Comparative transcriptome analysis reveals that tricarboxylic acid cycle-related genes are associated with maize CMS-C fertility restoration

Abstract Background C-type cytoplasmic male sterility (CMS-C) is one of the three major types of cytoplasmic male sterility (CMS) in maize. Rf4 is a dominant restorer gene for CMS-C and has great value in hybrid maize breeding, but little information concerning its functional mechanism is known. Res...

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Main Authors: Yongming Liu, Gui Wei, Yuanyan Xia, Xiaowei Liu, Jin Tang, Yanli Lu, Hai Lan, Suzhi Zhang, Chuan Li, Moju Cao
Format: Article
Language:English
Published: BMC 2018-09-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-018-1409-z
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author Yongming Liu
Gui Wei
Yuanyan Xia
Xiaowei Liu
Jin Tang
Yanli Lu
Hai Lan
Suzhi Zhang
Chuan Li
Moju Cao
author_facet Yongming Liu
Gui Wei
Yuanyan Xia
Xiaowei Liu
Jin Tang
Yanli Lu
Hai Lan
Suzhi Zhang
Chuan Li
Moju Cao
author_sort Yongming Liu
collection DOAJ
description Abstract Background C-type cytoplasmic male sterility (CMS-C) is one of the three major types of cytoplasmic male sterility (CMS) in maize. Rf4 is a dominant restorer gene for CMS-C and has great value in hybrid maize breeding, but little information concerning its functional mechanism is known. Results To reveal the functional mechanism of Rf4, we developed a pair of maize near-isogenic lines (NILs) for the Rf4 locus, which included a NIL_rf4 male-sterile line and a NIL_Rf4 male fertility-restored line. Genetic analysis and molecular marker detection indicated that the male fertility of NIL_Rf4 was controlled by Rf4. Whole-genome sequencing demonstrated genomic differences between the two NILs was clustered in the Rf4 mapping region. Unmapped reads of NILs were further assembled to uncover Rf4 candidates. RNA-Seq was then performed for the developing anthers of the NILs to identify critical genes and pathways associated with fertility restoration. A total of 7125 differentially expressed genes (DEGs) were identified. These DEGs were significantly enriched in 242 Gene Ontology (GO) categories, wherein 100 DEGs were involved in pollen tube development, pollen tube growth, pollen development, and gametophyte development. Homology analysis revealed 198 male fertility-related DEGs, and pathway enrichment analysis revealed that 58 DEGs were enriched in cell energy metabolism processes involved in glycolysis, the pentose phosphate pathway, and pyruvate metabolism. By querying the Plant Reactome Pathway database, we found that 14 of the DEGs were involved in the mitochondrial tricarboxylic acid (TCA) cycle and that most of them belonged to the isocitrate dehydrogenase (IDH) and oxoglutarate dehydrogenase (OGDH) enzyme complexes. Transcriptome sequencing and real-time quantitative PCR (qPCR) showed that all the above TCA cycle-related genes were up-regulated in NIL_Rf4. The results of our subsequent enzyme-linked immunosorbent assay (ELISA) experiments pointed out that the contents of both the IDH and OGDH enzymes accumulated more in the spikelets of NIL_Rf4 than in those of NIL_rf4. Conclusion The present research provides valuable genomic resources for deep insight into the molecular mechanism underlying CMS-C male fertility restoration. Importantly, our results indicated that genes involved in energy metabolism, especially some mitochondrial TCA cycle-related genes, were associated with maize CMS-C male fertility restoration.
