All Ways Lead to Rome—Meiotic Stabilization Can Take Many Routes in Nascent Polyploid Plants

Newly formed polyploids often show extensive meiotic defects, resulting in aneuploid gametes, and thus reduced fertility. However, while many neopolyploids are meiotically unstable, polyploid lineages that survive in nature are generally stable and fertile; thus, those lineages that survive are those that are able to overcome these challenges. Several genes that promote polyploid stabilization are now known in plants, allowing speculation on the evolutionary origin of these meiotic adjustments. Here, I discuss results that show that meiotic stability can be achieved through the differentiation of certain alleles of certain genes between ploidies. These alleles, at least sometimes, seem to arise by novel mutation, while standing variation in either ancestral diploids or related polyploids, from which alleles can introgress, may also contribute. Growing evidence also suggests that the coevolution of multiple interacting genes has contributed to polyploid stabilization, and in allopolyploids, the return of duplicated genes to single copies (genome fractionation) may also play a role in meiotic stabilization. There is also some evidence that epigenetic regulation may be important, which can help explain why some polyploid lineages can partly stabilize quite rapidly.

Genetic factors inherited from both diploid parents interact to affect genome stability and fertility in resynthesized allotetraploid B. napus

The genetic diversity in Brassica napus (canola, rapeseed) is limited because of few hybridization events and selection for important oil quality traits. One possible means of overcoming this challenge is through resynthesizing B. napus hybrids by crossing the diploid parents in order to broaden its gene pool. However, resynthesized B. napus lines are often unstable and infertile, unlike B. napus cultivars. Meiotic stability in established B. napus may have arisen through allele inheritance from the progenitor species. We tested this hypothesis by characterizing 41 resynthesized B. napus lines produced by crosses between eight B. rapa and eight B. oleracea lines for copy number variation resulting from non-homologous recombination events, allele inheritance, and fertility. We resequenced eight B. rapa and five B. oleracea parent accessions, and analyzed the allelic variation in a list of meiosis gene homologs. SNP genotyping was performed using the Illumina Infinium Brassica 60K array for three individuals per line. Self-pollinated seed-set and genome stability (number of copy number variants) were significantly affected by the interaction between both B. rapa and B. oleracea parental genotypes. We identified two putative meiosis gene candidates ( HEI10 and MCM8 ) which were significantly associated with meiosis and/or fertility as well as genome stability. Our results support the hypothesis that allelic variants inherited from parental genotypes affect genome stability and fertility in resynthesized rapeseed.

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.

A novel allele of ASY3 promotes meiotic stability in autotetraploid Arabidopsis lyrata

In this study we performed a genotype-phenotype association analysis of meiotic stability in ten autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations collected from the Wachau region and East Austrian Forealps. The aim was to determine the effect of eight meiosis genes under extreme selection upon adaptation to whole genome duplication. Individual plants were genotyped by high-throughput sequencing of the eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation and phenotyped by assessing meiotic metaphase I chromosome configurations. Our results reveal that meiotic stability varied greatly (20-100%) between individual tetraploid plants and was associated with segregation of a novel allele orthologous to the budding yeast RED1 chromosome axis protein, Asynapsis3 (ASY3), derived from A. lyrata. The adaptive ASY3 protein possesses a putative in-frame tandem duplication (TD) of a serine-rich region upstream of the coiled-coil domain that has arisen at sites of DNA microhomology. The frequency of multivalents observed in plants homozygous for the ASY3 TD haplotype was significantly lower than plants heterozygous for TD/ND (non-duplicated) ASY3 haplotypes. Chiasma distribution was significantly altered in the stable plants compared to the unstable plants with a shift from proximal and interstitial to predominantly distal locations. The number of HEI10 foci at pachtyene that mark class I crossovers was significantly reduced in meiotic nuclei from ASY3 TD homozygous plants compared to ASY3 ND/TD heterozygotes, indicating an adaptive consequence of the ASY3 TD allele. From the ten populations, fifty-eight alleles of these 8 meiosis genes were identified, demonstrating dynamic population variability at these loci which nevertheless exhibit signatures of strong hard selective sweeps. Widespread chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them.Author summaryWhole genome duplication can promote adaptability, but is a dramatic mutation usually resulting in meiotic catastrophe and genome instability. Here we focus on a case of coordinated stabilization of meiotic recombination in ten autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations from the Wachau region and East Austrian Forealps. We fuse population genomic data with a genotype-phenotype association study, concentrating on the effects of eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation in the tetraploids under extreme selection. Our analysis demonstrates that a novel allele of the meiotic chromosome axis protein Asynapsis3 that contains an in-frame duplication of a serine-rich region is the major determinant of male meiotic stability. This adaptive restabilisation appears to be achieved by a reduction in the number of meiotic crossovers as well as a shift in their positioning towards the chromosome ends. Of the eight genes, fifty-eight alleles were identified, indicating dynamic population variability at these loci under extreme selection. In addition, widespread allelic chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them.

