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J Exp Bot. Author manuscript; available in PMC Jul 15, 2013.
Published in final edited form as:
Published online Nov 7, 2012. doi:  10.1093/jxb/ers314
PMCID: PMC3711010
EMSID: EMS53936

Tinkering with meiosis

Abstract

Meiosis is at the heart of Mendelian heredity. Recently, much progress has been made in the understanding of this process, in various organisms. In the last fifteen years, the functional characterization of numerous genes involved in meiosis has dramatically deepened our knowledge of key events, including recombination, cell cycle and chromosome distribution. Through a constantly advancing tool set and knowledge base, a number of advances have been made that will allow manipulation of meiosis from a plant breeding perspective. This review focuses on the aspects of meiosis that can be tinkered with to create and propagate new varieties.

We would like to dedicate this review to the memory of Simon W. Chan (1974-2012) http://www.plb.ucdavis.edu/labs/srchan/

Keywords: apomixis, crossover, diploid gametes, haploid, meiosis, recombination, reverse breeding, plant breeding

Introduction

In the coming decades high quality food must be produced to feed billions of people on this planet (Tester and Langridge 2010). Research is making advances on how this may be possible by introgressing certain traits, more specifically alleles of genes, into the elite crop varieties that already exist. Methods are required to transfer genetic material between plant varieties. For this to occur, with the exception of transgenesis, the genetic material must pass by a peculiar cell division known as meiosis. Meiosis generates genetic diversity and maintains ploidy (the number of sets of chromosomes in a cell) through successive generations. During meiosis, chromosomes which will be transmitted to the next generation are recombined, redistributed and then their number halved. Molecular data on plant meiosis has rapidly been accumulating in the last decade, mostly in the model species Arabidopsis thaliana, but notably also in rice (Oriza sativa) and maize (Zea maiz). This led to the functional characterization of over sixty genes involved in various aspects of meiosis, from recombination to cell cycle and chromosome movement. A more global view of plant meiosis mechanism is thus emerging, as described in several recent reviews (Osman et al. 2011; Berchowitz and Copenhaver 2010; Harrison et al. 2010; Mercier and Grelon 2008). Such a global understanding of these meiotic mechanisms, beyond its intrinsic scientific interest, opens up novel applied possibilities. In this review, we describe how tinkering with the basic mechanisms of meiosis provide potential new technologies to control plant reproduction, such as mastering the level of recombination, manipulation of the ploidy of gametes, recreation of parental plants from a hybrid, and the implementation of clonal reproduction through seeds.

Wild type meiosis: how to make recombined haploid gametes

Two major features define meiosis: recombination that produces a patchwork of the pre-meiotic chromosomes and reduction of ploidy by half (Fig. 1). Ploidy is reduced because two rounds of chromosome distribution follow a single replication. Homologous chromosomes are separated at the first division, and sister chromatids are separated at the second division. To be more accurate, this statement is correct because the chromosome identity is arbitrarily defined by its centromere. See in Fig. 1 that indeed at centromere chromosome distribution follows this rule, but that away from centromeres the occurrence of crossovers (COs), which are exchanges of continuity between two homologous chromatids, modifies this pattern. At both divisions, entities that will be separated must be physically connected beforehand. In the case of the first division, crossovers provide this link in partnership with sister chromatid cohesion (ensured by cohesins, a molecular glue that is established at the onset of their replication). This mechanical role of COs is crucial to understand and to tinker with meiosis. This is illustrated on Fig. 1: The two sister chromatids are held together by cohesins. A CO converts this inter-sister cohesion into an inter-homologue link. Hence, if the CO on Fig.1 is absent, there is no longer a link between the homologous chromosomes (Grelon et al. 2001). In such a case, chromosomes segregate randomly generating a high level of unviable aneuploid gametes. At anaphase I, sister chromatid cohesion is released from the chromosome arms, freeing the recombinant homologous chromosomes to migrate to opposite poles. However, sister chromatid cohesion is kept in centromeric regions and provides the link between the sister chromatids which is required for their segregation at the second division. The centromeric cohesion is released at anaphase II, allowing the distribution of sister chromatids.