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spelling doaj.art-5e24956ab8b545b6bc9a8fc19a413b4d2022-12-21T19:27:36ZengBMCBMC Plant Biology1471-22292018-09-0118111410.1186/s12870-018-1409-zComparative transcriptome analysis reveals that tricarboxylic acid cycle-related genes are associated with maize CMS-C fertility restorationYongming Liu0Gui Wei1Yuanyan Xia2Xiaowei Liu3Jin Tang4Yanli Lu5Hai Lan6Suzhi Zhang7Chuan Li8Moju Cao9Key Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural UniversityKey Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural UniversityKey Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural UniversityKey Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural UniversityKey Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural UniversityKey Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural UniversityKey Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural UniversityKey Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural UniversityKey Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural UniversityKey Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural UniversityAbstract Background C-type cytoplasmic male sterility (CMS-C) is one of the three major types of cytoplasmic male sterility (CMS) in maize. Rf4 is a dominant restorer gene for CMS-C and has great value in hybrid maize breeding, but little information concerning its functional mechanism is known. Results To reveal the functional mechanism of Rf4, we developed a pair of maize near-isogenic lines (NILs) for the Rf4 locus, which included a NIL_rf4 male-sterile line and a NIL_Rf4 male fertility-restored line. Genetic analysis and molecular marker detection indicated that the male fertility of NIL_Rf4 was controlled by Rf4. Whole-genome sequencing demonstrated genomic differences between the two NILs was clustered in the Rf4 mapping region. Unmapped reads of NILs were further assembled to uncover Rf4 candidates. RNA-Seq was then performed for the developing anthers of the NILs to identify critical genes and pathways associated with fertility restoration. A total of 7125 differentially expressed genes (DEGs) were identified. These DEGs were significantly enriched in 242 Gene Ontology (GO) categories, wherein 100 DEGs were involved in pollen tube development, pollen tube growth, pollen development, and gametophyte development. Homology analysis revealed 198 male fertility-related DEGs, and pathway enrichment analysis revealed that 58 DEGs were enriched in cell energy metabolism processes involved in glycolysis, the pentose phosphate pathway, and pyruvate metabolism. By querying the Plant Reactome Pathway database, we found that 14 of the DEGs were involved in the mitochondrial tricarboxylic acid (TCA) cycle and that most of them belonged to the isocitrate dehydrogenase (IDH) and oxoglutarate dehydrogenase (OGDH) enzyme complexes. Transcriptome sequencing and real-time quantitative PCR (qPCR) showed that all the above TCA cycle-related genes were up-regulated in NIL_Rf4. The results of our subsequent enzyme-linked immunosorbent assay (ELISA) experiments pointed out that the contents of both the IDH and OGDH enzymes accumulated more in the spikelets of NIL_Rf4 than in those of NIL_rf4. Conclusion The present research provides valuable genomic resources for deep insight into the molecular mechanism underlying CMS-C male fertility restoration. Importantly, our results indicated that genes involved in energy metabolism, especially some mitochondrial TCA cycle-related genes, were associated with maize CMS-C male fertility restoration.http://link.springer.com/article/10.1186/s12870-018-1409-zMaizeCytoplasmic male sterilityFertility restorationOxoglutarate dehydrogenaseIsocitrate dehydrogenaseTranscriptome sequencing
spellingShingle Yongming Liu
Gui Wei
Yuanyan Xia
Xiaowei Liu
Jin Tang
Yanli Lu
Hai Lan
Suzhi Zhang
Chuan Li
Moju Cao
Comparative transcriptome analysis reveals that tricarboxylic acid cycle-related genes are associated with maize CMS-C fertility restoration
BMC Plant Biology
Maize
Cytoplasmic male sterility
Fertility restoration
Oxoglutarate dehydrogenase
Isocitrate dehydrogenase
Transcriptome sequencing
title Comparative transcriptome analysis reveals that tricarboxylic acid cycle-related genes are associated with maize CMS-C fertility restoration
title_full Comparative transcriptome analysis reveals that tricarboxylic acid cycle-related genes are associated with maize CMS-C fertility restoration
title_fullStr Comparative transcriptome analysis reveals that tricarboxylic acid cycle-related genes are associated with maize CMS-C fertility restoration
title_full_unstemmed Comparative transcriptome analysis reveals that tricarboxylic acid cycle-related genes are associated with maize CMS-C fertility restoration
title_short Comparative transcriptome analysis reveals that tricarboxylic acid cycle-related genes are associated with maize CMS-C fertility restoration
title_sort comparative transcriptome analysis reveals that tricarboxylic acid cycle related genes are associated with maize cms c fertility restoration
topic Maize
Cytoplasmic male sterility
Fertility restoration
Oxoglutarate dehydrogenase
Isocitrate dehydrogenase
Transcriptome sequencing
url http://link.springer.com/article/10.1186/s12870-018-1409-z
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