The asparagus genome sheds light on the origin and evolution of a young Y chromosome

Alex Harkess,Zhen Yue,Yueping Zhang,Yanling Chen,Ron Van Der Hulst,Sandra M Mathioni,Siwaret Arikit,Mayumi Nakano,Michael R Mckain,Wenqi Li,Haibao Tang,Atul Kakrana,Rod A Wing,Alexa Telgmann-Rauber,Hongzhi Kong,Yin Ye,Pierre Lavrijsen,Asdrúbal Falavigna ,Jianming Gao,Dave Kudrna,Haixin Chen,Sisi Luo ,Blake C Meyers,Paolo Riccardi,John E Bowers,Zichao Mao,Xiangyang Xu,Francesco Mercati,John Groenendijk,Jeremy N Ray ,Francesco Sunseri,Hongyan Shan,Akira Kanno,Meizhong Luo,Kexian Yi,Saravanaraj Ayyampalayam,J Chris Pires,Jinsong Zhou,James H Leebens‐Mack ,Chunyan Xu,Helong Chen,Guangyu Chen

doi:10.1038/s41467-017-01064-8

Abstract

Sex chromosomes evolved from autosomes many times across the eukaryote phylogeny. Several models have been proposed to explain this transition, some involving male and female sterility mutations linked in a region of suppressed recombination between X and Y (or Z/W, U/V) chromosomes. Comparative and experimental analysis of a reference genome assembly for a double haploid YY male garden asparagus (Asparagus officinalis L.) individual implicates separate but linked genes as responsible for sex determination. Dioecy has evolved recently within Asparagus and sex chromosomes are cytogenetically identical with the Y, harboring a megabase segment that is missing from the X. We show that deletion of this entire region results in a male-to-female conversion, whereas loss of a single suppressor of female development drives male-to-hermaphrodite conversion. A single copy anther-specific gene with a male sterile Arabidopsis knockout phenotype is also in the Y-specific region, supporting a two-gene model for sex chromosome evolution.

Highlights

Sex chromosomes evolved from autosomes many times across the eukaryote phylogeny
The genome is largely comprised of recently-inserted Long Terminal Repeat (LTR) retrotransposons (Supplementary Fig. 1), nearly 95% of the Core Eukaryotic Gene Model Annotations (CEGMA) and 88.2% of the BUSCO plant gene annotations were identified in the asparagus gene models
As seen in papaya[25], most of the non-recombining sex determination region of the Y chromosome is hemizygous with an increased density of retrotransposons compared to the surrounding pseudoautosomal region (Fig. 1a)

Summary

Introduction

Sex chromosomes evolved from autosomes many times across the eukaryote phylogeny. Several models have been proposed to explain this transition, some involving male and female sterility mutations linked in a region of suppressed recombination between X and Y (or Z/W, U/V) chromosomes. On the basis of his own work in Silene latifolia (formerly Melandrium album) and a review of data from other diecious plant systems including garden asparagus, Mogens Westergaard posited in 1958 that the evolution of an active Y chromosome from an autosome involved at least two genes: a dominant suppressor of female function and a gene essential for male function that is missing from the X chromosome[8] This two-gene hypothesis was later advanced by Brian and Deborah Charlesworth in an evolutionary model for the conversion of an autosomal chromosome pair to sex chromosomes in association with a transition from hermaphroditism to dioecy[4]. Suppressor of Female Function (SOFF) Unannotated Transformation/transcription domain-associated protein Unannotated AP2 ethylene-responsive transcription factor Nudix hydrolase 15, mitochondrial-like DEFECTIVE IN TAPETUM DEVELOPMENT AND FUNCTION 1 (TDF1) Unannotated Outer envelope protein 80, chloroplastic-like isoform X1 Photosystem I reaction center subunit XI, chloroplastic Photosystem I reaction center subunit XI, chloroplastic Unannotated Unannotated

Methods

Results

Conclusion