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Bacteria and fungi controlling plant growth by

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development and defense

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DOI: 10.1016/j.jplph.2014.01.002

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Contents lists available at ScienceDirect

Journal of Plant Physiology

journal homepage: www.elsevier.com/locate/jplph

Review

Bacteria and fungi controlling plant growth by manipulating auxin:

Balance between development and defense
Jutta Ludwig-Mller
Technische Universitt Dresden, Institut fr Botanik, 01062 Dresden, Germany

a r t i c l e i n f o s u m m a r y

Article history: Plant diseases cause huge losses by changing the quality and quantity of harvested crops. Many disease
Received 18 December 2013 symptoms caused by bacteria or fungi rely on the involvement of plant hormones, while other plant
Received in revised form 15 January 2014 hormones act as defense signals in the plant. In this review the role of auxins in these processes will
Accepted 17 January 2014
be evaluated. Some growth promoting plant hormones cause disease symptoms. For example auxins
stimulate cell division and cell elongation in a healthy plant, but tumor formation after bacterial infection.
Keywords:
Thus, control of auxin levels and auxin signaling pathways signicantly contribute to the defense network
Auxin homeostasis
in plants. Auxin can also act directly as defense molecule with antimicrobial activity. Since much research
Auxin signaling
Defense
has been done in the recent years on auxin as a pathogenicity factor for many diseases, several examples
Plant disease will be presented to highlight the complexity between normal plant growth, which is regulated by auxin,
Resistance and processes determining resistance or susceptibility, triggered by the same class of molecules.
2014 Elsevier GmbH. All rights reserved.

Contents

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
Auxin biosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
Auxin signaling and transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Auxin homeostasis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

Introduction
This could be a dilemma, because the balance between defense and
Plant growth and development is controlled by many signaling benecial growth responses has to be maintained. Plant hormones
molecules, the so-called plant hormones, but these are also some- can integrate the response to developmental and environmental
times signals for defense responses. In their natural environment cues and thus limit defense-associated tness costs. Many plant
plants have to cope with a plethora of different organisms by which hormones, especially those controlling plant growth responses, t
they are challenged. They have therefore developed many resis- into this category (reviewed in Denanc et al., 2013), but here auxin
tance mechanisms, using different cues for the recognition of a will be taken as an example to explain the concept of balance
diverse range of pathogens. As outlined by Mausz and Pohnert between benet and pathogen. In plantpathogen interactions the
(2015) metabolic properties are relevant for the defense status not term race of arms has been coined to describe the ongoing co-
only for single cells but also for whole organisms. In many cases the evolution of defense and colonization strategies between the two
defense response is induced, but on behalf of the tness of the plant. partners (Anderson et al., 2010). This term could also be adjusted
for the growth promotion (for instance by nitrogen xation, see
Gresshoff et al., 2015) vs. defense responses. If the hormonal bal-
ance is on the plants side, then the plant will win the race, but
when the pathogen can turn the hormonal system to its own advan-
Abbreviations: IAA, indole-3-acetic acid; IAA-Asp, IAA-Aspartate; IAN, indole-3- tage, the pathogen is the winner. The pathways to be regulated
acetonitrile; IBA, indole-3-butyric acid; JA, jasmonic acid; NPA, napthylphthalamic by hormones include direct defense pathways, nutritional aspects,
acid; SA, salicylic acid.
but also cell wall maintenance (reviewed in Lpez et al., 2008).
This article is part of a Special Issue entitled: Plant Physiology meets Biodiversity.
Tel.: +49 351 463 33939; fax: +49 351 463 37032. Auxins play many different roles in plant growth and develop-
E-mail address: Jutta.Ludwig-Mueller@tu-dresden.de ment (Davies, 2010). On the cellular levels they are involved in the

