Review - The Molecular Biology of Meiosis in Plants.

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Annu. Rev. Plant Biol. 2015. 66:297–327 Keywords

First published online as a Review in Advance on recombination, crossovers, cell cycle, sister chromatid cohesion, polyploids
December 1, 2014
The Annual Review of Plant Biology is online at Abstract

plant.annualreviews.org
Meiosis is the cell division that reshuffles genetic information between gen-
This article’s doi: erations. Recently, much progress has been made in understanding this pro-
10.1146/annurev-arplant-050213-035923
cess; in particular, the identification and functional analysis of more than
Copyright c 2015 by Annual Reviews. 80 plant genes involved in meiosis have dramatically deepened our knowl-
All rights reserved
edge of this peculiar cell division. In this review, we provide an overview of
advancements in the understanding of all aspects of plant meiosis, includ-
ing recombination, chromosome synapsis, cell cycle control, chromosome
distribution, and the challenge of polyploidy.
297
Contents
1. INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 298
2. MEIOTIC RECOMBINATION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 300
2.1. The Nature and Distribution of Recombination Events . . . . . . . . . . . . . . . . . . . . . . 300
2.2. Molecular Events: The Current Model and the Genes Involved . . . . . . . . . . . . . . . 309
3. THE SYNAPTONEMAL COMPLEX . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 312
4. CHROMOSOME DISTRIBUTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 313
5. MEIOSIS PROGRESSION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 314
5.1. Entry into Meiosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 314
5.2. Cell Cycle Control: Two Divisions Following a Single Replication . . . . . . . . . . . . 314
6. MEIOSIS IN POLYPLOIDS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315
7. APPLICATIONS IN PLANT BREEDING . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 317

8. FUTURE PROSPECTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 317
Bivalent:
a pair of homologous 1. INTRODUCTION
chromosomes Most eukaryotes reproduce sexually, although the reasons for the persistence of this mode of re-
physically connected
production are still poorly understood (96). This process involves an alternation between halving
(usually by COs)
the number of chromosome sets during meiosis and restoring the original ploidy level during
Crossover (CO):
fertilization. Meiosis is thus a key step in the sexual life cycle. It consists of two rounds of chromo-
a reciprocal exchange
between two DNA some segregation that follow a single round of DNA replication (Figure 1): a first round (which is
molecules; also called a very specific to meiosis) in which the pairs of homologous chromosomes segregate, and a second
crossing-over round in which the sister chromatids are separated.
Chiasma: These two chromosome segregations rely on a series of innovations compared with mitosis.
the cytological First, the efficiency of the first division depends on the formation of a structure called a bivalent,
manifestation of a CO which is composed of a pair of homologous chromosomes, each made of two replicated sister
Sister chromatid chromatids and physically linked to the other. In most species, this physical link depends on the
cohesion: protein formation of at least one reciprocal exchange between two homologous nonsister chromatids
complexes set up at S
called a crossover (CO) or chiasma (Figure 1). The presence of at least one CO per bivalent is an
phase that associate
two sister chromatids absolute requirement for properly segregating homologous chromosomes and thus for obtaining
with each other fully viable gametes in most species. Second, specific controls of sister chromatid cohesion release
and kinetochore orientation must be implemented to ensure that at each step of meiotic division
−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 1
Overview of meiosis. (A) Premeiosis encompasses meiocyte differentiation and meiotic S phase. (B) At leptotene, chromosome axes
form and recombination is initiated. (C) At zygotene, synapsis takes place through the polymerization of the synaptonemal complex and
recombination progresses. (D) At pachytene, synapsis is complete and recombination further progresses. (E) At diplotene, the
synaptonemal complex disassembles. Homologous chromosomes are connected by crossovers. (F) At diakinesis, chromosome
condensation occurs and bivalents can be distinguished. (G) Prophase I finishes and the nuclear envelope breaks down. (H) At metaphase
I, the spindle aligns bivalents on the metaphase plate. (I) At anaphase I, the release of arm sister chromatid cohesion allows the migration
of chromosomes at two poles. Pericentromeric cohesion is specifically protected. (J ) At interkinesis, two nuclei form and chromosomes
briefly decondensate. This stage encompasses telophase I and prophase II. In monocotyledons, cytokinesis occurs before meiosis II
starts; in dicotyledons, cytokinesis happens only at telophase II. (K) At metaphase II, two spindles form that align chromosomes on two
metaphase plates. (L) At anaphase II, sister chromatids separate following centromeric cohesion release. (M) At telophase II, four nuclei
form. (N) At cytokinesis, haploid spores are released. The proteins presumed to act at each stage are listed in Table 1.
298 Mercier et al.

F G H
Metaphase I
I
Anaphase I
Diakinesis
Meiocyte
E A
S phase
Diplotene Prophase I
Interkinesis
(includes telophase I J
and prophase II)
B
D Pachytene
Leptotene
Zygotene
C
Spores
K
Metaphase II
L
Anaphase II
Telophase II
N M
www.annualreviews.org • Molecular Biology of Meiosis in Plants 299

(meiosis I and meiosis II), the chromosome distribution is balanced. Finally, the mitotic rules of
the cell cycle that ensure a strict alternation between replication and division must be bent to
prevent an intervening replication between the two meiotic divisions.
Double-strand break
(DSB): two DNA Meiosis arose early during the evolution of eukaryotes (150). Recent genetic, molecular, and
breaks, one on each molecular phylogenetic analyses have shown that the core mechanisms are widely conserved
strand of a DNA among animals, fungi, and plants but also that significant differences exist between species (69, 150,
molecule, formed 176). During the early twentieth century, plants were at the forefront of meiotic studies for several
closed to each other
reasons. First, their large genomes (and therefore large chromosomes) made them particularly
(zero to a few
nucleotides apart) interesting for the emerging field of cytogenetics (41). Second, because plant meiosis studies deal
with crop fertility and genetic variation, they have tremendous potential for agronomical applica-
Noncrossover
(NCO): local and tions. In addition to faithful chromosome transmission, meiotic recombination (CO) is responsible
nonreciprocal for allelic shuffling over generations and thus produces genetic diversity on which selection can
replacement of one act. Finally, plants are particularly suitable for genetic analyses, and the 1980s saw the develop-
DNA sequence with a

ment of meiotic mutant collections in many plant species, including corn, tomato, and rye (107).
homologous one
Nevertheless, it was not until the emergence of Arabidopsis thaliana as a model species in the late
1990s that scientists were able to combine cytogenetic, molecular, and genetic approaches. More
recently, other plant species, such as rice, maize, rapeseed, barley, and wheat, joined Arabidopsis
in the field and allowed considerable advancement in our understanding of meiotic processes.
Table 1 lists the large number of plant proteins currently known to play a role in meiosis.
2. MEIOTIC RECOMBINATION
2.1. The Nature and Distribution of Recombination Events

Meiotic recombination is initiated by the formation of programmed DNA double-strand breaks
(DSBs) (see below). The repair of these DSBs on the nonsister homologous chromatids produces
either COs (see above) or noncrossovers (NCOs) (Figure 2). Unlike COs, which are reciprocal
exchanges of large DNA fragments between homologous chromatids, NCOs copy a small patch of
the intact homologous chromosome to the broken chromosome, without affecting the template.
Thus, a CO modifies two chromatids, whereas an NCO modifies only one.
Remarkably, in almost all species, the distribution of these recombination events is not ho-
mogeneous along chromosomes, at any scale. At the finest scale, COs and NCOs cluster in small
regions of a few kilobases called hot spots, whose localization reflects the position of the meiotic
DSBs (35, 39, 61, 131, 140). Parts of the mechanisms that govern DSB localization have been
recently deciphered in Saccharomyces cerevisiae, mice, and humans, revealing both conserved and
specific molecular strategies (reviewed in 18, 52). A common feature in these three species is that
DSBs occur in chromatin regions that contain histone H3 trimethylated on lysine 4 (H3K4me3).
In mice and humans, this mark is deposited at hot spots by PRDM9, a SET domain protein
with a zinc-finger array that recognizes a DNA-specific sequence; how this chromatin mark is
recognized by the DSB-forming machinery remains to be understood. In S. cerevisiae, the SET1
complex deposits an H3K4me3 mark at future meiotic DSB sites, and the Set1-protein complex
Spp1 makes the connection between this mark and the DSB-forming complexes (164). In spite of
this common feature, however, in S. cerevisiae DSBs preferentially occur in promoters of actively
transcribed genes, whereas in mice they seem to be moved away from the transcription start sites
by PRDM9 (reviewed in 52).
In plants, the PRDM9 subfamily has been lost (198). However, recent works have pointed
out links between chromatin and/or DNA features and DSB localization. In maize, there is a
correlation between DNA methylation, Mu transposon insertion sites, and CO-rich regions (119).
300 Mercier et al.

