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Self-incompatibility systems based on self-recognition evolved in hermaphroditic plants to maintain genetic variation of offspring and mitigate inbreeding depression. Despite these benefits in diploid plants, for polyploids who often face a scarcity of mating partners, self-incompatibility can thwart reproduction. In contrast, self- compatibility provides an immediate advantage: a route to reproductive viability. Thus, diploid selfing lineages may facilitate the formation of new allopolyploid species. Here, we describe the mechanism of establishment of at least four allopolyploid species in Brassicaceae ( Arabidopsis suecica , Arabidopsis kamchatica, Capsella bursa-pastoris, and Brassica napus ), in a manner dependent on the prior loss of the self-incompatibility mechanism in one of the ancestors. In each case, the degraded S -locus from one parental lineage was dominant over the functional S -locus of the outcrossing parental lineage. Such dominant loss-of-function mutations promote an immediate transition to selfing in allopolyploids and may facilitate their establishment.

Polyploidy is common and an important evolutionary factor in most land plant lineages, but it is rare in gymnosperms. Coast redwood (Sequoia sempervirens) is one of just two polyploid conifer species and the only hexaploid. Evidence from fossil guard cell size suggests that polyploidy in Sequoia dates to the Eocene. Numerous hypotheses about the mechanism of polyploidy and parental genome donors have been proposed, based primarily on morphological and cytological data, but it remains unclear how Sequoia became polyploid and why this lineage overcame an apparent gymnosperm barrier to whole-genome duplication (WGD). We sequenced transcriptomes and used phylogenetic inference, Bayesian concordance analysis and paralog age distributions to resolve relationships among gene copies in hexaploid coast redwood and close relatives. Our data show that hexaploidy in coast redwood is best explained by autopolyploidy or, if there was allopolyploidy, it happened within the Californian redwood clade. We found that duplicate genes have more similar sequences than expected, given the age of the inferred polyploidization. Conflict between molecular and fossil estimates of WGD can be explained if diploidization occurred very slowly following polyploidization. We extrapolate from this to suggest that the rarity of polyploidy in gymnosperms may be due to slow diploidization in this clade.

Understanding the relationship between macro- and microevolutionary processes and their delimitation remains a challenge. This review focuses on the role of chromosomal rearrangements in plant population differentiation and lineage diversification resulting in speciation, helping bridge the gap between macro- and microevolution through chromosomal evolution. We focus on angiosperms, a group that comprises the majority of extant plant species diversity and exhibits the largest chromosomal and genomic variations. Here, we address the following questions: Are macroevolutionary patterns of chromosome evolution the result of accumulated microevolutionary changes, or do chromosomal dynamics drive larger shifts along the speciation continuum? At the macroevolutionary level, we investigated the association between karyotype diversity and diversification rates using evidence from comparative genomics, chromosomal evolution modelling across phylogenies, and the association with several traits across different angiosperm lineages. At the microevolutionary level, we explore if different karyotypes are linked to morphological changes and population genetic differentiation in the same lineages. Polyploidy (autopolyploidy and allopolyploidy) and dysploidy are known drivers of speciation, with karyotypic differences often leading to reproductive barriers. We found that dysploidy, involving gains and losses of single chromosomes with no significant change in overall content of the genome, appears to be relatively more frequent and persistent across macroevolutionary histories than polyploidy. Additionally, chromosomal rearrangements that do not entail change in chromosome number, such as insertions, deletions, inversions, and duplications of chromosome fragments, as well as translocations between chromosomes, are increasingly recognized for their role in local adaptation and speciation. We argue that there is more evidence linking chromosomal rearrangements with genetic and morphological trait differentiation at microevolutionary scales than at macroevolutionary ones. Our findings highlight the importance of selection across evolutionary scales, where certain chromosomal dynamics become fixed over macroevolutionary time. Consequently, at microevolutionary scales, chromosome rearrangements are frequent and diverse, serving as key drivers of plant diversification and adaptation by providing a pool of variation from which beneficial chromosomal changes can be selected and fixed by evolutionary forces.