0176-1617/$ see front matter 2014 Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.jplph.2014.01.002
 J. Ludwig-Mller / Journal of Plant Physiology 172 (2015) 412
regulation of cell division, cell expansion, cell differentiation and
polarity. On the whole plant levels they also contribute to organ
development, such as roots (lateral and adventitious), shoots (i.e.
apical dominance), leaves, as well as ower organs and fruits.
They are also involved in vascular patterning and orientation in
the environment (e.g. gravi- and phototropism). These examples
indicate their roles in all major developmental processes of a plant.
Auxins are also involved in the regulation of changes in different
growth processes associated with pathogens and symbionts. While
pathogens can alter the auxin response to induce specic disease
symptoms during disease development, benecial microorganisms
interfere with the auxin metabolism of the host plant to induce
plant growth for their own benet (for review see Ludwig-Mller,
2014).
Even though auxin has long been recognized as a regulator
of plant defense, the molecular mechanisms involved have been
only recently taken under investigation. Similar to the signaling
pathways of the defense-associated compounds salicylic acid (SA)
and jasmonic acid (JA), auxin signaling differentially affects resis-
tance to various pathogen groups (reviewed in Kazan and Manners,
2009). Recent evidence suggested that the auxin and SA path-
ways act antagonistically during plant defense reactions, whereas
auxin and jasmonate pathways have many similarities regarding
plant defense responses (Kazan and Manners, 2009). Auxin may
also affect disease outcomes indirectly through effects on plant
development (Gil et al., 2001). The evolutionary reasons behind
the antagonistic interactions between SA and auxin might be
that plants divert limited resources to defense-related processes
at the expense of plant growth when attacked by a pathogen
(Kazan and Manners, 2009). The growth of plants is dependent on
energy, mainly from photosynthesis and respiration. SA-mediated
induction of PR (pathogenesis related) proteins was dependent
on the presence of intact photoreceptors, linking light to defense
(Karpinski et al., 2003). A connection between SA and photosyn-
thesis is the protein isochorismate synthase, which is involved in
SA synthesis, but also in the synthesis of phylloquinone, which is
incorporated into photosystem I (Szechynska-Hebda and Karpinski,
2013). An excess excitation energy has similar effects on the expres-
sion of nuclear genes involved systemic acquired acclimation and
systemic acquired resistance, which are both tightly linked to pro-
grammed cell death (reviewed in Szechynska-Hebda and Karpinski,
2013). However, recently we have shown that auxin and SA sys-
temically co-increased during infection of Arabidopsis thaliana with
Cucumber mosaic virus (Likic et al., 2014), so that not in all cases
an antagonism of auxin and SA can be anticipated.
When talking about auxin the major compounds in plants,
indole-3-acetic acid (IAA) is usually meant, but there are some
indole and other derivatives with auxin activity (Epstein and
Ludwig-Mller, 1993; Ludwig-Mller, 2000; Ludwig-Mller and
Cohen, 2002). Also, only the free form of IAA and related com-
pounds is considered to be active, the majority of auxin in a given
tissue, however, is conjugated mainly to amino acids and sugars
and thereby inactivated (Ludwig-Mller, 2011). Since IAA can be
even growth inhibitory at high concentrations, the tight control of
auxin homeostasis is essential. Here, several processes are impor-
tant: (1) biosynthesis, (2) degradation, (3) reversible conjugation,
and (4) transport, the latter includes long distance and cell-to-cell
movement of auxin, leading to local auxin maxima or auxin gra-
dients (e.g. Smith, 2008). These four main possibilities to control
auxin concentrations in a given tissue are connected to transcrip-
tional activation of auxin-inducible genes, which can be growth or
defense related (Fig. 1). In the case of expansins the proteins can
act in developmental responses, for example cell expansion, or in
changing the penetration environment (cell wall) for pathogens.
In addition to developmental processes, IAA has come into focus
to play a role in plant defense processes against pathogens, mainly
5
bacteria and fungi. In some cases the pathogens use the auxin
machinery to induce disease symptoms (Fig. 1), such as crown gall
disease (Gelwin, 1990) or clubroots (Ludwig-Mller et al., 2009b).
In other instances, they highjack the auxin signaling or conjugation
pathways in their own favor to manipulate plant defense responses
(Figs. 2 and 3). Finally, there are some examples where auxins could
be directly inhibitory and thus involved in the defense response of
the plant (Fig. 3). These examples show that the benet for a plant
can be turned against it by pathogens, but vice versa the pathogens
can be fought off as well (Table 1). Some examples indicative of the
above dilemma will be discussed for plantpathogens from diverse
evolutionary groups to demonstrate the use of similar strategies
among different organisms, but also how variable such strategies
can turn out.
On the other hand there are plant growth promoting soil
microbes either producing IAA (Patten and Glick, 2002), or medi-
ating the IAA levels in the plants (Fig. 1). The growth promoting
basidiomycete Piriformospora indica has been shown to produce
auxin in culture (Sirrenberg et al., 2007; Vadassery et al., 2008),
but the contribution of IAA to the growth promotion phenotype
of colonized plants is still a matter of debate. Only recent work
has reported that P. indica uses the auxin biosynthesis pathway
via tryptamine as an intermediate (Hilbert et al., 2012). It was also
shown that a gene encoding one protein from the pathway was
expressed during the biotrophic phase of the interaction. However,
attenuation of IAA synthesis in a transgenic fungus did not have an
effect on growth promotion (Hilbert et al., 2012), conrming earlier
results (Vadassery et al., 2008). Addition of low IAA concentra-
tions led to suppression of an oxidative burst in barley, suggesting
that the IAA produced by the fungus could interfere/suppress host
plant defense (Hilbert et al., 2012, 2013). For arbuscular mycor-
rhiza it has been shown that two auxin might play a role, IAA and
indole-3-butyric acid (IBA) (Ludwig-Mller et al., 1997; Kaldorf and
Ludwig-Mller, 2000). Auxin could be involved in the mediation of
the root phenotype seen in some species, i.e. more lateral roots in
mycorrhized plants of maize (Kaldorf and Ludwig-Mller, 2000).
In the rhizobiumlegume interaction also some indications have
been published that IAA is needed for the initiation of the root
nodules as organs, especially the intact auxin transport machinery
(Wasson et al., 2006). Also, Campanella et al. (2008) have shown
that some members of an auxin conjugate hydrolase family from
Medicago truncatula were transcriptionally upregulated both dur-
ing arbusuclar mycorrhiza formation and nodulation, which could
lead to higher free IAA levels. While these are examples for the
benecial role of auxin in plantmicrobe interactions, in the fol-
lowing different strategies of plantpathogens will be specically
discussed.
Auxin biosynthesis
Auxin biosynthesis can contribute to the symptoms of certain
plant diseases, but is also essential for the normal development of
the plant and its orientation in the environment. Either a pathogen
highjacks the biosynthetic system of the host plant, or it can pro-
duce the auxin itself. One prominent example for the latter is
the tumor formation induced by the soil bacterium Agrobacterium
tumefaciens, where genes for auxin and cytokinin biosynthesis are
stably transformed into the plant tissue (Zupan and Zambryski,
1995). Other bacteria, which do not transform their host, are also
capable to synthesize IAA via various routes (for review see Spaepen
et al., 2007).
Another example is the clubroot disease of Brassicaceae,
caused by the obligate biotrophic protist Plasmodiophora brassi-
cae (Ludwig-Mller et al., 2009b), where the increased levels of
IAA are produced by the plant. Of importance is the conversion
6 J. Ludwig-Mller / Journal of Plant Physiology 172 (2015) 412

