Chromosomal inversions have the potential to play an important role in evolution by reducing recombination between favorable combinations of alleles. Until recently, however, most evidence for their ...likely importance derived from dipteran flies, whose giant larval salivary chromosomes aided early cytogenetic studies. The widespread application of new genomic technologies has revealed that inversions are ubiquitous across much of the plant and animal kingdoms. Here we review the rapidly accumulating literature on inversions in the plant kingdom and discuss what we have learned about their establishment and likely evolutionary role. We show that inversions are prevalent across a wide range of plant groups. We find that inversions are often associated with locally favored traits, as well as with traits that contribute to assortative mating, suggesting that they may be key to adaptation and speciation in the face of gene flow. We also discuss the role of inversions in sex chromosome formation, and explore possible parallels with inversion establishment on autosomes. The identification of inversion origins, as well as the causal variants within them, will advance our understanding of chromosomal evolution in plants.
Genomic studies often attempt to link natural genetic variation with important phenotypic variation. To succeed, robust and reliable phenotypic data, as well as curated genomic assemblies, are ...required. Wild sunflowers, originally from North America, are adapted to diverse and often extreme environments and have historically been a widely used model plant system for the study of population genomics, adaptation, and speciation. Moreover, cultivated sunflower, domesticated from a wild relative (Helianthus annuus) is a global oil crop, ranking fourth in production of vegetable oils worldwide. Public availability of data resources both for the plant research community and for the associated agricultural sector, are extremely valuable. We have created HeliantHOME ( http://www.helianthome.org ), a curated, public, and interactive database of phenotypes including developmental, structural and environmental ones, obtained from a large collection of both wild and cultivated sunflower individuals. Additionally, the database is enriched with external genomic data and results of genome-wide association studies. Finally, being a community open-source platform, HeliantHOME is expected to expand as new knowledge and resources become available.
Both models and case studies suggest that chromosomal inversions can facilitate adaptation and speciation in the presence of gene flow by suppressing recombination between locally adapted alleles. ...Until recently, however, it has been laborious and time‐consuming to identify and genotype inversions in natural populations. Here we apply RAD sequencing data and newly developed population genomic approaches to identify putative inversions that differentiate a sand dune ecotype of the prairie sunflower (Helianthus petiolaris) from populations found on the adjacent sand sheet. We detected seven large genomic regions that exhibit a different population structure than the rest of the genome and that vary in frequency between dune and nondune populations. These regions also show high linkage disequilibrium and high heterozygosity between, but not within, arrangements, consistent with the behaviour of large inversions, an inference subsequently validated in part by comparative genetic mapping. Genome–environment association analyses show that key environmental variables, including vegetation cover and soil nitrogen, are significantly associated with inversions. The inversions colocate with previously described “islands of differentiation,” and appear to play an important role in adaptive divergence and incipient speciation within H. petiolaris.
see also the Perspective by Claire Mérot.
Sunflowers of the genus Helianthus are models for hybridization research and contain three of the best-studied examples of homoploid hybrid speciation. To understand a broader picture of ...hybridization within the annual sunflowers, we used whole-genome resequencing to conduct a phylogenomic analysis and test for gene flow between lineages. We find that all annual sunflower species tested have evidence of admixture, suggesting hybridization was common during the radiation of the genus. Support for the major species tree decreases with increasing recombination rate, consistent with hybridization and introgression contributing to discordant topologies. Admixture graphs found hybridization to be associated with the origins of the three putative hybrid species (Helianthus anomalus, Helianthus deserticola, and Helianthus paradoxus). However, the hybridization events are more ancient than suggested by previous work. Furthermore, H. anomalus and H. deserticola appear to have arisen from a single hybridization event involving an unexpected donor, rather than through multiple independent events as previously proposed. This means our results are consistent with, but not definitive proof of, two ancient independent homoploid hybrid speciation events in the genus. Using a broader data set that covers the whole Helianthus genus, including perennial species, we find that signals of introgression span the genus and beyond, suggesting highly divergent introgression and/or the sorting of ancient haplotypes. Thus, Helianthus can be viewed as a syngameon in which largely reproductively isolated species are linked together by occasional or frequent gene flow.
Species often include multiple ecotypes that are adapted to different environments1. However, it is unclear how ecotypes arise and how their distinctive combinations of adaptive alleles are ...maintained despite hybridization with non-adapted populations2-4. Here, by resequencing 1,506 wild sunflowers from 3 species (Helianthus annuus, Helianthus petiolaris and Helianthus argophyllus), we identify 37 large (1-100 Mbp in size), non-recombining haplotype blocks that are associated with numerous ecologically relevant traits, as well as soil and climate characteristics. Limited recombination in these haplotype blocks keeps adaptive alleles together, and these regions differentiate sunflower ecotypes. For example, haplotype blocks control a 77-day difference in flowering between ecotypes ofthe silverleaf sunflower H. argophyllus (probably through deletion of a homologue of FLOWERING LOCUS T (FT)), and are associated with seed size, flowering time and soil fertility in dune-adapted sunflowers. These haplotypes are highly divergent, frequently associated with structural variants and often appear to represent introgressions from other-possibly now-extinct-congeners. These results highlight a pervasive role of structural variation in ecotypic adaptation.
