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The Major Factors Causing the Microspore Abortion of Genic Male Sterile Mutant NWMS1 in Wheat (Triticum aestivum L.).

ABSTRACT: Male sterility is a valuable trait for genetic research and production application of wheat (Triticum aestivum L.). NWMS1, a novel typical genic male sterility mutant, was obtained from Shengnong 1, mutagenized with ethyl methane sulfonate (EMS). Microstructure and ultrastructure observations of the anthers and microspores indicated that the pollen abortion of NWMS1 started at the early uninucleate microspore stage. Pollen grain collapse, plasmolysis, and absent starch grains were the three typical characteristics of the abnormal microspores. The anther transcriptomes of NWMS1 and its wild type Shengnong 1 were compared at the early anther development stage, pollen mother cell meiotic stage, and binucleate microspore stage. Several biological pathways clearly involved in abnormal anther development were identified, including protein processing in endoplasmic reticulum, starch and sucrose metabolism, lipid metabolism, and plant hormone signal transduction. There were 20 key genes involved in the abnormal anther development, screened out by weighted gene co-expression network analysis (WGCNA), including SKP1B, BIP5, KCS11, ADH3, BGLU6, and TIFY10B. The results indicated that the defect in starch and sucrose metabolism was the most important factor causing male sterility in NWMS1. Based on the experimental data, a primary molecular regulation model of abnormal anther and pollen developments in mutant NWMS1 was established. These results laid a solid foundation for further research on the molecular mechanism of wheat male sterility.

SUBMITTER: Li J

PROVIDER: S-EPMC6940770 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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The Major Factors Causing the Microspore Abortion of Genic Male Sterile Mutant NWMS1 in Wheat (Triticum aestivum L.).

Li Junchang J Zhang Jing J Li Huijuan H Niu Hao H Xu Qiaoqiao Q Jiao Zhixin Z An Junhang J Jiang Yumei Y Li Qiaoyun Q Niu Jishan J

International journal of molecular sciences 20191211 24

Male sterility is a valuable trait for genetic research and production application of wheat (Triticum aestivum L.). NWMS1, a novel typical genic male sterility mutant, was obtained from Shengnong 1, mutagenized with ethyl methane sulfonate (EMS). Microstructure and ultrastructure observations of the anthers and microspores indicated that the pollen abortion of NWMS1 started at the early uninucleate microspore stage. Pollen grain collapse, plasmolysis, and absent starch grain ...[more]

PMID: 31835796

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Project description:BackgroundCytoplasmic male sterility (CMS) plays a crucial role in hybrid production. K-type CMS, a cytoplasmic male sterile line of wheat with the cytoplasms of Aegilops kotschyi, is widely used due to its excellent characteristics of agronomic performance, easy maintenance and easy restoration. However, the mechanism of its pollen abortion is not yet clear.ResultsIn this study, wheat K-type CMS MS(KOTS)-90-110 (MS line) and it's fertile near-isogenic line MR (KOTS)-90-110 (MR line) were investigated. Cytological analysis indicated that the anthers of MS line microspore nucleus failed to divide normally into two sperm nucleus and lacked starch in mature pollen grains, and the key abortive period was the uninucleate stage to dinuclear stage. Then, we compared the transcriptome of MS line and MR line anthers at these two stages. 11,360 and 5182 differentially expressed genes (DEGs) were identified between the MS and MR lines in the early uninucleate and binucleate stages, respectively. Based on GO enrichment and KEGG pathways analysis, it was evident that significant transcriptomic differences were "plant hormone signal transduction", "MAPK signaling pathway" and "spliceosome". We identified 17 and 10 DEGs associated with the IAA and ABA signal transduction pathways, respectively. DEGs related to IAA signal transduction pathway were downregulated in the early uninucleate stage of MS line. The expression level of DEGs related to ABA pathway was significantly upregulated in MS line at the binucleate stage compared to MR line. The determination of plant hormone content and qRT-PCR further confirmed that hormone imbalance in MS lines. Meanwhile, 1 and 2 DEGs involved in ABA and Ethylene metabolism were also identified in the MAPK cascade pathway, respectively; the significant up regulation of spliceosome related genes in MS line may be another important factor leading to pollen abortion.ConclusionsWe proposed a transcriptome-mediated pollen abortion network for K-type CMS in wheat. The main idea is hormone imbalance may be the primary factor, MAPK cascade pathway and alternative splicing (AS) may also play important regulatory roles in this process. These findings provided intriguing insights for the molecular mechanism of microspore abortion in K-type CMS, and also give useful clues to identify the crucial genes of CMS in wheat.

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.

Project description:BACKGROUND:Aegilops crassa cytoplasm is an important source for investigating cytoplasmic male sterility (CMS). Moreover, the stamens of line C303A exhibit a high degree of pistillody, turning almost white. However, the molecular mechanism that underlies pistillody in C303A remains unclear. Therefore, to obtain a better understanding of pistillody in C303A, the phenotypic and cytological features of C303A were observed to identify the key stage for the homeotic transformation of stamens into pistil-like structures. Transcriptome profiles were determined for stamens using Illumina RNA sequencing. RESULTS:Morphological observations of the CMS wheat line with Aegilops crassa cytoplasm C303A showed that the pistils developed normally, but the stamens were ultimately aborted and they released no pollen when mature. According to paraffin section observations, the stamens began to transform into pistils or pistil-like structures in the binucleate stage (BNS). Therefore, the stamens were collected from line C303A and its maintainer 303B in the BNS for transcriptome sequencing. In total, 20,444 wheat genes were determined as differentially expressed in C303A and 303B stamens, with 10,283 upregulated and 10,161 downregulated genes. Gene Ontology enrichment analyses showed that most of the differentially expressed genes (DEGs) were annotated with GO terms comprising metabolic process, cell, cellular process, catalytic activity, and cell part. Analysis based on the Kyoto Encyclopedia of Genes and Genomes database showed that the enriched DEGs were mainly associated with energy metabolism. We also found several essential genes that may contribute to pistillody in C303A. These findings suggest that disrupted energy metabolism and reactive oxygen metabolism induce pistillody and eventually lead to abortion in C303A. CONCLUSION:We determined the complex transcriptome profiles for C303A stamens and demonstrated that disrupted energy metabolism and class B MADS-box genes are related to pistillody. These findings may facilitate future studies of the mechanistic response of the wheat stamen and pollen development in CMS.

Dataset Information

The Major Factors Causing the Microspore Abortion of Genic Male Sterile Mutant NWMS1 in Wheat (Triticum aestivum L.).

Publications

The Major Factors Causing the Microspore Abortion of Genic Male Sterile Mutant <i>NWMS1</i> in Wheat (<i>Triticum aestivum</i> L.).

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