Fig. 1. Scheme how auxin signaling and homeostasis interacts with plant pathogens. The concentration of auxin is controlled by biosynthesis, transport, degradation and
reversible conjugation. IAA is perceived by receptors, one class may presumably directly activate target genes (or proteins). The second pathway is controlled by transcriptional
repressors, which need to be inactivated (see Fig. 2). After inactivation this leads to target gene activation. Benecial microbes can also contribute to auxin levels. These
pathways lead to a balance between growth and defense.

via the indole-3-acetonitrile (IAN) pathway (Ludwig-Mller et al.,
2009b). Alterations in this auxin biosynthesis pathways conse-
quently results in fewer symptoms, but also the growth of the
aboveground plant parts is hampered as shown for the infec-
tion of nitrilase mutants of A. thaliana infected with P. brassicae
(Grsic-Rausch et al., 2000; Neuhaus et al., 2000). In the Ustilago
maydis-mediated formation of corn smut the involvement of auxin
has been postulated, but so far not unequivocally proven (Basse
et al., 1996; Guevara-Lara et al., 2000; Reineke et al., 2008). Other
diseases where auxin might be involved in the symptoms are
caused by Taphrina species, who cause hypertrophied plum fruit
or the leaf deformation on peach trees (Bassi et al., 1984; Yamada
et al., 1990). Even though the plant has a machinery to regulate the
levels of auxin within a given tissue (Ludwig-Mller, 2011), in the
cases mentioned here the plants control mechanisms seem to fall
short (see below).
Although the role of auxin in biotrophic interactions has been
well studied throughout the past, less is known about its role
in the resistance response to necrotrophs. There are reports that
hemibiotrophic or necrotrophic fungi also produce IAA. The rice

Fig. 2. The role of auxin signaling via the nuclear TIR receptor family in plant development and plant pathogen interaction. High auxin levels lead via perception at the
F-box protein TIR1 (and homologs) to the ubiquitination of a transcriptional repressor Aux/IAA. This repressor is degraded in the 26S proteasome, leading to transcriptional
activation by ARFs as positive transcriptional regulators. Bold arrows show where auxin signaling and transcriptional activation could be altered by pathogens.
 J. Ludwig-Mller / Journal of Plant Physiology 172 (2015) 412 7