PP66CH12-Grelon
Supplemental Material
Table 1 Plant proteins that have been shown to play a role in meiosis
ARI
Link to Figures Supplemental

Protein Species Putative homologs Meiotic function 1 and 2a reference(s)b
Entry into meiosis
MIL1 Rice CC-type glutaredoxin Male meiocyte differentiation A 77
24 March 2015
MEL2 Rice DAZ-associated protein 1 Meiotic G1 –S transition A 110

MEL1 Rice Argonaute (AGO5) Prophase I progression A 111
A. thaliana Prevention of female meiocyte differentiation A 54
13:49
AGO9/AGO104 Argonaute (AGO9) Somatic fate in germ cells, meiotic

Maize A 137
chromosome condensation
A. thaliana Setup of meiotic chromosome structure A 2, 103, 105, 107, 135
SWI1/DYAD/AM1 Rice Leptotene–zygotene transition B 24
Maize Meiotic entry A 177
MEI1 A. thaliana TopBP1/DPB11 Meiotic S-phase DNA repair A 65
CDC45 A. thaliana Cdc45 Meiotic and mitotic S-phase DNA repair A 139
XRI1 A. thaliana Meiotic S-phase DNA repair A 49
Recombination: DSB formation
A. thaliana 66
SPO11-1 Spo11/Rec12 DSB formation (catalytic subunit) B, a
Rice 161
SPO11-2 A. thaliana Spo11/Rec12 DSB formation (catalytic subunit) B, a 72, 138
PRD1 A. thaliana MEI1 DSB formation B, a 47
PRD2 A. thaliana Mei4/Rec24/MEI4 DSB formation B, a 46
PAIR1/PRD3 A. thaliana 46
DSB formation B, a
Rice 109
DFO A. thaliana DSB formation B, a 169
Maize Likely DSB formation B, a 116
PHS1 Rec114/Rec7/REC114
A. thaliana To be clarified 124
www.annualreviews.org • Molecular Biology of Meiosis in Plants

Rice DSB formation, CE component B–D, a 106
CRC1/PCH2 Pch2 C. Franklin, personal
301
A. thaliana Regulation of synapsis and CO formation C, D
communication
(Continued )
Table 1 (Continued )
Putative Link to Figures Supplemental
PP66CH12-Grelon
Protein Species homologs Meiotic function 1 and 2a reference(s)b

Recombination: early DSB repair
ARI
A. thaliana 18, 119, 127

MRE11 Mre11 SPO11-induced DSB repair B, b
Rice 81
302
RAD50 A. thaliana Rad50 SPO11-induced DSB repair B, b 12, 59
NBS1 A. thaliana Xrs2/Nbs1 Dispensable for DSB repair, except in an atm mutant B, b 154
A. thaliana 144
COM1/AtGR1 Com1/Sae2 SPO11-induced DSB repair B, b
24 March 2015
Rice 82
Mercier et al.
A. thaliana CO formation and DSB repair redundantly with RPA1C 114
RPA1A Rpa1 B, c, d
13:49
Rice DSB repair 23

A. thaliana DSB repair redundantly with RPA1A 3
RPA1C Rpa1 B, c, d
Rice CO formation 94
RPA2C Rice Rpa2 CO formation 94
RAD51A1, RAD51A2 Maize 58, 91
Rad51 SPO11-induced DSB repair C, c, d
RAD51 A. thaliana 43, 92, 118
P. patens Meiotic DSB repair 23a

RAD51B RAD51B C, c, d
A. thaliana Possible anti-CO activity 11, 44
A. thaliana 1, 11, 93, 113
RAD51C RAD51C SPO11-induced DSB repair (c, d) C, c, d
Rice 87, 141
A. thaliana None 11
RAD51D RAD51D
Rice DSB repair C, c, d 19
BRCA2(IV), BRCA2(V) A. thaliana BRCA2 SPO11-induced DSB repair C, c, d 134
XRCC3 A. thaliana XRCC3 SPO11-induced DSB repair C, c, d 13, 14
ATM A. thaliana ATM/Tel1 SPO11-induced DSB repair B, C, c, d 38, 60
ATR A. thaliana ATR/Mec1 SPO11-induced DSB repair redundantly with ATM B, C, c, d 38, 89
MCM8 A. thaliana MCM8 SPO11-induced DSB repair in parallel with DMC1 C, c 35
Recombination: IH bias
A. thaliana 33
DMC1 Dmc1 IH bias C, d
Rice 50
AHP2/HOP2 A. thaliana Hop2 SPO11-induced DSB repair and IH bias C, d 129, 140, 143
MND1 A. thaliana Mnd1 SPO11-induced DSB repair C, d 53, 85, 115, 145
A. thaliana 6, 46
SDS Cyclin D IH bias C, d
Rice 22
R. Mercier,
PP66CH12-Grelon
FIGL1 A. thaliana FIDGETIN L1 Anti-CO activity C, c, d

unpublished data
XRCC2 A. thaliana XRCC2 Anti-CO activity C, c, d 44
ARI
Recombination: CO and NCO outcome

BLAP75/RMI1 A. thaliana BLAP75/RMI1 Late recombination intermediate repair C, D, h, i 16, 27, 70
Replication factor C
RFC1 A. thaliana SPO11-induced DSB repair C, D 97
complex subunit
24 March 2015
70; R. Mercier,
Top3α A. thaliana Top3 α Late recombination intermediate repair, anti-CO activity C, D, g, h, i
unpublished data
RECQ4A, 71; R. Mercier,
Sgs1/BLM Redundant anti-CO activity C, D, g, i
13:49
A. thaliana
RECQ4B unpublished data
FANCM A. thaliana FANCM/Mph1/Fml1 Anti-CO activity C, D, g, i 34, 86
MHF1 A. thaliana MHF1 Anti-CO activity C, D, g, i 45, 61

MHF2 A. thaliana MHF2 Anti-CO activity C, D, g, i 61
MSH2 A. thaliana Msh2 Anti-CO activity (hybrid context) C, D 55
MUS81 A. thaliana Mus81 Class II CO pathway (j) C, D, j 6, 69, 74
RBR A. thaliana Rb-related gene Meiotic gene transcription, class I and class II CO pathways C, D 31
CDKG1 A. thaliana CDK Promotion of synapsis and CO formation C, D 173
ARP6 A. thaliana ARP6, SWR1 subunit Promotion of CO formation B–D 32, 120, 125
MSH4 A. thaliana Msh4 Class I CO pathway C, D, e 73
A. thaliana 76
MSH5 Msh5 Class I CO pathway C, D, e
Rice 100
A. thaliana 26, 88
ZIP4 Zip4/Spo22 Class I CO pathway C, D, e
Rice 133
A. thaliana 30, 104
MER3/RCK Mer3 Class I CO pathway C, D, e
Rice 22, 146
PTD A. thaliana Class I CO pathway C, D, e 99, 102, 155
SHOC1/ZIP2 A. thaliana Zip2 Class I CO pathway C, D, e 101, 102

A. thaliana 28
HEI10 HEI10 Class I CO pathway C–F, e
Rice 147
303
MLH1 A. thaliana Mlh1 Class I CO pathway D–F, f 28, 51
A. thaliana 79
MLH3 Mlh3 Class I CO pathway D–F, f
I. Colas, personal
Barley
communication
(Continued )
Table 1 (Continued )
Link to Figures Supplemental
PP66CH12-Grelon
Protein Species Putative homologs Meiotic function 1 and 2a reference(s)b

Recombination: control of CO distribution
ARI
AXR1 A. thaliana E1 RUB ligase Regulation of CO distribution C, D 80

A. thaliana Regulation of synapsis and CO distribution C, D 54a
304
PSS1 Kinesin 1
Rice Spindle defects (possibly caused by CO defect) 174
Heterochromatin in a
Ph1 Wheat Homeologous recombination inhibition A–C 4, 67
Cdc2 cluster
24 March 2015
Axis-SC
Mercier et al.
A. thaliana 5, 21, 126, 128
ASY1/PAIR2 Hop1 AE-associated protein, IH bias B–D, c, d
Rice 108, 112
13:49
Rice 148, 165

PAIR3/ASY3 Red1 AE-associated protein, IH bias (c, d) B–D, c, d
A. thaliana 57
A. thaliana CE component, limiting of ectopic COs 75
ZYP1/ZEP1 Barley Zip1/Scyp1 CE component, promoting of CO formation C, D 8
Rice CE component, limiting of CO formation 151
Sister chromatid cohesion
SYN1/DIF1/REC8 A. thaliana 7, 10, 20, 25

