.4. Stabilization of structure 111
47 when the seed acquired desiccation tolerance by a similar proteo- 112
48 mic analysis (Cha ^telain et al., 2012). In the pea seed proteome, the amounts of two proteins related 113
49 Recently, Delahaie et al. (2013) compared the heat-stable pro- to structural stabilization, the TCP-1/cpn60 chaperonin family 114
50 teome between recalcitrant Castanospermum australe and orthodox protein and tubulin a-1 chain decreased during seed germination. 115
51 M. truncatula seeds, both of which belong to the Papilionaceae Pea seeds imbibed in CaCl2 and MV were more and less tolerant to 116
52 subfamily. They found that, out of 12 LEA proteins, six (EM1, EM6, dehydration, respectively, compared to seeds imbibed in distilled 117
53 MP2, PM25, LEAm and SBP65) accumulated only at low levels and water. In agreement, the chaperonin TCP-1/cpn60 showed lower 118
54 six (PM1, D113.I, two D34 members, PM10 and PM18) were unde- accumulation in seeds imbibed in MV than in seeds imbibed in 119
55 tectable in the C. austral seed proteome. Nine of these proteins distilled water, while tubulin a-1 chain had higher accumulation in 120
56 (EM1, EM6, MP2, PM25, SBP65, D113.I, D34.I, PM10, and PM18) seeds imbibed in CaCl2 (Wang et al., 2012b). Members of the TCP-1 121
57 were also absent from or accumulated only to low levels in the chaperonin family act as molecular chaperones for the cytoskeleton 122
58 desiccation-sensitive seeds of M. truncatula mutants of ABI3 proteins, tubulin and actin and probably also for other proteins 123
59 (Delahaie et al., 2013). This further validates a correlation between (Yaffe et al., 1992; Vinh and Drubin, 1994), while tubulin is an 124
60 the absence of LEA protein accumulation and seed desiccation important cytoskeleton component. 125
61 sensitivity. This study also revealed that most of the desiccation 126
62 tolerance-related LEA proteins were positively regulated by ABI3. 3.5. Other mechanisms 127
63 Analysis of the proteome changes during pea seed germination 128
64 revealed that the abundance of SBP65 (belonging to the group 3 of Other mechanisms for desiccation tolerance highlighted by 129
65 LEA proteins) continuously decreased after 18 h of germination, seed proteomic studies include pathogen resistance (Huang et al., 130
1 2012; Wang et al., 2012b), removal of unneeded or damaged radicle, through the structures surrounding it (Bewley et al., 2013). 66
2 proteins (Huang et al., 2012), and/or stabilization of long-lived This is known as germination sensu stricto (simply called 67
3 mRNAs (Sano et al., 2013b). Accumulation of vicilin-like antimi- germination in the following) and does not include seedling 68
4 crobial peptides 2e3 in pea seeds, NBS-LRR resistance-like protein growth. During germination and seedling growth, the fresh weight 69
5 RGC456 and major allergen Bet v 1.01C in maize seeds and some follows a tri-phasic curve (Fig. 2). In phase I there is a rapid in- 70
6 storage proteins in both pea and maize seeds all correlated well crease in fresh weight caused by water uptake. During the slower 71
7 with the loss or acquisition of desiccation tolerance (Huang et al., phase II metabolism gets underway initially supported by mRNA 72
8 2012; Wang et al., 2012b). The proteasome is a multi-subunit present in the mature seed. After emergence of the radicle, 73
9 proteinase complex that is involved in ATP/ubiquitin-dependent signaling the end to germination, a rapid growth phase follows 74
10 proteolytic pathways (Sassa et al., 2000), which removes redun- (phase III) (Bewley et al., 2013). Note that the term seed vigor 75
11 dant or damaged proteins (Grune et al., 1997; Li et al., 2010). In discussed in the following section includes both germination and 76
12 maize seeds, the change in the amount of proteasome subunit a growth. 77
13 type l correlated with the change in desiccation tolerance during 78
14 seed development and germination (Huang et al., 2012). It has 79
4.2. Proteomic changes during seed germination
15 been proposed that the synthesis of proteins, but not mRNAs, is a 80
16 prerequisite for seed germination (Rajjou et al., 2004; Sano et al., 81
The ability of the seeds to germinate rapidly and vigorously
17 2012). Dry seeds contain a large amount of stored long-lived 82
under suitable environmental conditions is an important trait for
18 mRNA (Nakabayashi et al., 2005; Howell et al., 2009), which 83
any plant species and no less so for agricultural species. The mature
19 may support protein biosynthesis during the early stages of seed 84
seed is an easily accessible, compact and well-dened object, which
20 germination. Sano et al. (2013b) suggested that the accumulation 85
is relatively simple to study under a variety of conditions. As a
21 of glycine-rich RBP 1A during seed development may play a role in 86
result, in more than 50 papers proteomics have been used to study
22 stabilizing these long-lived mRNA during dehydration and in the 87
changes in the seed proteome during germination as affected by a
23 dry seeds. 88
range of physical, chemical and biological conditions. In this section
24 89
we will describe the way the proteome changes during normal
25 90
4. Seed germination and dormancy release germination while proteomic changes associated with processes
26 91
like dormancy release and responses to environmental stress will
27 92
4.1. Seed germination versus seedling growth be treated in the following sections. Because of the limited space
28 93
available, we have been quite selective in our coverage of the
29 94
Germination begins with water uptake by the seed (imbibition) literature in this section. The discussion will also focus more on the
30 95
and ends with the emergence of the embryonic axis, usually the protein groups involved and less on the individual proteins than in
31 96
32 97
33 98
34 99
35 100
36 101
37 102
38 103
39 104
40 105
41 106
42 107
43 108
44 109
45 110
46 111
47 112
48 113
49 114
50 115
51 116
52 117
53 118
54 119
55 120
56 121
57 122
Fig. 2. Major biological processes identied by proteomic studies during germination sensu stricto (phases I and II). The gure was modied from Nonogaki et al. (2010) using data
58 123
reported for barley (Hordeum vulgare, Hv) (Bnsager et al., 2007), cress (Lepidium sativum, Ls) (Mller et al., 2010), alfalfa (Medicago sativa, Ms) (Yacoubi et al., 2011), pea (Pisum
59 sativum, Ps) (Wang et al., 2012), Arabidopsis (At) (Galland et al., 2014) and rice (Os) (Han et al., 2014a,b). Phase I of germination has only been investigated by proteomics for barley 124
60 and Arabidopsis seeds and the biological processes identied in both species are shown in the gure. Proteins involved in amino acid metabolism, translation, reserve mobilization, 125
61 energy production and detoxication increase in abundance during phase II of germination in at least three species. Only these biological processes are shown in the gure. APX, 126
62 Ascorbate peroxidase; ASL, O-acetylserine (thiol) lyase; ASP, aspartate aminotransferase; CAT, catalase; Cys, cysteine; DHAR, dehydroascorbate reductase; GR, glutathione reductase; 127
HSPs, heat shock proteins; LEA, Late embryogenesis abundant protein; LGL, lactoylglutathione lyase; MDAR, monodehydroascorbate reductase; Met, methionine; PDI, protein
63 128
disulde isomerase; PER, peroxiredoxin; ROC, rotamase cyclophilin; SAM, S-adenosylmethionine synthetase; SHM, serine hydroxymethyltransferase; SOD, superoxide dismutase.
64 Abbreviations of proteins involved in glycolysis are same to Fig. 1. Note that different translation elongation factors, ribosomal proteins, proteasomes, proteases, chaperonins, HSPs, 129