Figure 1
Chromosome behavior at meiosis. Meiosis consists of two rounds of chromosome segregation following a single replication. At the onset of replication, the sister chromatids are held together by cohesion (purple rings). Homologous chromosomes pair during ...

Thus for a correct meiotic division certain requirements must be met: (1) at least one crossover must occur per pair of homologues (the so called obligate crossover). Note that only one chromatid from each homologue is engaged in any given crossover, thus even with the obligate crossover rule, some chromatids can be crossover free. (2) Cohesion between sister chromatids must be released along the arm at anaphase I but maintained at centromeres until being released at anaphase II. (3) Sister centromeres must co-segregate at first division and separate at second division. (4) The rule of the mitotic cell cycle must be bent to permit two divisions to follow a single replication.

Now, with the knowledge of how wild-type meiosis makes recombined haploid gametes, let’s see how we can tinker with it.

Can crossover formation be controlled?

We explained above that there is at least one crossover per homologue pair. Surprisingly, in most species the frequency of crossover per pair of homologue does not deviate far above 1, typically in the range of 1-4 (chromosome genetic size of 50 to 200 cM), plants being no exception (see for example Giraut et al. 2011; Sim et al. 2012; Wei-Wei Zhang et al. 2012; Bowers et al. 2012; Cloutier et al. 2012; Guihua Zou et al. 2012; Hudson et al. 2012). This low level of COs occurs despite a large excess of DNA double-strand breaks which are the precursors of COs (estimated to be 20-40 fold in plants, with for example 230 DSBs (estimated with DMC1 foci) for about 11 COs in Arabidopsis (Chelysheva et al. 2007; Anderson and Stack 2005; Giraut et al. 2011). In addition, COs can also be largely confined to certain regions. In many species, a large proportion of the genome (proximal to the centromere) is CO free while there are many genes within these hyporecombinogenic regions (e.g. in melon and tomato (Garcia-Mas et al. 2012; The Tomato Genome Consortium 2012; Sim et al. 2012)). Another constraint on CO distribution is interference which prevents the occurrence of two close COs from occurring in a single meiosis. Hence interference prevents the recovery of double recombinants in a gamete, therefore easily adding one generation to the introgression of a chromosomal fragment of a limited size from one variety to another. Further, recombination tends to be inhibited in crosses involving distant relatives, while often desirable traits would ideally be introgressed into elite varieties from exotic germplasm (Gur and Zamir 2004). Because the CO number and distribution is tightly regulated, this limits the genetic diversity that could otherwise be created in breeding programs in addition to limits mapping and positional cloning power in research. Thus there is a clear interest for breeding programs to be able to control the many aspects of recombination (Wijnker and de Jong 2008). A number of recent studies have provided clues how this may be achieved.

Homologous recombination

There is evidence showing that some simple methods can influence recombination rates. For example, using a very sensitive assay which measures male recombination in Arabidopsis, it has been shown that CO frequency can be slightly increased by using flowers from secondary and tertiary branches rather than from the primary bolt or by elevating temperature (Francis et al. 2007). A more pronounced effect is seen when comparing male with female in Arabidopsis: on average male crossover outnumbers female crossovers by 67%, with most of the difference coming from sub-telomeric regions. Hence, if you require a recombinant in Arabidopsis, it would probably be best to use a male as the source of gametes, using flowers from the secondary or tertiary branch from plants grown at 28°C. It will be interesting to test if these effects are seen in other plant species.

