Abstract

Separate sexes in dioecious plants display different morphology and physiological characteristics. The differences between the two sexes lie in their highly differentiated floral characteristics and in sex-related phenotype, which is genetically determined and epigenetically modified. In dioecious papaya (Carica papaya L.), global comparisons of epigenetic DNA methylation and gene expressions were still limited. We conducted bisulfite sequencing of early-stage flowers grown in three seasons (spring, summer and winter) and compared their methylome and transcriptome profiles to investigate the differential characteristics of male and female in papaya. Methylation variances between female and male papaya were conserved among three different seasons. However, combined genome-scale transcriptomic evidence revealed that most methylation variances did not have influence on the expression profiles of neighboring genes, and the differentially expressed genes were most overrepresented in phytohormone signal transduction pathways. Further analyses showed diverse stress-responsive methylation alteration in male and female flowers. Male flower methylation was more responsive to stress whereas female flower methylation varied less under stress. Early flowering of male papaya in spring might be associated with the variation in the transcription of CpSVP and CpAP1 coinciding with their gene-specific hypomethylation. These findings provide insights into the sex-specific DNA methylation and gene expression landscapes of dioecious papaya and a foundation to investigate the correlation between differentiated floral characteristics and their candidate genes.

Highlights

  • Dioecious species represent 6% of angiosperm species and 10% of land plant species[1]

  • 9000 conserved sex-special DMCs (CsDMCs) were stably detected in different sexual flowers across three seasons

  • Those conserved CsDMCs among different seasons should be a minimal evidence of DNA methylation variances between female and male papaya flowers

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Summary

Introduction

Dioecious species represent 6% of angiosperm species and 10% of land plant species[1]. Sex determination genes regulate developmental process of floral organs and sex chromosomes ensure the stability of sex differences in dioecious species. Epigenetic reprogramming, in addition to genetic regulation, could play important roles in sex determination of some flowering plants due to the phenomena that some flowering plants often have sex reversal under stress conditions. Plants can perceive developmental or environmental stimuli and carry out a variety of epigenetic alterations, including DNA methylation, histone modification and microRNA-dependent gene silencing, to reprogram the expression of floral genes. Epigenetic reprogramming might have a negative impact on the differentiation or development of stamen and carpel primordia, causing the abortion of reproductive organs and thereby the sex separation in flowering plants. Several epigenetic mechanisms of sex determination in some species were reported recently.

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