65 LEA and PDI were identied in different species. 130
1 the other sections. Several recent reviews have been published on 4.3. Proteomic changes associated with seed dormancy 66
2 proteomic changes associated with various aspects of seed germi- 67
3 nation (Arc et al., 2011; Rajjou et al., 2012; He and Yang, 2013; Tan Dormancy is the temporary failure of a seed to complete 68
4 et al., 2013). germination under favorable conditions. This means that they 69
5 The processes taking place during germination, identied cannot complete phase II (Bewley et al., 2013). According to the 70
6 mainly by physiological and genomic methods, are well illustrated hormone balance theory, the relative actions of abscisic acid (ABA) 71
7 in the tri-phasic germination model (Bewley, 1997; Nonogaki et al., (inhibitory) and gibberellic acid (GA) (promotive) are the primary 72
8 2010; Weitbrecht et al., 2011; Bewley et al., 2013). Some of the determinants of seed dormancy and germination (Bewley et al., 73
9 processes occurring during germination, especially during germi- 2013). However, a proteomic study in Arabidopsis showed that 74
10 nation sensu stricto (phase I and II) have also been identied by the proteomic prole of dormant seeds was quite different from 75
11 many proteomic studies (Fig. 2) e translation, reserve mobilization that of non-dormant seeds treated with exogenous ABA to make 76
12 and detoxication occurs during both phase I and II of germination them dormant. This indicates that the mechanism of dormancy 77
13 (Fig. 2). In many species, amino acid metabolism and energy induction also differed (Chibani et al., 2006). 78
14 production are mainly activated during phase II of germination Seed dormancy can be broken by a number of treatments where 79
15 Q4 (Fig. 2). low temperature for longer periods of time (cold stratication) is 80
16 The mature seed contains all the proteins and mRNA needed to probably the best studied. However, nitrate or nitrite treatment can 81
17 get metabolism started. During the early stages of seed imbibition also break certain types of dormancy (e.g. Arc et al., 2012). It is likely 82
18 de novo protein biosynthesis is at least partly dependent on these that this is connected to the production of NO from nitrite in the 83
19 stored mRNAs (Nonogaki et al., 2010; Rajjou et al., 2012). The mitochondria under the hypoxic conditions of the seed interior 84
20 general changes in the seed proteome during germination will be (Hebelstrup and Mller, in press), since NO by itself can also break 85
21 exemplied by two studies, one on Arabidopsis (Galland et al., dormancy. In Arabidopsis, dormancy breaking by stratication and 86
22 2014) and one on rice (Yang et al., 2007). by exogenous nitrate gave very similar proteome adjustments (Arc 87
23 In Arabidopsis seeds, Galland et al. (2014) carried out a very et al., 2012). About 35 proteins belonging to the groups of storage 88
24 interesting study where not only differential protein expression, proteins and stress response and detoxication were more abun- 89
25 but also de novo protein synthesis measured as 35S-methionine dant in the dormant seeds, while proteins belonging to the groups 90
26 (Met) incorporation, was followed during different germination of energy (20), amino acid metabolism, folding and stability, pro- 91
27 phases. A total of 202 proteins spots (representing 158 non- teolysis and mRNA metabolism and protein synthesis (about 10 92
28 redundant proteins) were radioactively labeled and therefore at each) were more abundant in the non-dormant seeds. 93
29 least partially de novo synthesized. Out of the 273 spots not 94
30 radioactively labeled (representing 140 non-redundant proteins), 95
31 123 spots showed increased abundance in spite of the fact that 4.4. Changes in post-translational modications during 96
32 they were not de novo synthesized. This demonstrates the extent germination 97
33 to which PTMs such as phosphorylation or protease degradation, 98
34 modify the proteome composition as viewed by 2D-PAGE (see also PTMs in proteins can be regulatory, e.g. phosphorylation, they 99
35 later). When the frequency distribution of functional categories can be part of protein degradation pathways, e.g. ubiquitination, or 100
36 was compared for de novo synthesized protein spots and the un- they can perhaps be both as proposed for carbonylation (Arc et al., 101
37 labeled protein spots also increasing in abundance, some marked 2011). Protein carbonylation occurs as a result of metal-catalyzed 102
38 differences were observed. The categories energy, metabolism oxidation involving ROS and it is probably the most common irre- 103
39 (including enzymes involved in Met metabolism e see later) and versible protein oxidation PTM (Mller et al., 2011). 104
40 protein fate included >53% of the de novo synthesized proteins, Han et al. (2014a,b) identied more than 800 phosphoproteins 105
41 but only 34% for unlabeled protein spots, the difference being the in rice seeds, out of which 149 changed in amount during germi- 106
42 35% unlabeled storage proteins, which was not unexpected. nation. Protein destination-related proteins were the largest func- 107
43 However, the de novo synthesized proteins included 9% cell tional category and half of these proteins were protein kinases and 108
44 components and cell cycle proteins, which were almost entirely phosphatases. This demonstrates that protein phosphorylation is 109
45 absent in unlabeled spots. Thus, these latter proteins were not heavily involved in reprogramming cellular metabolism during 110
46 present in the mature seeds, but were synthesized during seed germination and provides a catalog of potential regulatory 111
47 germination. proteins. 112
48 In rice seeds, the abundance of 63 proteins was observed to Job et al. (2005) investigated the occurrence of protein 113
49 decrease during germination, while the abundance of 69 proteins carbonylation during germination of Arabidopsis seeds. They found 114
50 increased (including 20 induced proteins) (Yang et al., 2007). The that the carbonylation of a number of important metabolic pro- 115
51 decreasing proteins were mainly storage proteins (globulins), proteins, e.g. glycolytic enzymes, mitochondrial ATP synthase and 116
52 teins associated with seed maturation (e.g. LEA proteins) and pro- Rubisco, increased during germination without any apparent ill 117
53 teins related to dehydration. Among the increasing proteins, effects on the seeds, which germinated at high rates and grew 118
54 enzymes involved in starch degradation and glycolysis dominated, vigorously. They therefore suggested that this could be a means to 119
55 but also breakdown products of storage proteins increased in adapt embryo metabolism to the oxidative conditions encountered 120
56 abundance. Most of these changes are quite predictable. during germination (Job et al., 2005). We need to get a more 121
57 Methionine-related enzymes have been observed to change in precise idea of the meaning of this metabolic adaption. However, 122
58 abundance during germination of seeds from a range of different since the tissues inside a mature seed are hypoxic (e.g. Rolletschek 123
59 species e Arabidopsis (Gallardo et al., 2001, 2002; Galland et al., et al., 2004), the sudden inux of oxygenated water into the seed 124
60 2014), pea (Wang et al., 2012b), wheat (Fercha et al., 2013), and during phase I will expose the seed to a serious oxidative challenge. 125
