DCET1 Controls Male Sterility Through Callose Regulation, Exine Formation, and Tapetal Programmed Cell Death in Rice

In angiosperms, anther development comprises of various complex and interrelated biological processes, critically needed for pollen viability. The transitory callose layer serves to separate the meiocytes. It helps in primexine formation, while the timely degradation of tapetal cells is essential fo...

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Autores principales:	Riaz Muhammad Khan, Ping Yu, Lianping Sun, Adil Abbas, Liaqat Shah, Xiaojiao Xiang, Dongfei Wang, Amir Sohail, Yingxin Zhang, Qunen Liu, Shihua Cheng, Liyong Cao
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	male sterility callose pollen exine tapetum PCD DCET1 Genetics QH426-470
Acceso en línea:	https://doaj.org/article/7bedd6092e11487eaa6d454a3aea1ce6
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spelling	oai:doaj.org-article:7bedd6092e11487eaa6d454a3aea1ce62021-11-30T18:55:04ZDCET1 Controls Male Sterility Through Callose Regulation, Exine Formation, and Tapetal Programmed Cell Death in Rice1664-802110.3389/fgene.2021.790789https://doaj.org/article/7bedd6092e11487eaa6d454a3aea1ce62021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fgene.2021.790789/fullhttps://doaj.org/toc/1664-8021In angiosperms, anther development comprises of various complex and interrelated biological processes, critically needed for pollen viability. The transitory callose layer serves to separate the meiocytes. It helps in primexine formation, while the timely degradation of tapetal cells is essential for the timely callose wall dissolution and pollen wall formation by providing nutrients for pollen growth. In rice, many genes have been reported and functionally characterized that are involved in callose regulation and pollen wall patterning, including timely programmed cell death (PCD) of the tapetum, but the mechanism of pollen development largely remains ambiguous. We identified and functionally characterized a rice mutant dcet1, having a complete male-sterile phenotype caused by defects in anther callose wall, exine patterning, and tapetal PCD. DCET1 belongs to the RNA recognition motif (RRM)-containing family also called as the ribonucleoprotein (RNP) domain or RNA-binding domain (RBD) protein, having single-nucleotide polymorphism (SNP) substitution from G (threonine-192) to A (isoleucine-192) located at the fifth exon of LOC_Os08g02330, was responsible for the male sterile phenotype in mutant dcet1. Our cytological analysis suggested that DCET1 regulates callose biosynthesis and degradation, pollen exine formation by affecting exine wall patterning, including abnormal nexine, collapsed bacula, and irregular tectum, and timely PCD by delaying the tapetal cell degeneration. As a result, the microspore of dcet1 was swollen and abnormally bursted and even collapsed within the anther locule characterizing complete male sterility. GUS and qRT-PCR analysis indicated that DCET1 is specifically expressed in the anther till the developmental stage 9, consistent with the observed phenotype. The characterization of DCET1 in callose regulation, pollen wall patterning, and tapetal cell PCD strengthens our knowledge for knowing the regulatory pathways involved in rice male reproductive development and has future prospects in hybrid rice breeding.Riaz Muhammad KhanPing YuLianping SunAdil AbbasLiaqat ShahXiaojiao XiangDongfei WangAmir SohailYingxin ZhangQunen LiuShihua ChengLiyong CaoFrontiers Media S.A.articlemale sterilitycallosepollen exinetapetumPCDDCET1GeneticsQH426-470ENFrontiers in Genetics, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	male sterility callose pollen exine tapetum PCD DCET1 Genetics QH426-470
spellingShingle	male sterility callose pollen exine tapetum PCD DCET1 Genetics QH426-470 Riaz Muhammad Khan Ping Yu Lianping Sun Adil Abbas Liaqat Shah Xiaojiao Xiang Dongfei Wang Amir Sohail Yingxin Zhang Qunen Liu Shihua Cheng Liyong Cao DCET1 Controls Male Sterility Through Callose Regulation, Exine Formation, and Tapetal Programmed Cell Death in Rice
description	In angiosperms, anther development comprises of various complex and interrelated biological processes, critically needed for pollen viability. The transitory callose layer serves to separate the meiocytes. It helps in primexine formation, while the timely degradation of tapetal cells is essential for the timely callose wall dissolution and pollen wall formation by providing nutrients for pollen growth. In rice, many genes have been reported and functionally characterized that are involved in callose regulation and pollen wall patterning, including timely programmed cell death (PCD) of the tapetum, but the mechanism of pollen development largely remains ambiguous. We identified and functionally characterized a rice mutant dcet1, having a complete male-sterile phenotype caused by defects in anther callose wall, exine patterning, and tapetal PCD. DCET1 belongs to the RNA recognition motif (RRM)-containing family also called as the ribonucleoprotein (RNP) domain or RNA-binding domain (RBD) protein, having single-nucleotide polymorphism (SNP) substitution from G (threonine-192) to A (isoleucine-192) located at the fifth exon of LOC_Os08g02330, was responsible for the male sterile phenotype in mutant dcet1. Our cytological analysis suggested that DCET1 regulates callose biosynthesis and degradation, pollen exine formation by affecting exine wall patterning, including abnormal nexine, collapsed bacula, and irregular tectum, and timely PCD by delaying the tapetal cell degeneration. As a result, the microspore of dcet1 was swollen and abnormally bursted and even collapsed within the anther locule characterizing complete male sterility. GUS and qRT-PCR analysis indicated that DCET1 is specifically expressed in the anther till the developmental stage 9, consistent with the observed phenotype. The characterization of DCET1 in callose regulation, pollen wall patterning, and tapetal cell PCD strengthens our knowledge for knowing the regulatory pathways involved in rice male reproductive development and has future prospects in hybrid rice breeding.
format	article
author	Riaz Muhammad Khan Ping Yu Lianping Sun Adil Abbas Liaqat Shah Xiaojiao Xiang Dongfei Wang Amir Sohail Yingxin Zhang Qunen Liu Shihua Cheng Liyong Cao
author_facet	Riaz Muhammad Khan Ping Yu Lianping Sun Adil Abbas Liaqat Shah Xiaojiao Xiang Dongfei Wang Amir Sohail Yingxin Zhang Qunen Liu Shihua Cheng Liyong Cao
author_sort	Riaz Muhammad Khan
title	DCET1 Controls Male Sterility Through Callose Regulation, Exine Formation, and Tapetal Programmed Cell Death in Rice
title_short	DCET1 Controls Male Sterility Through Callose Regulation, Exine Formation, and Tapetal Programmed Cell Death in Rice
title_full	DCET1 Controls Male Sterility Through Callose Regulation, Exine Formation, and Tapetal Programmed Cell Death in Rice
title_fullStr	DCET1 Controls Male Sterility Through Callose Regulation, Exine Formation, and Tapetal Programmed Cell Death in Rice
title_full_unstemmed	DCET1 Controls Male Sterility Through Callose Regulation, Exine Formation, and Tapetal Programmed Cell Death in Rice
title_sort	dcet1 controls male sterility through callose regulation, exine formation, and tapetal programmed cell death in rice
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/7bedd6092e11487eaa6d454a3aea1ce6
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DCET1 Controls Male Sterility Through Callose Regulation, Exine Formation, and Tapetal Programmed Cell Death in Rice

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