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Impact of Autophagy on Gene Expression and Tapetal Programmed Cell Death During Pollen Development in Rice

Autophagy has recently been shown to be required for tapetal programmed cell death (PCD) and pollen maturation in rice. A transcriptional regulatory network is also known to play a key role in the progression of tapetal PCD. However, the relationship between the gene regulatory network and autophagy...

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Autores principales: Hanamata, Shigeru, Sawada, Jumpei, Ono, Seijiro, Ogawa, Kazunori, Fukunaga, Togo, Nonomura, Ken–Ichi, Kimura, Seisuke, Kurusu, Takamitsu, Kuchitsu, Kazuyuki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7068715/
https://www.ncbi.nlm.nih.gov/pubmed/32210988
http://dx.doi.org/10.3389/fpls.2020.00172
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author Hanamata, Shigeru
Sawada, Jumpei
Ono, Seijiro
Ogawa, Kazunori
Fukunaga, Togo
Nonomura, Ken–Ichi
Kimura, Seisuke
Kurusu, Takamitsu
Kuchitsu, Kazuyuki
author_facet Hanamata, Shigeru
Sawada, Jumpei
Ono, Seijiro
Ogawa, Kazunori
Fukunaga, Togo
Nonomura, Ken–Ichi
Kimura, Seisuke
Kurusu, Takamitsu
Kuchitsu, Kazuyuki
author_sort Hanamata, Shigeru
collection PubMed
description Autophagy has recently been shown to be required for tapetal programmed cell death (PCD) and pollen maturation in rice. A transcriptional regulatory network is also known to play a key role in the progression of tapetal PCD. However, the relationship between the gene regulatory network and autophagy in rice anther development is mostly unknown. Here, we comprehensively analyzed the effect of autophagy disruption on gene expression profile during the tapetal PCD in rice anther development using high-throughput RNA sequencing. Expression of thousands of genes, including specific transcription factors and several proteases required for tapetal degradation, fluctuated synchronously at specific stages during tapetal PCD progression in the wild-type anthers, while this fluctuation showed significant delay in the autophagy-deficient mutant Osatg7-1. Moreover, gene ontology enrichment analysis in combination with self-organizing map clustering as well as pathway analysis revealed that the expression patterns of a variety of organelle-related genes as well as genes involved in carbohydrate/lipid metabolism were affected in the Osatg7-1 mutant during pollen maturation. These results suggest that autophagy is required for proper regulation of gene expression and quality control of organelles and timely progression of tapetal PCD during rice pollen development.
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spelling pubmed-70687152020-03-24 Impact of Autophagy on Gene Expression and Tapetal Programmed Cell Death During Pollen Development in Rice Hanamata, Shigeru Sawada, Jumpei Ono, Seijiro Ogawa, Kazunori Fukunaga, Togo Nonomura, Ken–Ichi Kimura, Seisuke Kurusu, Takamitsu Kuchitsu, Kazuyuki Front Plant Sci Plant Science Autophagy has recently been shown to be required for tapetal programmed cell death (PCD) and pollen maturation in rice. A transcriptional regulatory network is also known to play a key role in the progression of tapetal PCD. However, the relationship between the gene regulatory network and autophagy in rice anther development is mostly unknown. Here, we comprehensively analyzed the effect of autophagy disruption on gene expression profile during the tapetal PCD in rice anther development using high-throughput RNA sequencing. Expression of thousands of genes, including specific transcription factors and several proteases required for tapetal degradation, fluctuated synchronously at specific stages during tapetal PCD progression in the wild-type anthers, while this fluctuation showed significant delay in the autophagy-deficient mutant Osatg7-1. Moreover, gene ontology enrichment analysis in combination with self-organizing map clustering as well as pathway analysis revealed that the expression patterns of a variety of organelle-related genes as well as genes involved in carbohydrate/lipid metabolism were affected in the Osatg7-1 mutant during pollen maturation. These results suggest that autophagy is required for proper regulation of gene expression and quality control of organelles and timely progression of tapetal PCD during rice pollen development. Frontiers Media S.A. 2020-03-06 /pmc/articles/PMC7068715/ /pubmed/32210988 http://dx.doi.org/10.3389/fpls.2020.00172 Text en Copyright © 2020 Hanamata, Sawada, Ono, Ogawa, Fukunaga, Nonomura, Kimura, Kurusu and Kuchitsu http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Hanamata, Shigeru
Sawada, Jumpei
Ono, Seijiro
Ogawa, Kazunori
Fukunaga, Togo
Nonomura, Ken–Ichi
Kimura, Seisuke
Kurusu, Takamitsu
Kuchitsu, Kazuyuki
Impact of Autophagy on Gene Expression and Tapetal Programmed Cell Death During Pollen Development in Rice
title Impact of Autophagy on Gene Expression and Tapetal Programmed Cell Death During Pollen Development in Rice
title_full Impact of Autophagy on Gene Expression and Tapetal Programmed Cell Death During Pollen Development in Rice
title_fullStr Impact of Autophagy on Gene Expression and Tapetal Programmed Cell Death During Pollen Development in Rice
title_full_unstemmed Impact of Autophagy on Gene Expression and Tapetal Programmed Cell Death During Pollen Development in Rice
title_short Impact of Autophagy on Gene Expression and Tapetal Programmed Cell Death During Pollen Development in Rice
title_sort impact of autophagy on gene expression and tapetal programmed cell death during pollen development in rice
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7068715/
https://www.ncbi.nlm.nih.gov/pubmed/32210988
http://dx.doi.org/10.3389/fpls.2020.00172
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