61 rice (Liu et al., 2014) as well as beech, Norway maple and sycamore Another type of protein oxidation involving Met sidechains, the 126
62 (Pawowski, 2010). In addition to the obvious importance of Met rst step of which to Met-SO is reversible, is involved in protecting 127
63 itself in protein biosynthesis, the role of Met in the biosynthesis of more sensitive sites from oxidative damage (Levine et al., 1996) and 128
64 polyamines, ethylene and biotin (Roje, 2006), all via S-adeno- in regulating metabolic processes (Rao et al., in press). Whether 129
65 sylmethionine (SAM), is probably also signicant. irreversible carbonylation, which is usually thought to lead to 130
1 protein degradation, can act in similar ways is still an open sulde (Rolland et al., 1996). In sugarbeet, this enzyme increased in 66
2 question. abundance in primed and aged-primed seeds, but decreased in 67
3 aged seeds (Catusse et al., 2011). Aging treatment also decreased 68
4 4.5. Proteomic changes in response to abiotic and biotic stress the accumulation of this protein during imbibition. The abundance 69
5 of Cys synthase decreased in untreated control seeds, but was 70
6 Tan et al. (2013) summarized the results from 13 studies in constant in osmoprimed seeds during germination in the presence 71
7 which proteomics had been used to study the effect of a range of of NaCl (Yacoubi et al., 2013). The de novo synthesis of cysteine 72
8 environmental conditions on the germinating seed proteome. A synthase was also inhibited in articially aged seeds during 73
9 total of 561 proteins changed their abundance level in response to germination (Rajjou et al., 2008). In plants, Ser is biosynthesized by 74
10 the treatments. The largest protein groups affected were glycolysis two different pathways: a phosphorylated pathway via 3- 75
11 (43 proteins), storage protein mobilization (117), protein processing phosphoglycerate and a photorespiratory pathway via glycine (Ho 76
12 (55), osmotic homeostasis (37) and ROS scavenging (42). However, et al., 1998). Catusse et al. (2011) observed that phosphoserine 77
13 the very diverse nature of the stresses studied e copper and cad- aminotransferase and serine hydroxymethyltransferase increased 78
14 mium ions, drought, low temperature, hormones (GA, ABA, salicylic in abundance in primed and aged-primed seeds, and decreased in 79
15 acid) and a-amanitin (inhibitor of RNA polymerase II), as well as aged sugarbeet seeds. 80
16 Fusarium graminearum infection e in combination with eight The conclusion from these observations is that proteins involved 81
17 different plant species meant that a consistent response could not in Met metabolism or the methyl cycle are very important in seed 82
18 be seen for any protein group. There was, for instance, no indication vigor. 83
19 that an increase in the abundance of ROS scavenging enzymes was a 84
20 general stress response (Tan et al., 2013 and references therein). 85
21 5.2. Protein synthesis and destination 86
22 5. Seed vigor 87
23 Proteins involved in protein synthesis. Seed aging has a strong 88
24 The denition of seed vigor adopted by the Association of Seed impact on the translation process. Many translation factors, 89
25 Analysts (AOSA) states: Seed vigor comprises those seed proper- including translation initiation factors eIf4A, eIf3 and EBP1 and 90
26 ties that determine the potential for rapid, uniform emergence, and translation elongation factor eIF-1a, eIF-1b, eIF-1 g and eEF-2 91
27 development of normal seedlings under a wide range of eld decreased in abundance in sugarbeet seeds during aging (Catusse 92
28 conditions (Black et al., 2006). Seed vigor is therefore central to the et al., 2011). In Arabidopsis seeds, several proteins related to 93
29 successful propagation of agricultural crops. However, this very translation, such as initiation factor 4A-1, elongation factor 1-g2, 94
30 complex property obviously depends on a wide range of elongation factor1B-g, and ribosomal protein 60S were less abun- 95
31 biochemical and molecular variables making it difcult to charac- dant in aged seeds than in control seeds during germination (Rajjou 96
32 terize (Rajjou et al., 2012). Seeds with different vigor resulting from et al., 2008). Articial aging of pre-harvest soybean seeds decreased 97
33 aging and priming, where aging decreases and priming increases signicantly the accumulation of translation elongation factor Tu1, 98
34 seed vigor, have been studied by proteomics (Gallardo et al., 2001; Tu2 and 1-a (Wang et al., 2012). Priming treatment enhances seed 99
35 Rajjou et al., 2008; Catusse et al., 2011; Wu et al., 2011; Xin et al., vigor and increases the accumulation of the proteins involved in 100
36 2011; Yacoubi et al., 2011, 2013; Chu et al., 2012; Cha ^telain et al., translation. In sugarbeet seeds, accumulation of eIF-1a, IF-1 g and 101
37 2012; Wang et al., 2012). These studies have led to the identica- eEF-2 was reversed when aged seeds were subjected to a priming 102
38 tion of many proteins and metabolic processes potentially impor- treatment (Catusse et al., 2011). All these results indicate that 103
39 tant for seed vigor. translation initiation and elongation factors are important for a 104
40 high degree of seed vigor. 105
41 5.1. Methionine metabolism Proteins involved in protein folding. The amounts of heat shock 106
42 proteins, chaperones and LEA proteins all correlate closely with 107
43 Met is essential in all organisms because it functions not only as seed vigor. In maize, HSP18, 17.2 and 16.9 were more abundant in 108
44 a building block for protein synthesis but also as the precursor of high-vigor seeds (Wu et al., 2011). Osmopriming treatment 109
45 SAM, the methyl group donor for the biosynthesis of polyamines, increased the abundance of HSP 70, 20 and 17.7, class I HSP 18.2 and 110
46 ethylene and biotin (Roje, 2006; Rajjou et al., 2012). Met synthase 17.4 in Arabidopsis (Gallardo et al., 2001) and alfalfa (Yacoubi et al., 111
47 catalyzes the formation of Met by the transfer of a methyl group 2011) seeds and GroEL, a complex oligomeric protein and a mo- 112
48 from 5-methyltetrahydrofolate to homocysteine. This reaction is lecular chaperone (Ryabova et al., 2013) in alfalfa (Yacoubi et al., 113
49 the last step in Met biosynthesis, and also serves to regenerate the 2011) seeds. In sugarbeet seeds, HSP17 decreased in abundance 114
50 methyl group of SAM (Eichel et al., 1995). Met synthase decreased during aging, but increased during priming for both control and 115
51 in abundance in untreated control alfalfa seeds in the presence of aged seeds (Catusse et al., 2011). De novo synthesis of HSP 101, 70 116
52 NaCl during germination (Yacoubi et al., 2013). This decrease did and 17.6 and T-complex protein 1 q-subunit (TCP-1-q), a molecular 117
53 not occur in osmoprimed seeds imbibed under salinity or control chaperone, was inhibited during germination in articially aged 118
54 (water) conditions, which paralleled an increased seed vigor sugarbeet seeds compared to control seeds (Rajjou et al., 2008). 119
55 afforded by the osmopriming treatment (Yacoubi et al., 2013). SAM LEA proteins are presumed to be involved in binding or 120
56 synthetase is a key enzyme converting the Met to SAM. For sug- replacement of water, in sequestering ions that will be concen- 121
57 arbeet seeds, priming treatment promoted germination and trated under dehydrated conditions, or in maintaining protein and 122
58 increased the accumulation of SAM synthetase, while aging treat- membrane structure (Cuming, 1999; Tunnacliffe and Wise, 2007; 123
