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The Gossypium genus is used to investigate emergent consequences of polyploidy in cotton species; comparative genomic analyses reveal a complex evolutionary history including interactions among subgenomes that result in genetic novelty in elite cottons and provide insight into the evolution of spinnable fibres. The evolution of domestic cotton plants A phylogenetic and genomic study of plants of the cotton genus Gossypium provides insights into the role of polyploidy in the angiosperm evolution, and specifically, in the emergence of spinnable fibres in domesticated cottons. The authors show that an abrupt five- to sixfold ploidy increase about 60 million years ago, and allopolyploidy reuniting divergent genomes approximately 1–2 million years ago, conferred a roughly 30-fold duplication of ancestral flowering plant genes in the 'elite' cottons G. hirsutum and G. barbadense compared to their presumed progenitor G. raimondii . Polyploidy often confers emergent properties, such as the higher fibre productivity and quality of tetraploid cottons than diploid cottons bred for the same environments 1 . Here we show that an abrupt five- to sixfold ploidy increase approximately 60 million years (Myr) ago, and allopolyploidy reuniting divergent Gossypium genomes approximately 1–2 Myr ago 2 , conferred about 30–36-fold duplication of ancestral angiosperm (flowering plant) genes in elite cottons ( Gossypium hirsutum and Gossypium barbadense ), genetic complexity equalled only by Brassica 3 among sequenced angiosperms. Nascent fibre evolution, before allopolyploidy, is elucidated by comparison of spinnable-fibred Gossypium herbaceum A and non-spinnable Gossypium longicalyx F genomes to one another and the outgroup D genome of non-spinnable Gossypium raimondii . The sequence of a G. hirsutum A t D t (in which ‘t’ indicates tetraploid) cultivar reveals many non-reciprocal DNA exchanges between subgenomes that may have contributed to phenotypic innovation and/or other emergent properties such as ecological adaptation by polyploids. Most DNA-level novelty in G. hirsutum recombines alleles from the D-genome progenitor native to its New World habitat and the Old World A-genome progenitor in which spinnable fibre evolved. Coordinated expression changes in proximal groups of functionally distinct genes, including a nuclear mitochondrial DNA block, may account for clusters of cotton-fibre quantitative trait loci affecting diverse traits. Opportunities abound for dissecting emergent properties of other polyploids, particularly angiosperms, by comparison to diploid progenitors and outgroups.

Partial resistance in plants generally exerts a low selective pressure on pathogens, and thus ensuring their durability in agrosystems. However, little is known about the effect of partial resistance on the molecular mechanisms of pathogenicity, a knowledge that could advance plant breeding for sustainable plant health. Here we investigate the gene expression of Phytophthora capsici during infection of pepper ( Capsicum annuum L.), where only partial genetic resistance is reported, using Illumina RNA-seq. Comparison of transcriptomes of P. capsici infecting susceptible and partially resistant peppers identified a small number of genes that redirected its own resources into lipid biosynthesis to subsist on partially resistant plants. The adapted and non-adapted isolates of P. capsici differed in expression of genes involved in nucleic acid synthesis and transporters. Transient ectopic expression of the RxLR effector genes CUST_2407 and CUST_16519 in pepper lines differing in resistance levels revealed specific host-isolate interactions that either triggered local necrotic lesions (hypersensitive response or HR) or elicited leave abscission (extreme resistance or ER), preventing the spread of the pathogen to healthy tissue. Although these effectors did not unequivocally explain the quantitative host resistance, our findings highlight the importance of plant genes limiting nutrient resources to select pepper cultivars with sustainable resistance to P. capsici .

Genetic diversity within and among populations lies at the heart of evolution. Unraveling the extent to which each intrinsic or extrinsic factor determines levels of diversity among genes, populations, and species is challenging, given the difficulty of isolating any single potentially important variable from all others. Allopolyploid species provide an opportunity to disentangle external and intrinsic factors, as the two (or more) homoeologous genomes co-occur in the same nucleus, often exhibiting high collinearity along homoeologous chromosomes. Here we evaluate the pace of molecular evolution and intraspecific, intragenomic diversity in two species of allopolyploid Gossypium, G. hirsutum and G. barbadense, using several hundred genes sequenced from multiple accessions of each species. Genie diversity in both species is low, having been influenced both by the polyploid bottleneck and a domestication bottleneck (for cultivated accessions), but with a directional bias in homoeolog diversity favoring the same genome in both allopolyploids. Total diversity is remarkably similar for the two homoeologous genomes overall, but the two copies of many gene pairs have accumulated statistically different diversity levels, and in a biased fashion with respect to genome. Domesticated accessions show reduced diversity in both genomes, as expected, but with a much greater reduction in one of the two homoeologous genomes. Furthermore, this biased reduction affects opposite homoeologous genomes in the two species. Interspecific introgression has played a role in shaping diversity within each species. Introgression was only detected for certain accessions, and only from G. barbadense into G. hirsutum in one of the two co-resident genomes.

