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

ABSTRACT: Cytoplasmic male sterility (CMS) is important for large-scale hybrid seed production. Rearrangements in the mitochondrial DNA (mtDNA) for the cotton (Gossypium hirsutum L.) CMS line J4A were responsible for pollen abortion. However, the expression patterns of nuclear genes associated with pollen abortion and the molecular basis of CMS for J4A are unknown, and were the objectives of this study by comparing J4A with the J4B maintainer line. Cytological evaluation of J4A anthers showed that microspore abortion occurs during meiosis preventing pollen development. Changes in enzyme activity of mitochondrial respiratory chain complex IV and mitochondrial respiratory chain complex V and the content of ribosomal protein and ATP during anther abortion were observed for J4A suggesting insufficient synthesis of ATP hindered pollen production. Additionally, levels of sucrose, starch, soluble sugar, and fructose were significantly altered in J4A during the meiosis stage, suggesting reduced sugar metabolism contributed to sterility. Transcriptome and miRNAomics analyses identified 4461 differentially expressed mRNAs (DEGs) and 26 differentially expressed microRNAs (DEMIs). Pathway enrichment analysis indicated that the DEMIs were associated with starch and sugar metabolism. Six deduced target gene regulatory pairs that may participate in CMS were identified, ghi-MIR7484-10/mitogen-activated protein kinase kinase 6 (MAPKK6), ghi-undef-156/agamous-like MADS-box protein AGL19 (AGL19), ghi-MIR171-1-22/SNF1-related protein kinase regulatory subunit gamma-1 and protein trichome birefringence-like 38, and ghi-MIR156-(8/36)/WRKY transcription factor 28 (WRKY28). Overall, a putative CMS mechanism involving mitochondrial dysfunction, the ghi-MIR7484-10/MAPKK6 network, and reduced glucose metabolism was suggested, and ghi-MIR7484-10/MAPKK6 may be related to abnormal microspore meiosis and induction of excessive sucrose accumulation in anthers.

SUBMITTER: Li M

PROVIDER: S-EPMC8124215 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Cotton (Gossypium hirsutum L.) is one of the most important cash crops worldwide. Cytoplasmic male sterility (CMS) is an excellent breeding system for exploitation of heterosis, which has great potential to increase crop yields. To understand the molecular mechanism of CMS in cotton, we compared transcriptome, cytomorphological, physiological and bioinformatics data between the CMS line C2P5A and its maintainer line C2P5B. By using high-throughput sequencing technology, 178,166 transcripts were assembled and 2013 differentially expression genes (DEGs) were identified at three different stages of C2P5A anther development. In this study, we identified DEGs associated with reactive oxygen species (ROS), peroxisomes, aldehyde dehydrogenases (ALDH), cytochrome oxidase subunit VI, and cytochrome P450, and DEGs associated with tapetum development, Jojoba acyl-CoA reductase-related male sterility protein, basic helix-loop-helix (bHLH) and MYB transcription factors. The abnormal expression of one of these genes may be responsible for the CMS C2P5A line. In gene ontology (GO) annotation and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment, DEGs were mainly related to carbohydrate metabolism, amino acid metabolism, transport and catabolism, and signal transduction. Carbohydrate metabolism provides energy for anther development, starch and sucrose metabolism, fatty acid biosynthesis and metabolism and ascorbate and aldarate metabolism. These results showed that numerous genes and multiple complex metabolic pathways regulate cotton anther development. Weighted correlation network analysis (WGCNA) indicated that three modules, 'turquoise,' 'blue,' and 'green,' were specific for the CMS C2P5A line. The 'turquoise' and 'blue' modules were mainly related to carbohydrate metabolism, amino acid metabolism, energy metabolism, peroxisomes, pyruvate metabolism as well as fatty acid degradation. The 'green' module was mainly related to energy metabolism, carbon metabolism, translation, and lipid metabolism. RNA-sequencing and WGCNA polymerization modules were screened for key genes and pathways related to CMS in cotton. This study presents a new perspective for further research into the metabolic pathways of pollen abortion in the CMS C2P5A line and also provides a theoretical basis for its breeding and production.

Project description:Abiotic stress is a major environmental factor that limits cotton growth and yield, moreover, this problem has become more and more serious recently, as multiple stresses often occur simultaneously due to the global climate change and environmental pollution. In this study, we sought to identify genes involved in diverse stresses including abscisic acid (ABA), cold, drought, salinity and alkalinity by comparative microarray analysis. Our result showed that 5790, 3067, 5608, 778 and 6148 transcripts, were differentially expressed in cotton seedlings under treatment of ABA (1 μM ABA), cold (4°C), drought (200 mM mannitol), salinity (200 mM NaCl) and alkalinity (pH=11) respectively. Among the induced or suppressed genes, 126 transcripts were shared by all of the five kinds of abiotic stresses, with 64 up-regulated and 62 down-regulated. These common members are grouped as stress signal transduction, transcription factors (TFs), stress response/defense proteins, metabolism, transport facilitation, as well as cell wall/structure, according to the function annotation. We also noticed that large proportion of significant differentially expressed genes specifically regulated in response to different stress. Nine of the common transcripts of multiple stresses were selected for further validation with quantitative real time RT-PCR (qRT-PCR). Furthermore, several well characterized TF families, for example, WRKY, MYB, NAC, AP2/ERF and zinc finger were shown to be involved in different stresses. As an original report using comparative microarray to analyze transcriptome of cotton under five abiotic stresses, valuable information about functional genes and related pathways of anti-stress, and/or stress tolerance in cotton seedlings was unveiled in our result. Besides this, some important common factors were focused for detailed identification and characterization. According to our analysis, it suggested that there was crosstalk of responsive genes or pathways to multiple abiotic or even biotic stresses, in cotton. These candidate genes will be worthy of functional study under diverse stresses.

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

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