59 ment caused a delay and decrease in seed germination and Battaglia et al., 2008). EMB564 (group 1 LEA family) and LEA-3 124
60 decreased the accumulation of this protein (Catusse et al., 2011). accumulated to a relatively high abundance in high vigor maize 125
61 Cysteine (Cys) is synthesized from serine (Ser), and serves as the seeds (Wu et al., 2011). De novo synthesis of Em-like protein GEA1 126
62 sulfur donor for Met. The amounts of several proteins responsible was inhibited during germination of sugarbeet seeds after aging 127
63 for Cys and Ser biosynthesis also exhibit a positive correlation with (Rajjou et al., 2008). In M. truncatula, the abundance of four LEA 128
64 seed vigor. Cys synthase (O-acetyl-serine (thiol) lyase) is respon- proteins, EM (LEA_5), D113.I/II (LEA_1), D-34.III (SMP) and CapLEA 129
65 sible for the formation of Cys from O-acetyl-serine and hydrogen I/II (LEA_4) and two chaperone-related proteins, glycine-rich RNA- 130
1 binding protein RPN-1 and sHSP20, increased in parallel to acqui- are thought to play an important role in intracellular trafcking in 66
2 ^telain et al., 2012).
sition of longevity during seed development (Cha various eukaryotic cells (Augustine et al., 2008; Ketelaar, 2013). 67
3 Protein involved in protein repair. One of the spontaneous Actin 7 was observed to accumulate less abundantly in articially 68
4 changes occurring in seed proteins during aging is the formation of aged Arabidopsis seeds than in control seeds during germination 69
5 isoaspartyl residues, which destabilizes the secondary protein (Rajjou et al., 2008). These results suggest that tubulin and actin 70
6 structure. The enzyme L-isoaspartyl methyltransferase recognizes might be a seed vigor markers. 71
7 such isoaspartyl residues and catalyzes the methylation of its free Annexins are multifunctional proteins characterized by their 72
8 acid group using S-adenosyl-L-methionine as the methyl donor. capacity to bind calcium ions and negatively charged lipids 73
9 This is the rst step towards the conversion back to an aspartyl (Mortimer et al., 2008; Laohavisit and Davies, 2011). One annexin 74
10 residue. This repair enzyme has been shown to be important for increased signicantly in abundance in sacred lotus (Nelumbo 75
11 both seed vigor and longevity in Arabidopsis (Oge et al., 2008). nucifera) seeds during heat stress. Transgenic Arabidopsis seeds 76
12 Met is very susceptible to ROS-mediated oxidation, but the rst ectopically expressing this annexin exhibited improved resistance 77
13 step is reversible as mentioned in Section 4.4. The enzyme to the accelerated aging treatment that is used for assessing seed 78
14 responsible for this, methionine sulfoxide reductase, has been vigor (Chu et al., 2012). Annexins could be a potential seed vigor 79
15 demonstrated to be important for seed longevity by repairing marker, which displayed decreased and increased abundance in 80
16 proteins oxidized on Met groups during aging (Ch^ atelain et al., untreated control and osmoprimed alfalfa seeds, respectively 81
17 2013). (Yacoubi et al., 2013). 82
18 83
19 5.3. Glycolysis 5.6. ROS detoxication 84
20 85
21 In central metabolism, the glycolytic pathway appears to be Production of ROS may be one of the main causes of loss of seed 86
22 affected much more by seed vigor than other pathways. Accumu- vigor. Rajjou et al. (2008) revealed that protein oxidation (carbon- 87
23 lation of glycolytic enzymes in many species, such as fructose-1,6- ylation) increased strongly in aged seeds. The amounts of enzymes 88
24 bisphosphatase in maize (Wu et al., 2011) and Arabidopsis (Rajjou involved in ROS removal correlate with seed vigor. SOD increased in 89
25 et al., 2008), phosphoglucomutase, 3-phosphoglycerate kinases abundance in high-vigor maize seeds (Wu et al., 2011) and in osmo- 90
26 and 3-phosphoglycerate kinases (cytosolic) in maize (Xin et al., primed alfalfa seeds (Yacoubi et al., 2011), while CAT 2 increased in 91
27 2011) and Arabidopsis (Rajjou et al., 2008), glyceraldehyde-3- hydro-primed Arabidopsis seeds (Gallardo et al., 2001). In addition, 92
28 phosphate dehydrogenase in sugarbeet (Catusse et al., 2011) and CAT and reduced glutathione-dependent dehydroascorbate reduc- 93
29 Arabidopsis (Rajjou et al., 2008) seeds all correlated positively with tase decreased in abundance in articially aged Arabidopsis seeds 94
30 seed vigor. during germination (Rajjou et al., 2008). The abundance of a 95
31 number of thiol-dependent antioxidant proteins and enzymes have 96
32 5.4. Signal transduction also been observed to relate to seed vigor. In maize seeds, 2-Cys Prx 97
33 BAS1, TPX and glutathione S-transferase accumulated abundantly 98
34 Phosphorylation and dephosphorylation of key regulatory pro- in high vigor seeds (Wu et al., 2011). Osmopriming treatment of 99
35 teins serve as an oneoff switch in the control of cellular activities alfalfa seeds increased the abundance of alkyl hydroperoxide 100
36 in eukaryotic cells. Serine/threonine protein phosphatases are reductase (thiol-specic antioxidant/Mal allergen), thioredoxin, 1- 101
37 ubiquitous enzymes in all eukaryotes. Protein phosphatase 2A Cys Prx, GST and mitochondrial Prx (Yacoubi et al., 2011). During 102
38 (PP2A), a subfamily of serine/threonine protein phosphatases, has aging, GST part A decreased signicantly in abundance in maize 103
39 been proposed to play positive and dynamic roles in stress seed (Xin et al., 2011). 104
40 signaling (Pas et al., 2009). The abundance of this protein Detoxication of aldehydes is also a necessary process for 105
41 decreased during aging, but increased during priming in sugarbeet acquisition of seed vigor. Glyoxalase, involved in the detoxication 106
42 seeds (Catusse et al., 2011). Plant 14-3-3 proteins function by of methylglyoxal, a highly reactive aldehyde derived from glycolysis 107
43 binding to phosphorylated client proteins to modulate their func- (Thornalley, 2003), increased in abundance in high-vigor maize 108
44 tion. Through the regulation of a diverse range of proteins including seeds (Wu et al., 2011). In maize seeds, aging decreased the accu- 109
45 kinases, transcription factors, structural proteins, ion channels and mulation level of glyoxalase and ADH (Xin et al., 2011). ADH, 110
46 pathogen defense-related proteins, they are being implicated in catalyzing the irreversible oxidation of a wide range of reactive 111
47 many physiological functions in plants (Denison et al., 2011). In aldehydes to their corresponding carboxylic acids, has been sug- 112
48 sugarbeet, 14-3-3 proteins decreased in abundance in aged seeds gested to play a pivotal role in detoxifying the aldehydes generated 113
49 and increased in primed and aged-primed seeds (Catusse et al., by environmental stress (Perozich et al., 1999). 114
50 2011). 115
51 6. Perspectives 116
52 5.5. Cell structure 117
53 In the proteomic studies discussed in the previous sections it 118
54 Microtubule arrays play critical roles in intracellular organiza- has generally been assumed that, when an increase in the abun- 119
55 tion and cell division in all eukaryotes. The a- and b-tubulin sub- dance of a given protein correlates with e.g. an increase in vigor or 120
56 units of microtubule heterodimerize in a head-to-tail fashion, some other benecial trait, it is an indication that the process in 121
57 giving rise to polarity that plays a crucial role in the function of the which the protein is involved is important for that process; and vice 122
58 microtubule array (Eckardt, 2006). In Arabidopsis, the tubulin b2b3 versa for proteins decreasing in abundance. Although that need not 123