Natural variation has also been identified as a factor that can influence CO frequency in a number of species such as maize, barley, rice, soybean, Arabidopsis, cow and mouse (Bovill et al. 2009; Esch et al. 2007; Li and Pfeiffer 2009; Stefaniak et al. 2006; Sandor et al. 2012; Yandeau-Nelson et al. 2006). This suggests that naturally occurring alleles that convey increased recombination frequencies could be stacked into a single genotype to increase or decrease CO rates. A key factor here will be to identify the underlying factors that regulate the frequency of homologous recombination. Recent results also suggest that manipulating karyotype composition could be a way to increase CO frequency in Brassica (Leflon et al. 2010). Indeed, comparing recombination between two homologues, in the presence or absence of an extra set of homoeologous chromosomes (i.e. an allotriploid) showed a staggering six times average increase compared to the euploid control. While the mechanism behind this effect remains elusive, it is a tool that can be used in Brassica and potentially other plant species. Changes in ploidy level have also been associated with an increase in recombination rate (~1.5-fold) in Brassica spp. (Leflon et al. 2010) and in Arabidopsis (Pecinka et al. 2011), where the rates of meiotic recombination were higher in tetraploids compared to diploids. This observation also holds true when comparing the size of genetic maps between diploid and natural allotetraploid Gossypium species (Desai et al. 2006) suggesting that it may be a general trend.

While many genes involved in CO formation were identified (Osman et al. 2011), no reports that we are aware of indicated that tinkering with only these elements can lead to an increase of CO frequency. A possible explanation for this may be that known pro-crossover genes are not controlling CO frequency, but rather are indispensable machinery to form the COs that occur in wild-type. However these elusive factors that regulate CO numbers and distribution are starting to be discovered and can be offered to plant breeders. MSH2 (MutS Homologue 2) is part of a very conserved DNA mismatch repair system that can prevent recombination between DNA sequences that are not perfectly homologous. This can occur meiotically and somatically in species as diverse as yeasts, mosses and flowering plants (Trouiller et al. 2006; Emmanuel et al. 2006; Hunter et al. 1996). It has been shown in an Atmsh2 mutant that meiotic recombination is increased by ≈40% between two polymorphic Arabidopsis accessions, in one interval (Emmanuel et al. 2006). Hence from a plant breeding perspective, the mismatch repair system is probably part of the meiocyte’s arsenal that prevents recombination between distantly related species. Exploiting this knowledge could allow a better control of introgression of foreign germplasm into elite varieties. Another mechanism that could be targeted to influence CO formation, is the DNA methylation machinery. Indeed the DNA hypomethylation Arabidopsis mutant Atmet1 (methyltransferase1) shows elevated centromere-proximal COs, decreased peri-centromeric CO and increased distal CO (Yelina et al. 2012). Furthermore Atmet1 and Atddm1 (decreased DNA methylation 1) mutants, and Atddm1-derived epiRILS, show altered global distribution while the final genome-wide CO frequency is unchanged, thus demonstrating that CO distribution can indeed be modified (Mirouze et al. 2012; Melamed-Bessudo and Levy 2012; Yelina et al. 2012; Colomé-Tatché et al. 2012).

Finally, the mutation of a single gene, AtFANCM, has been shown to increase meiotic recombination on eight intervals by a factor of three (Crismani et al. 2012). FANCM, is a conserved helicase that also limits meiotic COs in the yeast S. pombe (Lorenz et al. 2012) and given the conservation of function of FANCM between two species as distant as Arabidopsis and S. pombe, it is reasonable to speculate that mutation of FANCM would have the same hyper-recombinogenic effect in other plants species. Interestingly, the extra COs that occur in fancm mutants are non-interfering (i.e. distributed independently from each other) (Crismani et al. 2012), which could facilitate the introgression of small fragments of chromosomes rather than undesirably large blocks. Tripling CO frequency (from ~2 to ~6 per chromosome) does not affect meiotic chromosome distribution and fertility of the plant, which leaves the door open to see how high CO frequency can be increased by stacking all the effects known or to be discovered. We have no reason to think that plant species are anyway near to the limit of crossovers that the chromosomes can tolerate. Most plant chromosomes receive an average of 2 COs per meiosis (e.g. Giraut et al. 2011; Sim et al. 2012; Wei-Wei Zhang et al. 2012; Bowers et al. 2012; Cloutier et al. 2012; Guihua Zou et al. 2012; Hudson et al. 2012). However, for example, the biggest chromosomes of chicken (200 Mb) (Groenen et al. 2009) or budding yeast (1.5 Mb) receive an unusual average of ~10 CO per meiosis. Simply applying the yeast density of COs per Mb, bread wheat chromosome 3B, which measures 1 Gb, would receive more than 6000 CO. It is hard to believe that such an extreme situation could be reached, but it is equally difficult to predict toward what limit the number of COs can actually be manipulated.

