Characterization and transcriptome analysis of a dominant genic male sterile cotton mutant

Xin-Qi Cheng,Yan-Jun Li,Xin-Yu Zhang,Shou-Hong Zhu,Qian-Hao Zhu,Feng Liu,Fei Xue,Jie Sun

doi:10.1186/s12870-020-02522-0

Abstract

BackgroundMale sterility is an efficient trait for hybrid seed production and germplasm innovation. Until now, most studies on male sterility were on cytoplasmic and recessive genic sterility, with few on dominant genic male sterility, especially in cotton, due to lack of such mutant.ResultsWe discovered a natural male sterile (MS) Sea Island cotton (G. barbadense) mutant. Genetic analysis showed the mutation was caused by a dominant mutation in a single nuclear gene. Comparative cytological observation of anther sections from MS and wild-type (WT) uncovered cellular differences in anther at and after the tetrad stage of pollen mother cells (PMC). In the MS anthers, the outer wall of pollen grains was free of spinules, the tapetum was vacuolated and showed delayed degradation, consequently, no functional pollen grains. Comparison of transcriptomes from meiosis, tetrad, mononuclear and binuclear pollen, and pollen maturation stages identified 13,783 non-redundant differentially expressed genes (DEGs) between MS and WT. Based on the number of DEGs, analyses of enriched GO terms and KEGG pathways, it was evident that significant transcriptomic changes occurred at and after the tetrad stage, consistent with cytological observation, and that the major differences were on metabolism of starch, sucrose, ascorbate, aldarate, alanine, aspartate and glutamate, and biosynthesis of cutin, suberine and wax. WGCNA analysis identified five modules containing 920 genes highly related to anther development, especially the greenyellow module with 54 genes that was highly associated with PMC meiosis and tetrad formation. A NAC transcription factor (Gh_D11G2469) was identified as a hub gene for this module, which warrants further functional characterization.ConclusionsWe demonstrated that the MS trait was controlled by a single dominant nuclear gene and caused by delayed tapetum degradation at the tetrad stage. Comparative transcriptome analysis and gene network construction identified DEGs, enriched GO terms and metabolic pathways, and hub genes potentially associated with anther development and the MS trait. These results contribute to our understanding of dominant genic male sterility (DGMS) and provided source for innovation of cotton germplasm.

Highlights

Male sterility is an efficient trait for hybrid seed production and germplasm innovation
Genetic analysis of the male sterile trait After discovery of the male sterile mutant, the male sterile trait has been transferred to Shida 98–6 (G. hirsutum) or Xinhai 53 (G. barbadense) background by five times of backcross using the sterile segregants as the female parent and Shida 98–6 or Xinhai 53 as the pollen donor
These results suggest that the male sterile trait was caused by a single dominant nuclear gene that can only be maintained in heterozygotes

Summary

Introduction

Male sterility is an efficient trait for hybrid seed production and germplasm innovation. Male sterility generally refers to a biological trait in which monoecious plants maintain fully normal female functions, while male gametes cannot be produced. Male sterility is typically divided into cytoplasmic sterility (CMS) and genic male sterility (GMS) [1]. GMS, controlled by nuclear genes, is generally recessive mutations which affect a huge number of biological functions of plants [3]. Male sterility is an effective pollination control system and an important tool for hybrid seed production. Many studies have probed physiological and biochemical changes during pollen and anther development in different plant species, and investigated the mechanisms of gene regulation and metabolism related to pollen development [4,5,6,7,8]. Some studies have identified key genes involved in pollen and anther development [9], such as MALE STERILITY 2 (MS2), CYP703A2, and CYP704B1 [10,11,12] that are involved in anther cell differentiation and division, pollen cell wall development, and anther dehiscence [13,14,15,16,17,18]

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