SCC, monopolar orientation of the kinetochore,
Rec8 DSB repair A–K, c, d
RAD21-4/REC8 Rice 132, 170
AFD Maize 63, 162
SYN3/RAD21.2 A. thaliana Involved in meiosis 83, 130, 163, 164
Rad21/Scc1
RAD21.3 Rice Not investigated 142
SCC, monopolar orientation of the kinetochore,
SCC3 A. thaliana Scc3 A–K, c, d 25, 130
DNA repair
SCC2/EMB2773 A. thaliana Scc2/Mis4 SCC establishment, axis formation, DNA repair A 131
CTF7/ECO1 A. thaliana Eco1 SCC establishment, DNA repair A 15, 84, 136
Maize 68
SGO1
Rice Sgo Centromeric cohesion protection at anaphase I H, I 150
SGO1 SGO2 A. thaliana 37, 166, 167
PANS1 A. thaliana Centromeric cohesion protection at interkinesis J 37, 167
AESP A. thaliana Separase Esp1 SCC release, microtubule organization I, L 98, 158
Mis12-1, Mis12-2 Maize Mis12 Sister kinetochore association at meiosis I H 95
Protection of centromeric cohesion, kinetochore
BRK1 Rice BUB1 H, I 149
attachment
PP66CH12-Grelon
ARI
Cell cycle control: spindle–cytokinesis

CDK1, spCDC2, 52; M. Grelon,
CDKA;1 A. thaliana IH bias and cell cycle meiotic transitions C, J, d
scCDC28 unpublished data
TAM/CYCA1;2
24 March 2015
A. thaliana Cyclin A Cell cycle meiotic transitions G, J, M 36, 39, 152
MS5/TDM A. thaliana Cell cycle meiotic transitions J, M 17, 36, 62, 126
13:49
OSD1/UVI4L/GIG1 A. thaliana Cell cycle meiotic transitions via APC/C regulation G, J 36, 39, 41, 78
SMG7 A. thaliana SMG7 Anaphase II progression L 17, 123

JASON A. thaliana Meiosis II spindle orientation K 48, 56
PS1 A. thaliana Meiosis II spindle orientation K 40
ATK1/KATA/KIN14a A. thaliana Kinesin 14 Male meiotic spindle morphogenesis H, K 29
MMD/DUET A. thaliana PHD-finger protein Chromatin structure and male meiotic progression A–M 121, 159
MPK4 A. thaliana MPK Male meiotic cytokinesis N 168
TES/NACK2/STD A. thaliana Kinesin 7 Male meiotic cytokinesis N 122, 156
ASK1 A. thaliana Skp1 Ubiquitination pathway, chromatin structure A–M 153, 157, 160, 172
Abbreviations: A. thaliana, Arabidopsis thaliana; AE, axial element; APC/C, anaphase-promoting complex/cyclosome; CE, central element; CO, crossover; DSB, double-strand break; IH,
inter-homologous; NCO, noncrossover; P. patens, Physcomitrella patens; SC, synaptonemal complex; SCC, sister chromatid cohesion.
a
Uppercase letters refer to the presumed stage of action as defined in Figure 1; lowercase letters refer, when applicable, to the presumed function in the recombination process as defined in
Figure 2. Blank cells indicate that no data are available.
b
All citations in this table refer to the separate Supplemental References available online; follow the Supplemental Material link from the Annual Reviews home page at http://www.
annualreviews.org.

305
a DSB formation
c
b Resection Inter-sister invasion
d Inter-homologous Inter-sister events

invasion
250
e ZMM pathway
g
100 Joint molecules SDSA
Cytologically associated
h
with ZMMs
dHJ dissolution
i
Other
dHJ mechanisms?
f Resolution j Resolution
10 1.5 NCOs
Class I COs Class II COs
Figure 2
Model of meiotic recombination mechanisms. Meiotic recombination is initiated by the formation of a large number of double-strand
breaks (DSBs) (a) that are processed (b) to yield 3 -OH single-stranded DNA. This DNA can then invade either the intact sister
chromatid (c) or one of the two homologous chromatids, forming a D loop (d ). Inter-homologous intermediates can be protected by
components of the ZMM pathway (e), generating double Holliday junction (dHJ) intermediates that can be resolved into class I
crossovers (COs) ( f ). Alternatively, the intermediates can be matured into noncrossovers (NCOs) through different mechanisms,
including synthesis-dependent strand annealing (SDSA) ( g), dHJ dissolution (h), and possibly other mechanisms (i ). In addition, a
ZMM-independent pathway produces class II COs ( j). The estimated number of each intermediate in Arabidopsis thaliana is indicated.
The proteins presumed to be involved in each step are listed in Table 1. This model was inspired by References 4, 53, and 170 and
takes into account Arabidopsis data.
In Arabidopsis, the localization of hot spots has been deciphered by coalescent analyses (35). They
tend to localize in promoters and terminators of genes that are associated with a series of chromatin
marks that promote RNA polymerase II transcription (such as low nucleosome density, H3K4me3,
and H2A.Z marks) and, more strongly, with hypomethylated DNA. A-rich and CTT motifs
enriched in hot spot regions (35, 97) may contribute to the chromatin reorganization in these
regions that is necessary for DSB formation. Consistent with these observations, the few hot spots
that have been analyzed in Arabidopsis by pollen typing also fall within promoter or terminator
regions (61, 191), and seven out of the eight hot spots described in maize are located next to genes
(85, 190). Thus, as in S. cerevisiae but in contrast to Schizosaccharomyces pombe and mice (52), hot
spots of meiotic recombination in plants could be located principally in gene regulatory regions.
306 Mercier et al.

At a higher scale, chromosomal domains with high CO rates alternate with domains where CO
rates are significantly lower than the genome average (39, 71, 112). In S. cerevisiae, Arabidopsis,
wheat, and humans, more than 80% of the recombination events occur in less than a quarter of
the genome (34, 35, 131, 135, 139). In many plant species, this distribution is skewed toward
the ends of chromosomes (i.e., distal chiasmata), the centromeric regions being devoid of COs
in all species. Although this pattern could reflect an early terminal initiation of recombination
in barley (90), recent results obtained with translocated wheat chromosomes indicate that the
pattern of chiasmata is independent of the position on the chromosome, demonstrating that
“relative crossover frequencies along chromosome arms are predetermined and independent of
the segment location” (125, p. 201; see also references therein). Much remains to be learned about
the origin of CO heterogeneity, and the recent identification of two Arabidopsis mutants in which
the localization but not the total number of COs is affected (62, 103) could shed light on this
important topic.
The number of COs per chromosome rarely exceeds three per bivalent irrespective of the
physical size of the chromosome: 76% of chromosomes in Figure 3 have three COs or fewer, and
84% have four or fewer (Figure 3, Supplemental Table 1; follow the Supplemental Material Supplemental Material
link from the Annual Reviews home page at http://www.annualreviews.org). For example, the
giant chromosome 3B of wheat, with a physical size of approximately 1 Gb, has an average of ∼3
COs per meiosis, which is comparable to the number in the longest chromosome of Arabidopsis
(31 Mb) and the smallest chromosome in budding yeast (0.3 Mb). This limitation is not due to a
shortage in DSBs, as in plant species the estimated number of DSBs far exceeds the number of
COs (in the range of 10–50-fold) (reviewed in 138), but several active mechanisms prevent DSBs
from becoming COs (see below). In addition, CO interference—the phenomenon that makes
successive COs farther apart on a chromosome than would be expected by chance—could also
participate in limiting the number of COs (13, 199). The small amount of variation in the number
of COs per chromosome raises the question of what evolutionary forces limit this number. Louis
& Borts (123) hypothesized that a large number of COs per chromosome could create topological
constraints that prevent proper segregation. This assertion is not supported in some exceptional
species, such as S. pombe and honeybees, in which faithful chromosome segregation occurs despite
high CO numbers and density (Figure 3). Likewise, recent data obtained in Arabidopsis showed
that meiosis can proceed normally even when the CO number is artificially increased threefold
(42) or ninefold (R. Mercier, unpublished data). The mechanical hypothesis thus being unlikely,
these results suggest that there is an optimal level of recombination for adaptation that is close to
one CO per chromosome.
A related question is the fate of DSBs that are not repaired as COs. One obvious possibility is
that they become NCOs, as is largely the case in S. cerevisiae (34, 131). NCO events are poorly
documented in plants because of the difficulty of detecting them; indeed, phenotypic screens can
barely detect NCO events. Clever screens performed in maize have detected NCO events at the
bronze (59, 59a) and a1 loci, but only two of them have been characterized at the molecular level
(188). Recent studies have tried to address the detection, rate, and molecular characterization of
meiotic NCOs in Arabidopsis, either by performing genome-wide sequencing of a few meiotic
products (124, 149, 186) or by characterizing NCO events at a few loci through pollen typing
(61) or visual assays based on fluorescent-tagged lines (168). These studies clearly confirmed the
existence of NCOs in plants, but they were detected at an astonishingly low frequency per meiosis.
Across three independent genome-wide studies (124, 186; C. Mézard, unpublished data), only 19
NCO events were detected in 11 independent meioses, an average of 1.7 NCOs detected per
meiosis. This leaves a large discrepancy between the ∼250 DSBs and ∼12 recombination events
detected per meiosis in Arabidopsis (10 COs and 2 NCOs). Two nonexclusive explanations can