Homoeologous recombination

Wild or distantly related species present a potential reservoir of genetic diversity which could be introgressed into a species of interest in a breeding program. However, meiosis is a species barrier which frequently prevents exactly this type of recombination which is termed homoeologous recombination. Homoeologous sequences are sequences which were once homologous in a common ancestor but have subsequently diverged during speciation and a hybridization event has brought these sequences back together in the same cell. These homoeologous sequences can align and interact (similar to the way two homologues would) and they can form COs. However, over-ruling mechanisms typically prevent this homoeologous recombination. Indeed, these mechanisms are required to ensure fertility and to maintain genome stability in allopolyploids where multiple similar genomes are present in the same nucleus. One of the best known examples is the Ph1 locus in allohexaploid bread wheat (Griffiths et al. 2006; Sears and Okamoto 1958; Riley and Chapman 1958; Riley et al. 1960) which prevents recombination between homoeologous chromosomes and hence this polyploid shows diploid-like behavior at meiosis. The naturally occurring mechanisms which prevent homoeologous recombination provide a major stumbling block for breeding programs as not only can introgressing a trait (gene) from wild germplasm be very difficult but equally so when backcrossing out undesirable linked traits in subsequent generations.

Fortunately some tools exist to partially mitigate these constraints, e.g. the deletion of the Ph1 locus in bread wheat allows some recombination between homoeologous regions, which for many decades has been used in plant breeding programs. For example, a ph1 mutant was exploited to break the linkage between a desirable and an undesirable trait that were introgressed into bread wheat from Imperial rye (Anugrahwati et al. 2008). The Ph1 locus was reduced to a cluster of CDC2-like genes (Griffiths et al. 2006) which have homology to mammalian CDK2. Subsequently, by exploiting the knowledge that globally the CDC2-like genes are overexpressed in ph1 (Al-Kaff et al. 2008), an appropriate chemical treatment was tested in an attempt to phenocopy the effects of ph1. An okadaic acid treatment, which stimulates the effects of CDK2, obtained promising results on metaphase I spreads which showed increased chromosome interactions in wheat-rye hybrids (Knight et al. 2010). Another potential tool would be to develop wheat lines containing the dominant Aegilops speltoides genes that suppress Ph1 activity thereby allowing increased gene transfer (Dvorak et al. 2006). The advantage of developing methods such as the okadaic acid treatment and Ae. speltoides-derived suppressors is that they are readily reversible when compared to breeding strategies relying on recessive mutations (e.g. ph1 deletion mutants). This is important because as mentioned above, Ph1-like machinery is essential for maintaining fertility and genome stability in allopolyploids and its function must be restored after the desired recombinants are obtained. Hence these strategies may provide plant breeders with simpler means to increase introgression of alien chromatin into elite varieties. Indeed, mechanisms which ensure diploid-like behavior at meiosis and hence fertility are not limited to bread wheat. In Brassica napus, it was discovered that there was natural variation for homoeologous CO frequency, with a major locus called PrBn (Jenczewski et al. 2003; Cifuentes et al. 2010; Nicolas et al. 2009). The locus has not been cloned yet, but could be already used to tinker with homoeologous recombination.