Cytogenetic and molecular characteristics of rye genome in octoploid triticale (× Triticosecale Wittmack)

Alloploidization resulting from remote (interspecific or intergeneric) hybridization is one of the main factors in plant evolution, leading to the formation of new species. Triticale (× Triticosecale Wittmack, 1889) is the first artificial species created by crossing wheat (Triticum spp.) and rye (Secale cereale Linnaeus, 1753) and has a great potential as a grain and forage crop. Remote hybridization is a stress factor that causes a rapid reorganization of the parental genomes in hybrid progeny (“genomic shock”) and is accompanied by abnormalities in the chromosome set of hybrids. The formation of the hybrid genome and its subsequent stabilization are directly related to the normalization of meiosis and the correct chromosome segregation. The aim of this work was to cytogenetically characterize triticale (× Triticosecale rimpaui Wittmack, 1899, AABBDDRR) obtained by crossing Triticum aestivum Linnaeus, 1753. Triple Dirk D × Secale cereale L. Korotkostebel’naya 69 in F3–F6 generations of hybrids, and to trace the process of genetic stabilization of hybrid genomes. Also, a comparative analysis of the nucleotide sequences of the centromeric histone CENH3 genes was performed in wheat-rye allopolyploids of various ploidy as well as their parental forms. In the hybrid genomes of octoploid triticale an increased expression of the rye CENH3 variants was detected. The octoploid triticale plants contain complete chromosome sets of the parental subgenomes maintaining the chromosome balance and meiotic stability. For three generations the percentage of aneuploids in the progeny of such plants has been gradually decreasing, and they maintain a complete set of the paternal rye chromosomes. However, the emergence of hexaploid and new aneuploid plants in F5 and F6 generations indicates that stabilization of the hybrid genome is not complete yet. This conclusion was confirmed by the analysis of morphological features in hybrid plants: the progeny of one plant having the whole chromosome sets of parental subgenomes showed significant morphological variations in awn length and spike density. Thus, we expect that the results of our karyotyping of octoploid triticales obtained by crossing hexaploid wheat to diploid rye supplemented by comparative analysis of CENH3 sequences will be applicable to targeted breeding of stable octo- and hexaploid hybrids.

Oligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis ×hytivus with dysploid parental karyotypes

