Spontaneous generation of diversity in Arachis neopolyploids (A. ipaënsis x A. duranensis)4x replays the early stages of peanut evolution

Polyploidy is considered a driving force in plant evolution and domestication. Although in the genus Arachis, several diploid species were traditionally cultivated for their seeds, only the allotetraploid peanut Arachis hypogaea became the successful, widely spread legume crop. This suggests that polyploidy has given selective advantage for domestication of peanut. Here we study induced allotetraploid (neopolyploid) lineages obtained from crosses between the peanut’s progenitor species, A. ipaënsis and A. duranensis, at earlier and later generations. We observed plant morphology, seed dimensions, and genome structure using cytogenetics (FISH and GISH) and SNP genotyping. The neopolyploid lineages show more variable fertility and seed morphology than their progenitors and cultivated peanut. They also showed sexual and somatic genome instability, evidenced by changes of number of detectable 45S rDNA sites, and extensive homoeologous recombination indicated by mosaic patterns of chromosomes and changes in dosage of SNP alleles derived from the diploid species. Genome instability was not randomly distributed across the genome: the more syntenic chromosomes, the higher homoeologous recombination. Instability levels are higher than observed on peanut lines, therefore it is likely that more unstable lines tend to perish. We conclude that early stages of the origin and domestication of the allotetraploid peanut involved two genetic bottlenecks: the first, common to most allotetraploids, is composed of the rare hybridization and polyploidization events, followed by sexual reproductive isolation from its wild diploid relatives. Here we suggest a second bottleneck: the survival of the only very few lineages that had stronger mechanisms for limiting genomic instability.

Homoeologous recombination is recurrent in the nascent synthetic allotetraploid Arachis ipaënsis × Arachis correntina4x and its derivatives

Genome instability in newly synthesized allotetraploids of peanut has breeding implications that have not been fully appreciated. Synthesis of wild species-derived neo-tetraploids offers the opportunity to broaden the gene pool of peanut; however, the dynamics among the newly merged genomes creates predictable and unpredictable variation. Selfed progenies from the neo-tetraploid Arachis ipaënsis × Arachis correntina (A. ipaënsis × A. correntina)4x and F1 hybrids and F2 progenies from crosses between A. hypogaea × [A. ipaënsis × A. correntina]4x were genotyped by the Axiom Arachis 48 K SNP array. Homoeologous recombination between the A. ipaënsis and A. correntina derived subgenomes was observed in the S0 generation. Among the S1 progenies, these recombined segments segregated and new events of homoeologous recombination emerged. The genomic regions undergoing homoeologous recombination segregated mostly disomically in the F2 progenies from A. hypogaea × [A. ipaënsis × A. correntina]4x crosses. New homoeologous recombination events also occurred in the F2 population, mostly found on chromosomes 03, 04, 05, and 06. From the breeding perspective, these phenomena offer both possibilities and perils; recombination between genomes increases genetic diversity, but genome instability could lead to instability of traits or even loss of viability within lineages.

Ph2 encodes the mismatch repair protein MSH7-3D that inhibits wheat homoeologous recombination

Meiotic recombination is a critical process for plant breeding, as it creates novel allele combinations that can be exploited for crop improvement. In wheat, a complex allohexaploid that has a diploid-like behaviour, meiotic recombination between homoeologous or alien chromosomes is suppressed through the action of several loci. Here, we report positional cloning of Pairing homoeologous 2 (Ph2) and functional validation of the wheat DNA mismatch repair protein MSH7-3D as a key inhibitor of homoeologous recombination, thus solving a half-century-old question. Similar to ph2 mutant phenotype, we show that mutating MSH7-3D induces a substantial increase in homoeologous recombination (up to 5.5 fold) in wheat-wild relative hybrids, which is also associated with a reduction in homologous recombination. These data reveal a role for MSH7-3D in meiotic stabilisation of allopolyploidy and provides an opportunity to improve wheat’s genetic diversity through alien gene introgression, a major bottleneck facing crop improvement.

Chromosome inheritance and meiotic stability in allopolyploidBrassica napus

Homoeologous recombination, aneuploidy, and other genetic changes are common in resynthesized allopolyploid Brassica napus. In contrast, the chromosomes of cultivars have long been considered to be meiotically stable. To gain a better understanding of the underlying mechanisms leading to stabilization in the allopolyploid, the behavior of chromosomes during meiosis can be compared by unambiguous chromosome identification between resynthesized and natural B. napus. Compared with natural B. napus, resynthesized lines show high rates of nonhomologous centromere association, homoeologous recombination leading to translocation, homoeologous chromosome replacement, and association and breakage of 45S rDNA loci. In both natural and resynthesized B. napus, we observed low rates of univalents, A–C bivalents, and early sister chromatid separations. Reciprocal homoeologous chromosome exchanges and double reductions were photographed for the first time in meiotic telophase I. Meiotic errors were non-uniformly distributed across the genome in resynthesized B. napus, and in particular homoeologs sharing synteny along their entire length exhibited multivalents at diakinesis and polysomic inheritance at telophase I. Natural B. napus appeared to resolve meiotic errors mainly by suppressing homoeologous pairing, resolving nonhomologous centromere associations and 45S rDNA associations before diakinesis, and reducing homoeologous cross-overs.

Homoeologous Recombination: A Novel and Efficient System for Broadening the Genetic Variability in Wheat

Gene transfer from wild wheat relatives to bread wheat is restricted to homologous recombination. The presence of the Pairing homoeologous 1 (Ph1) gene in the long arm of wheat chromosome 5B allows only homologous chromosomes to pair and recombine, resulting in diploid inheritance of polyploid wheat. Previously, we identified a potent homoeologous pairing promotor gene(s) (Hpp-5Mg); its carrier chromosome 5Mg derived from Aegilops geniculata and its wheat homoeologous chromosome 5D freely recombined in the presence of the Ph1 gene. In this study, we investigated the effect of Hpp-5Mg on homoeologous recombination in the absence of Ph1. In Hpp-5Mg/ph1bph1b plants, we observed a vast genome-wide increase in homoeologous recombination and multiple crossovers (CO), including CO breakpoints in proximal regions of the chromosomes where recombination is known to be suppressed. We tested the efficacy of Hpp-5Mg/ph1bph1b-induced homoeologous recombination by producing new recombinants for the wheat streak mosaic virus resistance gene, Wsm3, present in the wheat-Thinopyrum intermedium Robertsonian translocation (RobT T7BS.7S#3L). A recombination frequency of 6.5% was detected by screening the progenies double monosomic for T7BS.7S#3L and 7B by genomic in situ hybridization. This recombination frequency was about 100-fold higher compared with the recombinant frequency of 0.06% observed by using ph1b-induced homoeologous recombination alone. Our results indicate that chromosome 5Mg promotes homoeologous recombination between wheat and wild wheat relative chromosomes, which helps in the generation of pre-breeding materials thereby accelerating wheat crop improvement.