Fig. 3. Different examples for the role of auxin conjugation by the GH3 family of IAA conjugate amino acid synthetases (see also Table 1). In the Magnaportherice interaction
upregulation of GH3 transcripts result in lower free IAA and higher resistance, because expansins are downregulated. The fungus itself induced auxin thereby decreasing via
expansins the cell wall rigidity, which leads to better entry points for the fungus. In the BotrytisArabidopsis interaction (this has also been observed for the phytopathogenic
bacterium Pseudomonas) the conjugation of IAA to aspartic acid by GH3.2 leads to the activation of pathogenicity genes in the fungus and thus to higher susceptibility,
whereas downregulation of GH3.2 gene expression leads to higher resistance. In the PlasmodiophoraArabidopsis interaction the downregulation of GH3 transcription leads
to higher auxin levels and thus to larger galls, increasing the susceptibility of the plant. Here, also the upper parts of the plant are compromised. In the PythiumPhyscomitrella
interaction knockout of both GH3 genes results in higher IAA levels and also in reduced growth. The mutants are more resistant to Pythium, maybe due to a growth inhibitory
effect of IAA on the oomycete.

blast fungus Magnaporthe oryzae produces IAA during its biotrophic
phase especially in the area of the infection hyphae (Tanaka et al.,
2011), but it is as yet not clear whether to manipulate the host
plant or also to its own benet. The activation of an auxin-
inducible promoter by the fungal IAA indicated that the host plant
responded transcriptionally to the secreted auxin. Similarly, in two
Colletotrichum species auxin biosynthesis was observed (Chung
et al., 2003; Maor et al., 2004). The role of auxin biosynthesis might
be to keep the host plant in a growing stage, where the fungus
is dependent on nutrients from the host, whereas later during
the necrotrophic stages the pathogens do not need a living plant
any more. Manipulating the plant by its own growth promoting

Table 1
Some examples of auxin effects in selected pathogenplant interactions and on the outcome of the disease on the plant side.

Pathogen Host plant Effect Auxin feature Outcome after alterations

Mutation Overexpression

Pseudomonas syringae Arabidopsis thaliana Infection Signaling

Fusarium oxysporum Arabidopsis thaliana Root infection Signaling More resistant

High IAA level induces High IAA More resistant
defense genes
Transport More susceptible

Plasmodiophora brassicae Arabidopsis thaliana Clubroot Signaling More susceptible

Conjugation More susceptible
Biosynthesis More resistant because No alteration
smaller galls by lower
IAA

Pythium debaryanum Physcomitrella patens Browning of plants Conjugation More resistant because
Pythium is sensitive to
IAA

Magnaporthe grisea Oryza sativa Better penetration via Conjugation More resistant
cell expansion because low IAA
cannot induce, e.g.
expansin genes

