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Identification and profiling of microRNAs and differentially expressed genes during anther development between a genetic male-sterile mutant and its wildtype cotton via high-throughput RNA sequencing.

ABSTRACT: Genetic male sterility (GMS) facilitates hybrid seed production in crops including cotton (Gossypium hirsutum). However, the genetic and molecular mechanisms specifically involved in this developmental process are poorly understood. In this study, small RNA sequencing, degradome sequencing, and transcriptome sequencing were performed to analyze miRNAs and their target genes during anther development in a GMS mutant ('Dong A') and its fertile wildtype (WT). A total of 80 known and 220 novel miRNAs were identified, 71 of which showed differential expressions during anther development. A further degradome sequencing revealed a total of 117 candidate target genes cleaved by 16 known and 36 novel miRNAs. Based on RNA-seq, 24, 11, and 21 predicted target genes showed expression correlations with the corresponding miRNAs at the meiosis, tetrad and uninucleate stages, respectively. In addition, a large number of differentially expressed genes were identified, most of which were involved in sucrose and starch metabolism, carbohydrate metabolism, and plant hormone signal transduction based on Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis. The results of our study provide valuable information for further functional investigations of the important miRNAs and target genes involved in genetic male sterility and advance our understanding of miRNA regulatory functions during cotton anther development.

SUBMITTER: Yu D

PROVIDER: S-EPMC7203095 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundCotton (Gossypium hirsutum) anther development involves a diverse range of gene interactions between sporophytic and gametophytic tissues. However, only a small number of genes are known to be specifically involved in this developmental process and the molecular mechanism of the genetic male sterility (GMS) is still poorly understand. To fully explore the global gene expression during cotton anther development and identify genes related to male sterility, a digital gene expression (DGE) analysis was adopted.ResultsSix DGE libraries were constructed from the cotton anthers of the wild type (WT) and GMS mutant (in the WT background) in three stages of anther development, resulting in 21,503 to 37,352 genes detected in WT and GMS mutant anthers. Compared with the fertile isogenic WT, 9,595 (30% of the expressed genes), 10,407 (25%), and 3,139 (10%) genes were differentially expressed at the meiosis, tetrad, and uninucleate microspore stages of GMS mutant anthers, respectively. Using both DGE experiments and real-time quantitative RT-PCR, the expression of many key genes required for anther development were suppressed in the meiosis stage and the uninucleate microspore stage in anthers of the mutant, but these genes were activated in the tetrad stage of anthers in the mutant. These genes were associated predominantly with hormone synthesis, sucrose and starch metabolism, the pentose phosphate pathway, glycolysis, flavonoid metabolism, and histone protein synthesis. In addition, several genes that participate in DNA methylation, cell wall loosening, programmed cell death, and reactive oxygen species generation/scavenging were activated during the three anther developmental stages in the mutant.ConclusionsCompared to the same anther developmental stage of the WT, many key genes involved in various aspects of anther development show a reverse gene expression pattern in the GMS mutant, which indicates that diverse gene regulation pathways are involved in the GMS mutant anther development. These findings provide the first insights into the mechanism that leads to genetic male sterility in cotton and contributes to a better understanding of the regulatory network involved in anther development in cotton.

Project description: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.

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Identification and profiling of microRNAs and differentially expressed genes during anther development between a genetic male-sterile mutant and its wildtype cotton via high-throughput RNA sequencing.

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