Evolution of a plant sex chromosome driven by expanding pericentromeric recombination suppression

Recombination suppression around sex-determining gene(s) is a key step in evolution of sex chromosomes, but it is not well understood how it evolves. Recently evolved sex-linked regions offer an opportunity to understand the mechanisms of recombination cessation. This paper analyses such a region on Silene latifolia (Caryophyllaceae) sex chromosomes, where recombination was suppressed in the last 120 thousand years ("stratum 3"). Locating the boundaries of the stratum 3 in S. latifolia genome sequence revealed that this region is far larger than assumed previously—it is about 14 Mb long and includes 202 annotated genes. A gradient of X:Y divergence detected in the stratum 3, with divergence increasing proximally, indicates gradual recombination cessation, possibly caused by expansion of pericentromeric recombination suppression (PRS) into the pseudoautosomal region. Expansion of PRS was also the likely cause for the formation of the older stratum 2 on S. latifolia sex chromosomes. The role of PRS in sex chromosome evolution has been underappreciated, but it may be a significant factor, especially in the species with large chromosomes where PRS is often extensive

How does speciation in marine plankton work?

Marine plankton species are ecologically important, yet, it remains unclear how they originate in the ocean, where few barriers are apparent to cause the most common type of speciation – divergence in isolation. Here I discuss the use of modern evolutionary genetic approaches to shed light on longstanding questions regarding their evolution

Heterochiasmy and sex chromosome evolution in Silene

The evolution of a non-recombining sex-specific region is a key step in sex chromosome evolution. Suppression of recombination between the (proto-) X- and Y-chromosomes in male meiosis creates a non-recombining Y-linked region (NRY), while the X-chromosome continues to recombine in females. Lack of recombination in the NRY defines its main properties—genetic degeneration and accumulation of repetitive DNA, making X and Y chromosomes very different from each other. How and why recombination suppression on sex chromosomes evolves remains controversial. A strong difference in recombination rates between the sexes (heterochiasmy) can facilitate or even cause recombination suppression. In the extreme case—complete lack of recombination in the heterogametic sex (achiasmy)—the entire sex-specific chromosome is automatically non-recombining. In this study, I analyse sex-specific recombination rates in a dioecious plant Silene latifolia (Caryophyllaceae), which evolved separate sexes and sex chromosomes ~11 million years ago. I reconstruct high-density RNAseq-based genetic maps including over five thousand genic markers for the two sexes separately. The comparison of the male and female maps reveals only modest heterochiasmy across the genome, with the exception of the sex chromosomes, where recombination is suppressed in males. This indicates that heterochiasmy likely played only a minor, if any, role in NRY evolution in S. latifolia, as recombination suppression is specific to NRY rather than to the entire genome in males. Other mechanisms such as structural rearrangements and/or epigenetic modifications were likely involved, and comparative genome analysis and genetic mapping in multiple Silene species will help to shed light on the mechanism(s) of recombination suppression that led to the evolution of sex chromosomes

Processing and population genetic analysis of multigenic datasets with ProSeq3 software

Motivation: The current tendency in molecular population genetics is to use increasing numbers of genes in the analysis. Here I describe a program for handling and population genetic analysis of DNA polymorphism data collected from multiple genes. The program includes a sequence/alignment editor and an internal relational database that simplify the preparation and manipulation of multigenic DNA polymorphism datasets. The most commonly used DNA polymorphism analyses are implemented in ProSeq3, facilitating population genetic analysis of large multigenic datasets. Extensive input/output options make ProSeq3 a convenient hub for sequence data processing and analysis

Rubisco evolution in C4 eudicots: an analysis of Amaranthaceae sensu lato

BACKGROUND Rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase) catalyses the key reaction in the photosynthetic assimilation of CO₂. In C₄ plants CO₂ is supplied to Rubisco by an auxiliary CO₂-concentrating pathway that helps to maximize the carboxylase activity of the enzyme while suppressing its oxygenase activity. As a consequence, C₄ Rubisco exhibits a higher maximum velocity but lower substrate specificity compared with the C₃ enzyme. Specific amino-acids in Rubisco are associated with C₄ photosynthesis in monocots, but it is not known whether selection has acted on Rubisco in a similar way in eudicots. METHODOLOGY/PRINCIPAL FINDINGS We investigated Rubisco evolution in Amaranthaceae sensu lato (including Chenopodiaceae), the third-largest family of C₄ plants, using phylogeny-based maximum likelihood and Bayesian methods to detect Darwinian selection on the chloroplast rbcL gene in a sample of 179 species. Two Rubisco residues, 281 and 309, were found to be under positive selection in C₄ Amaranthaceae with multiple parallel replacements of alanine by serine at position 281 and methionine by isoleucine at position 309. Remarkably, both amino-acids have been detected in other C₄ plant groups, such as C₄ monocots, illustrating a striking parallelism in molecular evolution. CONCLUSIONS/SIGNIFICANCE Our findings illustrate how simple genetic changes can contribute to the evolution of photosynthesis and strengthen the hypothesis that parallel amino-acid replacements are associated with adaptive changes in Rubisco.This research was funded by NERC (http://www.nerc.ac.uk/; grant number NE/H007741/1)

Molecular Adaptation during Adaptive Radiation in the Hawaiian Endemic Genus Schiedea

