Sex is determined by XY chromosomes across the radiation of dioecious Nepenthes pitcher plants.

Mathias Scharmann,Alex Widmer,Faizah Metali,T Ulmar Grafe

doi:10.1002/evl3.142

Mathias Scharmann, Alex Widmer + Show 2 more

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https://doi.org/10.1002/evl3.142

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Abstract

Species with separate sexes (dioecy) are a minority among flowering plants, but dioecy has evolved multiple times independently in their history. The sex‐determination system and sex‐linked genomic regions are currently identified in a limited number of dioecious plants only. Here, we study the sex‐determination system in a genus of dioecious plants that lack heteromorphic sex chromosomes and are not amenable to controlled breeding: Nepenthes pitcher plants. We genotyped wild populations of flowering males and females of three Nepenthes taxa using ddRAD‐seq and sequenced a male inflorescence transcriptome. We developed a statistical tool (privacy rarefaction) to distinguish true sex specificity from stochastic noise in read coverage of sequencing data from wild populations and identified male‐specific loci and XY‐patterned single nucleotide polymorphsims (SNPs) in all three Nepenthes taxa, suggesting the presence of homomorphic XY sex chromosomes. The male‐specific region of the Y chromosome showed little conservation among the three taxa, except for the essential pollen development gene DYT1 that was confirmed as male specific by PCR in additional Nepenthes taxa. Hence, dioecy and part of the male‐specific region of the Nepenthes Y‐chromosomes likely have a single evolutionary origin.

Highlights

One of the most striking polymorphisms observed in organismal populations is the existence of male and female individuals
In contrast to outcrossing–selfing transitions due to loss of selfincompatbility, for some of which the underlying genetic changes have recently been uncovered (e.g., Shimizu and Tsuchimatsu 2015), relatively little is known about the genes involved in transitions from hermaphroditism to dioecy and in sex determination in plants (Charlesworth 2016), sex-determining genes have been identified in three dioecious plant species: persimmon (Diospyros lotus, Akagi et al 2014), Asparagus officinalis (Harkess et al 2017; Murase et al 2017), and kiwifruit (Actinidia, Akagi et al 2018)
SEX-LINKED LOCI We first searched for sex-specific contigs in the illustrative example of S. latifolia GBS data using privacy rarefaction

Summary

Introduction

One of the most striking polymorphisms observed in organismal populations is the existence of male and female individuals. Dioecy has evolved hundreds of times independently in plants, which offers the potential for comparative studies of sex chromosome evolution and for investigating the genetic basis of transitions between hermaphroditism and dioecy (Charlesworth 2015). Empirical data to test hypotheses about why some species are dioecious and others hermaphroditic, and how such transitions are achieved, are lacking Despite their potential, the sexdetermination mechanisms of most dioecious plants are not known, and few new species have been investigated since the seminal review by Westergaard (1958). 5–6% of species have female and male flowers on separate individuals (dioecy), but the evolutionary transition to dioecy may have occurred as many as 800 times independently in angiosperms (Renner 2014). The main hypotheses for the evolution of separate sexes in plants involve a combination of trade-offs between the sex functions, plus disadvantage of inbreeding (Charlesworth and Charlesworth 1978)

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