Making diploid gametes

Diploid gametes (2n gametes) are abnormal gametes, as they have the somatic level of ploidy rather than half. If such gametes participate in fertilisation, this leads to an increase of ploidy of the offspring compared to the parent. It is generally accepted that whole genome duplications that occurred in the evolution of many lineages of eukaryotes, and particularly frequently in plants, originated from sexual polyploidizations through 2n gametes (Ramanna and E Jacobsen 2003). From an applied perspective, diploid gametes can allow crosses between related species with different levels of ploidy. This has been used to transfer genetic diversity from diploids, through 2n gametes, to polyploid crop varieties as demonstrated for example in potato or alfalfa (Peloquin et al. 1999; Ramanna and E Jacobsen 2003). Fertilisation involving 2n gametes, could be also used to produce synthetic vigorous tetraploid or triploid individuals, whose sterility is a suited character in some species (e.g. seedless banana, watermelon and oyster) (Heslop-Harrison and Schwarzacher 2007). In addition, 2n gametes can be used to produce innovative powerful mapping populations (Van Dun and Dirks 2006). Various meiotic defects (see below) can lead to the production of diploid gametes. It has been known for a long time that 2n gamete production is under genetic control and a series of mutants producing 2n gametes have been described in various plants (Cai and Xu 2007; Ramanna and E Jacobsen 2003), but only a few responsible genes have been recently identified, shedding light on the molecular control of 2n gamete formation.

Making diploid gametes via spindle orientation defects

The first cloned gene whose mutation leads to the production of diploid gamete at a high frequency is Arabidopsis thaliana PARALLEL SPINDLE 1 (AtPS1) (d’ Erfurth et al. 2008). The same phenotype was subsequently observed in jason mutants (Erilova et al. 2009; De Storme and Geelen 2011). In wild-type male meiosis of Arabidopsis, no cytokinesis is observed before telophase II, meaning that the two sets of chromosomes formed after the first division remain in a common cytoplasm. During metaphase II, the two spindles are roughly perpendicular to each other, leading to four well-separated poles at anaphase II. The Atps1 and jas mutants present fused or parallel spindles in male meiosis II (Fig. 2A). Thus, the two sets of chromosomes that were separated during the first division are re-gathered into a single metaphase plate. This creates a situation where it is as if the first segregation did not occur, and the resulting 2n gametes are called FDR gametes (first division restitution), but with recombination. Because the fusion of the spindle is not complete in all meiocytes, ~60% of gametes are diploid, but ~40% are haploid. When using genetics to analyse products of meiosis in Atps1 or jas, a mitotic-like division is observed, but with meiotic recombination occurring: i.e. the recombined sister chromatids are segregated to opposite poles. The resulting 2n gametes are heterozygous at centromeres (because sister centromeres are separated from one another, one copy of each homologous chromosome in each gamete) and tend towards random segregation at loci away from the centromeres because of recombination (66 % of heterozygosity, i.e. from an A/a parent, genotype of non-centromeric loci would be 2/3 A/a, 1/6 AA, 1/6 aa) (Fig. 2B). As Atps1 and jas affect only male meiosis, spontaneous triploid progeny is recovered after self-pollination, resulting from the fusion of 2n male gametes with 1n female gametes. While the molecular function of AtPS1 remains elusive, it has been suggested that JASON positively regulates AtPS1 transcription levels (De Storme and Geelen 2011).