59 chain decreased in abundance not only during the aging process, be the case, the proteomic studies have identied many proteins 124
60 but also during imbibition of aged seed (Rajjou et al., 2008). Hydro- that are potentially important for seed development, seed vigor 125
61 priming increased the abundance of both tubulin a-chain and and/or seed germination or for more specic seed traits such as 126
62 tubulin b-2, while osmo-priming only promoted the accumulation resistance to fungal pathogens. Proteins that have been identied 127
63 of tubulin b-2 (Gallardo et al., 2001). In eukaryotic cells, a large to be particularly important for at least two of these seed processes 128
64 number of proteins are targeted after translation to specic or- are involved in ROS detoxication, the cytoskeleton, glycolysis, 129
65 ganelles by a process called intracellular trafcking. Actin laments protein biosynthesis, post-translational modications, methionine 130
1 metabolism, and late embryogenesis-abundant (LEA) proteins. This Bantscheff, M., Lemeer, S., Savitski, M.M., Kuster, B., 2012. Quantitative mass spec- 66
trometry in proteomics: critical review update from 2007 to the present. Anal.
2 type of data cannot be obtained by transcriptomics as there is 67
Bioanal. Chem. 404, 939e965.
3 generally a poor correlation between mRNA amounts and protein Battaglia, M., Olvera-Carrillo, Y., Garciarrubio, A., Campos, F., Covarrubias, A.A., 2008. 68
4 amounts. However, even when we know which proteins are The enigmatic LEA proteins and other hydrophilins. Plant Physiol. 148, 6e24. 69
5 particularly important for a specic process, we still need infor- Berjak, P., Pammenter, N.W., 2008. From avicennia to zizania: seed recalcitrance in 70
perspective. Ann. Bot. 101, 213e228.
6 mation about the extent to which each individual protein is post- Bewley, 1997. Seed germination and dormancy. Plant Cell 9, 1055e1066. 71
7 translationally modied, e.g. by oxidation, phosphorylation or by Bewley, J.D., Bradford, K.J., Hilborst, H.W.M., Nonogaki, H., 2013. Seeds e Physiology 72
8 proteases. These modications can strongly affect the function of of Development, Germination and Dormancy, third ed. Springer, New York. 73
Black, M., Bewley, J.D., Halmer, P., 2006. The Encyclopedia of Seeds. Science, Tech-
9 the protein and often give strong hints about metabolic regulation nology and Uses. CABI International, Oxfordshire.
74
10 or metabolic adjustments to environmental factors. To study these Bnsager, B.C., Finnie, C., Roepstorff, P., Svensson, B., 2007. Spatio-temporal changes 75
11 PTMs often requires special enrichment steps because the PTMs are in germination and radical elongation of barley seeds tracked by proteome 76
analysis of dissected embryo, aleurone layer, and endosperm tissues. Prote-
12 sub-stoichiometric and because they in some cases (e.g. protein omics 7, 4528e4540.
77
13 phosphorylation) make the modied peptide more difcult to Borisjuk, L., Neuberger, T., Schwender, J., Heinzel, N., Sunderhaus, S., Fuchs, J., 78
14 detect by mass spectrometry. To study PTMs, gel-free systems and Hay, J.O., Tschiersch, H., Braun, H.P., Denolf, P., Lambert, B., Jakob, P.M., 79
Rolletschek, H., 2013. Seed architecture shapes embryo metabolism in oilseed
15 shot-gun proteomics using some type of quantication tagging will 80
rape. Plant Cell 25, 1625e1640.
16 be increasingly useful. Borisjuk, L., Rolletschek, H., 2009. The oxygen status of the developing seed. New. 81
17 The highlighting of potentially important proteins by prote- Phytol. 182, 17e30. 82
Boston, R.S., Fontes, E.B.P., Shank, B.B., Wrobel, R.L., 1991. Increased expression of
18 omics provides researchers and plant breeders with starting points 83
the maize immunoglobulin binding-protein homolog B-70 in 3 zein regulatory
19 for further studies where the next step will often be to look at the mutants. Plant Cell 3, 497e505. 84
20 expression and regulation of the gene encoding the protein of in- Boudet, J., Buitink, J., Hoekstra, F.A., Rogniaux, H., Larre, C., Satour, P., Leprince, O., 85
21 terest in their favorite crop plant. The ultimate aim is to incorporate 2006. Comparative analysis of the heat stable proteome of radicles of Medicago 86
truncatula seeds during germination identies late embryogenesis abundant
22 genes encoding particularly promising proteins into the breeding proteins associated with desiccation tolerance. Plant Physiol. 140, 1418e1436. 87
23 programs. Bruggink, T., van der Toorn, P., 1995. Induction of desiccation tolerance in germi- 88
24 nated seeds. Seed Sci. Res. 5, 1e4. 89
Catusse, J., Meinhard, J., Job, C., Strub, J.M., Fischer, U., Pestsova, E., Westhoff, P.,
25 Q5 Contributions Dorsselaer, A.V., Job, D., 2011. Proteomics reveals potential biomarkers of seed
90
26 vigor in sugarbeet. Proteomics 11, 1569e1580. 91
27 Ch^atelain, E., Hundertmark, M., Leprince, O., Le Gall, S., Satour, P., Deligny- 92
Abstract, Introduction, Seed germination and dormancy and Penninck, S., Rogniaux, H., Buitink, J., 2012. Temporal proling of the heat-stable
28 Perspectives were written by IMM, Seed development was written proteome during late maturation of Medicago truncatula seeds identies a
93
29 by WQW and SJL, Seed desiccation tolerance was written by WQW, restricted subset of late embryogenesis abundant proteins associated with 94
30 Seed vigor was written by SQS, while IMM, SQS and WQW revised longevity. Plant Cell Environ. 35, 1440e1455. 95
Ch^atelain, E., Satour, P., Laugier, E., Vu, B.L., Payet, N., Rey, P., Montrichard, F., 2013.
31 the manuscript. 96
Evidence for participation of the methionine sulfoxide reductase repair system
32 in plant seed longevity. Proc. Natl. Acad. Sci. U. S. A. 110 (9), 3633e3638. 97
33 Chen, Q., Yang, L.M., Ahmad, P., Wan, X.C., Hu, X.Y., 2011. Proteomic proling and 98
Uncited reference redox status alteration of recalcitrant tea (Camellia sinensis) seed in response to
34 99
desiccation. Planta 233, 583e592.
35 Chibani, K., Ali-Rachedi, S., Job, C., Job, D., Jullien, M., Grappin, P., 2006. Proteomic 100
Liu et al., 2015.
36 analysis of seed dormancy in Arabidopsis. Plant Physiol. 142, 1493e1510. 101
37 Chu, P., Chen, H., Zhou, Y., Li, Y., Ding, Y., Jiang, L., Tsang, E.W.T., Wu, K., Huang, S., 102
Acknowledgments 2012. Proteomic and functional analyses of Nelumbo nucifera annexins, involved
38 in seed thermotolerance and germination vigor. Planta 235, 1271e1288. 103
39 Cuming, A.C., 1999. LEA proteins. In: Shewry, P.R., Casey, R. (Eds.), Seed Proteins. 104
This work was supported by the National Science and Tech- Kluwer Academic Press, Dordrecht, The Netherlands, pp. 753e780.
40 105
nology Support Program (2012BAC01B05) and by National Science Delahaie, J., Hundertmark, M., Bove, J., Leprince, O., Rogniaux, H., Buitink, J., 2013.
41 LEA polypeptide proling of recalcitrant and orthodox legume seeds reveals
106
Foundation of China (31171624). IMM was supported by a Chinese
42 ABI3-regulated LEA protein abundance linked to desiccation tolerance. J. Exp. 107
Academy of Sciences Visiting Professorship for senior international Bot. 64, 4559e4573.
43 108
scientists. Deng, Z.Y., Gong, C.Y., Wang, T., 2013. Use of proteomics to understand seed
44 development in rice. Proteomics 13, 1784e1800.
109
45 Denison, F.C., Paul, A.L., Agata, K., Zupanska, A.K., Robert, J., Ferl, R.J., 2011. 14-3-3 110
46 References proteins in plant physiology. Semin. Cell Dev. Biol. 22, 720e727. 111
Dhugga, K.S., Tiwari, S.C., Ray, P.M., 1997. A reversibly glycosylated polypeptide
47 112
