Big Grain3, encoding a purine permease, regulates grain size via modulating cytokinin transport in rice

Grain size is an important agronomic trait affecting grain yield, but the underlying molecular mechanisms remain to be elucidated. Here, we isolated a dominant mutant, big grain3 (bg3‐D), which exhibits a remarkable increase of grain size caused by activation of the PURINE PERMEASE gene, OsPUP4. BG3...

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Published inJournal of integrative plant biology Vol. 61; no. 5; pp. 581 - 597
Main Authors Xiao, Yunhua, Liu, Dapu, Zhang, Guoxia, Gao, Shaopei, Liu, Linchuan, Xu, Fan, Che, Ronghui, Wang, Yiqin, Tong, Hongning, Chu, Chengcai
Format Journal Article
LanguageEnglish
Published China (Republic : 1949- ) Wiley Subscription Services, Inc 01.05.2019
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research(Beijing), Institute of Genetics and Developmental Biology, the Chinese Academy of Sciences, Beijing 100101, China%National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, the Chinese Academy of Agricultural Sciences, Beijing 100081, China
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Online AccessGet full text
ISSN1672-9072
1744-7909
1744-7909
DOI10.1111/jipb.12727

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Abstract Grain size is an important agronomic trait affecting grain yield, but the underlying molecular mechanisms remain to be elucidated. Here, we isolated a dominant mutant, big grain3 (bg3‐D), which exhibits a remarkable increase of grain size caused by activation of the PURINE PERMEASE gene, OsPUP4. BG3/OsPUP4 is predominantly expressed in vascular tissues and is specifically suppressed by exogenous cytokinin application. Hormone profiling revealed that the distribution of different cytokinin forms, in roots and shoots of the bg3‐D mutant, is altered. Quantitative reverse transcription‐PCR (qRT‐PCR) analysis indicated that expression of rice cytokinin type‐A RESPONSE REGULATOR (OsRR) genes is enhanced in the roots of the bg3‐D mutant. These results suggest that OsPUP4 might contribute to the long‐distance transport of cytokinin, by reinforcing cytokinin loading into vascular bundle cells. Furthermore, plants overexpressing OsPUP7, the closest homolog of OsPUP4, also exhibited a similar phenotype to the bg3‐D mutant. Interestingly, subcellular localization demonstrated that OsPUP4 was localized on the plasma membrane, whereas OsPUP7 was localized to the endoplasmic reticulum. Based on these findings, we propose that OsPUP4 and OsPUP7 function in a linear pathway to direct cytokinin cell‐to‐cell transport, affecting both its long‐distance movement and local allocation. This study cloned a new grain size controlling gene, named Big Grain3, which encodes a cytokinin transporter that localized on cell membrane, thus for the first time revealed that strengthened cytokinin transport can greatly enhance grain size, which could be utilized as a novel strategy for yield improvement.
AbstractList Grain size is an important agronomic trait affecting grain yield,but the underlying molecular mechanisms remain to be elucidated.Here,we isolated a dominant mutant,big grain3 (bg3-D),which exhibits a remarkable increase of grain size caused by activation of the PURINE PERMEASE gene,OsPUP4.BG3/OsPUP4 is predominantly expressed in vascular tissues and is specifically suppressed by exogenous cytokinin application.Hormone profiling revealed that the distribution of different cytokinin forms,in roots and shoots of the bg3-D mutant,is altered.Quantitative reverse transcription-PCR (qRT-PCR) analysis indicated that expression of rice cytokinin type-A RESPONSE REGULATOR (OsRR) genes is enhanced in the roots of the bg3-D mutant.These results suggest that OsPUP4 might contribute to the long-distance transport of cytokinin,by reinforcing cytokinin loading into vascular bundle cells.Furthermore,plants overexpressing OsPUP7,the closest homolog of OsPUP4,also exhibited a similar phenotype to the bg3-D mutant.Interestingly,subcellular localization demonstrated that OsPUP4 was localized on the plasma membrane,whereas OsPUP7 was localized to the endoplasmic reticulum.Based on these findings,we propose that OsPUP4 and OsPUP7 function in a linear pathway to direct cytokinin cell-to-cell transport,affecting both its long-distance movement and local allocation.
