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2863–2875, 2010
doi:10.1093/jxb/erq191
Introduction
Man has selected from natural genetic variation to breed from a single diploid parent cell (Villeneuve and Hillers,
crop species useful for agriculture. Considerable genetic 2001; Hamant et al., 2006; Mezard et al., 2007). This
diversity remains to be fully exploited, including variation reductive division is achieved by a single round of DNA
capable of increasing yield and broadening crop range. replication followed by two rounds of chromosome segre-
Sustainable increases in agricultural yield in the range of gation and cell division (meiosis-I and meiosis-II) (Fig. 1).
50% will be required to feed the 9 billion people estimated to Meiosis appears to be an ancestral trait within eukaryotes
exist by 2050 (The Royal Society, 2009). To increase the and is speculated to have arisen close to the group’s origin
efficiency of crop breeding, it is important to understand the (Villeneuve and Hillers, 2001; Cavalier-Smith, 2002). This
mechanism by which variation is generated and transmitted. idea is strengthened by observations that many unicellular
Variation is generated in a specialized, reductive cell di- eukaryotes, once presumed to be asexual, have since been
vision termed meiosis during which recombination between found to possess conserved meiosis-specific genes (Ramesh
homologous chromosomes, termed crossover (CO), occurs. et al., 2005; Malik et al., 2007). The first meiotic division
CO frequency varies within and between species and can be differs dramatically from mitosis as homologous chromo-
limiting such that useful variation is not accessible for somes pair before segregation. During the second division
breeding. Although the majority of crops are angiosperms sister chromatids segregate to opposite poles in the same
in which meiosis occurs within floral organs, non-flowering manner as during mitosis. While homologues are paired
plants have provided novel insights into the control of plant during meiosis-I they are tightly associated via the synapto-
meiosis. The nature of the meiotic cell division in plants, the nemal complex that forms along their length (Page and
genetic mechanisms that promote variation, and the de- Hawley, 2004). Meiosis-specific expression of an endo-
velopmental context in which meiosis occurs in land plants nuclease, SPO11, causes a large number of double strand
and their closest sister groups are reviewed here. breaks (DSBs) along the paired chromosomes (Villeneuve
and Hillers, 2001). A subset of these break sites are repaired
through recombination pathways that lead to physical
Meiotic cell divisions
exchange between the paired chromosomes (CO) (Villeneuve
Meiosis is a mode of cell division specific to eukaryotic and Hillers, 2001; Hamant et al., 2006; Mezard et al., 2007).
organisms whereby four haploid daughter cells are produced As paired chromosomes segregate during meiosis-I, CO sites
ª The Author [2010]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
For Permissions, please e-mail: journals.permissions@oxfordjournals.org
2864 | Harrison et al.
and DMC1 are both thought to act at the step of encodes a protein similar to structure-specific endonucleases
ssDNA invasion, rad51 mutants show SPO11-dependent (Berchowitz et al., 2007; Higgins et al., 2008a).
chromosome fragmentation, whereas dmc1 mutants show Paired chromosomes generally show at least one CO
univalent segregation (Couteau et al., 1999; Li et al., 2004). event, the obligate CO, that is required for proper patterns
One explanation for this difference may be that DSBs are of chromosome segregation in A. thaliana (Grelon et al.,
repaired using sister chromatids in dmc1, but not in rad51 2001). Each A. thaliana chromosome shows approximately
(Couteau et al., 1999; Li et al., 2004). 1.8 CO per meiosis and very few chromosomes show no CO
DSBs lead to CO via formation of a double Holliday (Copenhaver et al., 1998, 2002; Higgins et al., 2004;
junction (dHJ) between paired homologous DNA duplexes Drouaud et al., 2006, 2007). CO position is highly variable
(Villeneuve and Hillers, 2001). Subsequent to strand in- and hot- and cold-spots of CO frequency exist along the
vasion, a series of events are required for dHJ formation, chromosomes (Copenhaver et al., 1998, 1999; Drouaud
including second end capture and DNA synthesis and et al., 2006, 2007). Pronounced increases in CO frequency
ligation (Villeneuve and Hillers, 2001). These junctions are and gene density are observed towards the telomeres of
ultimately resolved into CO events via an unknown dHJ wheat and maize chromosomes (Liu et al., 2009; Saintenac
resolvase in plants, although the structure-specific endonu- et al., 2009; Schnable et al., 2009). A recombination hotspot
implicated in the regulation of meiotic progression have novel protein required for chromosome pairing and synapsis,
been identified in A. thaliana. A novel, cyclin-like gene which causes high levels of non-homologous pairing when
SOLO DANCERS (SDS) is specifically expressed during mutated (Pawlowski et al., 2004; Ronceret et al., 2009).