Botrytis Arabidopsis thaliana Induction of Conjugation More resistant because

pathogenicity genes by fewer pathogenicity
IAA-Asp genes induced by
IAA-Asp
Apple High IAA More resistant
8 J. Ludwig-Mller / Journal of Plant Physiology 172 (2015) 412
signaling molecules might therefore be a widespread strategy.
Also, auxin can induce many genes, so that the cellular program
can be kept in favor of the pathogenic fungus (see paragraph on
auxin homeostasis, where an example for the Magnaportherice
interaction is discussed). Arabidopsis mutants defective in differ-
ent aspects of the auxin pathway including biosynthesis, transport
or signaling mutants are generally more susceptible than wild-
type plants to the necrotrophic fungus Alternaria brassicicola (Qi
et al., 2012). After infection the plant produces more IAA and this
could lead to the induction of some defense-related genes of the
JA-pathway. The authors hypothesized that both signals interact
positively with each other to increase the defense response against
the necrotrophic pathogen (Qi et al., 2012).
Auxin biosynthesis is indirectly connected to the synthesis of
a variety of defense compounds, which contain an indole moiety
(Fig. 1; Bender and Celenza, 2008). An example is the model plant
A. thaliana, where major defense compounds such as camalexin and
indole glucosinolates are derived from similar precursors (Halkier
and Gershenzon, 2006; Glawischnig, 2007). If the defense pathways
draw metabolites from the auxin route, then a decrease in IAA can
be postulated, so that the plants remain smaller. It can be assumed
that the statement is true for both roots and shoots, depending on
the type of pathogen. Reversing this scenario, for example in the
mutant sur1, which is decient in indole glucosinolate biosynthesis,
the IAA levels are much higher resulting in the so-called superroot
phenotype (Mikkelsen et al., 2004).
Auxin signaling and transport
Auxin signaling is central to many plantpathogen interactions.
Therefore, modulation of the signaling pathway is a hallmark for
many pathogenic organisms (for detailed review see Fu and Wang,
2011). The role of auxin in plant susceptibility to microbes was
rst demonstrated in A. thaliana when miR393-mediated down-
regulation of auxin receptors (TIR1, AFB1-3) led to the suppression
of auxin signaling and to a higher resistance of the plant (Navarro
et al., 2006). Later, Navarro et al. (2008) found that effector pro-
teins from the phytopathogenic bacterium Pseudomonas syringae,
which promote the bacterial infection, target directly the miR393
pathway. A pathogen has different possibilities where it can inter-
act with the nuclear auxin signaling pathway, for example the
binding of IAA by the receptor itself, which would in turn affect
binding of the repressor family Aux/IAAs (see Fig. 2, red arrows),
the ubiquitination of a transcriptional repressor, and the degra-
dation of the repressor in the 26S proteasome. Also binding of
transcriptional repressors or activators (ARFs) to the promoter of
auxin-inducible genes could be affected (Fig. 2). It was shown that
miRNA-decient mutants of Arabidopsis partly restore the growth
of a P. syringae mutant defective in type III secretion. Interestingly,
the effect was visible also with non-phytopathogenic bacteria such
as Pseudomonas uorescens and Escherichia coli, indicating a more
general role for miRNAs in plant basal defense responses (Navarro
et al., 2008). A type III effector protein from P. syringae affects the
turnover of Aux/IAA proteins (Cui et al., 2013), which are transcrip-
tional repressors of the auxin response. The virulence of the bacteria
is correlated with faster turnover, which enables transcriptional
activation of auxin-response genes. Consequently, the dominant
Arabidopsis mutant axr2-1 (AXR2 encodes the Aux/IAA repressor
IAA7) with more stable IAA7 protein showed less virulence of P.
syringae on the host plant (Cui et al., 2013).
The P. syringae type III effector protein AvrRpt2 results in the
promotion of virulence on Arabidopsis plants without the respec-
tive receptor (RPS2). When the gene encoding the bacterial effector
protein was overexpressed in Arabidopsis receptor mutants rps2,
the phenotype was reminiscent of an auxin-related one (Chen et al.,
2007). This included longer primary roots and an increased num-
ber of lateral roots. Further, the plants showed an increased auxin
sensitivity along with higher levels of free IAA. In agreement with
these data the application of 1-napthalene acetic acid increased
the plants susceptibility to the pathogenic bacterium. Auxin lev-
els were also increased in plants infected with P. syringae having
intact AvrRpt2 (Chen et al., 2007). In this context another obser-
vation concerning the ability of a P. syringae strain (pv. syringae
B728a) to convert IAN to IAA is of interest (Howden et al., 2009). The
bacterium produces a nitrilase with homologies to other bacterial
but not plant nitrilases, which could contribute to IAA levels in the
plant, but also enables the bacterium to use IAN as nitrogen source.
Also, a putative enzyme for the metabolism of aldoximes to IAN was
also detected. Interestingly, P. syringae pv. tomato DC3000 cannot
convert IAN to IAA despite the presence of a homologous nitrilase
gene (Howden et al., 2009). Further evidence for the involvement
of auxin signaling in the resistance response against P. syringae
came from Mutka et al. (2013), who investigated elevated auxin
levels on the disease severity after bacterial infection. The applica-
tion of IAA increases disease symptoms and plants overexpressing
the YUCCA1 gene involved in IAA biosynthesis in Arabidopsis also
showed enhanced susceptibility against the phytopathogenic bac-
terium. In addition, the authors could show that this response is