Recombination is a major mechanism generating genetic diversity, but the control of the crossover rate remains a key question. In Brassica napus (AACC, 2n = 38), we can increase the homologous recombination between A genomes in AAC hybrids. Hypotheses for this effect include the number of C univalent chromosomes, the ratio between univalents and bivalents and, finally, which of the chromosomes are univalents. To test these hypotheses, we produced AA hybrids with zero, one, three, six or nine additional C chromosomes and four different hybrids carrying 2n = 32 and 2n = 35 chromosomes. The genetic map lengths for each hybrid were established to compare their recombination rates. The rates were 1.4 and 2.7 times higher in the hybrids having C6 or C9 alone than in the control (0C). This enhancement reached 3.1 and 4.1 times in hybrids carrying six and nine C chromosomes, and it was also higher for each pair of hybrids carrying 2n = 32 or 2n = 35 chromosomes, with a dependence on which chromosomes remained as univalents. We have shown, for the first time, that the presence of one chromosome, C9, affects significantly the recombination rate and reduces crossover interference. This result will have fundamental implications on the regulation of crossover frequency.

Allopolyploidy is an evolutionary and mechanistically intriguing process, in that it entails the reconciliation of two or more sets of diverged genomes and regulatory interactions. In this study, we explored gene expression patterns in interspecific hybrid F(1), and synthetic and natural allopolyploid cotton using RNA-Seq reads from leaf transcriptomes. We determined how the extent and direction of expression level dominance (total level of expression for both homoeologs) and homoeolog expression bias (relative contribution of homoeologs to the transcriptome) changed from hybridization through evolution at the polyploid level and following cotton domestication. Genome-wide expression level dominance was biased toward the A-genome in the diploid hybrid and natural allopolyploids, whereas the direction was reversed in the synthetic allopolyploid. This biased expression level dominance was mainly caused by up- or downregulation of the homoeolog from the 'non-dominant' parent. Extensive alterations in homoeolog expression bias and expression level dominance accompany the initial merger of two diverged diploid genomes, suggesting a combination of regulatory (cis or trans) and epigenetic interactions that may arise and propagate through the transcriptome network. The extent of homoeolog expression bias and expression level dominance increases over time, from genome merger through evolution at the polyploid level. Higher rates of transgressive and novel gene expression patterns as well as homoeolog silencing were observed in natural allopolyploids than in F(1) hybrid and synthetic allopolyploid cottons. These observations suggest that natural selection reconciles the regulatory mismatches caused by initial genomic merger, while new gene expression conditions are generated for evaluation by selection.

Allopolyploidy is an evolutionary and mechanistically intriguing process, in that it entails the reconciliation of two or more sets of diverged genomes and regulatory interactions. In this study, we explored gene expression patterns in interspecific hybrid F(1), and synthetic and natural allopolyploid cotton using RNA-Seq reads from leaf transcriptomes. We determined how the extent and direction of expression level dominance (total level of expression for both homoeologs) and homoeolog expression bias (relative contribution of homoeologs to the transcriptome) changed from hybridization through evolution at the polyploid level and following cotton domestication. Genome-wide expression level dominance was biased toward the A-genome in the diploid hybrid and natural allopolyploids, whereas the direction was reversed in the synthetic allopolyploid. This biased expression level dominance was mainly caused by up- or downregulation of the homoeolog from the 'non-dominant' parent. Extensive alterations in homoeolog expression bias and expression level dominance accompany the initial merger of two diverged diploid genomes, suggesting a combination of regulatory (cis or trans) and epigenetic interactions that may arise and propagate through the transcriptome network. The extent of homoeolog expression bias and expression level dominance increases over time, from genome merger through evolution at the polyploid level. Higher rates of transgressive and novel gene expression patterns as well as homoeolog silencing were observed in natural allopolyploids than in F(1) hybrid and synthetic allopolyploid cottons. These observations suggest that natural selection reconciles the regulatory mismatches caused by initial genomic merger, while new gene expression conditions are generated for evaluation by selection.

