Temperature and photoperiod changes affect cucumber sex expression by different epigenetic regulations

Yun-Song Lai,Xiaohui Zhang,Xixiang Li,Jiangping Song,Xinxin Dou,Sigeng Li,Guanyu Ji,Wei Zhang,Haiping Wang,Yuanqi Wu,Di Shen,Yang Qiu

doi:10.1186/s12870-018-1490-3

Abstract

BackgroundCucumbers (Cucumis sativus) are known for their plasticity in sex expression. DNA methylation status determines gene activity but is susceptible to environmental condition changes. Thus, DNA methylation-based epigenetic regulation may at least partially account for the instability of cucumber sex expression. Do temperature and photoperiod that are the two most important environmental factors have equal effect on cucumber sex expression by similar epigenetic regulation mechanism? To answer this question, we did a two-factor experiment of temperature and photoperiod and generated methylome and transcriptome data from cucumber shoot apices.ResultsThe seasonal change in the femaleness of a cucumber core germplasm collection was investigated over five consecutive years. As a result, 71.3% of the 359 cucumber accessions significantly decreased their femaleness in early autumn when compared with spring. High temperature and long-day photoperiod treatments, which mimic early autumn conditions, are both unfavorable for female flower formation, and temperature is the predominant factor. High temperatures and long-day treatments both predominantly resulted in hypermethylation compared to demethylation, and temperature effect was decisive. The targeted cytosines shared in high-temperature and long-day photoperiod treatment showed the same change in DNA methylation level. Moreover, differentially expressed TEs (DETs) and the predicted epiregulation sites were clustered across chromosomes, and importantly, these sites were reproducible among different treatments. Essentially, the photoperiod treatment preferentially and significantly influenced flower development processes, while temperature treatment produced stronger responses from phytohormone-pathway-related genes. Cucumber AGAMOUS was likely epicontrolled exclusively by photoperiod while CAULIFLOWER A and CsACO3 were likely epicontrolled by both photoperiod and temperature.ConclusionsSeasonal change of sex expression is a germplasm-wide phenomenon in cucumbers. High temperature and long-day photoperiod might have the same effect on the methylome via the same mechanism of gene-TE interaction but resulted in different epicontrol sites that account for different mechanisms between temperature- and photoperiod-dependent sex expression changes.

Highlights

Cucumbers (Cucumis sativus) are known for their plasticity in sex expression
The seasonal plasticity of female/male flower ratios in the cucumber germplasm is related to temperature and photoperiod The seasonal sex stability of 359 accessions from a cucumber core germplasm collection was assessed for 5 consecutive years (2010–2014) (Additional file 1: Table S1)
Over 93.3% of the total accessions had proportion of nodes with pistillate flowers (PNPF) values that decreased by more than 40% in early autumn, among which 71.3% showed a statistical significance (p < 0.05) (Fig. 1b). These results indicated that the response of femaleness to seasonal change is a germplasm-wide manner

Summary

Introduction

Cucumbers (Cucumis sativus) are known for their plasticity in sex expression. DNA methylation status determines gene activity but is susceptible to environmental condition changes. DNA methylation-based epigenetic regulation may at least partially account for the instability of cucumber sex expression. Do temperature and photoperiod that are the two most important environmental factors have equal effect on cucumber sex expression by similar epigenetic regulation mechanism? The female/male flower ratio in cucumbers is largely unstable, which is affected by environment condition change. The effects of light intensity [2], light quality [3], nitrogen and watering stress [4], and mechanical stress [5] have been reported These environmental factors are relatively less decisive than temperature and photoperiod of which effects on cucumber sex expression have been characterized many years ago [2, 4, 6,7,8,9]. The phenomenon of environment-dependent sex expression is restricted to cucumbers but seem a common feature in higher plants [10]

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Conclusion