Agrawal, G.K., Hajduch, M., Graham, K., Thelen, J.J., 2008. In-depth investigation of (RGP1) possibly involved in plant cell wall synthesis: purication, gene cloning,
48 the soybean seed lling proteome and comparison with a parallel study of and trans-Golgi localization. Proc. Natl. Acad. Sci. U. S. A. 94, 7679e7684. 113
49 rapeseed. Plant Physiol. 148, 504e518. Eckardt, N.A., 2006. Function of g-tubulin in plants. Plant Cell 18, 1327e1329. 114
Allen, D.K., Ohlrogge, J.B., Shachar-Hill, Y., 2009. The role of light in soybean seed Eichel, J., Gonzalez, J.C., Hotze, M., Matthews, R.G., Schro der, J., 1995. Vitamin-B12-
50 115
lling metabolism. Plant J. 58, 220e234. independent methionine synthase from a higher plant (Catharanthus roseus).
51 Arc, E., Galland, M., Cueff, G., Godin, B., Louni, I., Job, D., Rajjou, L., 2011. Reboot the Molecular characterization, regulation, heterologous expression, and enzyme 116
52 system thanks to protein post-translational modications and proteome di- properties. Eur. J. Biochem. 230, 1053e1058. 117
53 versity: how quiescent seeds restart their metabolism to prepare seedling Fercha, A., Capriotti, A.L., Caruso, G., Cavaliere, C., Gherrouchac, H., Samperi, R., 118
establishment. Proteomics 22, 1606e1618. Stampachiacchiere, S., Lagana, A., 2013. Gel-free proteomics reveal potential
54 Arc, E., Chibani, K., Grappin, P., Jullien, M., Godin, B., Cueff, G., Valot, B., Balliau, T., biomarkers of priming-induced salt tolerance in durum wheat. J. Proteomics 91, 119
55 Job, D., Rajjou, L., 2012. Cold stratication and exogenous nitrates entail similar 486e499. 120
56 functional proteome adjustments during Arabidopsis seed dormancy release. Finnie, C., Melchior, S., Roepstorff, P., Svensson, B., 2002. Proteome analysis of grain 121
J. Proteome Res. 11, 5418e5432. lling and seed maturation in barley. Plant Physiol. 129, 1308e1319.
57 Galland, M., Huguet, R., Erwann Arc, E., Cueff, G., Job, D., Rajjou, L., 2014. Dynamic
122
Augustine, R.C., Vidali, L., Kleinman, K.P., Bezanilla, M., 2008. Actin depolymerizing
58 factor is essential for viability in plants, and its phosphoregulation is important proteomics emphasizes the importance of selective mRNA translation and 123
59 for tip growth. Plant J. 54, 863e875. protein turnover during Arabidopsis seed germination. Mol. Cell. Proteomics 13, 124
Bai, X.G., Yang, L.M., Tian, M.H., Chen, J.H., Shi, J.S., Yang, Y.P., Hu, X.Y., 2011. Nitric 252e268.
60 Gallardo, K., Firnhaber, C., Zuber, H., Hericher, D., Belghazi, M., Henry, C., Kuster, H.,
125
oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via
61 protein S-nitrosylation and carbonylation. PLoS One 6 (6), e20714. Thompson, R., 2007. A combined proteome and transcriptome analysis of 126
62 Bailly, C., 2004. Active oxygen species and antioxidants in seed biology. Seed Sci. developing Medicago truncatula seeds: evidence for metabolic specialization of 127
Res. 14, 93e107. maternal and lial tissues. Mol. Cell. Proteomics 6, 2165e2179.
63 128
Bailly, C., El-Maarouf-Bouteau, H., Corbineau, F., 2008. From intracellular signaling Gallardo, K., Job, C., Groot, S.P.C., Puype, M., Demol, H., Vandekerckhove, J., Job, D.,
64 networks to cell death: the dual role of reactive oxygen species in seed phys- 2001. Proteomic analysis of Arabidopsis seed germination and priming. Plant 129
65 iology. CR Biol. 331, 806e814. Physiol. 126, 835e848. 130
1 Gallardo, K., Job, C., Groot, S.P.C., Puype, M., Demol, H., Vandekerckhove, J., Job, D., Levine, R.L., Mosoni, L., Berlett, B.S., Stadtman, E.R., 1996. Methionine residues as 66
2002. Importance of methionine biosynthesis for Arabidopsis seed germination endogenous antioxidants in proteins. Proc. Natl. Acad. Sci. U. S. A. 93,
2 67
and seedling growth. Physiol. Plant 116, 238e247. 15036e15040.
3 Gallardo, K., Le Signor, C., Vandekerckhove, J., Thompson, R.D., Burstin, J., 2003. Li, X.J., Yang, M.F., Chen, H., Qu, L.Q., Chen, F., Shen, S.H., 2010. Abscisic acid pre- 68
4 Proteomics of Medicago truncatula seed development establishes the time treatment enhances salt tolerance of rice seedlings: proteomic evidence. BBA 69
5 frame of diverse metabolic processes related to reserve accumulation. Plant Proteins Proteomics 1804, 929e940. 70
Physiol. 133, 664e682. Liu, H., Wang, C., Komatsu, S., He, M., Liu, G., Shen, S., 2013. Proteomic analysis of the
6 Geigenberger, P., 2003. Response of plant metabolism to too little oxygen. Curr. seed development in Jatropha curcas: from carbon ux to the lipid accumula- 71
7 Opin. Plant Biol. 6, 247e256. tion. J. Proteomics 91, 23e40. 72
8 Goffman, F.D., Alonso, A.P., Schwender, J., Shachar-Hill, Y., Ohlrogge, J.B., 2005. Light Liu, S.J., Xu, H.H., Wang, W.Q., Li, N., Wang, W.P., Mller, I.M., Song, S.Q., 2015. 73
enables a very high efciency of carbon storage in developing embryos of A proteomic analysis of rice seed germination as affected by high temperature
9 rapeseed. Plant Physiol. 138, 2269e2279. and ABA treatment. Physiol. Plant. http://dx.doi.org/10.1111/ppl.12292. Q7
74
10 Grune, T., Reinheckel, T., Davies, K.J.A., 1997. Degradation of oxidized proteins in Mayer, U., Jrgens, G., 2002. Microtubule cytoskeleton: a track record. Curr. Opin. 75
11 mammalian cells. FASEB J. 11, 526e534. Plant Biol. 5, 494e501. 76
Guo, G., Lv, D., Yan, X., Subburaj, S., Ge, P., Li, X., Hu, Y., Yan, Y., 2012. Proteome McDonald, M.B., 2000. Seed priming. In: Black, M., Bewley, J.D. (Eds.), Seed Tech-
12 characterization of developing grains in bread wheat cultivars (Triticum aesti- nology and its Biological Basis. Shefeld Acad, Shefeld, UK, pp. 287e325.
77
13 vum L.). BMC Plant Biol. 12, 147. Me chin, V., Thevenot, C., Le Guilloux, M., Prioul, J.L., Damerval, C., 2007. Develop- 78
14 Hajduch, M., Casteel, J.E., Hurrelmeyer, K.E., Song, Z., Agrawal, G.K., Thelen, J.J., 2006. mental analysis of maize endosperm proteome suggests a pivotal role for py- 79
Proteomic analysis of seed lling in Brassica napus. Developmental character- ruvate orthophosphate dikinase. Plant Physiol. 143, 1203e1219.
15 80
ization of metabolic isozymes using high-resolution two-dimensional gel Meyer, L.J., Gao, J., Xu, D., Thelen, J.J., 2012. Phosphoproteomic analysis of seed
16 electrophoresis. Plant Physiol. 141, 32e46. maturation in Arabidopsis, rapeseed, and soybean. Plant Physiol. 159, 517e528. 81
17 Hajduch, M., Ganapathy, A., Stein, J.W., Thelen, J.J., 2005. A systematic proteomic Miernyk, J.A., 2014. Seed proteomics. In: Jorrin-Novo, J.V., Komatsu, S., 82
study of seed lling in soybean. Establishment of high-resolution two-dimen- Weckwerth, W., Wienkoop, S. (Eds.), Plant Proteomics: Methods and Protocols,
18 83
sional reference maps, expression proles, and an interactive proteome data- second ed. Springer, New York, pp. 361e377.
19 base. Plant Physiol. 137, 1397e1419. Miernyk, J.A., Hajduch, M., 2011. Seed proteomics. J. Proteomics 74, 289e400. 84
20 Hajduch, M., Hearne, L.B., Miernyk, J.A., Casteel, J.E., Joshi, T., Agrawal, G.K., Song, Z., Miernyk, J.A., Johnston, M.L., 2013. Proteomic analysis of the testa from developing 85
21 Zhou, M.Y., Xu, D., Thelen, J.J., 2010. Systems analysis of feed lling in Arabi- soybean seeds. J. Proteomics 89, 265e272. 86
dopsis: using general linear modeling to assess concordance of transcript and Minic, Z., 2008. Physiological roles of plant glycoside hydrolases. Planta 227,
22 protein expression. Plant Physiol. 152, 2078e2087. 723e740. 87
23 Han, C., He, D., Li, M., Yang, P., 2014a. In-depth proteomic analysis of rice embryo Mller, I.M., 2001. Plant mitochondria and oxidative stress: electron transport, 88