independent of SA (Mutka et al., 2013).
In addition to altering auxin synthesis of the plant (see para-
graph on auxin synthesis) Agrobacteria are able to inuence auxin
biology in their host via a protein with unknown function (Lacroix
et al., 2013). The gene Atu6002 is highly expressed in A. tumefaciens
induced plant tumors. The respective protein is targeted to the host
cells plasma membrane. These Atu6002-expressing plants display
impaired response to auxin, whereas uptake and polar transport of
auxin were not inhibited in these plants, suggesting that Atu6002
interferes with auxin perception or signaling pathways.
Also the phytopathogenic phytoplasma organisms altering the
habitus of plants, such as witches broom, alter the auxin signaling
machinery (Hoshi et al., 2009). When the gene encoding a small pro-
teinaceous pathogenicity factor from the bacteria was transformed
into tobacco and Arabidopsis, the transgenic plants also showed
the typical disease symptoms, without any bacteria present. The
protein could be involved in the inhibition of the normal auxin-
signaling pathway, thereby altering plant developmental programs
(Hoshi et al., 2009).
Many soilborne pathogens infect the roots through auxin-rich
regions, such as root tips and lateral root initials. Since several
auxin mutants show defects in lateral root, root hair and vascular
tissue development, such developmental alterations in plant root
architecture or vascular tissue could restrict pathogen entry into
the roots and/or movement within the plant (Kazan and Manners,
2009). The root-infection fungus Fusarium oxysporum leads to
alterations in auxin homeostasis, i.e. it induces gene expression
for indole glucosinolate and auxin biosynthetic genes. However,
mutants in these respective pathways were not altered in disease
susceptibility (Kidd et al., 2011). In addition it was tested whether F.
oxysporum infection could be reduced by treatment of plants with
IAA, but such a treatment did not reduce disease severity. Further
experiments revealed that here, like for bacteria, the auxin signal
transduction and transport machinery was needed for efcient col-
onization of the host plant Arabidopsis by the fungus (Kidd et al.,
2011). Indeed, Arabidopsis auxin signaling mutants show increased
resistance to F. oxysporum. Furthermore, treatment with an auxin
transport inhibitor resulted in a reduction of disease development,
suggesting that auxin transport is also needed for the successful
establishment of the fungus in the plant (Kidd et al., 2011). How-
ever, it needs to be mentioned that auxin transport mutants show
growth defects, so even if lower auxin transport rates generate
more tolerant plants, under normal conditions the plant would
 J. Ludwig-Mller / Journal of Plant Physiology 172 (2015) 412
not be able to use this mechanism for the induction of a resistance
response.
The Arabidopsis auxin mutants axr1, axr2, and axr6 have defects
in the auxin-stimulated ubiquitination pathway, which leads to the
proteolytic degradation of transcriptional repressors (Aux/IAA pro-
teins). These plants with a compromised auxin signaling pathway
exhibit increased susceptibility to the necrotrophic fungi Plec-
tosphaerella cucumerina and Botrytis cinerea (Llorente et al., 2008).
Pharmacological inhibition of proteasome function compromised
the plants resistance to these necrotrophic fungi. In addition it
was shown that P. cucumerina can induce the stabilization of the
auxin transcriptional repressor protein AXR3, which is normally
targeted for degradation in the 26S proteasome. From these results
the authors concluded that nuclear auxin signaling is important
for resistance to the necrotrophic pathogens P. cucumerina and B.
cinerea (Llorente et al., 2008).
The clubroot pathogen P. brassicae confers disease symptoms
also partially using the TIR pathway. The Arabidopsis mutant axr3
showed more resistance to club formation, indicating a role for
nuclear signaling for gall development (Alix et al., 2007). Trans-
cripts for TIR1 and two receptor homologs were upregulated during
club formation (Jahn et al., 2013). Contrary to the above ndings
for Fusarium, this protist leads to more susceptible plants in auxin
receptor mutants. It was hypothesized that the TIR pathway also
controls the expression of auxin conjugate synthetase (GH3) genes,
which would then decrease auxin levels (see below). Therefore,
reduced GH3 protein levels would increase auxin and thus suscep-
tibility of the host plants. Next to the nuclear signaling pathway,
the clubroot pathogen transcriptionally activates also the plasma
membrane receptor ABP1 (Jahn et al., 2013). The receptor might
be involved in the regulation of cell expansion (Scherer, 2011), by
possibly activating target genes such as expansins (S. Marschollek
and J. Ludwig-Mller, unpublished results) or potassium channels
(Jahn et al., 2013). Evidence for a role of auxin transport in the club-
root disease was provided by Devos et al. (2006) who showed that
a mutant defective in the cross-talk between ethylene and auxins
(alh1), probably at the level of auxin transport was more tolerant
to clubroot. In this mutant it was postulated that IAA cannot reach
the site of infection, thereby reducing the size of the root galls. In
addition, treatment with the auxin transport inhibitor napthylph-
thalamic acid (NPA) early in infection is important for the reduction
of gall growth (Devos and Prinsen, 2006). A treatment with NPA
during later time points did not reduce clubroot symptoms, but
treatment with avonoids (which are discussed to be modulators
of auxin efux carriers; Peer and Murphy, 2007) resulted in the
retaining of auxin in plasmodia containing cells (Psold et al., 2010).
Auxin homeostasis
While the level of free (active) auxin is controlled by several