20
19
18
Average number of COs per chromosome per meiosis

17
16
15
14
13
12
11
10
9
8
7
6
5
4
3
2
1
0
0 1 10 100 1,000
Physical size (Mb)
Fungi Plants
Agaricus bisporus (button mushroom) Arabidopsis thaliana
Gibberella zeae (fusarium) Beta vulgaris (sugar beet)
Saccharomyces cerevisiae (budding yeast) Brachypodium distachyon
Schizosaccharomyces pombe (fission yeast) Brassica rapa (Chinese cabbage)
Cucumis sativus L. (cucumber)
Animals Fragaria vesca (wild strawberry)
Apis mellifera (honeybee) Gossypium arboreum (cotton)
Bos taurus (cattle) Hordeum vulgare (barley)
Caenorhabditis elegans Malus domestica (apple)
Canis familiaris (dog) Medicago truncatula
Gallus gallus domesticus (chicken) Prunus persica (peach)
Homo sapiens (human) Solanum lycopersicum × Solanum pennellii (tomato)
Monodelphis domestica (opossum) Sorghum bicolor (sorghum)
Mus musculus (mouse) Theobroma cacao (cacao)
Triticum aestivum 3B (wheat, chromosome 3B)
Other Zea mays IBM (maize, IBM population)
Trypanosoma brucei gambiense Zea mays LHRF (maize, LHRF population)
Figure 3
Number of crossovers (COs) per chromosome per meiosis in a variety of eukaryotes. The number of COs,
deduced from male/female-average genetic maps, is plotted against the physical size of each autosomal
Supplemental Material chromosome (Mb, log scale). Data and references are provided in Supplemental Table 1.
be proposed for this discrepancy. First, a proportion of DSBs may be repaired using the sister
chromatid as a template, as observed in yeasts (24, 73, 98, 109), leaving no genetic trace. In plants,
a study of meiosis in haploid Arabidopsis plants showed that meiotic DSBs can indeed be repaired
using the sister as a template (37), but this does not establish the extent to which this type of repair
occurs in wild-type diploids. Second, detected NCOs could represent only a small proportion of
308 Mercier et al.

all NCOs. Indeed, it could be that NCOs are in fact much more numerous, and the lack of a
sufficient level of genetic polymorphism (which was ∼0.5% in all these studies) led the studies to
miss the short NCOs. Consistent with this idea, the majority of detected NCOs convert only one
single-nucleotide polymorphism (61, 186) and thus could be very short.
2.2. Molecular Events: The Current Model and the Genes Involved
Meiotic recombination consists of the formation and repair of DNA DSBs. Several pathways lead
to the formation of COs and NCOs (Figure 2).
2.2.1. DNA double-strand-break formation. Meiotic DNA DSBs are formed by the highly
conserved SPO11 protein (52, 63). The catalytic function of SPO11 was understood because of
its similarity to the A subunit of a new class of topoisomerase (topoisomerase VI) identified in
the Archaea (15). These enzymes modulate DNA catenation by inducing DSBs in DNA, forcing
the passage of a DNA strand through the break, and eventually religating the two break ends.
Topoisomerase VI acts as an A2 B2 heterotetramer (68). However, no B subunits have been found
to be involved in meiotic recombination. SPO11 is thus thought to act in a dimeric form to
catalyze meiotic DSBs. In most species, SPO11 is encoded by a single gene, but the genomes of
plants and some other eukaryotic lineages contain several SPO11 homologs (130). Genetic studies
of each single mutant in Arabidopsis showed that both AtSPO11-1 and AtSPO11-2 are required
for meiotic recombination (78, 84, 165), likely as a heterodimer (84); by contrast, AtSPO11-3
is involved in somatic endoreduplication and does not play a role in meiosis (82, 167, 192; M.
Grelon, unpublished data). The situation in rice could be more complex, because five putative
homologs of topoisomerase VIA were described (5, 104). However, so far, only OsSPO11-1 has
been convincingly shown to be involved in meiotic recombination (193).
In S. cerevisiae, Spo11 requires nine other proteins (Rad50, Mre11, Xrs2, Rec102, Rec104,
Rec114, Ski8, Mer2, and Mei4) for meiotic DSB formation. These proteins form several subcom-
plexes whose function is still poorly understood (52). Unlike SPO11, they are poorly conserved at
the sequence level across kingdoms, and even when the protein sequences are conserved, functional
divergences are often observed. For example, Rad50, Mre11, and Xrs2 orthologs are not required
for DSB formation in Arabidopsis, S. pombe, or Coprinopsis cinereus, although they are required for
meiotic DSB processing. Ski8 is conserved at the sequence level but has no meiotic function (106).
Classical genetic screens isolated five new genes required for meiotic DSB formation in plants
(PRD1, PRD2, AtPRD3/OsPAIR1, DFO, and CRC1) (54, 55, 137, 143, 197). AtPRD3/OsPAIR1
(54, 143) and AtDFO (197) appear to be plant specific. PRD1 shows similarities with MEI1, a
mouse protein also required for meiotic initiation (55). PRD2 shows limited structural similarities
with the yeast DSB proteins ScMei4 and SpRec24 (113). Such limited structural similarities were
also detected between the S. cerevisiae DSB formation protein Rec114 and the plant meiotic gene
PHS1 (113), but the phs1 mutant in neither maize nor Arabidopsis (153) exhibited the expected
DSB-defective phenotype. Finally, the CRC1 protein, which is the yeast Pch2 homolog in rice,
was recently shown to be required for DSB formation (137) and to interact with OsPAIR1/PRD3
in vitro. Intriguingly, PCH2 is not required for DSB formation in either yeast or Arabidopsis (17;
C. Franklin, personal communication) but rather is needed later in the recombination pathway.
This further highlights the variation in DSB formation machinery among species. Because plants
are one of the rare eukaryotes for which such a number of important DSB proteins have been
identified, it will now be crucial to investigate their respective roles during DSB formation and to
decipher the mechanisms that regulate DSB formation spatially and temporally.

2.2.2. Double-strand-break processing and homologous template choice. In yeast and mam-
mals, SPO11 remains covalently attached to the 5 extremities of the DNA DSBs after cleavage.
The nucleolytic activity of the MRX/MRN complex (Mre11/Rad50/Xrs2 or Mre11/Rad50/Nbs2)
Synapsis:
polymerization of the together with Com1/Sae2 releases short oligonucleotides bound to Spo11 (141). Functional anal-
synaptonemal complex yses of the plant MRE11, RAD50, and COM1 genes are compatible with a conserved role of the
proteins encoded by these genes in the early steps of DSB processing; their respective mutants all
display strong chromosome fragmentation at anaphase I (Table 1), which was shown to be SPO11
dependent for Atcom1 (174) and Atmre11 (148). In addition, Atcom1 mutants accumulate SPO11-1
and fail to form RAD51 foci (174). However, the NBS1/XRS2 homolog appears to be dispensable
for homologous recombination, except in some checkpoint-defective backgrounds (182).
Molecular studies in S. cerevisiae have shown that the DNA DSBs are then further resected to
generate longer 3 -OH single-stranded DNA, which are subsequently bound by the Rpa proteins
and loaded by the recombinases Rad51 and Dmc1 to form nucleofilaments competent for
homology search and heteroduplex formation. In a diploid cell after replication, three intact DNA
molecules are available: the sister chromatid and the two chromatids of the homologous chromo-
some. The formation of at least one CO per homologous pair requires that at least a subset of DSB
repair is directed toward the homologous chromosome, a phenomenon largely prevented during
somatic recombination and known as the inter-homologous (IH) bias. The mechanisms at the
origin of the recognition and choice of the intact DNA repair template are still largely unknown.
In plants, each component of the heterotrimeric RPA complex (RPA1, 2, and 3, also called
the RPA 70-, 32-, and 14-kDa subunits, respectively) is encoded by a multigene family. Genetic
and biochemical data obtained in rice and Arabidopsis have only begun to elucidate the role of
each of these components and have led to the idea that several RPA complexes coexist that are
only partially redundant (2, 65, 99, 154), some of which are required for meiotic recombination
(Table 1).
The stoichiometry of both the RAD51 and DMC1 recombinases inside the nucleofilament
is still under debate, but cytological evidence recently obtained in Arabidopsis suggests that they
tend to localize to the two opposite sides of a meiotic DSB, which is compatible with the differing
faithfulness of these two extremities according to the DSB repair model (Figure 2, steps c and d )
(114). RAD51 is involved in both mitotic and meiotic recombination, whereas DMC1 is exclu-
sively active at meiosis. During wild-type meiosis, DMC1-mediated IH DNA repair appears to be
the predominant pathway. In yeast, as in Arabidopsis, the catalytic activity of RAD51 is dispensable
for CO formation at meiosis, indicating that RAD51 functions as a DMC1 accessory factor during
meiotic CO formation (38, 51). In addition, RAD51 works as a backup pathway to repair meiotic
DSBs when DMC1 fails (114, 175). In the absence of DMC1, meiotic DSBs are efficiently re-
paired in a RAD51-dependent manner, most likely using the sister chromatid as a repair template,
leading to a complete absence of synapsis and bivalent formation but correct DNA repair (40, 57).
However, when DMC1 is present, it represses RAD51 repair activity (173), reminiscent of the
situation in yeast, where a negative regulatory mechanism suppressing RAD51 function during
meiosis is known to operate (116, 172).
So far, hardly any biochemical or structural differences have been identified between RAD51
and DMC1 (161), but a large number of factors have been found that are required for proper
loading, stabilization, and/or activation of one or the other of these recombinases (Table 1).
These accessory proteins could therefore explain the diverging roles of RAD51 and DMC1 during
meiosis. For example, ASY1, the plant Hop1 homolog, is an axial protein that stabilizes DMC1 but
not RAD51 during Arabidopsis meiosis and allows proper IH repair (156). Similarly, SDS, a plant-
specific cyclin-D-like protein, is required for DMC1 loading and/or stabilization (54) and could
act with CDKA;1 to promote IH repair (M. Grelon, unpublished data). Similarly, the checkpoint
310 Mercier et al.