meiosis and sds mutants show defects in chromosome Co-incident with pairing, the SC forms between homolo-
pairing, segregation, and CO (Azumi et al., 2002). Recently, gous chromosomes (Page and Hawley, 2004) and SC
sds mutants have been observed to form DSBs but repair components identified in A. thaliana include ASYNAPTIC1
them efficiently, most likely via RAD51-mediated inter- (ASY1), ZYP1A, ZYP1B, SCC3, and REC8/DIF1/SYN1
sister repair (De Muyt et al., 2009). The novel gene (Bai et al., 1999; Bhatt et al., 1999; Caryl et al., 2000;
OMISSION OF SECOND DIVISION1 (OSD1) is required Armstrong et al., 2002; Cai et al., 2003; Chelysheva et al.,
for meiosis-II and osd1 produces diploid dyad products of 2005; Higgins et al., 2005). ASY1 and ZYP1 show distant
meiosis instead of haploid tetrads (d’Erfurth et al., 2009). A identity with the animal HOP1 and ZIP1 SC proteins,
temperature-sensitive substitution allele of CYCLINA1;2, respectively (Caryl et al., 2000; Armstrong et al., 2002;
termed tardy asynchronous meiosis1 (tam1) causes a delay in Higgins et al., 2005). Loss of SC proteins causes failures in
meiotic progression, which also leads to dyad formation synapsis and CO formation, and can lead to univalent
(Magnard et al., 2001; Wang et al., 2004). Regulation of segregation and chromosome fragmentation (Bai et al.,
meiosis immediately following fertilization (Fig. 2A). By numerous small spores (microspores) that have a dispersal
contrast, in all land plants mitotic divisions intercede function (Bower, 1935). Gender can also influence patterns
fertilization and meiosis, and meiosis occurs after a period of CO frequency (Drouaud et al., 2007). Thus the initiation
of diploid development in specialized structures termed and progression of meiosis depend on the developmental
sporangia that produce numerous spores (Bower, 1935; identity of the tissue in which it is activated, discussed by
Becker and Marin, 2009). The initiation of sporangium plant group below.
development pathways often follows a switch in meristem
identity from a vegetative to a reproductive fate (Steeves
and Sussex, 1989). The location and structure of sporangia
Meiosis in chlorophyte and charophyte algae
vary by plant group and are associated with their secondary
functions, which are spore dispersal and nutrition. Hetero- In both chlorophyte and charophyte algal sister groups to
morphic sporangia and spores have evolved convergently in the land plants meiosis occurs immediately following
vascular plants and associate with specialized functions fertilization (Becker and Marin, 2009). In the single-celled
(Fig. 2). Female megasporangia have fewer, larger spores chlorophyte alga, Chlamydomonas reinhardtii two haploid
(megaspores) that may be retained within the parent plant mating types, plus and minus, differentiate into gametes
Fig. 2. Phylogenetic distribution of characters associated with meiosis in plants. (A) Phylogenetic relationships between major plant groups
showing synapomorphies associated with meiosis. Heterospory has a polyphyletic origin in lycophytes, monilophytes, and spermatophytes,
indicated by asterisks. (B) Reproductive structures of representatives of clades illustrated in (A), and extinct protracheophyte fossil forms.
1. Electron micrograph of Chlamydomonas monoica zygospores (photograph courtesy of Professor Karen P Van Winkle-Swift and by kind
permission of John Wiley and Sons: see VanWinkle-Swift KP, Rickoll WL. 1997. The zygospore wall of Chlamydomonas monoica
(Chlorophyceae): Morphogenesis and evidence for the presence of sporopollenin1. Journal of Phycology 33, 655–665.) 2. Light micrograph
of the haploid plant and oogonium (inset) in the charophyte alga Chara sp. 3. The creeping haploid thallus and a diploid erect and
determinate sporophyte of Pellia epiphylla (photographs of bryophytes courtesy of Li Zhang). 4. The haploid leafy gametophyte of Atrichum
angustatum bearing diploid unbranched determinate sporophytes. 5. The haploid creeping thallus of Folioceros sp. with upright
indeterminate sporophytes. 6. A fossil sporophtye of Cooksonia sp. showing branching with terminal sporangia (photo courtesy of Jenny
Morris and Dianne Edwards). 7. A fossil sporophyte of Zosterophyllum showing lateral sporangia (photo courtesy of Jenny Morris and
Dianne Edwards). 8. A Selaginella kraussiana sporophyte showing vegetative branching habit, an unbranched reproductive strobilus, and
a mega- and microsporangium (inset). 9. Sporangia formed on the stem of Psilotum nudum. 10. A frond of Adiantum mairisi showing
marginal sori that contain sporangia. 11. The terminal cones of Cupressus sp. that contain the mega- and microsporangia. 12. The
stamens and carpels of a Magnolia sp. flower that contain the micro- and megasporangia, respectively.