mechanisms (biosynthesis and transport also belong to them),
auxin homeostasis is mainly dened as the binding of free auxin
to small or large molecules as inactive auxin conjugates and the
reversible hydrolysis which yields again the active hormone. Auxin
conjugate synthetases of the GH3 family and auxin amino acid con-
jugate hydrolases (short auxin amidohydrolases) are the enzymes
involved in these processes (reviewed in Ludwig-Mller, 2011).
In addition to the conjugation of IAA to various amino acids, it
was shown that several members of the GH3 family can conju-
gate other plant hormones. For example, GH3.11 conjugates JA to
the amino acid isoleucine, thereby activating the signaling path-
way (Staswick and Tiryaki, 2004). The GH3.5 protein was shown to
have dual functions in the regulation of the IAA and the SA path-
way (Zhang et al., 2007). Finally, GH3.12 regulates the SA defense
pathway (Nobuta et al., 2007) not by direct conjugation of SA, but
by modulating the general benzoate pathway. It was demonstrated
9
that GH3.12 converts preferably 4-substituted benzoates such as 4-
aminobenzoate and 4-hydroxybenzoate to amino acid conjugates,
whereas the preference for benzoic acid itself was only moderate
(Okrent et al., 2009). Interestingly, the authors reported that the
conjugation of 4-substituted benzoates was inhibited strongly by
SA.
Because auxin promotes cell elongation, several auxin mutants
show defects in this process. Such defects could interfere with the
infection processes of pathogens that interact with the cell wall and
colonize the extracellular spaces (Kazan and Manners, 2009). Along
these lines a strategy is to keep the cell wall loose by increasing lev-
els of expansins (Figs. 1 and 3). These provide a better entry place
for the fungus. It is known that genes encoding expansins can be
induced by IAA (Cosgrove et al., 2002). Therefore, high auxin levels
would confer cell expansion, and cells with a less rigid cell wall are
better entry points for pathogens (see model in Fig. 3). Ding et al.
(2008) observed that the overexpression of rice GH3.8 (it should be
noted that for rice the numbering of enzymes is different than for
Arabidopsis) suppressed expansin expression and promoted basal
immunity responses in rice against the phytopathogenic bacterium
Xanthomonas oryzae without activating the JA- or SA-pathways for
defense. Similarly, in the Magnaportherice interaction a down-
regulation of expansins increased resistance against the fungus
(Fu et al., 2011). The observation that overexpression of a GH3.2
gene in rice could confer broad spectrum resistance by reducing
pathogen-induced auxin accumulation, has led to the hypothesis
that at low free IAA levels the cell walls are more rigid and there-
fore the fungi cannot easily penetrate (Fu et al., 2011). The area of
lesions induced by the fungi signicantly decreased in overexpres-
sors. Application of IAA to rice plants increased susceptibility to the
fungal pathogens, highlighting the importance of IAA for disease
establishment (Fu et al., 2011). Disease progression in the plants
inoculated with Magnaporthe grisea was correlated with high lev-
els of expansin gene expression, whereas in lines overexpressing
GH3.2 the expansins were not induced by the fungus (Fu et al.,
2011). Since cell wall structure functions in at least two completely
different pathosystems, a role for expansins at least in rice could be
demonstrated.
Most conjugates are hydrolyzed back to free IAA by ami-
dohydrolases. However, there is the exception of IAA-Aspartate
(IAA-Asp) and IAA-Glutamate, which are thought to be substrates
for irreversible degradation in plants (Ludwig-Mller, 2011). Plant
pathogens use in their intricate relationship with their host such
signals for their own benet. In an intriguing study it was shown
that IAA-Asp could induce plant disease development (Gonzlez-
Lamothe et al., 2012). First, the authors showed that IAA-Asp was
increased in Arabidopsis after infection with two phytopathogens,
the fungus B. cinerea and the bacterium P. syringae. Second, they
demonstrated that the addition of IAA-Asp enhanced disease sus-
ceptibility in Arabidopsis after infection with B. cinerea. Third, it
was conrmed that auxin conjugation is indeed the important fac-
tor, because overexpression of a member of the GH3 family, GH3.2,
resulted in more susceptible Arabidopsis plants, whereas the gh3.2
mutant was less susceptible (see model in Fig. 3). It should be
noted that the effect was specically conferred only by this mem-
ber of the large GH3 family. Finally, it could be shown for both
phytopathogens that a set of known pathogenicity genes was trans-
criptionally reduced in gh3.2 mutants and gene expression could be
restored by addition of IAA-Asp. This demonstrates the role of one
specic auxin conjugate that has evolved as inductor for disease
development. The gene expression machinery of the pathogens had
to be adapted to this molecule.
Our recent work (Jahn et al., 2013) demonstrated that double
mutants in the auxin conjugation pathway were more susceptible
to P. brassicae than wild type. Various GH3 genes exhibit strong
upregulation in infected roots, especially in cells harboring large
10 J. Ludwig-Mller / Journal of Plant Physiology 172 (2015) 412
mature plasmodia, as shown by laser microdissection coupled to
transcriptional proling (Schuller et al., 2014), so that the strategy
might be here to counteract the high auxin levels in the cells which
are growth inhibitory. Increasing the IAA levels could lead to larger
galls, but also to growth inhibition of the upper plant parts, which
can further weaken the host plant (see model in Fig. 3). In addition,
since a mutant in gh3.5 was used, an additional effect could come
from disturbing SA signaling.
