DNA methylation-mediated phenylpropane and starch metabolism causes male poplars to be more tolerant to nitrogen deficiency than females

Abstract

Nitrogen (N) is an essential nutrient for plant growth and development. Dioecious plants, especially perennial plants, are often faced with a shortage of N supply in nature. Poplar is one of the most important dioecious and perennials species. Due to the different ecological functions, female and male poplars adopt different adaptation strategies to N limitation. However, the regulation in epigenetic mechanism is poorly understood on sexes. Here, the integrative analysis of whole-genome bisulfite sequencing (WGBS), RNA sequencing, and plant physiological analysis on female and male Populus cathayana were performed. We found that N deficiency reprograms methylation in both sexes, and the CG and CHH methylation types played critical roles in female and male poplars, respectively. Induced by DNA methylation, N-deficient males had a stronger phenylpropanoid synthesis pathway and less anthocyanin accumulation than females, which not only strengthened the N cycle but also reduced the defense cost of males. In addition, compared with male poplars, females accumulated more starch to expend excess energy under N limited condition. Additionally, DNA methylation also mediated hormone signalling involved in anthocyanin synthesis and starch metabolism. Therefore, our study reveals new molecular evidences that male poplars are more tolerant to N deficiency than females, which provides a reference for ecological adaptability of forest trees.