Comparative cytological and transcriptome analyses of ny2 mutant delayed degeneration of tapetal cells and promotes abnormal microspore development in neo-tetraploid rice

We aimed to investigate the genetic defects related to pollen development and infertility in NY2, a novel tetraploid rice germplasm known as Neo-tetraploid rice. This rice variety was created through the crossbreeding and selective breeding of various autotetraploid rice lines and has previously sho...

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Main Authors: Nabieu Kamara, Yamin Jiao, Weicong Huang, Lichong Cao, Lianjun Zhu, Chongchong Zhao, Xu Huang, Fimanekeni Ndaitavela Shivute, Xiangdong Liu, Jinwen Wu, Muhammad Qasim Shahid
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1229870/full
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author Nabieu Kamara
Nabieu Kamara
Nabieu Kamara
Nabieu Kamara
Nabieu Kamara
Yamin Jiao
Yamin Jiao
Yamin Jiao
Yamin Jiao
Weicong Huang
Weicong Huang
Weicong Huang
Weicong Huang
Lichong Cao
Lichong Cao
Lichong Cao
Lichong Cao
Lianjun Zhu
Lianjun Zhu
Lianjun Zhu
Lianjun Zhu
Chongchong Zhao
Chongchong Zhao
Chongchong Zhao
Chongchong Zhao
Xu Huang
Xu Huang
Xu Huang
Xu Huang
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Xiangdong Liu
Xiangdong Liu
Xiangdong Liu
Xiangdong Liu
Jinwen Wu
Jinwen Wu
Jinwen Wu
Jinwen Wu
Muhammad Qasim Shahid
Muhammad Qasim Shahid
Muhammad Qasim Shahid
Muhammad Qasim Shahid
author_facet Nabieu Kamara
Nabieu Kamara
Nabieu Kamara
Nabieu Kamara
Nabieu Kamara
Yamin Jiao
Yamin Jiao
Yamin Jiao
Yamin Jiao
Weicong Huang
Weicong Huang
Weicong Huang
Weicong Huang
Lichong Cao
Lichong Cao
Lichong Cao
Lichong Cao
Lianjun Zhu
Lianjun Zhu
Lianjun Zhu
Lianjun Zhu
Chongchong Zhao
Chongchong Zhao
Chongchong Zhao
Chongchong Zhao
Xu Huang
Xu Huang
Xu Huang
Xu Huang
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Xiangdong Liu
Xiangdong Liu
Xiangdong Liu
Xiangdong Liu
Jinwen Wu
Jinwen Wu
Jinwen Wu
Jinwen Wu
Muhammad Qasim Shahid
Muhammad Qasim Shahid
Muhammad Qasim Shahid
Muhammad Qasim Shahid
author_sort Nabieu Kamara
collection DOAJ
description We aimed to investigate the genetic defects related to pollen development and infertility in NY2, a novel tetraploid rice germplasm known as Neo-tetraploid rice. This rice variety was created through the crossbreeding and selective breeding of various autotetraploid rice lines and has previously shown high fertility. Our previous research has revealed that the NY2 gene, encoding a eukaryotic translation initiation factor 3 subunit E, regulates pollen fertility. However, the underlying mechanism behind this fertility is yet to be understood. To shed light on this matter, we performed a combined cytological and transcriptome analysis of the NY2 gene. Cytological analysis indicated that ny2 underwent abnormal tapetal cells, microspore, and middle layer development, which led to pollen abortion and ultimately to male sterility. Genetic analysis revealed that the F1 plants showed normal fertility and an obvious advantage for seed setting compared to ny2. Global gene expression analysis in ny2 revealed a total of 7545 genes were detected at the meiosis stage, and 3925 and 3620 displayed upregulation and downregulation, respectively. The genes were significantly enriched for the gene ontology (GO) term “carbohydrate metabolic process. Moreover, 9 genes related to tapetum or pollen fertility showed down-regulation, such as OsABCG26 (ATP Binding Cassette G26), TMS9-1 (Thermosensitive Male Sterility), EAT1 (Programmed cell death regulatory), KIN14M (Kinesin Motor), OsMT1a (Metallothionein), and OsSTRL2 (Atypical strictosidine synthase), which were validated by qRT-PCR. Further analyses of DEGs identified nine down-regulated transcription factor genes related to pollen development. NY2 is an important regulator of the development of tapetum and microspore. The regulatory gene network described in this study may offer important understandings into the molecular processes that underlie fertility control in tetraploid rice.