kinase ATR regulates DMC1 loading at DSB sites (114). In addition, a recent study showed that a
threshold level of functional HOP2/MND1 is required to promote correct DMC1 activity (173).
Finally, the unfoldase FIGL1 limits COs by regulating the RAD51/DMC1 dynamic (R. Mercier,
unpublished data). The RAD51-driven inter-sister repair pathway probably also requires accessory
proteins, one of which is likely to be the MCM8 helicase (44).
Several other proteins are also likely to be recombinase cofactors during meiosis, includ-
ing BRCA2 (60, 162) and several of the RAD51 paralogs (XRCC3, RAD51B, RAD51C, and
RAD51D). However, the requirement for one or another of these RAD51 paralogs appears to
vary from species to species (Table 1).
2.2.3. Two pathways for crossover formation. One major discovery of the last decade in the
meiotic recombination field is the existence, downstream of the invasion step, of two pathways for
CO formation in most eukaryotes (class I and class II COs). The first pathway relies on a group of
proteins initially identified in S. cerevisiae and called collectively ZMMs (Zip1, Zip2, Zip3, Zip4,
Mer3, Msh4, and Msh5) (20). In the Arabidopsis mutants Atmsh4, Atmsh5, Atshoc1 (zip2), Athei10
(the likely Zip3 functional homolog), and Atzip4, and in combinations of these, COs were strongly
reduced but not eliminated (∼15% of the wild-type level) (29, 32, 88, 92, 127, 128). The residual
CO level is similar in the mutant for PTD, which encodes what appears to be a plant-specific ZMM
that forms an XPF/ERCC1-like dimer with SHOC1/ZIP2 (128, 183). Atmer3 mutants showed a
slightly higher level of residual CO frequency (∼25%). However, combining the Atmer3 mutation
with another zmm mutation results in the typical 15% residual CO frequency (33, 128, 136). In
rice, similarly, the Osmsh5 single mutant has a residual CO frequency of ∼10% (126). Oszip4,
Osmer3, and Oshei10 single mutants have residual CO frequencies of ∼30%, which suggests that
these genes are partially dispensable in the pathway (27, 160, 177, 178), but whether the mutants
are null is unclear. When several mutations are combined, CO frequency tends toward 10% and
does not decrease further (126, 160, 177, 178). It is thus clear that the ZMM pathway is a major
one in plants but is not unique, accounting for 85–90% of COs. Although they are not classified as
ZMMs, two other conserved proteins, MLH1 and MLH3, act in the ZMM pathway (Figure 2).
Arabidopsis mlh1 and mlh3 mutants are less affected than zmm mutants, with a CO frequency
reduced to ∼50% of the wild-type level (32, 102), but mlh3 zmm and mlh1 zmm double mutants
are indistinguishable from zmm single mutants (180; M. Grelon, unpublished data). COs are also
reduced but not eliminated in the barley mlh3/des10 mutant (I. Colas, personal communication).
In contrast to MLH1, which specifically marks ZMM COs at late prophase (30), plant MSH5,
ZIP4, MER3, and HEI10 form numerous foci (more than ten times the number of eventual COs)
at early prophase (leptotene-zygotene). Whereas the other ZMM foci disappear during pachytene
(88, 92, 126, 160, 177, 178), HEI10 concentrates in a limited number of bright foci that colocalize
with MLH1 and chiasmata from late pachytene to diakinesis (32, 178). Thus, among numerous
early recombination intermediates processed by ZMMs, only a few progressively mature into COs
marked by late HEI10 and MLH1 foci. A major challenge for future research is to understand the
mechanism of CO designation among these ZMM-marked intermediates.
Much less is known about the molecular players of the non-ZMM CO pathways in plants,
MUS81 being the only one characterized (Figure 2). Mutating MUS81 reduces recombination
by ∼10% in a wild-type background and eliminates approximately one-third of the residual COs
in a zmm mutant background (14, 89, 128). This shows that MUS81 accounts for part of the non-
ZMM COs, but what accounts for the rest is unknown. One candidate was RAD1/XPF1/MEI-9,
which is involved in CO formation in Drosophila melanogaster and Caenorhabditis elegans (1, 158),
but AtXPF1 has no apparent function at meiosis in either a wild-type or zmm background (44).
The nucleases GEN1 and SLX1, which are involved in non-ZMM CO formation in S. cerevisiae

(195) and for which homologs are present in the plant genomes, are good candidates (12) but have
not been functionally characterized.
The two CO pathways differ not only in their molecular machinery but also in the distribution
of the produced COs. Whereas ZMM-dependent COs are farther apart along the chromosome
than expected by chance (CO interference), non-ZMM COs are distributed independently of
one another (13). Indeed, the residual COs in a zmm mutant are noninterfering (29, 32, 128,
136), whereas interference is increased in a mus81 mutant (14). Further, statistical modeling has
shown that interfering and noninterfering COs cohabit in wild-type plants (10, 11, 66, 115). These
studies further suggest that the relative proportion of the two CO classes varies between sexes,
among genotypes, and along the genome. In tomato, coupling the detection of late recombination
nodules (which mark all COs) via electron microscopy with the localization of class I COs using
MLH1 immunofluorescence via light microscopy has made it possible to observe the distribution
along the chromosome of both classes of COs in wild-type plants (6). These results show that
the proportion of noninterfering COs is higher in the pericentromeric region than in the rest
of the genome. Further, while confirming that ZMM COs interfere with one another and that
non-ZMM COs do not interfere with one another in a wild-type background, this study showed
that class I and class II COs are not distributed independently of each other. The two types of
COs indeed interfere with each other (6), suggesting that whereas class II COs do not detect other
class II COs, class I and class II COs can detect each other.
2.2.4. Noncrossover pathways. In addition to the two CO pathways described above, additional
mechanisms contribute to meiotic DSB repair (Figure 2). First, in Arabidopsis, topoisomerase IIIα
and the associated protein AtBLAP75/AtRMI1 are both required for recombination completion
(31, 83). In the corresponding mutants, homologous chromosomes are connected at metaphase I
by SPO11-dependent but ZMM-independent links, and anaphase I shows chromosome fragmen-
tation, suggesting that recombination intermediates would require single-strand topoisomerase
activity to be resolved as NCOs (187). Second, the helicase AtFANCM and its two cofactors MHF1
and MHF2 (42, 70, 111) as well as the helicase RECQ4 (RECQ4A and RECQ4B) (R. Mercier,
unpublished data), a BLOOM/Sgs1 homolog, prevent CO formation. Compared with the wild
type, CO frequency increases three- and sixfold in the Atfancm single mutant and the recq4a recq4b
double mutant, respectively. In both cases, these extra COs arise from the class II pathway, which
suggests that in the wild type, both FANCM and RECQ4 helicases direct recombination inter-
mediates toward the synthesis-dependent strand-annealing NCO pathway (Figure 2). A third
helicase, RTEL, which limits COs in C. elegans, exists in plants but has not been characterized.
Third, the AAA-ATPase (unfoldase) FIDGTIN-L1 also prevents CO formation independently of
FANCM, likely by regulating the early invasion step catalyzed by DMC1/RAD51 (R. Mercier, un-
published data) (Figure 2). Finally, the RAD51 paralogs XRCC2 and (possibly) RAD51D appear
to also limit CO formation, likely by regulating the same step (50). It thus appears that multiple
pathways promote DSB repair in a manner that does not lead to COs.
3. THE SYNAPTONEMAL COMPLEX

During meiosis, chromatin from sister chromatids forms loops anchored on a common protein axis
called the axial element. This axis is composed of cohesins and meiosis-specific proteins. In plants,
two axial proteins have been described: the Horma domain–containing protein ASY1/PAIR2 and
ASY3/PAIR3 (7, 67, 144, 194). Mutants deficient in any of these axial proteins show recombination
defects (DSB formation, DSB repair, and IH bias), highlighting the fact that the axes play a central
role in several steps of meiotic recombination (155).
312 Mercier et al.