Figure 2
Mutants producing dipoid gametes in Arabidopsis thaliana

Making diploid gametes by skipping the second division

Another way of producing diploid gametes is to simply skip the second division (giving so called SDR gametes, for second division restitution). Only two genes whose mutation gives this phenotype have been isolated. The Arabidopsis osd1 (omission of second division) and tam (initially described as tardy asynchronous meiosis (Magnard et al. 2001; Wang et al. 2004)) mutants skip the second meiotic division, producing dyads instead of tetrad of spores (Wang et al. 2010; d’ Erfurth et al. 2010, 2009). In both osd1 and tam mutants, prophase and meiosis I are indistinguishable from the equivalent stages in wild type with recombination and segregation of homologous chromosomes. From there, the resulting two sets of chromosomes will constitute the genome of the gametes, omitting the second meiotic division (Fig 2A). As these mutations affect both male and female meiosis, 4n plants are recovered when selfed. Both genes are components of the cell cycle machinery, and contribute to the cell cycle-specific regulation that allows a second division to occur without an intervening replication at meiosis. TAM is one of the 10 A type cyclins of Arabidopsis thaliana (CYCA1;2 ). TAM is involved in all the meiotic cell cycle transitions (Bulankova et al. 2010; d’ Erfurth et al. 2010; Cromer et al. 2012). OSD1 is a regulator of the Anaphase Promoting Complex (APC) (Cromer et al. 2012; Iwata et al. 2011), a conserved component of the cell cycle machinery, which notably destroys cyclins to promote exit from mitosis or meiosis (Cooper and Strich 2011). Genetically, as the sister kinetochores migrate together at meiosis I in tam and osd1, the diploid gametes are systematically homozygous close to centromeres (Fig. 2B). Away from centromere, recombination distributes the alleles towards randomness (66% of heterozygosity).

Making diploid gametes by turning meiosis into mitosis

Finally, diploid gametes can be produced by turning meiosis into a single, mitotic-like division. As such, any heterozygosity present in the parent is transmitted into the 2n gamete. This is observed in mutants of several genes. In maize, the dominant mutation of AGO104 (which belongs to the ARGONAUTE multigenic family acting on transcriptional and post-transcriptional gene silencing as well as on RNA interference) leads to the production of 30-40% of unreduced gametes in both male and female (Singh et al. 2011). A histone modification marker, used to discriminate meiosis from mitosis, suggests that meiocytes in ago104 undergo mitotic-like division rather than a meiotic division. Interestingly, maize AGO104 is an orthologue of AGO9 of Arabidopsis and Atago9 mutants show spontaneous development of somatic cells into functional diploid gametes (completely skipping meiotic development, so called apospory) (Olmedo-Monfil et al. 2010). Other maize mutations in the epigenetic machinery can induce phenotypes reminiscent of mitotic-like divisions at meiosis (Garcia-Aguilar et al. 2010).

The SWI1/DYAD/DSY10 gene was identified more than a decade ago, and its molecular function remains elusive despite the characterization of a range of mutant alleles (Mercier et al. 2001; Agashe et al. 2002; Boateng et al. 2008; Mercier et al. 2003; Siddiqi et al. 2000; Xue and Makaroff 2001). While male meiosis is variously affected, female meiosis appears to be similarly modified in all of them. Indeed, in female meiosis 10 univalents are observed, with a balanced segregation of the sister chromatids, mimicking mitosis. The fertility of these plants is massively reduced, but among the few seeds produced, 78% originates from a mitotically derived female gamete (Fig. 2A) (Ravi et al. 2008). The same phenotype is observed in maize when AM1, the orthologue of SWI1/DYAD is mutated (Pawlowski et al. 2009). Furthermore, it has been shown that the rare spontaneous descendants of dyad are triploid, resulting from the fertilization of a mitotically-derived unreduced female gametophyte by reduced pollen (Ravi et al. 2008).

