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The tomato WV gene encoding a thioredoxin protein is essential for chloroplast development at low temperature and high light intensity

BACKGROUND: Chloroplast biogenesis, a complex process in higher plants, is the key to photoautotrophic growth in plants. White virescent (wv) mutants have been used to unfold the molecular mechanisms underlying the regulation of chloroplast development and chloroplast gene expression in plants. Howe...

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Autores principales: Gao, Shenghua, Gao, Wenjing, Liao, Xiaoli, Xiong, Cheng, Yu, Gang, Yang, Qihong, Yang, Changxian, Ye, Zhibiao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6585109/
https://www.ncbi.nlm.nih.gov/pubmed/31221088
http://dx.doi.org/10.1186/s12870-019-1829-4
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author Gao, Shenghua
Gao, Wenjing
Liao, Xiaoli
Xiong, Cheng
Yu, Gang
Yang, Qihong
Yang, Changxian
Ye, Zhibiao
author_facet Gao, Shenghua
Gao, Wenjing
Liao, Xiaoli
Xiong, Cheng
Yu, Gang
Yang, Qihong
Yang, Changxian
Ye, Zhibiao
author_sort Gao, Shenghua
collection PubMed
description BACKGROUND: Chloroplast biogenesis, a complex process in higher plants, is the key to photoautotrophic growth in plants. White virescent (wv) mutants have been used to unfold the molecular mechanisms underlying the regulation of chloroplast development and chloroplast gene expression in plants. However, most of genes controlling white virescent phenotype still remain unknown. RESULTS: In this study, we identified a temperature- and light intensity-sensitive mutant, named as wv. The content of chlorophyll was dramatically decreased in the immature leaves of wv mutant under the conditions of low temperature and high-light intensity. TEM observation showed that the chloroplasts in the young leaves of wv mutant lacked an organized thylakoid membrane, whereas crescent-shaped chloroplasts with well-developed stromal and stacked grana thylakoids in the mature leaves were developed. Immunoblot analyses suggested that proteins of photosynthetic complexes were decreased substantially in wv mutants. Based on map-based cloning and transgenic analysis, we determined that the wv phenotype was caused by single base mutation in the first intron of WV gene, which encoded a thioredoxin protein with 365 amino acids. qRT-PCR analysis revealed that the expression of WV gene was significantly down-regulated in wv mutant. In addition, knockdown of WV gene through RNAi also resulted in white virescent young leaves, suggesting that the mutation possibly blocks the differentiation of chloroplasts through inhibiting the expression of WV gene. Furthermore, the expression of WV peaked in apical buds and gradually decreased along with the developmental stage, which was consistent with the wv mutant phenotype. Expression analysis of chloroplast-encoded genes by qRT-PCR showed that the wv mutation affected the expression pattern of chloroplast-encoded PEP dependent genes. CONCLUSION: Our results suggested that wv mutant was sensitive to low temperature and light intensity. WV gene was essential for chloroplast differentiation. A single base mutation in the first intron resulted in down-regulation of WV gene expression, which inhibited the expression of chloroplast-encoded genes, thereby blocking chloroplast formation and chlorophyll synthesis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1829-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-65851092019-06-27 The tomato WV gene encoding a thioredoxin protein is essential for chloroplast development at low temperature and high light intensity Gao, Shenghua Gao, Wenjing Liao, Xiaoli Xiong, Cheng Yu, Gang Yang, Qihong Yang, Changxian Ye, Zhibiao BMC Plant Biol Research Article BACKGROUND: Chloroplast biogenesis, a complex process in higher plants, is the key to photoautotrophic growth in plants. White virescent (wv) mutants have been used to unfold the molecular mechanisms underlying the regulation of chloroplast development and chloroplast gene expression in plants. However, most of genes controlling white virescent phenotype still remain unknown. RESULTS: In this study, we identified a temperature- and light intensity-sensitive mutant, named as wv. The content of chlorophyll was dramatically decreased in the immature leaves of wv mutant under the conditions of low temperature and high-light intensity. TEM observation showed that the chloroplasts in the young leaves of wv mutant lacked an organized thylakoid membrane, whereas crescent-shaped chloroplasts with well-developed stromal and stacked grana thylakoids in the mature leaves were developed. Immunoblot analyses suggested that proteins of photosynthetic complexes were decreased substantially in wv mutants. Based on map-based cloning and transgenic analysis, we determined that the wv phenotype was caused by single base mutation in the first intron of WV gene, which encoded a thioredoxin protein with 365 amino acids. qRT-PCR analysis revealed that the expression of WV gene was significantly down-regulated in wv mutant. In addition, knockdown of WV gene through RNAi also resulted in white virescent young leaves, suggesting that the mutation possibly blocks the differentiation of chloroplasts through inhibiting the expression of WV gene. Furthermore, the expression of WV peaked in apical buds and gradually decreased along with the developmental stage, which was consistent with the wv mutant phenotype. Expression analysis of chloroplast-encoded genes by qRT-PCR showed that the wv mutation affected the expression pattern of chloroplast-encoded PEP dependent genes. CONCLUSION: Our results suggested that wv mutant was sensitive to low temperature and light intensity. WV gene was essential for chloroplast differentiation. A single base mutation in the first intron resulted in down-regulation of WV gene expression, which inhibited the expression of chloroplast-encoded genes, thereby blocking chloroplast formation and chlorophyll synthesis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1829-4) contains supplementary material, which is available to authorized users. BioMed Central 2019-06-20 /pmc/articles/PMC6585109/ /pubmed/31221088 http://dx.doi.org/10.1186/s12870-019-1829-4 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Gao, Shenghua
Gao, Wenjing
Liao, Xiaoli
Xiong, Cheng
Yu, Gang
Yang, Qihong
Yang, Changxian
Ye, Zhibiao
The tomato WV gene encoding a thioredoxin protein is essential for chloroplast development at low temperature and high light intensity
title The tomato WV gene encoding a thioredoxin protein is essential for chloroplast development at low temperature and high light intensity
title_full The tomato WV gene encoding a thioredoxin protein is essential for chloroplast development at low temperature and high light intensity
title_fullStr The tomato WV gene encoding a thioredoxin protein is essential for chloroplast development at low temperature and high light intensity
title_full_unstemmed The tomato WV gene encoding a thioredoxin protein is essential for chloroplast development at low temperature and high light intensity
title_short The tomato WV gene encoding a thioredoxin protein is essential for chloroplast development at low temperature and high light intensity
title_sort tomato wv gene encoding a thioredoxin protein is essential for chloroplast development at low temperature and high light intensity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6585109/
https://www.ncbi.nlm.nih.gov/pubmed/31221088
http://dx.doi.org/10.1186/s12870-019-1829-4
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