Starting in mid-prophase, a central element polymerizes between the two homologous chro-
mosome axes (axial elements, referred to as lateral elements in later stages) in a tripartite struc-
ture called the synaptonemal complex (SC), whose exact function is a long-standing question.
Chromosome axis:
The structure of the SC is amazingly consistent across species. The central-element proteins a proteinaceous
are poorly conserved at the sequence level, but they display the canonical structure of the yeast structure set up at
central-element Zip1 protein, with a coiled-coil domain in the central region and a globular do- meiotic prophase I on
main at each end. Zip1 homologs have been characterized in three plant species: rice (OsZEP1), which chromosome
DNA fibers anchor,
Arabidopsis (AtZYP1A and AtZYP1B), and barley (ZYP1) (9, 91, 180). In rice, the Oszep1 mutant
forming large DNA
shows an increase in chiasma formation at diakinesis, indicating that OsZEP1 could limit CO loops
formation (180). In Arabidopsis, study of RNA interference (RNAi) knockdown lines has suggested
Synaptonemal
that ZYP1 prevents recombination between nonhomologous chromosomes rather than limiting complex (SC):
homologous CO formation. This contrasts with the function of ZYP1 in promoting CO in barley a proteinaceous
(9), similar to the role of Zip1 in S. cerevisiae (20). structure set up from
zygotene to pachytene
Further complicating our understanding of the relationship between SC central-element

of prophase I that
polymerization and CO controls, SC polymerization depends on ZMMs (see above) in S. cerevisiae
associates homologous
but not in plants. In both cases, however, SC formation is known to rely on the production chromosome axes
of homologous recombination intermediates, because no synapsis is observed in Arabidopsis
spo11, dmc1, or rad51 mutants. Thus the interplay between SC and recombination varies among
eukaryotes. In addition, the rice CRC1 protein (the Pch2 homolog; see above) plays a double
role, functioning in both DSB formation (see above) and central-element structure (137). Indeed,
CRC1 localizes with ZEP1, and the localizations of these two proteins are interdependent. CRC1
is also necessary for the loading of the axial-element protein OsPAIR2, further exemplifying the
complex interconnections between chromosome structure and recombination processes.
4. CHROMOSOME DISTRIBUTION
As mentioned in Section 1, two rounds of chromosome segregation ensure ploidy reduction
during meiosis (Figure 1). This process relies on a stepwise release of sister chromatid cohesion
and a change in kinetochore orientation. During meiosis I, sister chromatid cohesion is released
along chromosome arms (at anaphase I), and the kinetochores of sister chromatids are oriented
to the same pole; this allows homologs, which are no longer interlinked and pulled in opposite
directions, to segregate faithfully. During meiosis II, the pericentromeric cohesion, which has
been protected until then, is released (at anaphase II), and the kinetochores of sister chromatids
are oriented to opposite poles, allowing the proper segregation of sister chromatids. Many actors
in these processes have been identified in plants (Table 1).
In plants, as in other eukaryotes, REC8 is a kleisin cohesin subunit specific to meiosis (16, 23,
28, 74, 159). Its absence leads to DSB repair defects, complete loss of sister chromatid cohesion
at anaphase I, and bipolar orientation of kinetochores at meiosis I. Thus, the combination of
spo11 and rec8 mutations leads to a mitosis-like first meiotic division (28). Further combination
with omission of the second division (Atosd1; see below) leads to the conversion of meiosis into a
mitosis-like division in both Arabidopsis (48) and rice (E. Guiderdoni & R. Mercier, unpublished
data). None of the other plant cohesin subunits appear to be meiosis specific. Notably, there is
only one representative of the three other cohesin subunits (SCC3, SMC1, and SMC3), all of
which are likely involved in both mitosis and meiosis.
Three other kleisin paralogs are present in plants, but their respective functions at meiosis
and mitosis remain to be further clarified (Table 1). The machineries that establish and release
cohesion at both mitosis and meiosis, such as adherin and separase, seem to be conserved in
plants (120, 157, 163). However, the factor that prevents premature activation of the separase

(i.e., the securin) remains elusive. A key innovation of meiosis is the protection of sister chromatid
cohesion until the second division. The SHUGOSHIN proteins protect centromeric cohesion
from separase cleavage at anaphase I (46, 80, 179). Another protein, PATRONUS, which appears
to be a regulator of the anaphase-promoting complex/cyclosome (APC/C; see below) and is specific
to dicotyledonous plants, prevents a loss of cohesion during interkinesis (the transient phase
when nuclei re-form that occurs between the two divisions) (46, 196) (Figure 1). In addition to
REC8, SCC3 and MIS12 (a core kinetochore component) are required for kinetochore monopolar
orientation at meiosis I (28, 118). However, the mechanism and the proteins that specifically ensure
monopolar orientation at meiosis, such as Moa in S. pombe and monopolin in S. cerevisiae (181),
remain to be identified in plants.
Aberrant chromosome distribution can also result from defects in the relative orientation of
spindles at the second division. Although metaphase II spindles are roughly perpendicular to
each other in wild-type plants, parallel and/or fused and/or tripolar spindles are observed in null
mutants for AtPS1 and JASON (49, 64). These mutants thus produce diploid spores by regrouping
the products of the first division. The mode of action of these two proteins on spindle orientation
remains to be elucidated.
5. MEIOSIS PROGRESSION
5.1. Entry into Meiosis

Very little data is available on the mechanisms that govern meiotic entry in plants (Table 1). The
recently isolated rice MIL1 gene, coding for a CC-type glutaredoxin, could be one important
factor of this step, because mil1 plants are the only described mutants for which male meiocyte
differentiation is completely prevented (95). Other mutants in rice, maize, and Arabidopsis are
blocked at a different level of meiotic prophase I (Table 1), but no global view of this important
step is available.
Several mutants showing meiotic chromosome fragmentation independent of the SPO11-
induced DSBs highlight the existence of S-phase-linked DNA repair mechanisms (Table 1).
Although CDC45 is also crucial for somatic replication, mei1 and xri1 mutants show no evi-
dence of somatic S-phase defects, suggesting that the meiotic replication requires adjustments in
comparison with its vegetative counterpart.
5.2. Cell Cycle Control: Two Divisions Following a Single Replication

The meiotic sequence of two cell divisions with no intervening DNA replication is a unique
bending of the cell cycle rules that typically ensure the strict alternation of one replication and
one division. The other well-known exceptions to this typical cell cycle control are endomitosis
and endoreplication, where several replications occur without chromosome segregation, leading
to cellular ploidy increase (56). Another unique feature of meiosis progression is the extended
G2 /prophase I that, for example, accounts for >90% of the time taken by an Arabidopsis male
meiosis (8). How the machinery that ensures cell cycle control at mitosis is modified for the purpose
of meiosis is not fully understood, but much progress has been made in the last few years (184).
The core cell cycle machinery that operates in both meiosis and mitosis is well conserved in
eukaryotes: Cyclins and cyclin-dependent kinases (CDKs) form complexes that are essential for
both meiotic and mitotic progression. Cyclins confer activity and target specificity to the CDKs.
High CDK-cyclin activity is required for entry and progression in metaphase. A rapid decrease of
CDK activity, achieved through the destruction of cyclins by the APC/C, promotes the anaphase
314 Mercier et al.