Abstract A transition to selfing can be beneficial when mating partners are scarce, for example, due to ploidy changes or at species range edges. Here, we explain how self-compatibility evolved in diploid Siberian Arabidopsis lyrata, and how it contributed to the establishment of allotetraploid Arabidopsis kamchatica. First, we provide chromosome-level genome assemblies for two self-fertilizing diploid A. lyrata accessions, one from North America and one from Siberia, including a fully assembled S-locus for the latter. We then propose a sequence of events leading to the loss of self-incompatibility in Siberian A. lyrata, date this independent transition to ∼90 Kya, and infer evolutionary relationships between Siberian and North American A. lyrata, showing an independent transition to selfing in Siberia. Finally, we provide evidence that this selfing Siberian A. lyrata lineage contributed to the formation of the allotetraploid A. kamchatica and propose that the selfing of the latter is mediated by the loss-of-function mutation in a dominant S-allele inherited from A. lyrata.

The majestic coast redwood (Sequoia sempervirens) is a California endemic tree of economic, ecological, and cultural value. Coast redwoods are also noteworthy due to their genomic composition; they are polyploid, having six copies of each chromosome rather than the two copies seen in almost all other conifers. It is known that polyploidy in Sequoia arose at least 34 millions years ago (Ma) because fossils from this era have stomatal guard-cells (known proxies for ploidy) whose size indicates polyploidy. Diverse mechanisms have been proposed to explain the origin of polyploidy in the coast redwood, and some authors have argued hybridization among multiple redwood lineages played a role. We sequenced leaf-expressed genes (a transcriptome) from all three redwood species and a close relative and used statistical analysis to show that polyploidy in coast redwood is unlikely to have involved hybridization. To further test this finding, we then sequenced a targeted subset of the genome for 8 redwood accessions and two outgroups. These data support the same conclusion: polyploidy did not involve hybridization among divergent species. We also used the sequences, combined with the fossil record, to infer the divergence dates of Sequoia from its sister group, giant sequoia (Sequoiadendron giganteum), and to determine when the different chromosomal copies of Sequoia genes last shared common ancestry. We found that the Sequoia and Sequoiadendron lineages diverged ~ 51 Ma, whereas most Sequoia gene copies diverged from one another ~13Ma. The latter date is noticeably much more recent than the polyploidy event itself (>34 Ma). We argued that this finding can be explained by inferring that the three pairs of genes (homeologs) in Sequoia exchanged genetic information long after polyploidization. This inference is consistent with observations that, even today, Sequoia chromosomes do not consistently pair up during cell division. Our elucidation of the complex genetics and genome history of the coast redwood provides important background information for efforts to ensure the long-term survival of this magnificent and iconic tree species in the face of rapid changes in the California climate.

Polyploidization or whole-genome duplication (WGD), followed by genome downsizing is a recurring evolutionary cycle with a significant impact on genome structure. Polyploidy originates from a cell cycle error and in species without a dedicated germline, mitotic as well as meiotic errors can be stably inherited. After the origin, polyploids face immediate challenges, particularly the need to adapt meiotic machinery to prevent improper chromosome pairing and segregation, such as multivalent formation. Over evolutionary timescales, surviving polyploids undergo rediploidization, reorganizing their genomes back to a diploid state. This study focuses on the evolution of a young allotetraploid Arabidopsis suecica, a hybrid species derived from A. thaliana and A. arenosa. Our genomic analyses reveal that A. suecica originated from diploid A. arenosa, contrary to earlier suggestions of a tetraploid origin, indicating that WGD in A. suecica likely occurred somatically rather than being inherited via unreduced gametes. Ecological niche modeling traces the geographic origin of A. suecica to the southeastern edge of the European glacier during the last ice age. We explore how A. suecica adapted to allopolyploidy from diploid ancestors and find evidence of positive selection on meiotic cell cycle genes in the A. arenosa sub-genome. Several of these genes overlap with those involved in autopolyploid adaptation in A. arenosa, but have distinct haplotypes. We also show that purifying selection is relaxed in A. suecica, however, functional compensation between homeologous gene pairs persists, with fewer gene pairs than expected having loss-of-function mutations in both copies. This is consistent with early signs of rediploidization just after ~16K years since the origin of A. suecica. Our study covers three key aspects of the evolution of allopolyploid A. suecica: origin, meiotic adaptation, and the beginning of rediploidization.Competing Interest StatementThe authors have declared no competing interest.

