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Regulation of homeologous recombination

Regulation of homeologous recombination

Research

Context and Issues

A polyploid species must have a regular meiosis generating genetically balanced gametes although it derives from species sharing a common ancestor. That necessitates inhibition of chromosomal pairing between related genomes (homeologous genomes) which can be due either to enough divergence between genomes or genetic control of pairing and recombination. Understanding of involved mechanisms can allow through their inhibition (1) either to increase frequencies of gene transfer from related species, (2) or to modify genome organization through increasing copy number of a genomic region of interest. In wheat, Ph1 gene carried by chromosome arm 5BL constitutes the major component of a genetic system inhibiting meiotic pairing between homoeologous chromosomes. The recessive mutation ph1b which is a deletion of a chromosomal segment with Ph1 induces recombination between wheat chromosomes and those of related species in interspecific hybrids or between wheat homoeologous chromosomes to (partially) isohomoeoallelic lines. In oilseed rape, we have shown that the level of pairing between genomes A and C in haploids of B. napus is essentially due to a major gene (PrBn for Pairing regulator in B. napus : Jenczewski et al., 2003). Understanding and utilization of both systems should allow higher efficiency in gene transfers.

Objectives

Understanding and utilization of both genetic control systems should allow higher efficiency in gene transfers in oilseed rape and bread wheat.

Methodology

In oilseed rape, programmes are developed in close collaboration with E. Jenczewski (IJPB, INRA Versailles) who is at the head of the project. We are presently studying (1) nature of preferential pairing generated by the PrBn system, (2) effect of that system on the regulation of homologous recombination, (3) effect of Arabidopsis candidate genes.

In wheat, the works are made in close collaboration with B. Chalhoub at INRA Evry. Our objective is to evaluate and characterize homoeologous within tetraploid synthetics derived from crosses between diploid wheat and Aegilops of the Sitopsis section.

Main Results

In oilseed rape, we have shown (1) that pairing in B. napus haploids is under control of a major QTL, PrBn and two or three minor QTLs with epistatic interactions (Jenczewski et al. 2003; Liu et al. 2006), (2) that system controls homoeologous recombination (Nicolas et al. 2007; 2009; 2012; Thesis S. Nicolas 2007), (3) that this system is related to the polyphyletic origin of oilseed rape (Cifuentes et al. 2010), (4) this control acts late in meiosis (Grandont et al. 2014). 

In the case of wheat, we analyzed the extent and pattern of genetic changes in relation to the meiotic behavior in synthetic wheat allotetraploids. Both inter-genomic translocations revealed by GISH and DNA rearrangments detected by molecular markers, were evidenced in these allotetraploids which level was correlated to that of homoeologous pairing. Genetic changes occurred only in some individual plants of a given allotetraploid and thus our study did not confirm previous claims on the extent and repeatability of genetic changes across generations and wheat polyploids. Our study suggests that wheat allotetraploids behave like other allopolyploid species, where homoeologous recombination represents the key mechanism of genetic changes.

Partners

  • UMR IJPB Versailles, France
  • UMR URGV Evry, France

Funding and Support

  • AAP BAP(2014-2015) (PI A.M. Chèvre): Caractérisation et mode d’action d’une machine à recombiner. Modèle Brassica
  • ANR CROC (2015-2018) (PI E. Jenczewski) : Controling Recombination rate in pOlyploid Crops
  • ANR Ploid-Ploid (2013-2015) (PI : B. Chalhoub)

Publications

Cifuentes M.*, Eber F.*, Lucas MO*, Lodé M., Chèvre A.M., Jenczewski E. (2010) Repeated polyploidy drove different levels of crossover suppression between homeologous chromosomes in Brassica napus allohaploids. The Plant Cell 22: 2265-276

Cifuentes M., Grandont L., Moore G., Chèvre A.M., Jenczewski E. (2010) Genetic regulation of meiosis in polyploid species: new insights into an old question. New Phytologist 186: 29-36

Dumur J, G. Branlard , A-M. Tanguy , M, Dardevet , O. Coriton , V. Huteau , J. Lemoine, J. Jahier  Development of isohomoeoallelic lines within the wheat cv. Courtot for high molecular weight glutenin subunits. Transfer of the Glu-D1 locus to chromosome 1A. Theor. Appl. Genet. DOI: 10.1007/s00122-009-1053-y

GRANDONT L., CUÑADO N., CORITON O., HUTEAU V., EBER F., CHÈVRE A.M.,GRELON M., CHELYSHEVA L., JENCZEWSKI E., 2014. Homoeologous Chromosome Sorting and Progression of Meiotic Recombination in Brassica napus: Ploidy Does Matter! Plant Cell doi/10.1105/tpc.114.122788

JENCZEWSKI E., EBER  F., GRIMAUD A., HUET S., LUCAS M.O., MONOD H., CHEVRE A.M., 2003. PrBn, a major gene controlling homoeologous pairing in oilseed rape (Brassica napus) haploids. Genetics 164 : 645-653

Liu Z., Adamczyk K., Manzanares-Dauleux M., Eber F., Lucas M.O., Delourme R., Chèvre A.M., Jenczewski E. (2006) Mapping PrBn and other quantitative trait loci responsible for the control of homoeologous chromosome pairing in oilseed rape (Brassica napus L.) haploids. Genetics 174: 1583-1596

NICOLAS S. (2007) Contrôle génétique de la recombinaison homéologue chez des haploïdes de colza (Brassica napus). Thèse de l’Université de Rennes I - Agrocampus Rennes. Mention : Biologie et Agronomie pp 188

NICOLAS S., LE MIGNON G., EBER F., CORITON O., MONOD H., CLOUET V., HUTEAU V., LOSTANLEN A., DELOURME R., CHALHOUB B., RYDER C., CHEVRE A.M., JENCZEWSKI E.,  2007. Homoeologous recombination plays a major role in chromosome rearrangments that occur during meiosis ofBrassica napushaploids. Genetics 175: 487-503

Nicolas S., Leflon M., Liu Z., Eber F., Chelysheva L., Coriton O., Chèvre A.M., Jenczewski E., 2008. Chromosome « speed dating » during meiosis of polyploid Brassica hybrids and haploids. Cytogenet Genome Res 120:331–338

Nicolas S., Leflon M., Monot H., Eber F., Coriton O., Huteau V., Chèvre A.M., Jenczewski E.,2009. Genetic regulation of meiotic crossovers between related genomes in Brassica napus haploids and hybrids. Plant Cell 21: 373-385.

Nicolas S., Monot H., Eber F., Chèvre A.M., Jenczewski E.,2012. Non random distribution of extensive chromosome rearrangements in Brassica napus depends on genome organization. The Plant Journal 70: 691-703