Comparative Proteomic Analysis of Developmental Changes in P-Type Cytoplasmic Male Sterile and Maintainer Anthers in Wheat

Abstract

Cytoplasmic male sterility (CMS) plays an important role in the application of heterosis in wheat (Triticum aestivum L.). However, the molecular mechanism underlying CMS remains unknown. This study provides a comprehensive morphological and proteomic analysis of the anthers of a P-type CMS wheat line (P) and its maintainer line, Yanshi 9 hao (Y). Cytological observations indicated that the P-type CMS line shows binucleate microspore abortion. In this line, the tapetum degraded early, leading to anther cuticle defects, which could not provide the nutrition needed for microspore development in a timely manner, thus preventing the development of the microspore to the normal binucleate stage. Proteomic analysis revealed novel proteins involved in P-type CMS. Up to 2576 differentially expressed proteins (DEPs) were quantified in all anthers, and these proteins were significantly enriched in oxidative phosphorylation, glycolysis/gluconeogenesis, citrate cycle (TCA cycle), starch and sucrose metabolism, phenylpropanoid biosynthesis, and pyruvate metabolism pathways. These proteins may comprise a network that regulates male sterility in wheat. Based on the function analysis of DEPs involved in the complex network, we concluded that the P-type CMS line may be due to cellular dysfunction caused by disturbed carbohydrate metabolism, inadequate energy supply, and disturbed protein synthesis. These results provide insights into the molecular mechanism underlying male sterility and serve as a valuable resource for researchers in plant biology, in general, and plant sexual reproduction, in particular.

Proteomic and Phosphoproteomic Analyses Reveal a Complex Network Regulating Pollen Abortion and Potential Candidate Proteins in TCMS Wheat

“…Two phosphoproteins (W5FM32 and A0A3B6HPU7) with unclear functions possessed 27 and 32 phosphosites, respectively. Compared with previous studies on cereal crops, more proteins and phosphosites were detected in the present experiment [ 8 , 11 , 18 , 19 , 20 ] ( Supplementary Materials Figure S3 ).…”

“…DAPs and DAPPs were enriched and significantly down-regulated in the fatty acid biosynthesis, elongation and the cutin, suberine and wax biosynthesis pathways ( Supplementary Materials Table S4 ). The cutin, suberine, and wax biosynthesis pathways are critical for the normal development of anthers at an early uninucleate stage in the P-type CMS of wheat [ 20 ]. The diffusion of cutin and wax onto the surface of anther cell walls is essential for maintaining pollen morphology [ 23 ].…”

Integrated Methylome and Transcriptome Analysis Widen the Knowledge of Cytoplasmic Male Sterility in Cotton (Gossypium barbadense L.)

“…Transcriptome sequencing (RNA-Seq) can provide the expression information of thousands of genes in a single experiment and has greatly contributed to the development of functional genomics. With the development of high-throughput sequencing and bioinformatic technologies, CMS-related genes have been identified through the construction of transcriptional regulatory networks, which are related to the tricarboxylic acid (TCA) cycle, oxidative phosphorylation, respiratory electron transport chain, toxic proteins, and carbohydrate metabolism ( Wu et al, 2013 ; Liao et al, 2016 ; Mei et al, 2016 ; Kong et al, 2017a ; Chen et al, 2018 ; Tang et al, 2018 ; Li et al, 2019 , 2021 ; Ning et al, 2019 ; Zheng et al, 2019 ; Zhang et al, 2021 ). Therefore, comparative transcriptome analysis has been widely used to study the molecular mechanisms of CMS in plants, including the red flax CMS line P3A ( Chen et al, 2014 ), the soybean CMS line NJCMS1A ( Li et al, 2015a ), the Welsh onion CMS line 64-2 ( Liu et al, 2016 ), and the cabbage CMS line PM ( Wang et al, 2016 ).…”

Transcriptome and MiRNAomics Analyses Identify Genes Associated with Cytoplasmic Male Sterility in Cotton (Gossypium hirsutum L.)

“…Altered metabolic pathways influence the biological processes leading to CMS [ 7 ]. With the development of the technology for high-throughput sequencing and bioinformatics, CMS-related genes are discovered through the construction of transcription regulatory networks, which are related to the tricarboxylic acid (TCA) cycle, oxidative phosphorylation, respiratory electron transport chain, toxic proteins, and carbohydrate metabolism [ 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 ]. Besides, miRNA also plays an important role in flower development in plants [ 32 ].…”