Whole-genome duplications yield varied chromosomal pairing patterns, ranging from strictly bivalent to multivalent, resulting in disomic and polysomic inheritance modes. In the bivalent case, homeologous chromosomes form pairs, where in a multivalent pattern all copies are homologous and are therefore free to pair and recombine. As sufficient sequencing data is more readily available than high-quality cytological assessments of meiotic behavior or population genetic assessment of allelic segregation, especially for non-model organisms, here we describe two bioinformatics approaches to infer origins and inheritance modes of polyploids using short-read sequencing data. The first approach is based on distributions of allelic read depth at the heterozygous sites within an individual, as the expectations of such distributions are different for disomic and polysomic inheritance modes. The second approach is more laborious and based on a phylogenetic assessment of partially phased haplotypes of a polyploid in comparison to the closest diploid relatives. We discuss the sources of deviations from expected inheritance patterns, advantages and pitfalls of both methods, effects of mating types on the performance of the methods, and possible future developments. Competing Interest Statement The authors have declared no competing interest.

A transition to selfing can be beneficial when mating partners are scarce, for example, due to ploidy changes or at species range edges. Here we explain how self-compatibility evolved in diploid Siberian Arabidopsis lyrata, and how it contributed to the establishment of allotetraploid A. kamchatica. First, we provide chromosome-level genome assemblies for two self-fertilizing diploid A. lyrata accessions, one from North America and one from Siberia, including a fully assembled S-locus for the latter. We then propose a sequence of events leading to the loss of self-incompatibility in Siberian A. lyrata, date this independent transition to ∼90 Kya, and infer evolutionary relationships between Siberian and North American A. lyrata, showing an independent transition to selfing in Siberia. Finally, we provide evidence that this selfing Siberian A. lyrata lineage contributed to the formation of the allotetraploid A. kamchatica and propose that the selfing of the latter is mediated by the loss-of-function mutation in a dominant S-allele inherited from A. lyrata.

Drought is a major limitation for survival and growth in plants. With more frequent and severe drought episodes occurring due to climate change, it is imperative to understand the genomic and physiological basis of drought tolerance to be able to predict how species will respond in the future. In this study, univariate and multitrait multivariate GWAS methods were used to identify candidate genes in two iconic and ecosystem-dominating species of the western US – coast redwood and giant sequoia – using ten drought-related physiological and anatomical traits and genome-wide sequence-capture SNPs. Population level phenotypic variation was found in carbon isotope discrimination, osmotic pressure at full turgor, xylem hydraulic diameter and total area of transporting fibers in both species. Our study identified new 78 new marker × trait associations in coast redwood and six in giant sequoia, with genes involved in a range of metabolic, stress and signaling pathways, among other functions. This study contributes to a better understanding of the genomic basis of drought tolerance in long-generation conifers and helps guide current and future conservation efforts in the species. Climate change brings more frequent and severe drought events that challenge the survival of natural populations of plants. While most of our knowledge about drought tolerance comes from annual and domesticated plants, the genomic basis of drought tolerance in long-generation trees is poorly understood. Here, we aim to fill this gap by identifying candidate genes in two conifer species, coast redwood and giant sequoia.

Whereas polyploidy is common and an important evolutionary factor in most land plant lineages it is a real rarity in gymnosperms. Coast redwood (Sequoia sempervirens) is the only hexaploid conifer and one of just two naturally polyploid conifer species. Numerous hypotheses about the mechanism of polyploidy in Sequoia and parental genome donors have been proffered over the years, primarily based on morphological and cytological data, but it remains unclear how Sequoia became polyploid and why this lineage overcame an apparent gymnosperm barrier to whole-genome duplication (WGD). We sequenced transcriptomes and used phylogenetic inference, Bayesian concordance analysis, and paralog age distributions to resolve relationships among gene copies in hexaploid coast redwood and its close relatives. Our data show that hexaploidy in the coast redwood lineage is best explained by autopolyploidy or, if there was allopolyploidy, this was restricted to within the Californian redwood clade. We found that duplicate genes have more similar sequences than would be expected given evidence from fossil guard cell size which suggest that polyploidy dates to the Eocene. Conflict between molecular and fossil estimates of WGD can be explained if diploidization occurred very slowly following whole genome duplication. We extrapolate from this to suggest that the rarity of polyploidy in conifers may be due to slow rates of diploidization in this clade.