Background Meiosis of newly formed allopolyploids frequently encounter perturbations induced by the merging of divergent and hybridizable genomes. However, to date, the meiotic properties of allopolyploids with dysploid parental karyotypes have not been studied in detail. The allotetraploid Cucumis ×hytivus (HHCC, 2n = 38) was obtained from interspecific hybridization between C. sativus (CC, 2n = 14) and C. hystrix (HH, 2n = 24) followed by chromosome doubling. The results of this study thus offer an excellent opportunity to explore the meiotic properties of allopolyploids with dysploid parental karyotypes. Results In this report, we describe the meiotic properties of five chromosomes (C5, C7, H1, H9 and H10) and two genomes in interspecific hybrids and C. ×hytivus (the 4th and 14th inbred family) through oligo-painting and genomic in situ hybridization (GISH). We show that 1) only two translocations carrying C5-oligo signals were detected on the chromosomes C2 and C4 of one 14th individual by the karyotyping of eight 4th and 36 14th plants based on C5- and C7-oligo painting, and possible cytological evidence was observed in meiosis of the 4th generation; 2) individual chromosome have biases for homoeologous pairing and univalent formation in F1 hybrids and allotetraploids; 3) extensive H-chromosome autosyndetic pairings (e.g., H-H, 25.5% PMCs) were observed in interspecific F1 hybrid, whereas no C-chromosome autosyndetic pairings were observed (e.g. C-C); 4) the meiotic properties of two subgenomes have significant biases in allotetraploids: H-subgenome exhibits higher univalent and chromosome lagging frequencies than C-subgenome; and 5) increased meiotic stability in the S14 generation compared with the S4 generation, including synchronous meiosis behavior, reduced incidents of univalent and chromosome lagging. Conclusions These results suggest that the meiotic behavior of two subgenomes has dramatic biases in response to interspecific hybridization and allopolyploidization, and the meiotic behavior harmony of subgenomes is a key subject of meiosis evolution in C. ×hytivus. This study helps to elucidate the meiotic properties and evolution of nascent allopolyploids with the dysploid parental karyotypes.

Domestication in Real Time: The Curious Case of a Trigenomic Sunflower Population

This study chronicles the ongoing process to domesticate an interspecific trigenomic tetraploid hybrid sunflower derived from a series of interspecific crosses between Helianthus annuus and Helianthus tuberosus. The goal of this process is to develop a perennial oilseed crop that can produce both high value vegetable oil and continuous ground-cover. Selection has focused on developing an ideotype with the domesticated morphology of H. annuus and the below-ground perennial features of H. tuberosus. The overarching challenge in the process of breeding and domesticating this interspecific perennial sunflower is overcoming obstacles associated with interploid meiosis in order to resolve a chromosomally stable hybrid population. As selection progresses through generations of intermating, there are improvements toward the desired ideotype, but selection efficiency is slowed by apparent antagonisms between annual- and perennial morphological targets and irregular meiosis which is especially problematic in a trigenomic tetraploid. This shows that keys toward perennial crop development through interspecific hybridization will be to capitalize on the abundant phenotypic variation within our population, achieve meiotic stability in order to maximize selection efficiency, and to break genetic correlations between annual and perennial traits.

Interspecific introgression mediates adaptation to whole genome duplication

Adaptive gene flow is a consequential evolutionary phenomenon across all kingdoms of life. While recognition of widespread gene flow is growing, examples lack of bidirectional gene flow mediating adaptations at specific loci that cooperatively manage core cellular processes. We previously described concerted molecular changes among physically interacting members of the meiotic machinery controlling crossover number and distribution upon adaptation to whole genome duplication (WGD) in Arabidopsis arenosa. Here we conduct a population genomic study to test the hypothesis that escape from extinction following the trauma of WGD was mediated by adaptive gene flow between A. arenosa and its congener Arabidopsis lyrata. We show that A. lyrata underwent WGD more recently than A. arenosa, indicating that specific pre-adapted alleles donated by A. arenosa underwent selection and rescued the nascent A. lyrata tetraploids from early extinction. At the same time, we detect specific signals of gene flow in the opposite direction at other functionally interacting gene coding loci that display dramatic signatures of selective sweep in both tetraploid species. Cytological analysis shows that A. lyrata tetraploids exhibit similar levels of meiotic stability as A. arenosa tetraploids. Taken together, these data indicate that bidirectional gene flow allowed for an escape from extinction of the young autopolyploids, especially the rare tetraploid A. lyrata, and suggest that the merger of these species is greater than the sum of their parts.