2n mitotic-like gametes can be obtained at a frequency of 100% by combining mutations that abolish each of the features that distinguish meiosis from mitosis (d’ Erfurth et al. 2009). The first feature is recombination, that can be eliminated by mutating the very conserved function of SPO11 (Grelon et al. 2001). SPO11 is essential for the formation of DNA double-strand breaks and thus the initiation of meiotic recombination. Hence in a spo11 mutant, no recombination can take place, leading to the random segregation of 10 univalents. Second, to convert meiosis into mitosis, sister kinetochores (and hence sister chromatids) must have bipolar orientation rather than monopolar orientation as they would during meiosis. Mutation of REC8 can satisfy this need. REC8 is a protein that ensures sister chromatid cohesion in meiosis (Bai et al. 1999; Bhatt et al. 1999). Hence a spo11 rec8 double mutant shows a balanced segregation of the two sets of 10 sister chromatids in meiosis I (Chelysheva et al. 2005), mimicking a mitosis at first division. However, as the second division occurs in this double mutant, the resulting free chromatids are unable to align at metaphase II and segregate randomly. Thus the last feature that has to be removed to convert meiosis into mitosis, is the occurrence of a second division, which can be achieved by mutating OSD1 or TAM (see above). In a triple spo11 rec8 osd1 (d’ Erfurth et al. 2009), or in a spo11 rec8 tam (d’ Erfurth et al. 2010) the two sets of 10 chromatids segregate perfectly once, and since no further division occurs, diploid gametes are obtained via a mitosis-like division instead of meiosis (see figure 1 in d’ Erfurth et al. (2009) for a graphical explanation). Hence this triple mutant, spo11 rec8 osd1, is called MiMe for Mitosis instead of Meiosis, and performs mitosis instead of meiosis at a rate of 100%. Self-fertilisation involving the clonal 2n gametes leads to doubling of ploidy at each generation

Genetic content of unreduced gametes differs

According to the mechanism of 2n gamete production, their genetic content may dramatically differ (Fig. 2B). This must be taken into account from an applied perspective to maximize the transfer of desirable alleles. There are two main features controlling the genotype of diplogametes: segregation of homologous or sister chromatids (more accurately their centromeres) and presence or absence of recombination. In the case of a mitotic-like division (e.g. dyad, MiMe), sister chromatids segregate without recombination, making 2n gametes genetically identical to their parent. In the case of Atps1 and jas, sister centromeres also segregate from each other, but in this case recombination occurred. Thus, heterozygosity is conserved at centromeres (if the parental plant was A/a, 2n gametes would be systemically A/a) and tends to be reduced toward randomness (2/3 A/a, 1/6 AA, 1/6 aa) away from centromeres (Fig. 2B). The opposite effect is seen in osd1 or tam mutants, sister centromeres migrate together and recombination occurs. Thus heterozygosity is completely lost at centromeres (i.e. the diploid parental plant being A/a, 2n gametes will be either A/A or a/a, never A/a). Away from centromeres, and because of recombination, the genetic composition of unreduced osd1 and tam gametes tends towards randomness (2/3 heterozygous).

Getting rid of recombination: how to fix the ideal genotype

Hybrids often have better field quality than their parent. This phenomenon called hybrid vigor or heterosis is widely exploited in plant and animal breeding, although its mechanism remains elusive (Chen 2010). F1 hybrids must be recreated continually because genetic segregation eliminates half of the heterozygosity in the F2 (97% by the F6) and would thus rapidly dilute the heterosis effect.

Reverse breeding

In traditional plant breeding, to take advantage of heterosis, the selection is applied to homozygous lines on the ability to produce the best hybrid (F1) when crossed by another genetically distinct homozygous line. The plants that are selected and the ones that express the sought phenotype are thus not the same. Reverse breeding is a novel plant breeding strategy that proposes to do it with a top down approach. First the best hybrid is selected and then the parental lines are recreated (Dirks et al. 2009). This strategy produces homozygous parental lines from any heterozygous plant and is based on the abolition of CO formation in the heterozygote and the production of doubled haploid plants from the gametes free of COs. Selecting and crossing two lines with complementary sets of chromosomes allow the production of the hybrid at a commercial scale. This technique also allows the production of so called substitution lines which are for example heterozygous for only one chromosome, facilitating the selection of the best alleles carried by this chromosome. The feasibility has been recently demonstrated in the model Arabidopsis (Wijnker et al. 2012), using the extinction of DMC1 a gene required for CO formation in most eukaryotes, to abolish CO formation. Due to the loss of most, if not all COs, chromosomes segregate randomly but balanced gametes are produced at a rate close to the expected rate (1/2chromosome number). These gametes have been turned into haploid plants using centromere mediated genome elimination (Ravi and Chan 2010) and then self-pollination resulted in double-haploid diploid plants which are homozygous at all loci in the genome. From these, both the original hybrid and a set of substitution lines have been obtained. The technique is therefore now a reality, however it can only be applied to crops with no more than 12 chromosomes, due to the difficulty in obtaining balanced gametes by chance, and in which spores can be regenerated into doubled haploids.

