TFIIB-Related Protein BRP5/PTF2 Is Required for Both Male and Female Gametogenesis and for Grain Formation in Rice

Transcription factor IIB (TFIIB) is a general transcription factor for RNA polymerase II, exerting its influence across various biological contexts. In the majority of eukaryotes, TFIIB typically has two homologs, serving as general transcription factors for RNA polymerase I and III. In plants, howe...

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Main Authors: Guangna Chen, Hongliang Hu, Xinhui Chen, Jialuo Chen, Siyi Wang, He Ning, Cheng Zhu, Su Yang
Format: Article
Language:English
Published: MDPI AG 2023-11-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/22/16473
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author Guangna Chen
Hongliang Hu
Xinhui Chen
Jialuo Chen
Siyi Wang
He Ning
Cheng Zhu
Su Yang
author_facet Guangna Chen
Hongliang Hu
Xinhui Chen
Jialuo Chen
Siyi Wang
He Ning
Cheng Zhu
Su Yang
author_sort Guangna Chen
collection DOAJ
description Transcription factor IIB (TFIIB) is a general transcription factor for RNA polymerase II, exerting its influence across various biological contexts. In the majority of eukaryotes, TFIIB typically has two homologs, serving as general transcription factors for RNA polymerase I and III. In plants, however, the TFIIB-related protein family has expanded greatly, with 14 and 9 members in Arabidopsis and rice, respectively. BRP5/pollen-expressed transcription factor 2 (PTF2) proteins belong to a subfamily of TFIIB-related proteins found only in plants and algae. The prior analysis of an <i>Arabidopsis atbrp5</i> mutant, characterized by a T-DNA insertion at the 5′ untranslated region, demonstrated the essential role of BRP5/PTF2 during the process of pollen germination and embryogenesis in <i>Arabidopsis</i>. Using a rice transformation system based on CRISPR/Cas9 technology, we have generated transgenic rice plants containing loss-of-function frameshift mutations in the <i>BRP5/PTF2</i> gene. Unlike in the <i>Arabidopsis atbrp5</i> mutant, the <i>brp5/ptf2</i> frameshift mutations were not transmitted to progeny in rice, indicating an essential role of BRP5/PTF2 in both male and female gamete development or viability. The silencing of rice <i>BRP5/PTF2</i> expression through RNA interference (RNAi) had little effect on vegetative growth and panicle formation but strongly affected pollen development and grain formation. Genetic analysis revealed that strong RNAi silencing of rice BRP5/PTF2 was still transmissible to progeny almost exclusively through female gametes, as found in the <i>Arabidopsis atbrp5</i> knockdown mutant. Thus, reduced rice <i>BRP5/PTF2</i> expression impacted pollen preferentially by interfering with male gamete development or viability. Drawing upon these findings, we posit that <i>BRP5/PTF2</i> assumes a distinct and imperative function in the realm of plant sexual reproduction.
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spelling doaj.art-f30f1ccb474d42f5b978f245d15368a82023-11-24T14:47:48ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-11-0124221647310.3390/ijms242216473TFIIB-Related Protein BRP5/PTF2 Is Required for Both Male and Female Gametogenesis and for Grain Formation in RiceGuangna Chen0Hongliang Hu1Xinhui Chen2Jialuo Chen3Siyi Wang4He Ning5Cheng Zhu6Su Yang7College of Life Sciences, China Jiliang University, 258 Xueyuan Street, Hangzhou 310018, ChinaCollege of Life Sciences, China Jiliang University, 258 Xueyuan Street, Hangzhou 310018, ChinaCollege of Life Sciences, China Jiliang University, 258 Xueyuan Street, Hangzhou 310018, ChinaCollege of Life Sciences, China Jiliang University, 258 Xueyuan Street, Hangzhou 310018, ChinaCollege of Life Sciences, China Jiliang University, 258 Xueyuan Street, Hangzhou 310018, ChinaCollege of Life Sciences, China Jiliang University, 258 Xueyuan Street, Hangzhou 310018, ChinaCollege of Life Sciences, China Jiliang University, 258 Xueyuan Street, Hangzhou 310018, ChinaCollege of Life Sciences, China Jiliang University, 258 Xueyuan Street, Hangzhou 310018, ChinaTranscription factor IIB (TFIIB) is a general transcription factor for RNA polymerase II, exerting its influence across various biological contexts. In the majority of eukaryotes, TFIIB typically has two homologs, serving as general transcription factors for RNA polymerase I and III. In plants, however, the TFIIB-related protein family has expanded greatly, with 14 and 9 members in Arabidopsis and rice, respectively. BRP5/pollen-expressed transcription factor 2 (PTF2) proteins belong to a subfamily of TFIIB-related proteins found only in plants and algae. The prior analysis of an <i>Arabidopsis atbrp5</i> mutant, characterized by a T-DNA insertion at the 5′ untranslated region, demonstrated the essential role of BRP5/PTF2 during the process of pollen germination and embryogenesis in <i>Arabidopsis</i>. Using a rice transformation system based on CRISPR/Cas9 technology, we have generated transgenic rice plants containing loss-of-function frameshift mutations in the <i>BRP5/PTF2</i> gene. Unlike in the <i>Arabidopsis atbrp5</i> mutant, the <i>brp5/ptf2</i> frameshift mutations were not transmitted to progeny in rice, indicating an essential role of BRP5/PTF2 in both male and female gamete development or viability. The silencing of rice <i>BRP5/PTF2</i> expression through RNA interference (RNAi) had little effect on vegetative growth and panicle formation but strongly affected pollen development and grain formation. Genetic analysis revealed that strong RNAi silencing of rice BRP5/PTF2 was still transmissible to progeny almost exclusively through female gametes, as found in the <i>Arabidopsis atbrp5</i> knockdown mutant. Thus, reduced rice <i>BRP5/PTF2</i> expression impacted pollen preferentially by interfering with male gamete development or viability. Drawing upon these findings, we posit that <i>BRP5/PTF2</i> assumes a distinct and imperative function in the realm of plant sexual reproduction.https://www.mdpi.com/1422-0067/24/22/16473ricetranscription factorTFIIBgametogenesispollen development
spellingShingle Guangna Chen
Hongliang Hu
Xinhui Chen
Jialuo Chen
Siyi Wang
He Ning
Cheng Zhu
Su Yang
TFIIB-Related Protein BRP5/PTF2 Is Required for Both Male and Female Gametogenesis and for Grain Formation in Rice
International Journal of Molecular Sciences
rice
transcription factor
TFIIB
gametogenesis
pollen development
title TFIIB-Related Protein BRP5/PTF2 Is Required for Both Male and Female Gametogenesis and for Grain Formation in Rice
title_full TFIIB-Related Protein BRP5/PTF2 Is Required for Both Male and Female Gametogenesis and for Grain Formation in Rice
title_fullStr TFIIB-Related Protein BRP5/PTF2 Is Required for Both Male and Female Gametogenesis and for Grain Formation in Rice
title_full_unstemmed TFIIB-Related Protein BRP5/PTF2 Is Required for Both Male and Female Gametogenesis and for Grain Formation in Rice
title_short TFIIB-Related Protein BRP5/PTF2 Is Required for Both Male and Female Gametogenesis and for Grain Formation in Rice
title_sort tfiib related protein brp5 ptf2 is required for both male and female gametogenesis and for grain formation in rice
topic rice
transcription factor
TFIIB
gametogenesis
pollen development
url https://www.mdpi.com/1422-0067/24/22/16473
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