2868 | Harrison et al.
(Fig. 2B) (Lee et al., 2008). Plus and minus gamete identity pha) models (Ishizaki et al., 2008; Rensing, 2008). Two gene
is specified from the MATING-TYPE locus and requires classes that affect sporangium development in P. patens are
cytoplasmic accumulation of BEL [GAMETE-SPECIFIC homologues of A. thaliana LEAFY (LFY) and KNOX genes
PLUS1 (GSP1)] and KNOX [GAMETE-SPECIFIC MI- (Champagne and Ashton, 2001; Tanahashi et al., 2005;
NUS1 (GSM1)] class homeodomain proteins, respectively Sakakibara et al., 2008). A pair of LFY homologues
(Ferris and Goodenough, 1994; Lee et al., 2008). Following redundantly control the first zygotic division in P. patens
fertilization GSP1 and GSM1 heterodimerize, translocate to and double mutants exhibit arrested zygotic development
the nucleus, and initiate zygotic gene expression patterns (Tanahashi et al., 2005). In mutants that do not arrest,
(Lee et al., 2008). Constitutive expression of either GSP1 or sporangium number, initiation, and development are per-
GSM1 in the opposite gamete type is sufficient to trigger turbed. These defects may arise as a consequence of
zygote development in the absence of fertilization (Zhao abnormal sporophytic development, although spore number
et al., 2001; Lee et al., 2008). Stable C. reinhardtii diploids and germination are also highly variable in the mutants,
that do not initiate meiosis can also be generated, and suggesting meiotic defects (Tanahashi et al., 2005). Similarly
constitutive expression of GSP1/GSM1 together in these Class I KNOX mutants in P. patens have abnormal
cells is sufficient to induce meiosis with normal patterns of sporangia and reduced spore numbers (Sano et al., 2005;
on leaves (Fig. 2B). With the exception of the leptosporan- KNOX gene SHOOTMERISTEMLESS (STM) is neces-
giate and whisk ferns, nutritive tapetal tissues arise from sary for the establishment of an indeterminate meristem
non-sporogenous tissue (Bower, 1935; Parkinson, 1987). As (Long et al., 1996), and STM and BREVIPEDICELLUS
in bryophytes, the genetic basis of diploid development is (BP) act redundantly to maintain indeterminacy and repress
poorly characterized in lycophytes and monilophytes. determinate leaf development (Byrne et al., 2002). Class I
Notably sporophytic KNOX expression is conserved, and KNOX proteins promote indeterminacy by dimerizing with
meristematic expression domains suggest likely roles in BEL transcription factors and triple bellringer, poundfoolish,
indeterminate growth (Bharathan et al., 2002; Harrison Arabidopsis thaliana homeobox1 BEL mutants phenocopy
et al., 2005; Sano et al., 2005), although reproductive roles stm mutants (Rutjens et al., 2009). Thus, in A. thaliana
have not yet been explored. Thus the structure and dispersal KNOX and BEL genes play key roles in elaboration of the
functions of sporangia vary broadly across the land plants diploid body, providing the context for later reproductive
and the developmental context for the initiation of meiosis development and meiosis. Flower development follows
is lineage specific. An evolutionary trend towards the conversion of indeterminate, vegetative shoot meristems to
amplification of spore numbers by alterations in body plan, reproductive fates. This switch is controlled by a large
sporangium size, and the number of sporangia is apparent network of genes that ensure reproduction is co-ordinated
female development. Male sporocyte identity in A. thaliana breeding and facilitate the generation of novel high-yielding
is also regulated by the leucine-rich repeat (LRR) receptor agricultural strains.
kinase EXTRA SPOROGENOUS CELLS/EXCESS
MICROSPOROCYTES1 (EXS/EMS1) in conjunction with
its small protein ligand TAPETUM DETERMINANT1
(TPD1) (Yang et al., 1999b, 2003; Canales et al., 2002; Zhao Acknowledgements
et al., 2002). The first archesporial cell division normally
We thank the Royal Society and the Gatsby Charitable
separates reproductive sporocyte fate from non-reproduc-
Foundation for funding, Karen Van Winkle-Swift, Vasily
tive wall and tapetal fates. Microsporangial development is
Kantsler, Li Zhang, Jenny Morris, and Dianne Edwards for
altered in exs/ems1 and tpd1 mutants such that sporogenous
photographs, and two anonymous reviewers for helpful
cells develop at the expense of tapetal cells (Yang et al.,
comments on the manuscript.
1999b, 2003; Canales et al., 2002; Zhao et al., 2002). This
implies that EXS/EMS1 kinase signalling is important either
to promote tapetal or to repress sporogenous cell identity.
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