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spelling doaj.art-1cda86f8c8804d10b0c559869edc85d52023-07-17T10:57:03ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-07-011410.3389/fpls.2023.12298701229870Comparative cytological and transcriptome analyses of ny2 mutant delayed degeneration of tapetal cells and promotes abnormal microspore development in neo-tetraploid riceNabieu Kamara0Nabieu Kamara1Nabieu Kamara2Nabieu Kamara3Nabieu Kamara4Yamin Jiao5Yamin Jiao6Yamin Jiao7Yamin Jiao8Weicong Huang9Weicong Huang10Weicong Huang11Weicong Huang12Lichong Cao13Lichong Cao14Lichong Cao15Lichong Cao16Lianjun Zhu17Lianjun Zhu18Lianjun Zhu19Lianjun Zhu20Chongchong Zhao21Chongchong Zhao22Chongchong Zhao23Chongchong Zhao24Xu Huang25Xu Huang26Xu Huang27Xu Huang28Fimanekeni Ndaitavela Shivute29Fimanekeni Ndaitavela Shivute30Fimanekeni Ndaitavela Shivute31Fimanekeni Ndaitavela Shivute32Fimanekeni Ndaitavela Shivute33Xiangdong Liu34Xiangdong Liu35Xiangdong Liu36Xiangdong Liu37Jinwen Wu38Jinwen Wu39Jinwen Wu40Jinwen Wu41Muhammad Qasim Shahid42Muhammad Qasim Shahid43Muhammad Qasim Shahid44Muhammad Qasim Shahid45State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaCrop Improvement Programme, Rokupr Agricultural Research Center, Rokupr - Sierra Leone Agricultural Research Institute (SLARI), Freetown, Sierra LeoneState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaMulti-disciplinary Research Services, University of Namibia, Windhoek, NamibiaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Agriculture, South China Agricultural University, Guangzhou, ChinaWe aimed to investigate the genetic defects related to pollen development and infertility in NY2, a novel tetraploid rice germplasm known as Neo-tetraploid rice. This rice variety was created through the crossbreeding and selective breeding of various autotetraploid rice lines and has previously shown high fertility. Our previous research has revealed that the NY2 gene, encoding a eukaryotic translation initiation factor 3 subunit E, regulates pollen fertility. However, the underlying mechanism behind this fertility is yet to be understood. To shed light on this matter, we performed a combined cytological and transcriptome analysis of the NY2 gene. Cytological analysis indicated that ny2 underwent abnormal tapetal cells, microspore, and middle layer development, which led to pollen abortion and ultimately to male sterility. Genetic analysis revealed that the F1 plants showed normal fertility and an obvious advantage for seed setting compared to ny2. Global gene expression analysis in ny2 revealed a total of 7545 genes were detected at the meiosis stage, and 3925 and 3620 displayed upregulation and downregulation, respectively. The genes were significantly enriched for the gene ontology (GO) term “carbohydrate metabolic process. Moreover, 9 genes related to tapetum or pollen fertility showed down-regulation, such as OsABCG26 (ATP Binding Cassette G26), TMS9-1 (Thermosensitive Male Sterility), EAT1 (Programmed cell death regulatory), KIN14M (Kinesin Motor), OsMT1a (Metallothionein), and OsSTRL2 (Atypical strictosidine synthase), which were validated by qRT-PCR. Further analyses of DEGs identified nine down-regulated transcription factor genes related to pollen development. NY2 is an important regulator of the development of tapetum and microspore. The regulatory gene network described in this study may offer important understandings into the molecular processes that underlie fertility control in tetraploid rice.https://www.frontiersin.org/articles/10.3389/fpls.2023.1229870/fullriceRNA-Seqpollen sterilitycarbohydrate metabolismtapetum
spellingShingle Nabieu Kamara
Nabieu Kamara
Nabieu Kamara
Nabieu Kamara
Nabieu Kamara
Yamin Jiao
Yamin Jiao
Yamin Jiao
Yamin Jiao
Weicong Huang
Weicong Huang
Weicong Huang
Weicong Huang
Lichong Cao
Lichong Cao
Lichong Cao
Lichong Cao
Lianjun Zhu
Lianjun Zhu
Lianjun Zhu
Lianjun Zhu
Chongchong Zhao
Chongchong Zhao
Chongchong Zhao
Chongchong Zhao
Xu Huang
Xu Huang
Xu Huang
Xu Huang
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Fimanekeni Ndaitavela Shivute
Xiangdong Liu
Xiangdong Liu
Xiangdong Liu
Xiangdong Liu
Jinwen Wu
Jinwen Wu
Jinwen Wu
Jinwen Wu
Muhammad Qasim Shahid
Muhammad Qasim Shahid
Muhammad Qasim Shahid
Muhammad Qasim Shahid
Comparative cytological and transcriptome analyses of ny2 mutant delayed degeneration of tapetal cells and promotes abnormal microspore development in neo-tetraploid rice
Frontiers in Plant Science
rice
RNA-Seq
pollen sterility
carbohydrate metabolism
tapetum
title Comparative cytological and transcriptome analyses of ny2 mutant delayed degeneration of tapetal cells and promotes abnormal microspore development in neo-tetraploid rice
title_full Comparative cytological and transcriptome analyses of ny2 mutant delayed degeneration of tapetal cells and promotes abnormal microspore development in neo-tetraploid rice
title_fullStr Comparative cytological and transcriptome analyses of ny2 mutant delayed degeneration of tapetal cells and promotes abnormal microspore development in neo-tetraploid rice
title_full_unstemmed Comparative cytological and transcriptome analyses of ny2 mutant delayed degeneration of tapetal cells and promotes abnormal microspore development in neo-tetraploid rice
title_short Comparative cytological and transcriptome analyses of ny2 mutant delayed degeneration of tapetal cells and promotes abnormal microspore development in neo-tetraploid rice
title_sort comparative cytological and transcriptome analyses of ny2 mutant delayed degeneration of tapetal cells and promotes abnormal microspore development in neo tetraploid rice
topic rice
RNA-Seq
pollen sterility
carbohydrate metabolism
tapetum
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1229870/full
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