Summary In this study, we looked for genetic factors in the pepper (Capsicum annuum) germplasm that control the number of potato virus Y (PVY) particles entering the plant (i.e. effective population size at inoculation) and the PVY accumulation at the systemic level (i.e. census population size). Using genotyping‐by‐sequencing (GBS) in a core collection of 256 pepper accessions, we obtained 10 307 single nucleotide polymorphisms (SNPs) covering the whole genome. Genome‐wide association studies (GWAS) detected seven SNPs significantly associated with the virus population size at inoculation and/or systemic level on chromosomes 4, 6, 9 and 12. Two SNPs on chromosome 4 associated with both PVY population sizes map closely to the major resistance gene pvr2 encoding the eukaryotic initiation factor 4E. No obvious candidates for resistance were identified in the confidence intervals for the other chromosomes. SNPs detected on chromosomes 6 and 12 colocalized with resistance quantitative trait loci (QTLs) previously identified with a biparental population. These results show the efficiency of GBS and GWAS in C. annuum, indicate highly consistent results between GWAS and classical QTL mapping, and suggest that resistance QTLs identified with a biparental population are representative of a much larger collection of pepper accessions. Moreover, the resistance alleles at these different loci were more frequently combined than expected by chance in the core collection, indicating widespread pyramiding of resistance QTLs and widespread combination of resistance QTLs and major effect genes. Such pyramiding may increase resistance efficiency and/or durability.

Polyploids can be produced by the union of unreduced gametes or through somatic doubling of F₁ interspecific hybrids. The first route is suspected to produce allopolyploid species under natural conditions, whereas experimental data have only been thoroughly gathered for the latter. We analyzed the meiotic behavior of an F₁ interspecific hybrid (by crossing Brassica oleracea and B. rapa, progenitors of B. napus) and the extent to which recombined homoeologous chromosomes were transmitted to its progeny. These results were then compared with results obtained for a plant generated by somatic doubling of this F₁ hybrid (CD.S₀) and an amphidiploid (UG.S₀) formed via a pathway involving unreduced gametes; we studied the impact of this method of polyploid formation on subsequent generations. This study revealed that meiosis of the F₁ interspecific hybrid generated more gametes with recombined chromosomes than did meiosis of the plant produced by somatic doubling, although the size of these translocations was smaller. In the progeny of the UG.S₀ plant, there was an unexpected increase in the frequency at which the C1 chromosome was replaced by the A1 chromosome. We conclude that polyploid formation pathways differ in their genetic outcome. Our study opens up perspectives for the understanding of polyploid origins.

Understanding the relationship between domesticated crop species and their wild relatives is paramount to germplasm maintenance and the utilization of wild relatives in breeding programs. Recently, Gossypium ekmanianum was resurrected as an independent species based on morphological analysis of specimens obtained from the Dominican Republic, where the original type specimen was collected. The molecular data presented here support the recognition of G. ekmanianum Wittmack as a distinct species that is phylogenetically close to G. hirsutum L. Analyses of chloroplast DNA data reveal species-specific, indel polymorphisms that unambiguously distinguish G. ekmanianum samples from other polyploid congeners. Furthermore, analysis of accessions that originated from the Dominican Republic demonstrate the cryptic inclusion of this sister taxon within the US National Plant Germplasm System, a germplasm collection maintained for diversity preservation and future breeding resources. The data presented here indicate that “wild” G. hirsutum accessions may include the closely related G. ekmanianum, and provide a method to easily distinguish the two.

In this study, we looked for genetic factors in the pepper (Capsicum annuum) germplasm that control the number of potato virus Y (PVY) particles entering the plant (i.e. effective population size at inoculation) and the PVY accumulation at the systemic level (i.e. census population size). Using genotyping-by-sequencing (GBS) in a core collection of 256 pepper accessions, we obtained 10 307 single nucleotide polymorphisms (SNPs) covering the whole genome. Genome-wide association studies (GWAS) detected seven SNPs significantly associated with the virus population size at inoculation and/or systemic level on chromosomes 4, 6, 9 and 12. Two SNPs on chromosome 4 associated with both PVY population sizes map closely to the major resistance gene pvr2 encoding the eukaryotic initiation factor 4E. No obvious candidates for resistance were identified in the confidence intervals for the other chromosomes. SNPs detected on chromosomes 6 and 12 colocalized with resistance quantitative trait loci (QTLs) previously identified with a biparental population. These results show the efficiency of GBS and GWAS in C. annuum, indicate highly consistent results between GWAS and classical QTL mapping, and suggest that resistance QTLs identified with a biparental population are representative of a much larger collection of pepper accessions. Moreover, the resistance alleles at these different loci were more frequently combined than expected by chance in the core collection, indicating widespread pyramiding of resistance QTLs and widespread combination of resistance QTLs and major effect genes. Such pyramiding may increase resistance efficiency and/or durability.