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The shift from outcrossing to selfing is common in flowering plants, but the genomic consequences and the speed at which they emerge remain poorly understood. An excellent model for understanding the evolution of self fertilization is provided by Capsella rubella, which became self compatible <200,000 years ago. We report a C. rubella reference genome sequence and compare RNA expression and polymorphism patterns between C. rubella and its outcrossing progenitor Capsella grandiflora. We found a clear shift in the expression of genes associated with flowering phenotypes, similar to that seen in Arabidopsis, in which self fertilization evolved about 1 million years ago. Comparisons of the two Capsella species showed evidence of rapid genome-wide relaxation of purifying selection in C. rubella without a concomitant change in transposable element abundance. Overall we document that the transition to selfing may be typified by parallel shifts in gene expression, along with a measurable reduction of purifying selection.

Pollen-specific receptor-like kinase 6 (PRK6), which signals through the guanine nucleotide-exchange factors ROPGEFs, is required for sensing of the LURE1 attractant peptide in Arabidopsis thaliana , and functions together with other PRK family kinases; when introduced into the pollen tubes of the related species Capsella rubella , PRK6 could confer responsiveness to AtLURE1. Multiple pollen-tube receptors for LURE1 In flowering plants, the female gametophyte secretes chemoattractant peptides to guide pollen tube growth so that it delivers the immobile sperm to the ovule-enclosed female gametophyte. Two papers published in this issue of Nature report the identification of male pollen tube cell-surface receptors for one of these female attractants, LURE1, in the model plant Arabidopsis thaliana . Wei-Cai Yang and colleagues show that LURE1 is perceived by a receptor-like kinase complex, the heteromer MDIS1–MIK. Tetsuya Higashiyama and Hidenori Takeuchi report that pollen-specific receptor-like kinase 6 (PRK6) is required for sensing LURE1, and PRK6 acts together with other PRK family receptors. Both groups demonstrate that by engineering pollen tubes of the sister species Capsella rubella to express a component of the A. thaliana receptors — either MDIS1 or PRK6 — the reproductive isolation barrier between the two species is partially broken down. Directional control of tip-growing cells is essential for proper tissue organization and cell-to-cell communication in animals and plants 1 , 2 . In the sexual reproduction of flowering plants, the tip growth of the male gametophyte, the pollen tube, is precisely guided by female cues to achieve fertilization 3 . Several female-secreted peptides have recently been identified as species-specific attractants that directly control the direction of pollen tube growth 4 , 5 , 6 . However, the method by which pollen tubes precisely and promptly respond to the guidance signal from their own species is unknown. Here we show that tip-localized pollen-specific receptor-like kinase 6 (PRK6) with an extracellular leucine-rich repeat domain is an essential receptor for sensing of the LURE1 attractant peptide in Arabidopsis thaliana under semi- in-vivo conditions, and is important for ovule targeting in the pistil. PRK6 interacted with pollen-expressed ROPGEFs (Rho of plant guanine nucleotide-exchange factors), which are important for pollen tube growth through activation of the signalling switch Rho GTPase ROP1 (refs 7 , 8 ). PRK6 conferred responsiveness to AtLURE1 in pollen tubes of the related species Capsella rubella . Furthermore, our genetic and physiological data suggest that PRK6 signalling through ROPGEFs and sensing of AtLURE1 are achieved in cooperation with the other PRK family receptors, PRK1, PRK3 and PRK8. Notably, the tip-focused PRK6 accumulated asymmetrically towards an external AtLURE1 source before reorientation of pollen tube tip growth. These results demonstrate that PRK6 acts as a key membrane receptor for external AtLURE1 attractants, and recruits the core tip-growth machinery, including ROP signalling proteins. This work provides insights into the orchestration of efficient pollen tube growth and species-specific pollen tube attraction by multiple receptors during male–female communication.