and
cause Phomopsis stem canker of sunflower (
L.) in the United States. Because Phomopsis stem canker did not gain importance until the disease epidemic in 2010, limited studies were conducted to ...understand the genetic basis of sunflower resistance to
and
. The objectives of this study were to evaluate the United States Department of Agriculture cultivated accessions for resistance to
and
as well as to utilize genome-wide association studies (GWAS) to identify quantitative trait loci (QTLs) and putative candidate genes underlying those loci common to both organisms. For each fungus, 213 accessions were screened in a complete randomized design in the greenhouse and the experiment was repeated once. Six plants per accession were inoculated with a single isolate of
or
at four to six true leaves using the mycelium-contact inoculation method. At 15 days (
) and 30 days (
) postinoculation, accessions were evaluated for disease severity and compared with the susceptible confection inbred PI 552934. GWAS identified 28 QTLs common to the two fungi, and 24 genes overlapped close to these QTLs. Additionally, it was observed that the resistance QTLs derived mainly from landraces rather than from wild species. Seventeen putative candidate genes associated with resistance to
or
were identified that may be related to plant-pathogen interactions. These findings advanced our understanding of the genetic basis of resistance to
and
and will help develop resources for genomics-assisted breeding.
Abstract
Recombination is critical both for accelerating adaptation and purging deleterious mutations. Chromosomal inversions can act as recombination modifiers that suppress local recombination in ...heterozygotes and thus, under some conditions, are predicted to accumulate such mutations. In this study, we investigated patterns of recombination, transposable element abundance, and coding sequence evolution across the genomes of 1,445 individuals from three sunflower species, as well as within nine inversions segregating within species. We also analyzed the effects of inversion genotypes on 87 phenotypic traits to test for overdominance. We found significant negative correlations of long terminal repeat retrotransposon abundance and deleterious mutations with recombination rates across the genome in all three species. However, we failed to detect an increase in these features in the inversions, except for a modest increase in the proportion of stop codon mutations in several very large or rare inversions. Consistent with this finding, there was little evidence of overdominance of inversions in phenotypes that may relate to fitness. On the other hand, significantly greater load was observed for inversions in populations polymorphic for a given inversion compared to populations monomorphic for one of the arrangements, suggesting that the local state of inversion polymorphism affects deleterious load. These seemingly contradictory results can be explained by the low frequency of inversion heterozygotes in wild sunflower populations, apparently due to divergent selection and associated geographic structure. Inversions contributing to local adaptation represent ideal recombination modifiers, acting to facilitate adaptive divergence with gene flow, while largely escaping the accumulation of deleterious mutations.
Abstract
Speciation in the face of gene flow is usually associated with a heterogeneous genomic landscape of divergence in nascent species pairs. However, multiple factors, such as divergent ...selection and local recombination rate variation, can influence the formation of these genomic islands. Examination of the genomic landscapes of species pairs that are still in the early stages of speciation provides an insight into this conundrum. In this study, population genomic analyses were undertaken using a wide range of sampling and whole-genome resequencing data from 96 unrelated individuals of Kentish plover (Charadrius alexandrinus) and white-faced plover (Charadrius dealbatus). We suggest that the two species exhibit varying levels of population admixture along the Chinese coast and on the Taiwan Island. Genome-wide analyses for introgression indicate that ancient introgression had occurred in Taiwan population, and gene flow is still ongoing in mainland coastal populations. Furthermore, we identified a few genomic regions with significant levels of interspecific differentiation and local recombination suppression, which contain several genes potentially associated with disease resistance, coloration, and regulation of plumage molting and thus may be relevant to the phenotypic and ecological divergence of the two nascent species. Overall, our findings suggest that divergent selection in low recombination regions may be a main force in shaping the genomic islands in two incipient shorebird species.
SUMMARY
Adaptation to new environments is a key evolutionary process which presumably involves complex genomic changes. Mangroves, a collection of approximately 80 woody plants that have ...independently invaded intertidal zones >20 times, are ideal for studying this process. We assembled near‐chromosome‐scale genomes of three Xylocarpus species as well as an outgroup species using single‐molecule real‐time sequencing. Phylogenomic analysis reveals two separate lineages, one with the mangrove Xylocarpus granatum and the other comprising a mangrove Xylocarpus moluccensis and a terrestrial Xylocarpus rumphii. In conjunction with previous studies, we identified several genomic features associated with mangroves: (i) signals of positive selection in genes related to salt tolerance and root development; (ii) genome‐wide elevated ratios of non‐synonymous to synonymous substitution relative to terrestrial relatives; and (iii) active elimination of long terminal repeats. These features are found in the terrestrial X. rumphii in addition to the two mangroves. These genomic features, not being strictly mangrove‐specific, are hence considered pre‐adaptive. We infer that the coastal but non‐intertidal habitat of X. rumphii may have predisposed the common ancestor to invasion of true mangrove habitats. Other features including the preferential retention of duplicated genes and intolerance to pseudogenization are not found in X. rumphii and are likely true adaptive features in mangroves. In conclusion, by studying adaptive shift and partial shifts among closely related species, we set up a framework to study genomic features that are acquired at different stages of the pre‐adaptation and adaptation to new environments.
Significance Statement
We sequenced and assembled high‐quality genomes for three Xylocarpus species and one Swietenia species using single‐molecule real‐time sequencing. By illustrating genomic features acquired in different stages of the complex process of adapting to the extreme intertidal environments, we provide evidences for pre‐adaptation and adaptation in different stages of transition to a new environment
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