Apomixis

Apomixis is the asexual formation of a seed from maternal material. Importantly this means that meiosis is replaced by mitosis and theoretically that heterozygosity could be maintained through generations. This would provide a major simplification of the production of hybrids that could be propagated indefinitely without losing the benefits of heterosis (Bicknel and Koltunow 2004).

Many plant species reproduce via apomixis (>400 known) however there is an under representation of important crop species that reproduce that way. This is speculated to have occurred by chance through human selection early in the history of agriculture (Bicknel and Koltunow 2004). Therefore the identification of the underlying genetic mechanisms would represent a holy grail for a simple way of increasing crop yields and global efforts are progressing towards identifying the genes required for apomixis. It is established that apomixis is under the genetic control of a limited number of loci, but the corresponding genes have not yet been identified (Pupilli and Barcaccia 2012; Koltunow et al. 2011; Koltunow et al. 2011). So far, the attempts to directly introgress apomixis into crops have been unsuccessful, making the identification and understanding of natural apomixis mechanisms crucial.

Another opportunity to introduce apomixis into plants exists through the possibility to engineer apomixis de novo through tinkering with sexual processes. The first step is to modify meiosis by turning it into a mitotic-like division, producing clonal gametes with the somatic level of ploidy as described above in Arabidopsis (dyad, MiMe, ago104, ago9). The second step is to produce seeds from these unreduced gametes, without any genetic contribution of another gamete. It could be achieved through parthenogenesis, or post-fertilization elimination of the unwanted chromosomes. The Arabidopsis GEM (Genome elimination) line provides the latter possibility, as the genome of the GEM line is eliminated post-fertilization when crossed to any other genotype (Ravi and Chan 2010). Indeed, when GEM was crossed to dyad or MiMe, clonal seeds were recovered (Marimuthu et al. 2011). This established that it is possible to mimic apomixis by tinkering with sexual processes. However the current system has some limitations, because it is still cross-dependent and does not recover clones at 100%. Future challenges include increasing the efficiency of clone production, reducing the dependence on a cross and making the system inducible.

Conclusion: The complete design

From the naïve view of a molecular geneticist, breeding can be summarized in two steps: to mix and to fix. The complete design would thus include a step of intense mixing (increased recombination) to provide new elite genotypes, that combine as many traits as desired, and then a step to fix and propagate the supreme individual at an industrial scale (apomixis or reverse breeding). Some genetic strategies have emerged recently to address these two issues, and one of the next challenges is to combine them. The other challenge is to transfer these technologies from model organisms like Arabidopsis to species as complex as wheat or rapeseed. Some obstacles stand in the way: the number of copies of each gene to tinker with due to polyploidy, the appropriate tools such as sequence information and mutant resources along with generation time and space limitations. However, there is no reason that the novel and future concepts developed in model plants could not be applied to crops.

Acknowledgements

We wish to thank Eric Jenczewski and Fabien Nogué for critical reading of the manuscript. Research in the Mercier lab is currently funded by the EU-FP7 program (Meiosys-KBBE-2009-222883), a European Research Council Starting Independent Researcher Grants (Meiosight-20101109), the French National Research Agency and the Rijk Zwaan Company.

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