Rapid phenotypic changes in traits of adaptive significance are crucial for organisms to thrive in changing environments. How such phenotypic variation is achieved rapidly, despite limited genetic variation in species that experience a genetic bottleneck is unknown. Capsella rubella, an annual and inbreeding forb (Brassicaceae), is a great system for studying this basic question. Its distribution is wider than those of its congeneric species, despite an extreme genetic bottleneck event that severely diminished its genetic variation. Here, we demonstrate that transposable elements (TEs) are an important source of genetic variation that could account for its high phenotypic diversity. TEs are (i) highly enriched in C. rubella compared with its outcrossing sister species Capsella grandiflora, and (ii) 4.2% of polymorphic TEs in C. rubella are associated with variation in the expression levels of their adjacent genes. Furthermore, we show that frequent TE insertions at FLOWERING LOCUS C (FLC) in natural populations of C. rubella could explain 12.5% of the natural variation in flowering time, a key life history trait correlated with fitness and adaptation. In particular, we show that a recent TE insertion at the 3′ UTR of FLC affects mRNA stability, which results in reducing its steady-state expression levels, to promote the onset of flowering. Our results highlight that TE insertions can drive rapid phenotypic variation, which could potentially help with adaptation to changing environments in a species with limited standing genetic variation.

Genetic drift is expected to remove polymorphism from populations over long periods of time, with the rate of polymorphism loss being accelerated when species experience strong reductions in population size. Adaptive forces that maintain genetic variation in populations, or balancing selection, might counteract this process. To understand the extent to which natural selection can drive the retention of genetic diversity, we document genomic variability after two parallel species-wide bottlenecks in the genus Capsella. We find that ancestral variation preferentially persists at immunity related loci, and that the same collection of alleles has been maintained in different lineages that have been separated for several million years. By reconstructing the evolution of the disease-related locus MLO2b, we find that divergence between ancient haplotypes can be obscured by referenced based re-sequencing methods, and that trans-specific alleles can encode substantially diverged protein sequences. Our data point to long-term balancing selection as an important factor shaping the genetics of immune systems in plants and as the predominant driver of genomic variability after a population bottleneck. Capsella rubella is a small plant that is found in southern and western Europe. This plant is young in evolutionary terms: it is thought to have emerged less than 200,000 years ago from a small group of plants belonging to an older species known as Capsella grandiflora. Individuals of the same species may carry alternative versions of the same genes – known as alleles – and the total number of alleles present in a population is referred to as genetic diversity. When a few individuals form a new species, the gene pool and the genetic diversity in the new species is initially much lower than in the ancestral species, which may make the new species less robust to fluctuations in the environment. For example, alternative versions of a gene might be preferable in hot or cold climates, and loss of one of these versions would limit the species’ ability to survive in both climates. A mechanism known as balancing selection can maintain various alleles in a species, even if the population is very small. However, it was not clear how common long-lasting balancing selection was after a species had split. To address this question, Koenig et al. assembled collections of wild C. rubella and C. grandiflora plants and sequenced their genomes in search of alleles that were shared between individuals of the two species. The analysis found not just a few, but thousands of examples where the same genetic differences had been maintained in both C. rubella and C. grandiflora. Some of these allele pairs were also shared with individuals of a third species of Capsella that had split from C. rubella and C. grandiflora over a million years ago. The shared alleles did not occur randomly in the genome; genes involved in immune responses were far more likely to be targets of balancing selection than other types of genes. These findings indicate that there is strong balancing selection to maintain different alleles of immunity genes in wild populations of plants, and that some of this diversity can be maintained over hundreds of thousands, if not millions of years. The strategy developed by Koenig et al. may help to identify new versions of immunity genes from wild relatives of crop plants that could be used to combat crop diseases.

Crucihimalaya himalaica, a close relative of Arabidopsis and Capsella, grows on the Qinghai–Tibet Plateau (QTP) about 4,000 m above sea level and represents an attractive model system for studying speciation and ecological adaptation in extreme environments. We assembled a draft genome sequence of 234.72 Mb encoding 27,019 genes and investigated its origin and adaptive evolutionary mechanisms. Phylogenomic analyses based on 4,586 single-copy genes revealed that C. himalaica is most closely related to Capsella (estimated divergence 8.8 to 12.2 Mya), whereas both species form a sister clade to Arabidopsis thaliana and Arabidopsis lyrata, from which they diverged between 12.7 and 17.2 Mya. LTR retrotransposons in C. himalaica proliferated shortly after the dramatic uplift and climatic change of the Himalayas from the Late Pliocene to Pleistocene. Compared with closely related species, C. himalaica showed significant contraction and pseudogenization in gene families associated with disease resistance and also significant expansion in gene families associated with ubiquitin-mediated proteolysis and DNA repair. We identified hundreds of genes involved in DNA repair, ubiquitin-mediated proteolysis, and reproductive processes with signs of positive selection. Gene families showing dramatic changes in size and genes showing signs of positive selection are likely candidates for C. himalaica’s adaptation to intense radiation, low temperature, and pathogen-depauperate environments in the QTP. Loss of function at the S-locus, the reason for the transition to self-fertilization of C. himalaica, might have enabled its QTP occupation. Overall, the genome sequence of C. himalaica provides insights into the mechanisms of plant adaptation to extreme environments.