onset and exit from the division phase (81, 133, 147). Plant meiosis seems to follow this general
model. CDKA;1 is essential for meiosis progression, and its activity peaks at both metaphase I
and metaphase II, suggesting that CDKA;1 is the major driver of meiosis progression (22, 58). By
Polyploid:
contrast, the cyclins that drive meiosis progression, and that are thus expected to peak during the an organism in which
metaphases, remain elusive. Indeed, the Arabidopsis genome encodes 21 A and B cyclins, but their cells contain more
functional and cytological characterizations have so far failed to identify the “cycling” cyclin(s) (21). than two pairs of
In addition, downregulation of the APC/C activator CDC20 results in sterility (108) associated related chromosomes
(homologous and/or
with metaphase I arrest (R. Mercier, unpublished data), indicating that APC/CCDC20 activation
homeologous)
is necessary to trigger anaphase I in plants, as in other organisms. The Arabidopsis genome also
encodes three homologs of the other family of APC/C activators, CDH1, but none of them have
been characterized at meiosis (87).
The transition from meiosis I to meiosis II through interkinesis requires a fine-tuning of
cyclin-CDK activity, which must be low enough to exit meiosis I but high enough to avoid
complete exit from meiosis and entry into the second division without replication (133, 147).
Surprisingly, the molecular players that ensure this specific regulation appear to be extremely
poorly conserved among eukaryotes, although they all directly modify the cyclin-CDK-APC/C
module. For example, S. pombe Mes1, vertebrate Emi2, and plant OSD1 (see below) seem to play
the same crucial function at meiosis, although they appear to be phylogenetically unrelated (25,
101, 110, 129, 145, 171).
In plants, four genes that control meiosis progression have been recently characterized in
Arabidopsis: (a) TAM, encoding one of the ten cyclin A proteins, expression of which peaks at
prophase I (22, 47); (b) OSD1, encoding an APC/C inhibitor (45, 48, 100); (c) SMG7, which
also plays an evolutionarily conserved role in nonsense-mediated RNA decay (152); and (d ) TDM,
encoding a protein of unknown molecular function (although it may also be related to the APC/C)
(22, 45, 72). TAM and OSD1 are essential for the transition from meiosis I to meiosis II. In plants
lacking either TAM or OSD1, meiosis consists only of the first division, leading to the production
of diploid spores and gametes (47, 48). By contrast, meiocytes lacking TDM appear to be unable
to exit from the meiotic program at the end of meiosis II and attempt a third aberrant division.
Strikingly, plants expressing an APC/C-insensitive version of TAM exhibit the same phenotype of
three meiotic divisions as the tdm mutant does (45, 72). Conversely, a phospo-mutant of TDM exits
meiosis prematurely, mimicking the tam or osd1 null mutant phenotype (R. Mercier, unpublished
data). Finally, SMG7 is essential for the progression through anaphase II, and its downregulation
leads to an arrest at this stage (22, 152). Notably, AtPS1 (49) (see above) possesses a PINc domain
that is present in proteins involved in RNA processing; along with the data on SMG7, this suggests
a link between RNA decay and the meiotic cell cycle.
Together, these results suggest that a functional network composed of the cyclin TAM, the
APC/C inhibitor OSD1, the mRNA decay protein SMG7, and TDM controls the three key
transitions of meiosis prophase–meiosis I, meiosis I–meiosis II, and exit from meiosis at the end
of meiosis II. How exactly this module decides to either promote another division or exit from
meiosis remains to be determined. Interestingly, several genotypes (tdm, tam/osd1) are affected
differently in male and female meiosis (although meiocytes of both sexes have the same genotype,
Arabidopsis being hermaphrodite), revealing differences in the control of male and female meiosis
cell cycle machinery.
6. MEIOSIS IN POLYPLOIDS
Polyploidy, a common occurrence in plants, poses a greater challenge for faithful chromosome
segregation because it gives every chromosome more than one possible match. Whenever a

chromosome engages in an illegitimate or multiple association, unbalanced gametes are formed

and fertility is reduced (151). However, the odds of this occurring differ across polyploids.
In autopolyploids, which have more than two copies of every chromosome, all potential partners
Homeologous
chromosome: are true homologs that share the same chance of recombining with one another. As a consequence,
a partially homologous chiasmatic multivalents are frequently, though not systematically, observed in natural and resyn-
chromosome that thesized autopolyploids (reviewed in 76). There are also autotetraploid species that do primarily
originates from form bivalents through a random assortment of homologs into pairs (i.e., polysomic inheritance);
different diploid
these species display “cytologically, but not genetically diploidized meiosis” (94, p. 3).
parents in an
allopolyploid species In theory, the meiotic hurdles faced by autopolyploid organisms are easy to overcome, as a
sharp reduction in CO frequency is expected to result in enhanced bivalent formation and thus
improved chromosome segregation (discussed in 36). This theory has recently gained concrete
support in the autotetraploid Arabidopsis arenosa, which shows fewer chiasmata per bivalent than
diploids do (189). Through population genetics approaches, this work also established a list of
candidate genes that may be instrumental in improving chromosome segregation by reducing CO

frequencies (94, 189). This list has highlighted mainly components of meiotic chromosome axes
(AaSYN1, AaSMC3, AaASY1, and AaASY3) and the SC (AaZYP1a and AaZYP1b) that are critical
to CO formation, notably by directing DSB repair toward homologs (see above). Preliminary
immunolocalization of ASY1 and ZYP1 has not revealed extensive differences between diploids
and natural autotetraploids (93), which suggests that the variants that are fixed in autotetraploid
populations have retained much of their biological activity. Further work is now needed to prove
that they still contribute to lower CO rates.
In allopolyploids, which have an interspecific hybrid origin, the situation is even more demand-
ing because the chromosomes that originated from different diploid parents (i.e., the homeologs)
are not fully interchangeable. The sorting of homologous and homeologous chromosomes is thus
necessary to ensure correct chromosome segregation. This process is genetically controlled in
most, if not all, allopolyploid species (105), but despite their crucial role, our knowledge of loci
regulating CO formation between homeologous chromosomes is extremely limited.
Only one of these loci has been molecularly characterized: the Ph1 locus of wheat, which
has been defined as a cluster of defective CDK-like genes related to mammalian CDK2 (3, 77,
79). This locus is thought to promote a diploid-like meiosis through alterations to chromatin
condensation that result from reduction of overall CDK2-type activity (77). Another gene whose
activity is altered in the absence of Ph1 is TaASY1 (17); however, it is unclear whether TaASY1 is a
downstream transcriptional target of Ph1 or a gene upregulated in response to the meiotic burden
caused by the absence of Ph1. To add to this complexity, reduced levels of TaASY1 transcripts
in wheat RNAi knockdown lines lead to increased nonhomologous recombination (17), echoing
results from ZYP1 RNAi knockdown lines in Arabidopsis (91).
Beyond Ph1, Ph2 in wheat (121, 169) and PrBn in oilseed rape are the most characterized—
though still unidentified—loci known to alter homeologous recombination in allopolyploids. Cur-
rent evidence suggests that Ph2 and PrBn do not work in the same way as Ph1. For example, the
absence of Ph2 leads to a reduction or delay in synapsis, whereas in ph1 wheat mutants most nu-
clei complete synapsis (134). In oilseed rape, in contrast to wheat, the mechanism that promotes
efficient chromosome sorting in allotetraploids seems to be adjusted to promote CO formation
between homeologs in allohaploids (75, 142). More recently, a quantitative trait locus contributing
to meiotic regularity and male fertility in the allotetraploid Arabidopsis suecica has been documented
(86); no obvious candidate gene could be identified in the corresponding region.
Finally, polyploidization increases meiotic CO rates between homologous chromosomes (117,
146). The effect is particularly pronounced in Brassica digenomic triploid AAC hybrids, where
316 Mercier et al.

recombination frequencies expanded fourfold compared with those in the diploid control (117).
The molecular mechanisms responsible for this increase, which is as strong as that in Arabidopsis
fancm mutants (42; see above), are not known, but they seem to be dependent on the addition of
some specific C chromosomes to AA backgrounds (166).
7. APPLICATIONS IN PLANT BREEDING

The better understanding of the meiotic process has allowed in recent years the emergence of
applied perspectives (43). First, the identification of anti-CO factors opens a route toward increased
recombination in crop breeding programs. This elevated recombination would be useful to break
undesirable linkages, create novel combinations of favorable alleles, or increase the power of
genetic mapping experiments. CO frequency can be increased almost ten times in Arabidopsis (42;
R. Mercier, unpublished data), but it remains to be confirmed that mutation of the same genes
would have the same effect in species of agronomic interest.

By contrast, recombination needs to be abolished for the propagation of elite genotypes, no-
tably F1 hybrids. Two technologies have been developed for this purpose that use manipulation of
meiotic genes. The first, called reverse breeding, produces homozygous parental lines from any
heterozygous plant (185). This approach is based on the abolition of CO formation in the het-
erozygote and the production of doubled haploid plants from the gametes. Selecting and crossing
two complementary lines allows the production of the hybrid on a commercial scale. The sec-
ond technology mimics apomixis, the clonal reproduction through seeds (132). It is based on the
modification of meiosis into mitosis and the conversion of the obtained diploid clonal gametes
into embryos by eliminating the other gamete genome. In both cases, a proof of concept has been
obtained in Arabidopsis and now needs to be transferred into crops.
8. FUTURE PROSPECTS
Although our knowledge of the molecular biology of meiosis, and in particular of plant meiosis,
has increased massively in the last decade, many questions remain. First, much progress needs to be
made in understanding the control of the localization of DSBs and the regulation of their fate (as
COs or not), which collectively shape the eventual distribution and number of COs. Notably, the
tight control of the number and distribution of class I COs, including the elusive CO interference
mechanism, will have to be deciphered. Second, the function of the SC is unclear in all eukaryotes,
but particularly in plants. Third, key components of the molecular machinery of meiosis, such
as the one that ensures monopolar segregation of sister chromatids at anaphase I, remain to be
identified. Finally, there is substantial work to be done in understanding the regulation of CO
rates in plants and in translating the knowledge gained in Arabidopsis (and, to a lesser extent,
rice) to other plant species. One of the difficulties here is to identify the genes that retained
equivalent functions after lineage-specific gene duplication(s) and loss(es). Recent results indicate
that meiotic recombination genes tend to return to a single copy following polyploidy, whereas
duplicated genes regulating the meiotic cell cycle are preferentially retained (122). This suggests
that the core meiotic tool kit identified in Arabidopsis and rice has not broadly diversified following
recurrent polyploidy in plants, a conclusion that remains to be confirmed functionally. The field
will continue to benefit from innovative genetic screens, progress in cytology, massive parallel
sequencing, and (soon) directed mutagenesis, which will extend our knowledge of all aspects of
meiosis.