While the GH3 family is rather large in Arabidopsis with 20
members, the moss Physcomitrella patens has only two GH3 pro-
teins, which have been previously characterized (Ludwig-Mller
et al., 2009a). In contrast to the Arabidopsis proteins, the P. patens
enzymes are able to convert IAA (and IBA) and JA to the respec-
tive amino acids. Double knockout mutants have no amino acid
conjugates with IAA, but possess ester conjugates. In addition, espe-
cially when the moss is grown on high IAA levels, the plants have
more free IAA and they grow more slowly than wild type plants
(Ludwig-Mller et al., 2009a). It was shown that P. patens can be
inoculated by various phytopathogens (Ponce de Len, 2011). We
used the oomycete Pythium debaryanum and found that the GH3
mutant lines were more tolerant to the pathogen (J. Mittag and J.
Ludwig-Mller, unpublished results). P. debaryanum was inhibited
in growth on medium supplemented with IAA (J. Mittag and J.
Ludwig-Mller, unpublished results), so that the higher IAA levels
in the GH3 mutant plants led to growth inhibition of the oomycete
(see model in Fig. 3). Since high auxin levels are growth inhibitory,
the moss plants do not sacrice better growth for higher resistance
against pathogens.
For Fusarium culmorum infection of barley a reduction of symp-
toms and yield losses were found after treatment of infected plants
with IAA, even though growth of the fungus was not inhibited by
IAA in vitro (Petti et al., 2012). The results indicated increases in the
gene regulation for defense-associated genes. Also, IAA has a pro-
tective effect against apple scab caused by the necrotrophic fungus
Botrytis cineria when applied before inoculation, but not when adi-
ministered post-pathogen (Yu et al., 2008). Whether this is a direct
growth inhibitory effect of IAA on Botrytis, or whether IAA is medi-
ating its effect by one or the other mechanisms discussed above
cannot be concluded.
Conclusion
In this review some aspects on the dual roles of the plant
hormone auxin in plant defense mechanisms and in plant develop-
mental processes have been discussed. Under non-stress conditions
the concentration of IAA needs to be tightly controlled to ensure
that growth is not limited by either too low or too high auxin lev-
els. This can be achieved by various processes, such as biosynthesis,
degradation, transport or reversible inactivation (Fig. 1). Also, con-
trol of auxin-induced gene expression is important for the outcome
of a given developmental program (Fig. 2). In the interaction with
pathogens the scenario can change in favor of the plant defense
responses or in favor of symptom development, which is depend-
ent on auxin. In both cases the balance of IAA can be disturbed.
The plant is able to control auxin levels to a certain extent, but
microbes can exploit these systems for their needs. That can result
in various scenarios (Fig. 3): (1) benecial microbes increase the
balance of auxin, so that the host plant is stimulated in growth,
probably for their own benet, but without harming the host too
much; (2) the auxin concentration is adjusted so that the microbes
can colonize the plant and exploit the auxin machinery for their
own pathogenic benet, e.g. by using auxin as a signal to regulate
their own pathogenicity genes; (3) auxin is used to increase gene
expression needed in the defense reaction, so downregulation of
auxin signaling is increasing susceptibility; (4) auxin can generate
better opportunities for the pathogen to penetrate, i.e. by higher
rate of expansin production, so that the cell wall is more readily
penetrable, opposing this auxin level results in resistance of the
host plant; (5) auxin itself is toxic to the colonizing microbes, so that
in this scenario high auxin levels are desirable for the plant. How-
ever, these high auxin concentrations in a given plant tissue can also
result in growth inhibition, so that the coordinated development of
the plant is probably not sacriced for better defense mechanism
against pathogens. Within these possibilities many variations exist,
that can be exploited by the pathogens, but also by plants to control
their enemies.
How do the results and thoughts presented in this
review t into the title of the workshop Biodiversity meets
physiologyPhysiology meets Biodiversity? Physiology and
molecular biology are used to investigate specic examples in
the laboratory. Additional experiments have to be carried out in
the eld. The complexity of the interactions between plants and
pathogens as outlined above clearly indicates their biodiversity.
Evolutionary aspects play major roles for these interactions,
because both partners always need to develop novel strategies
to cope with each other. Some examples have been described
where the role of auxin might shift toward either host or pathogen,
controlling processes of development or defense, respectively. It is
dependent on the adaptation of a plant species to its environment
whether such alterations can be tolerated or even be further
exploited toward (novel) defense mechanisms against a given
pathogen species. The observation that mycorrhiza infection
stimulates lateral root formation via auxin production (Herrbach
et al., 2014) clearly shows that a better functional understanding
of auxin metabolims is crucial for explaining mycorrhiza driven
biodiversity changes (Buscot, 2015).
Acknowledgements
Work in the authors laboratory was supported by the European
Union, the State of Saxony, and the Deutsche Forschungsgemein-
schaft. This paper is a joint effort of the corresponding authors and
an outcome of a workshop kindly supported by sDiv, the Synthesis
Centre of the German Centre for Integrative Biodiversity Research
(iDiv) Halle-Jena-Leipzig (DFG FZT 118).
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