A male cell-surface receptor-like kinase that responds to the female chemoattractant LURE1 on the pollen tube of Arabidopsis thaliana is identified; LURE1 triggers dimerization of the receptor components and activation of the kinase activity, and the transformation of a component of the A. thaliana receptor to the Capsella rubella species partially breaks down the reproductive isolation barrier. Multiple pollen-tube receptors for LURE1 In flowering plants, the female gametophyte secretes chemoattractant peptides to guide pollen tube growth so that it delivers the immobile sperm to the ovule-enclosed female gametophyte. Two papers published in this issue of Nature report the identification of male pollen tube cell-surface receptors for one of these female attractants, LURE1, in the model plant Arabidopsis thaliana . Wei-Cai Yang and colleagues show that LURE1 is perceived by a receptor-like kinase complex, the heteromer MDIS1–MIK. Tetsuya Higashiyama and Hidenori Takeuchi report that pollen-specific receptor-like kinase 6 (PRK6) is required for sensing LURE1, and PRK6 acts together with other PRK family receptors. Both groups demonstrate that by engineering pollen tubes of the sister species Capsella rubella to express a component of the A. thaliana receptors — either MDIS1 or PRK6 — the reproductive isolation barrier between the two species is partially broken down. Sexual reproduction requires recognition between the male and female gametes. In flowering plants, the immobile sperms are delivered to the ovule-enclosed female gametophyte by guided pollen tube growth. Although the female gametophyte-secreted peptides have been identified to be the chemotactic attractant to the pollen tube 1 , 2 , 3 , the male receptor(s) is still unknown. Here we identify a cell-surface receptor heteromer, MDIS1–MIK, on the pollen tube that perceives female attractant LURE1 in Arabidopsis thaliana . MDIS1, MIK1 and MIK2 are plasma-membrane-localized receptor-like kinases with extracellular leucine-rich repeats and an intracellular kinase domain. LURE1 specifically binds the extracellular domains of MDIS1, MIK1 and MIK2, whereas mdis1 and mik1 mik2 mutant pollen tubes respond less sensitively to LURE1. Furthermore, LURE1 triggers dimerization of the receptors and activates the kinase activity of MIK1. Importantly, transformation of At MDIS1 to the sister species Capsella rubella can partially break down the reproductive isolation barrier. Our findings reveal a new mechanism of the male perception of the female attracting signals.

Background In contrast to positive selection, which reduces genetic variation by fixing beneficial alleles, balancing selection maintains genetic variation within a population or species and plays crucial roles in adaptation in diverse organisms. However, which genes, genome-wide, are under balancing selection and the extent to which these genes are involved in adaptation are largely unknown. Results We performed a genome-wide scan for genes under balancing selection across two plant species, Arabidopsis thaliana and its relative Capsella rubella , which diverged about 8 million generations ago. Among hundreds of genes with shared coding-region polymorphisms, we find evidence for long-term balancing selection in five genes: AT1G35220, AT2G16570, AT4G29360, AT5G38460, and AT5G44000. These genes are involved in the response to biotic and abiotic stress and other fundamental biochemical processes. More intriguingly, for these genes, we detected significant ecological diversification between the two haplotype groups, suggesting that balancing selection has been very important for adaptation. Conclusions Our results indicate that beyond the well-known S-locus genes and resistance genes, many loci are under balancing selection. These genes are mostly correlated with resistance to stress or other fundamental functions and likely play a more important role in adaptation to diverse habitats than previously thought.

