Integrative genomics reveals paths to sex dimorphism in Salix purpurea L

Kerrie Barry,Stephen P DiFazio,Matthew S Olson,Lawrence B Smart,Laura Sandor,Guanqiao Feng,Aditi Sharma,Fred E Gouker,Craig H Carlson,Anna Lipzen,Gerald A Tuskan,Jeremy Schmutz,Brennan Hyden

doi:10.1038/s41438-021-00606-y

Abstract

Sex dimorphism and gene expression were studied in developing catkins in 159 F2 individuals from the bioenergy crop Salix purpurea, and potential mechanisms and pathways for regulating sex development were explored. Differential expression, eQTL, bisulfite sequencing, and network analysis were used to characterize sex dimorphism, detect candidate master regulator genes, and identify pathways through which the sex determination region (SDR) may mediate sex dimorphism. Eleven genes are presented as candidates for master regulators of sex, supported by gene expression and network analyses. These include genes putatively involved in hormone signaling, epigenetic modification, and regulation of transcription. eQTL analysis revealed a suite of transcription factors and genes involved in secondary metabolism and floral development that were predicted to be under direct control of the sex determination region. Furthermore, data from bisulfite sequencing and small RNA sequencing revealed strong differences in expression between males and females that would implicate both of these processes in sex dimorphism pathways. These data indicate that the mechanism of sex determination in Salix purpurea is likely different from that observed in the related genus Populus. This further demonstrates the dynamic nature of SDRs in plants, which involves a multitude of mechanisms of sex determination and a high rate of turnover.

Highlights

1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; Introduction Major progress has been made in recent years in identifying the master regulators of sex determination in plants, but less is known about the transcriptional networks that account for sex dimorphism
We identified multiple genes associated in trans with the sex determination region (SDR) that could serve as toplevel regulators of primary and secondary floral sex dimorphisms under direct control by master regulator genes, as well as enriched pathways predicted to serve as intermediate pathways involved in sex dimorphism
The male-upregulated gene set showed an underrepresentation for 71 terms, including terms relating to transcription and RNA regulation, splicing, and modification (Table S2)

Summary

Introduction

Major progress has been made in recent years in identifying the master regulators of sex determination in plants, but less is known about the transcriptional networks that account for sex dimorphism. Development of separate sexes, requires that the genes controlling sex determination regulate the transcription of many genes and metabolic pathways in order to coordinate development (andrecium and gynecium development) as well as secondary sex dimorphisms, such as floral volatile profiles, pigmentation, floral phenology, and organ morphology, and often involve both sex-linked and autosomal genes[8]. Because their expression in the opposite sex may be deleterious, linkage between sex determination genes and genes controlling secondary sexual dimorphisms may be favored by natural selection. Such genes are termed “sexually antagonistic”[9]. It can be challenging to discriminate among sex determination genes and other sexlinked genes that influence sex dimorphisms

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Discussion

Conclusion