SUMMARY POINTS
1. In recent years, a combination of approaches have revealed the depth of the hetero-
geneity of recombination along the genome. However, the origins of the recombination
landscape remain obscure.
2. Recent data obtained in plants and in other organisms have led to a large revision of our
view of mechanisms of meiotic recombination.
3. More than 50 years after the discovery of the synaptonemal complex and a century after
the description of crossover interference, the function of the former and the mechanisms
of the latter remain mysterious.
4. Much progress has been made on understanding how the cell cycle machinery is modified
to allow the sequence of two divisions following a single replication and how the balanced
distribution of chromosomes is ensured during these two divisions.
5. Pervasive polyploidy complicates chromosome segregation in many plant species. Studies
over the last few years have provided some insights into the molecular underpinnings of
meiotic stabilization in polyploids.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
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PP66-FrontMatter ARI 23 January 2015 17:42
Annual Review of
Plant Biology
Contents Volume 66, 2015
From the Concept of Totipotency to Biofortified Cereals

Ingo Potrykus p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
The Structure of Photosystem II and the Mechanism of Water
Oxidation in Photosynthesis
Jian-Ren Shen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p23
The Plastid Terminal Oxidase: Its Elusive Function Points to Multiple
Contributions to Plastid Physiology
Wojciech J. Nawrocki, Nicolas J. Tourasse, Antoine Taly, Fabrice Rappaport,
and Francis-André Wollman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p49
Protein Maturation and Proteolysis in Plant Plastids, Mitochondria,
and Peroxisomes
Klaas J. van Wijk p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p75
United in Diversity: Mechanosensitive Ion Channels in Plants
Eric S. Hamilton, Angela M. Schlegel, and Elizabeth S. Haswell p p p p p p p p p p p p p p p p p p p p p p p p 113
The Evolution of Plant Secretory Structures and Emergence of
Terpenoid Chemical Diversity
Bernd Markus Lange p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 139
Strigolactones, a Novel Carotenoid-Derived Plant Hormone
Salim Al-Babili and Harro J. Bouwmeester p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 161
Moving Toward a Comprehensive Map of Central Plant Metabolism
Ronan Sulpice and Peter C. McKeown p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 187
Engineering Plastid Genomes: Methods, Tools, and Applications in
Basic Research and Biotechnology
Ralph Bock p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 211
RNA-Directed DNA Methylation: The Evolution of a Complex
Epigenetic Pathway in Flowering Plants
Marjori A. Matzke, Tatsuo Kanno, and Antonius J.M. Matzke p p p p p p p p p p p p p p p p p p p p p p p p p 243
The Polycomb Group Protein Regulatory Network
Iva Mozgova and Lars Hennig p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 269
v
PP66-FrontMatter ARI 23 January 2015 17:42
The Molecular Biology of Meiosis in Plants

Raphaël Mercier, Christine Mézard, Eric Jenczewski, Nicolas Macaisne,
and Mathilde Grelon p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 297
Genome Evolution in Maize: From Genomes Back to Genes
James C. Schnable p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 329
Oxygen Sensing and Signaling
Joost T. van Dongen and Francesco Licausi p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 345
Diverse Stomatal Signaling and the Signal Integration Mechanism
Yoshiyuki Murata, Izumi C. Mori, and Shintaro Munemasa p p p p p p p p p p p p p p p p p p p p p p p p p p p p 369
The Mechanism and Key Molecules Involved in Pollen Tube Guidance
Tetsuya Higashiyama and Hidenori Takeuchi p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 393

Signaling to Actin Stochastic Dynamics
Jiejie Li, Laurent Blanchoin, and Christopher J. Staiger p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 415
Photoperiodic Flowering: Time Measurement Mechanisms in Leaves
Young Hun Song, Jae Sung Shim, Hannah A. Kinmonth-Schultz,
and Takato Imaizumi p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 441
Brachypodium distachyon and Setaria viridis: Model Genetic Systems
for the Grasses
Thomas P. Brutnell, Jeffrey L. Bennetzen, and John P. Vogel p p p p p p p p p p p p p p p p p p p p p p p p p p p 465
Effector-Triggered Immunity: From Pathogen Perception
to Robust Defense
Haitao Cui, Kenichi Tsuda, and Jane E. Parker p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 487
Fungal Effectors and Plant Susceptibility
Libera Lo Presti, Daniel Lanver, Gabriel Schweizer, Shigeyuki Tanaka,
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Review - The Molecular Biology of Meiosis in Plants.

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PP66CH12-Grelon ARI 24 March 2015 13:49

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Annu. Rev. Plant Biol. 2015. 66:297–327 Keywords

The Annual Review of Plant Biology is online at Abstract

7. APPLICATIONS IN PLANT BREEDING . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 317

8. FUTURE PROSPECTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 317

298 Mercier et al.

www.annualreviews.org • Molecular Biology of Meiosis in Plants 299

DNA sequence with a

2.1. The Nature and Distribution of Recombination Events

300 Mercier et al.

Link to Figures Supplemental

MEL2 Rice DAZ-associated protein 1 Meiotic G1 –S transition A 110

AGO9/AGO104 Argonaute (AGO9) Somatic fate in germ cells, meiotic

www.annualreviews.org • Molecular Biology of Meiosis in Plants

Protein Species homologs Meiotic function 1 and 2a reference(s)b

A. thaliana 18, 119, 127

Rice DSB repair 23

P. patens Meiotic DSB repair 23a

FIGL1 A. thaliana FIDGETIN L1 Anti-CO activity C, c, d

Recombination: CO and NCO outcome

FANCM A. thaliana FANCM/Mph1/Fml1 Anti-CO activity C, D, g, i 34, 86

MHF1 A. thaliana MHF1 Anti-CO activity C, D, g, i 45, 61

www.annualreviews.org • Molecular Biology of Meiosis in Plants

Protein Species Putative homologs Meiotic function 1 and 2a reference(s)b

AXR1 A. thaliana E1 RUB ligase Regulation of CO distribution C, D 80

Rice 148, 165

SYN1/DIF1/REC8 A. thaliana 7, 10, 20, 25

Cell cycle control: spindle–cytokinesis

A. thaliana Cyclin A Cell cycle meiotic transitions G, J, M 36, 39, 152

SMG7 A. thaliana SMG7 Anaphase II progression L 17, 123

ATK1/KATA/KIN14a A. thaliana Kinesin 14 Male meiotic spindle morphogenesis H, K 29

TES/NACK2/STD A. thaliana Kinesin 7 Male meiotic cytokinesis N 122, 156

www.annualreviews.org • Molecular Biology of Meiosis in Plants

d Inter-homologous Inter-sister events

Class I COs Class II COs

306 Mercier et al.

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Average number of COs per chromosome per meiosis

308 Mercier et al.

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310 Mercier et al.

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3. THE SYNAPTONEMAL COMPLEX

312 Mercier et al.

Further complicating our understanding of the relationship between SC central-element

www.annualreviews.org • Molecular Biology of Meiosis in Plants 313

5.1. Entry into Meiosis

5.2. Cell Cycle Control: Two Divisions Following a Single Replication

314 Mercier et al.

www.annualreviews.org • Molecular Biology of Meiosis in Plants 315

chromosome engages in an illegitimate or multiple association, unbalanced gametes are formed

candidate genes that may be instrumental in improving chromosome segregation by reducing CO

316 Mercier et al.

7. APPLICATIONS IN PLANT BREEDING

would have the same effect in species of agronomic interest.

www.annualreviews.org • Molecular Biology of Meiosis in Plants 317

318 Mercier et al.

interactions and is affected by deletion of Ph1. Plant J. 57:487–97

www.annualreviews.org • Molecular Biology of Meiosis in Plants 319

melanogaster. PLOS Genet. 8:e1002905

320 Mercier et al.

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