24 reveals its important roles in seed germination. Plant Cell Physiol. 55, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant 89
1826e1847. Physiol. Plant Mol. Biol. 52, 561e591.
25 Han, C., Yang, P., Sakata, K., Komatsu, S., He, D., 2014b. Quantitative proteomics Mller, I.M., Jensen, P.E., Hansson, A., 2007. Oxidative modications to cellular
90
26 reveals the role of protein phosphorylation in rice embryos during early stages components in plants. Annu. Rev. Plant Biol. 58, 459e481. 91
27 of germination. J. Proteome Res. 13, 1766e1782. Mller, I.M., Sweetlove, L.J., 2010. ROS signalling e specicity is required. Trends 92
He, D., Yang, P., 2013. Proteomics of rice seed germination. Front. Plant Sci. 4, 246. Plant Sci. 15, 370e374.
28 Hebelstrup, K.H., Mller, I.M., 2014. Mitochondrial signaling in plants under hyp- Mller, I.M., Rogowska-Wrzesinska, A., Rao, R.S.P., 2011. Protein carbonylation and
93
29 oxia: use of reactive oxygen species (ROS) and reactive nitrogen species (RNS). metal-catalyzed protein oxidation in a cellular perspective. J. Proteomics 74, 94
30 In: Gupta, K.J., Igamberdiev, A.U. (Eds.), Reactive Oxygen and Nitrogen Species 2228e2242. 95
Signaling and Communication in Plants. Springer, New York (in press). Mller, I.M., Rasmusson, A.G., Browse, J.J., 2014. Plant respiration and lipid meta-
31 Q6 96
Henty-Ridilla, J.L., Li, J.J., Blanchoin, L., Staiger, C.J., 2013. Actin dynamics in the bolism. In: Taiz, L., Zeiger, E., Mller, I.M., Murphy, A. (Eds.), Plant Physiology
32 cortical array of plant cells. Curr. Opin. Plant Biol. 16, 678e687. and Development. Sinauer Press, Sunderland, MA, USA (in press). 97
33 Heydecker, W., Higgins, J., Gulliver, R.L., 1973. Accelerated germination by osmotic Mortimer, J.C., Laohavisit, A., Macpherson, N., Webb, A., Brownlee, C., Battey, N.H., 98
seed treatment. Nature 246, 42e44. Davies, J.M., 2008. Annexins: multifunctional components of growth and
34 99
Ho, C.L., Noji, M., Saito, M., Yamazaki, M., Saito, K., 1998. Molecular characterization adaptation. J. Exp. Bot. 59, 533e544.
35 of plastidic phosphoserine aminotransferase in serine biosynthesis from Ara- Mller, K., Job, C., Belghazi, M., Job, D., Leubner-Metzger, G., 2010. Proteomics reveal 100
36 bidopsis. Plant J. 16, 443e452. tissue-specic features of the cress (Lepidium sativum L.) endosperm cap pro- 101
37 Hoekstra, F.A., Golovina, E.A., Buitink, J., 2001. Mechanisms of plant desiccation teome and its hormone-induced changes during seed germination. Proteomics 102
tolerance. Trends Plant Sci. 6, 431e438. 10, 406e416.
38 Hortin, G.L., Sviridov, D., 2010. The dynamic range problem in the analysis of the Nakabayashi, K., Okamoto, M., Koshiba, T., Kamiya, Y., Nambara, E., 2005. 103
39 plasma proteome. J. Proteomics 73, 629e636. Genome-wide proling of stored mRNA in Arabidopsis thaliana seed germi- 104
40 Houston, N.L., Hajduch, M., Thelen, J.J., 2009. Quantitative proteomics of seed lling nation: epigenetic and genetic regulation of transcription in seed. Plant J. 41, 105
in castor: comparison with soybean and rapeseed reveals differences between 697e709.
41 photosynthetic and nonphotosynthetic seed metabolism. Plant Physiol. 151, Nogueira, F.C.S., Palmisano, G., Soares, E.L., Shah, M., Soares, A.A., Roepstorff, P.,
106
42 857e868. Campos, F.A.P., Domont, G.B., 2012. Proteomic prole of the nucellus of castor 107
43 Howell, K.A., Narsai, R., Carroll, A., Ivanova, A., Lohse, M., Usadel, B., Millar, A.H., bean (Ricinus communis L.) seeds during development. J. Proteomics 75, 108
Whelan, J., 2009. Mapping metabolic and transcript temporal switches during 1933e1939.
44 germination in rice highlights specic transcription factors and the role of RNA Nogueira, F.C.S., Palmisano, G., Schwammle, V., Soares, E.L., Soares, A.A.,
109
45 instability in the germination process. Plant Physiol. 149, 961e980. Roepstorff, P., Domont, G.B., Campos, F.A.P., 2013. Isotope labeling-based 110
46 Huang, H., Mller, I.M., Song, S.Q., 2012. Proteomics of desiccation tolerance during quantitative proteomics of developing seeds of castor oil seed (Ricinus com- 111
development and germination of maize embryos. J. Proteomics 75, 1247e1262. munis L.). J. Proteome Res. 12, 5012e5024.
47 112
Jin, X.N., Fu, Z.Y., Ding, D., Li, W.H., Liu, Z.H., Tang, J.H., 2013. Proteomic identication Nonogaki, H., Bassel, G.W., Bewley, J.D., 2010. Germination e still a mystery. Plant
48 of genes associated with maize grain-lling rate. PLoS One 8, e59353. Sci. 179, 574e581. 113
49 Job, C., Rajjou, L., Lovigny, Y., Belghazi, M., Job, D., 2005. Patterns of protein oxidation Oge , L., Bourdais, G., Bove, J., Collet, B., Godin, B., Granier, F., Boutin, J.P., Job, D., 114
in arabidopsis seeds and during germination. Plant Physiol. 138, 790e802. Jullien, M., Grappin, P., 2008. Protein repair L-isoaspartyl methyltransferase1 is
50 115
Kermode, A.R., 1997. Approaches to elucidate the basis of desiccation-tolerance in involved in both seed longevity and germination vigor in Arabidopsis. Plant Cell
51 seeds. Seed Sci. Res. 7, 75e95. 20, 3022e3037. 116
52 Kermode, A., Finch-Savage, B., 2002. Desiccation sensitivity in orthodox and Oliver, M.J., Guo, L.N., Alexander, D.C., Ryals, J.A., Wone, B.W.M., Cushman, J.C., 2011. 117
53 recalcitrant seeds in relation to development. In: Black, M., Pritchard, H. (Eds.), A sister group contrast using untargeted global metabolomic analysis delineates 118
Desiccation and Survival in Plants, Drying without Drying. CAB International, the biochemical regulation underlying desiccation tolerance in Sporobolus
54 Wallingford, pp. 149e184. stapanus. Plant Cell 23, 1231e1248. 119
55 Ketelaar, T., 2013. The actin cytoskeleton in root hairs: all is ne at the tip. Curr. Oliver, M.J., Velten, J., Mishler, B.D., 2005. Desiccation tolerance in bryophytes: a 120
56 Opin. Plant Biol. 16, 749e756. reection of the primitive strategy for plant survival in dehydrating habitats? 121
Kim, Y.J., Yeu, S.Y., Park, B.S., Koh, H.J., Song, J.T., Seo, H.S., 2012. Protein disulde Integr. Comp. Biol. 45, 788e799.
57 isomerase-like protein 1-1 controls endosperm development through regula- Pas, S.M., Te llez-In
~o n, M.T., Capiati, D.A., 2009. Serine/threonine protein phos- 122
58 tion of the amount and composition of seed proteins in rice. PLoS One 7, phatases type 2A and their roles in stress signaling. Plant Signal Behav. 4, 123
59 e44493. 1013e1015. 124
Kranner, I., Birtic, S., 2005. A modulating role for antioxidants in desiccation Pammenter, N.W., Berjak, P., 1999. A review of recalcitrant seed physiology in
60 tolerance. Integr. Comp. Biol. 45, 734e740. relation to desiccation tolerance mechanisms. Seed Sci. Res. 9, 13e37.
125
61 Laohavisit, A., Davies, J.M., 2011. Annexins. New. Phytol. 189, 40e53. Pan, S., Aebersold, R., Chen, R., Rush, J., Goodlett, D.R., McIntosh, M.W., Zhang, J., 126
62 Lee, J., Koh, H.J., 2011. A label-free quantitative shotgun proteomics analysis of rice Brentnall, T.A., 2009. Mass spectrometry based targeted protein quantication: 127
grain development. Proteome Sci. 9, 61. methods and applications. J. Proteome Res. 8, 787e797.
63 128
Leprince, O., Buitink, J., 2010. Desiccation tolerance: from genomics to the eld. Pawowski, T.A., 2010. Proteomic approach to analyze dormancy breaking of tree
64 Plant Sci. 179, 554e564. seeds. Plant Mol. Biol. 73, 15e25. 129
65 130
1 Perozich, J., Nicholas, H., Lindahl, R., Hempel, J., 1999. The big book of aldehyde Tan, L., Chen, S., Wang, T., Dai, S., 2013. Proteomic insights into seed germination in 43
dehydrogenase sequences. An overview of the extended family. Adv. Exp. Med. response to environmental factors. Proteomics 13, 1850e1870.