Allopolyploidy is generally perceived as a major source of evolutionary novelties and as an instantaneous way to create isolation barriers. However, we do not have a clear understanding of how two subgenomes evolve and interact once they have fused in an allopolyploid species nor how isolated they are from their relatives. Here, we address these questions by analyzing genomic and transcriptomic data of allotetraploid Capsella bursa-pastoris in three differentiated populations, Asia, Europe, and the Middle East. We phased the two subge-nomes, one descended from the outcrossing and highly diverse Capsella grandiflora (Cbp Cg) and the other one from the selfing and genetically depauperate Capsella orientalis (Cbp Co). For each subgenome, we assessed its relationship with the diploid relatives, temporal changes of effective population size (N e), signatures of positive and negative selection , and gene expression patterns. In all three regions, N e of the two subgenomes decreased gradually over time and the Cbp Co subgenome accumulated more deleterious changes than Cbp Cg. There were signs of widespread admixture between C. bursa-pastoris and its diploid relatives. The two subgenomes were impacted differentially depending on geographic region suggesting either strong interploidy gene flow or multiple origins of C. bursa-pastoris. Selective sweeps were more common on the Cbp Cg subgenome in Europe and the Middle East, and on the Cbp Co subgenome in Asia. In contrast, differences in expression were limited with the Cbp Cg subgenome slightly more expressed than Cbp Co in Europe and the Middle-East. In summary, after more than 100,000 generations of co-existence , the two subgenomes of C. bursa-pastoris still retained a strong signature of parental legacy but their evolutionary trajectory strongly varied across geographic regions.

The evolutionary forces that maintain genetic variation in quantitative traits within populations remain poorly understood. One hypothesis suggests that variation is under purifying selection, resulting in an excess of low-frequency variants and a negative correlation between minor allele frequency and selection coefficients. Here, we test these predictions using the genetic loci associated with total expression variation (eQTLs) and allele-specific expression variation (aseQTLs) mapped within a single population of the plantCapsella grandiflora. In addition to finding eQTLs and aseQTLs for a large fraction of genes, we show that alleles at these loci are rarer than expected and exhibit a negative correlation between phenotypic effect size and frequency. Overall, our results show that the distribution of frequencies and effect sizes of the loci responsible for local expression variationwithin a single outcrossing population are consistent with the effects of purifying selection.

Significance Plants have undergone repeated rounds of whole-genome duplication, followed by gene degeneration and loss. Using whole-genome resequencing, we examined the origins of the recent tetraploid Capsella bursa-pastoris and the earliest stages of genome evolution after polyploidization. We conclude the species had a hybrid origin from two distinct Capsella lineages within the past 100,000–300,000 y. Our analyses suggest the absence of rapid gene loss but provide evidence that the species has large numbers of inactivating mutations, many of which were inherited from the parental species. Our results suggest that genome evolution following polyploidy is determined not only by genome redundancy but also by demography, the mating system, and the evolutionary history of the parental species. Whole-genome duplication (WGD) events have occurred repeatedly during flowering plant evolution, and there is growing evidence for predictable patterns of gene retention and loss following polyploidization. Despite these important insights, the rate and processes governing the earliest stages of diploidization remain poorly understood, and the relative importance of genetic drift, positive selection, and relaxed purifying selection in the process of gene degeneration and loss is unclear. Here, we conduct whole-genome resequencing in Capsella bursa-pastoris , a recently formed tetraploid with one of the most widespread species distributions of any angiosperm. Whole-genome data provide strong support for recent hybrid origins of the tetraploid species within the past 100,000–300,000 y from two diploid progenitors in the Capsella genus. Major-effect inactivating mutations are frequent, but many were inherited from the parental species and show no evidence of being fixed by positive selection. Despite a lack of large-scale gene loss, we observe a decrease in the efficacy of natural selection genome-wide due to the combined effects of demography, selfing, and genome redundancy from WGD. Our results suggest that the earliest stages of diploidization are associated with quantitative genome-wide decreases in the strength and efficacy of selection rather than rapid gene loss, and that nonfunctionalization can receive a “head start” through a legacy of deleterious variants and differential expression originating in parental diploid populations.