BACKGROUND: “Explosive” adaptive radiations on islands remain one of the most puzzling evolutionary phenomena. The rate of phenotypic and ecological adaptations is extremely fast during such events, suggesting that many genes may be under fairly strong selection. However, no evidence for adaptation at the level of protein coding genes was found, so it has been suggested that selection may work mainly on regulatory elements. Here we report the first evidence that positive selection does operate at the level of protein coding genes during rapid adaptive radiations. We studied molecular adaptation in Hawaiian endemic plant genus Schiedea (Caryophyllaceae), which includes closely related species with a striking range of morphological and ecological forms, varying from rainforest vines to woody shrubs growing in desert-like conditions on cliffs. Given the remarkable difference in photosynthetic performance between Schiedea species from different habitats, we focused on the “photosynthetic” Rubisco enzyme, the efficiency of which is known to be a limiting step in plant photosynthesis. RESULTS: We demonstrate that the chloroplast rbcL gene, encoding the large subunit of Rubisco enzyme, evolved under strong positive selection in Schiedea. Adaptive amino acid changes occurred in functionally important regions of Rubisco that interact with Rubisco activase, a chaperone which promotes and maintains the catalytic activity of Rubisco. Interestingly, positive selection acting on the rbcL might have caused favorable cytotypes to spread across several Schiedea species. SIGNIFICANCE: We report the first evidence for adaptive changes at the DNA and protein sequence level that may have been associated with the evolution of photosynthetic performance and colonization of new habitats during a recent adaptive radiation in an island plant genus. This illustrates how small changes at the molecular level may change ecological species performance and helps us to understand the molecular bases of extremely fast rate of adaptation during island adaptive radiations

Widespread positive selection in the photosynthetic Rubisco enzyme

Background: Rubisco enzyme catalyzes the first step in net photosynthetic CO2 assimilation and photorespiratory carbon oxidation and is responsible for almost all carbon fixation on Earth. The large subunit of Rubisco is encoded by the chloroplast rbcL gene, which is widely used for reconstruction of plant phylogenies due to its conservative nature. Plant systematicists have mainly used rbcL paying little attention to its function, and the question whether it evolves under Darwinian selection has received little attention. The purpose of our study was to evaluate how common is positive selection in Rubisco among the phototrophs and where in the Rubisco structure does positive selection occur. Results: We searched for positive selection in rbcL sequences from over 3000 species representing all lineages of green plants and some lineages of other phototrophs, such as brown and red algae, diatoms, euglenids and cyanobacteria. Our molecular phylogenetic analysis found the presence of positive selection in rbcL of most analyzed land plants, but not in algae and cyanobacteria. The mapping of the positively selected residues on the Rubisco tertiary structure revealed that they are located in regions important for dimer-dimer, intradimer, large subunit-small subunit and Rubisco-Rubisco activase interactions, and that some of the positively selected residues are close to the active site. Conclusion: Our results demonstrate that despite its conservative nature, Rubisco evolves under positive selection in most lineages of land plants, and after billions of years of evolution Darwinian selection still fine-tunes its performance. Widespread positive selection in rbcL has to be taken into account when this gene is used for phylogenetic reconstructions. </p

The role of recombination landscape in species hybridisation and speciation

It is now well recognised that closely related species can hybridize and exchange genetic material, which may promote or oppose adaptation and speciation. In some cases, interspecific hybridisation is very common, making it surprising that species identity is preserved despite active gene exchange. The genomes of most eukaryotic species are highly heterogeneous with regard to gene density, abundance of repetitive DNA, chromatin compactisation etc, which can make certain genomic regions more prone or more resistant to introgression of genetic material from other species. Heterogeneity in local recombination rate underpins many of the observed patterns across the genome (e.g. actively recombining regions are typically gene rich and depleted for repetitive DNA) and it can strongly affect the permeability of genomic regions to interspecific introgression. The larger the region lacking recombination, the higher the chance for the presence of species incompatibility gene(s) in that region, making the entire non- or rarely recombining block impermeable to interspecific introgression. Large plant genomes tend to have highly heterogeneous recombination landscape, with recombination frequently occurring at the ends of the chromosomes and central regions lacking recombination. In this paper we review the relationship between recombination and introgression in plants and argue that large rarely recombining regions likely play a major role in preserving species identity in actively hybridising plant species

Evolution of sex-determination in dioecious plants: from active Y to X/A balance?

Sex chromosomes in plants have been known for a century, but only recently have we begun to understand the mechanisms behind sex determination in dioecious plants. Here, we discuss evolution of sex determination, focusing on Silene latifolia, where evolution of separate sexes is consistent with the classic “two mutations” model—a loss of function male sterility mutation and a gain of function gynoecium suppression mutation, which turned an ancestral hermaphroditic population into separate males and females. Interestingly, the gynoecium suppression function in S. latifolia evolved via loss of function in at least two sex-linked genes and works via gene dosage balance between sex-linked, and autosomal genes. This system resembles X/A-ratio-based sex determination systems in Drosophila and Rumex, and could represent a steppingstone in the evolution of X/A-ratio-based sex determination from an active Y system

Evolution of Sex chromosomes and gynoecium suppression in plants

White campion (Silene latifolia, Caryophyllaceae) is a classical model species for studies of sex determination and sex chromosome evolution in dioecious plants. Deletion mapping in this species revealed the presence of two Y-linked sex determining genes—the stamen promoting factor (SPF) gene and a gynoecium suppressing factor (GSF), which inspired the development of the classic ‘two genes’ model for dioecy evolution. We recently identified a Y-linked GSFY gene that encodes a CLAVATA3 homolog and causes gynoecium suppression in S. latifolia via WUSCHEL-CLAVATA feedback loop. Interestingly, the WUSCHEL homolog in S. latifolia (SlWUS1) is also sex-linked and both GSFY and SlWUS1 are located in the oldest part of the sex chromosomes, suggesting that selection to prevent recombination between these genes may have contributed to the origination of sex chromosomes in this species. The WUS-CLV3 pathway is also involved in the sexual differentiation of gynoecium development in kiwifruits and melon, indicating that this pathway plays central role in gynoecium suppression in dioecious and monoecious plants