2 44
Biol. 463, 1e7. Tan-Wilson, A.L., Wilson, K.A., 2012. Mobilization of seed protein reserves. Physiol.
3 Rajjou, L., Duval, M., Gallardo, K., Catusse, J., Bally, J., Job, C., Job, D., 2012. Seed Plant 145, 140e153. 45
4 germination and vigor. Annu. Rev. Plant Biol. 63, 507e533. Thornalley, P.J., 2003. Glyoxalase I e structure, function and a critical role in the 46
5 Rajjou, L., Gallardo, K., Debeaujon, I., Vandekerckhove, J., Job, C., Job, D., 2004. The enzymatic defence against glycation. Biochem. Soc. Trans. 31, 1343e1348. 47
effect of alpha-amanitin on the Arabidopsis seed proteome highlights the Tunnacliffe, A., Wise, M.J., 2007. The continuing conundrum of the LEA proteins.
6 distinct roles of stored and neosynthesized mRNAs during germination. Plant Naturwissenschaften 94, 791e812. 48
7 Physiol. 134, 1598e1613. Vinh, D.B.N., Drubin, D.G., 1994. A yeast tcp-1-like protein is required for actin 49
8 Rajjou, L., Lovigny, Y., Groot, S.P.C., Belghazi, M., Job, C., Job, D., 2008. Proteome-wide function in vivo. Proc. Natl. Acad. Sci. U. S. A. 91, 9116e9120. 50
characterization of seed aging in Arabidopsis: a comparison between articial Vitale, A., Ceriotti, A., 2004. Protein quality control mechanisms and protein storage
9 and natural aging protocols. Plant Physiol. 148, 620e641. in the endoplasmic reticulum. A conict of interests? Plant Physiol. 136,
51
10 Rao, R.S.P., Mller, I.M., 2012. Large-scale analysis of phosphorylation site occupancy 3420e3426. 52
11 in eukaryotic proteins. BBA Proteins Proteomics 1824, 405e412. Walters, C., Wheeler, L.M., Grotenhuis, J.M., 2005. Longevity of seeds stored in a 53
Rao, R.S.P., Mller, I.M., Thelen, J.J., Miernyk, J.A., 2015. Convergent signaling path- genebank: species characteristics. Seed Sci. Res. 15, 1e20.
12 ways e interaction between methionine oxidation and serine/threonine/tyro- Walther, T.C., Mann, M., 2010. Mass spectrometry-based proteomics in cell biology.
54
13 sine O-phosphorylation. Cell Stress Chaperones (in press). J. Cell. Biol. 190, 491e500. 55
14 Rogers, L.D., Overall, C.M., 2013. Proteolytic post-translational modication of pro- Wang, L., Ma, H., Song, L., Shu, Y., Gu, W., 2012. Comparative proteomics analysis 56
teins: proteomic tools and methodology. Mol. Cell. Proteomics 12, 3532e3542. reveals the mechanism of pre-harvest seed deterioration of soybean under high
15 57
Rogowska-Wrzesinska, A., Le Bihan, M.C., Thaysen-Andersen, M., Roepstorff, P., temperature and humidity stress. J. Proteomics 75, 2109e2127.
16 2013. 2D gels still have a niche in proteomics. J. Proteomics 88, 4e13. Wang, W.Q., Cheng, H.Y., Mller, I.M., Song, S.Q., 2012a. The role of recovery of 58
17 Roje, S., 2006. S-Adenosyl-L-methionine: beyond the universal methyl group donor. mitochondrial structure and function in desiccation tolerance of pea seeds. 59
Phytochemistry 67, 1686e1698. Physiol. Plant 144, 20e34.
18 60
Rolland, N., Ruffet, M.L., Job, D., Douce, R., Droux, M., 1996. Spinach chloroplast O- Wang, W.Q., Mller, I.M., Song, S.Q., 2012b. Proteomic analysis of embryonic axis of
19 acetylserine (thiol)-lyase exhibits two catalytically non-equivalent pyridoxal- Pisum sativum seeds during germination and identication of proteins associ- 61
20 50-phosphate-containing active sites. Eur. J. Biochem. 236, 272e282. ated with loss of desiccation tolerance. J. Proteomics 77, 68e86. 62
21 Rolletschek, H., Weschke, W., Weber, H., Wobus, U., Borisjuk, L., 2004. Energy state Wang, W.Q., Ye, J.Q., Rogowska-Wrzesinska, A., Wojdyla, K.I., Jensen, O.N., 63
and its control on seed development: starch accumulation is associated with high Mller, I.M., Song, S.Q., 2014. Proteomic comparison between maturation drying
22 ATP and steep oxygen gradients within barley grains. J. Exp. Bot. 55, 1351e1359. and prematurely imposed drying of Zea mays seeds reveals a potential role of 64
23 Ruuska, S.A., Ohlrogge, J.B., 2004. The capacity of green oilseeds to utilize photo- maturation drying in preparing proteins for seed germination, seedling vigor, 65
24 synthesis to drive biosynthetic processes. Plant Physiol. 136, 3409. and pathogen resistance. J. Proteome Res. 13, 606e626. 66
Ryabova, N.A., Marchenkov, V.V., Marchenkova, SYu, Kotova, N.V., Semisotnov, G.V., Wu, X., Liu, H., Wang, W., Chen, S., Hu, X., Li, C., 2011. Proteomic analysis of seed
25 2013. Molecular chaperone GroEL/ES: unfolding and refolding processes. Bio- viability in maize. Acta Physiol. Plant 33, 181e191.
67
26 chem. Mosc. 78, 1405e1414. Xin, X., Lin, X.H., Zhou, Y.C., Chen, X.L., Liu, X., Lu, X.X., 2011. Proteome analysis of 68
27 Sano, N., Masaki, S., Tanabata, T., Yamada, T., Hirasawa, T., Kanekatsu, M., 2013a. maize seeds: the effect of articial ageing. Physiol. Plant 143, 126e138. 69
Proteomic analysis of stress-related proteins in rice seeds during the desicca- Xu, H., Zhang, W., Gao, Y., Zhao, Y., Guo, L., Wang, J., 2012. Proteomic analysis of
28 tion phase of grain lling. Plant Biotechnol. 30, 147e156. embryo development in rice (Oryza sativa). Planta 235, 687e701.
70
29 Sano, N., Masaki, S., Tanabata, T., Yamada, T., Hirasawa, T., Kashiwagi, M., Xu, S.B., Li, T., Deng, Z.Y., Chong, K., Xue, Y.B., Wang, T., 2008. Dynamic proteomic 71
30 Kanekatsu, M., 2013b. RNA-binding proteins associated with desiccation during analysis reveals a switch between central carbon metabolism and alcoholic 72
seed development in rice. Biotechnol. Lett. 35, 1945e1952. fermentation in rice lling grains. Plant Physiol. 148, 908e925.
31 73
Sano, N., Permana, H., Kumada, R., Shinozaki, Y., Tanabata, T., Yamada, T., Yacoubi, R., Job, C., Belghazi, M., Chaibi, W., Job, D., 2011. Toward characterizing seed
32 Hirasawa, T., Kanekatsu, M., 2012. Proteomic analysis of embryonic proteins vigor in alfalfa through proteomic analysis of germination and priming. 74
33 synthesized from long-lived mRNAs during germination of rice seeds. Plant Cell J. Proteome Res. 10, 3891e3903. 75
Physiol. 53, 687e698. Yacoubi, R., Job, C., Belghazi, M., Chaibi, W., Job, D., 2013. Proteomic analysis of the
34 76
Sassa, H., Oguchi, S., Inoue, T., Hirano, H., 2000. Primary structural features of the enhancement of seed vigour in osmoprimed alfalfa seeds germinated under
35 20S proteasome subunits of rice (Oryza sativa). Gene 250, 61e66. salinity stress. Seed Sci. Res. 23, 99e110. 77
36 Schwender, J., Goffman, F., Ohlrogge, J.B., Shachar-Hill, Y., 2004. Rubisco without the Yaffe, M.B., Farr, G.W., Miklos, D., Horwich, A.L., Sternlicht, M.L., Sternlicht, H., 1992. 78
37 Calvin cycle improves the carbon efciency of developing green seeds. Nature Tcp1 complex is a molecular chaperone in tubulin biogenesis. Nature 358, 79
432, 779e782. 245e248.
38 Staiger, C.J., Gibbon, B.C., Kovar, D.R., Zonia, L.E., 1997. Prolin and actin- Yang, P., Li, X., Wang, X., Chen, H., Chen, F., Shen, S., 2007. Proteomic analysis of rice 80
39 depolymerizing factor: modulators of actin organization in plants. Trends (Oryza sativa) seeds during germination. Proteomics 7, 3358e3368. 81
40 Plant Sci. 2, 275e281. 82
41 83
42 84

Proteomics of Seed Development, Desiccation Tolerance, Germination

Hochgeladen von

Dokumentinformationen

Copyright

Verfügbare Formate

Dieses Dokument teilen

Dokument teilen oder einbetten

Freigabeoptionen

Stufen Sie dieses Dokument als nützlich ein?

Sind diese Inhalte unangemessen?

Copyright:

Verfügbare Formate

Proteomics of Seed Development, Desiccation Tolerance, Germination

Hochgeladen von

Copyright:

Verfügbare Formate

PLAPHY4085_proof 5 November 2014 1/15

Plant Physiology and Biochemistry xxx (2014) 1e15

Das könnte Ihnen auch gefallen