Transcriptomics reveals a core transcriptional network of K-type cytoplasmic male sterility microspore abortion in wheat (Triticum aestivum L.)

Abstract Background Cytoplasmic 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 resto...

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Main Authors: Baolin Wu, Yu Xia, Gaisheng Zhang, Yongqing Wang, Junwei Wang, Shoucai Ma, Yulong Song, Zhiquan Yang, Lingjian Ma, Na Niu
Format: Article
Language:English
Published: BMC 2023-12-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04611-2
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author Baolin Wu
Yu Xia
Gaisheng Zhang
Yongqing Wang
Junwei Wang
Shoucai Ma
Yulong Song
Zhiquan Yang
Lingjian Ma
Na Niu
author_facet Baolin Wu
Yu Xia
Gaisheng Zhang
Yongqing Wang
Junwei Wang
Shoucai Ma
Yulong Song
Zhiquan Yang
Lingjian Ma
Na Niu
author_sort Baolin Wu
collection DOAJ
description Abstract Background Cytoplasmic 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. Results In 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. Conclusions We 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.
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spelling doaj.art-e0c9f15eb7ec4294ae8e954499a887e12023-12-10T12:13:13ZengBMCBMC Plant Biology1471-22292023-12-0123112110.1186/s12870-023-04611-2Transcriptomics reveals a core transcriptional network of K-type cytoplasmic male sterility microspore abortion in wheat (Triticum aestivum L.)Baolin Wu0Yu Xia1Gaisheng Zhang2Yongqing Wang3Junwei Wang4Shoucai Ma5Yulong Song6Zhiquan Yang7Lingjian Ma8Na Niu9College of Agronomy, Northwest A & F University, Key Laboratory of Crop Heterosis of Shaanxi Province, Wheat Breeding Engineering Research Center, Ministry of EducationCollege of Agronomy, Northwest A & F University, Key Laboratory of Crop Heterosis of Shaanxi Province, Wheat Breeding Engineering Research Center, Ministry of EducationCollege of Agronomy, Northwest A & F University, Key Laboratory of Crop Heterosis of Shaanxi Province, Wheat Breeding Engineering Research Center, Ministry of EducationCollege of Agronomy, Northwest A & F University, Key Laboratory of Crop Heterosis of Shaanxi Province, Wheat Breeding Engineering Research Center, Ministry of EducationCollege of Agronomy, Northwest A & F University, Key Laboratory of Crop Heterosis of Shaanxi Province, Wheat Breeding Engineering Research Center, Ministry of EducationCollege of Agronomy, Northwest A & F University, Key Laboratory of Crop Heterosis of Shaanxi Province, Wheat Breeding Engineering Research Center, Ministry of EducationCollege of Agronomy, Northwest A & F University, Key Laboratory of Crop Heterosis of Shaanxi Province, Wheat Breeding Engineering Research Center, Ministry of EducationCollege of Agronomy, Northwest A & F University, Key Laboratory of Crop Heterosis of Shaanxi Province, Wheat Breeding Engineering Research Center, Ministry of EducationCollege of Agronomy, Northwest A & F University, Key Laboratory of Crop Heterosis of Shaanxi Province, Wheat Breeding Engineering Research Center, Ministry of EducationCollege of Agronomy, Northwest A & F University, Key Laboratory of Crop Heterosis of Shaanxi Province, Wheat Breeding Engineering Research Center, Ministry of EducationAbstract Background Cytoplasmic 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. Results In 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. Conclusions We 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.https://doi.org/10.1186/s12870-023-04611-2Cytoplasmic male sterilityTranscriptome sequencingPlant hormoneMAPK pathwaySpliceosomeWheat
spellingShingle Baolin Wu
Yu Xia
Gaisheng Zhang
Yongqing Wang
Junwei Wang
Shoucai Ma
Yulong Song
Zhiquan Yang
Lingjian Ma
Na Niu
Transcriptomics reveals a core transcriptional network of K-type cytoplasmic male sterility microspore abortion in wheat (Triticum aestivum L.)
BMC Plant Biology
Cytoplasmic male sterility
Transcriptome sequencing
Plant hormone
MAPK pathway
Spliceosome
Wheat
title Transcriptomics reveals a core transcriptional network of K-type cytoplasmic male sterility microspore abortion in wheat (Triticum aestivum L.)
title_full Transcriptomics reveals a core transcriptional network of K-type cytoplasmic male sterility microspore abortion in wheat (Triticum aestivum L.)
title_fullStr Transcriptomics reveals a core transcriptional network of K-type cytoplasmic male sterility microspore abortion in wheat (Triticum aestivum L.)
title_full_unstemmed Transcriptomics reveals a core transcriptional network of K-type cytoplasmic male sterility microspore abortion in wheat (Triticum aestivum L.)
title_short Transcriptomics reveals a core transcriptional network of K-type cytoplasmic male sterility microspore abortion in wheat (Triticum aestivum L.)
title_sort transcriptomics reveals a core transcriptional network of k type cytoplasmic male sterility microspore abortion in wheat triticum aestivum l
topic Cytoplasmic male sterility
Transcriptome sequencing
Plant hormone
MAPK pathway
Spliceosome
Wheat
url https://doi.org/10.1186/s12870-023-04611-2
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