Grain size is an important agronomic trait affecting grain yield, but the underlying molecular mechanisms remain to be elucidated. Here, we isolated a dominant mutant, big grain3 (bg3-D), which exhibits a remarkable increase of grain size caused by activation of the PURINE PERMEASE gene, OsPUP4. BG3/OsPUP4 is predominantly expressed in vascular tissues and is specifically suppressed by exogenous cytokinin application. Hormone profiling revealed that the distribution of different cytokinin forms, in roots and shoots of the bg3-D mutant, is altered. Quantitative reverse transcription-PCR (qRT-PCR) analysis indicated that expression of rice cytokinin type-A RESPONSE REGULATOR (OsRR) genes is enhanced in the roots of the bg3-D mutant. These results suggest that OsPUP4 might contribute to the long-distance transport of cytokinin, by reinforcing cytokinin loading into vascular bundle cells. Furthermore, plants overexpressing OsPUP7, the closest homolog of OsPUP4, also exhibited a similar phenotype to the bg3-D mutant. Interestingly, subcellular localization demonstrated that OsPUP4 was localized on the plasma membrane, whereas OsPUP7 was localized to the endoplasmic reticulum. Based on these findings, we propose that OsPUP4 and OsPUP7 function in a linear pathway to direct cytokinin cell-to-cell transport, affecting both its long-distance movement and local allocation.Grain size is an important agronomic trait affecting grain yield, but the underlying molecular mechanisms remain to be elucidated. Here, we isolated a dominant mutant, big grain3 (bg3-D), which exhibits a remarkable increase of grain size caused by activation of the PURINE PERMEASE gene, OsPUP4. BG3/OsPUP4 is predominantly expressed in vascular tissues and is specifically suppressed by exogenous cytokinin application. Hormone profiling revealed that the distribution of different cytokinin forms, in roots and shoots of the bg3-D mutant, is altered. Quantitative reverse transcription-PCR (qRT-PCR) analysis indicated that expression of rice cytokinin type-A RESPONSE REGULATOR (OsRR) genes is enhanced in the roots of the bg3-D mutant. These results suggest that OsPUP4 might contribute to the long-distance transport of cytokinin, by reinforcing cytokinin loading into vascular bundle cells. Furthermore, plants overexpressing OsPUP7, the closest homolog of OsPUP4, also exhibited a similar phenotype to the bg3-D mutant. Interestingly, subcellular localization demonstrated that OsPUP4 was localized on the plasma membrane, whereas OsPUP7 was localized to the endoplasmic reticulum. Based on these findings, we propose that OsPUP4 and OsPUP7 function in a linear pathway to direct cytokinin cell-to-cell transport, affecting both its long-distance movement and local allocation.
Grain size is an important agronomic trait affecting grain yield, but the underlying molecular mechanisms remain to be elucidated. Here, we isolated a dominant mutant, big grain3 (bg3‐D), which exhibits a remarkable increase of grain size caused by activation of the PURINE PERMEASE gene, OsPUP4. BG3/OsPUP4 is predominantly expressed in vascular tissues and is specifically suppressed by exogenous cytokinin application. Hormone profiling revealed that the distribution of different cytokinin forms, in roots and shoots of the bg3‐D mutant, is altered. Quantitative reverse transcription‐PCR (qRT‐PCR) analysis indicated that expression of rice cytokinin type‐A RESPONSE REGULATOR (OsRR) genes is enhanced in the roots of the bg3‐D mutant. These results suggest that OsPUP4 might contribute to the long‐distance transport of cytokinin, by reinforcing cytokinin loading into vascular bundle cells. Furthermore, plants overexpressing OsPUP7, the closest homolog of OsPUP4, also exhibited a similar phenotype to the bg3‐D mutant. Interestingly, subcellular localization demonstrated that OsPUP4 was localized on the plasma membrane, whereas OsPUP7 was localized to the endoplasmic reticulum. Based on these findings, we propose that OsPUP4 and OsPUP7 function in a linear pathway to direct cytokinin cell‐to‐cell transport, affecting both its long‐distance movement and local allocation. This study cloned a new grain size controlling gene, named Big Grain3, which encodes a cytokinin transporter that localized on cell membrane, thus for the first time revealed that strengthened cytokinin transport can greatly enhance grain size, which could be utilized as a novel strategy for yield improvement.
Author Chu, Chengcai
Che, Ronghui
Liu, Dapu
Tong, Hongning
Xu, Fan
Xiao, Yunhua
Zhang, Guoxia
Gao, Shaopei
Wang, Yiqin
Liu, Linchuan
AuthorAffiliation State Key Laboratory of Plant Genomics and National Center for Plant Gene Research(Beijing), Institute of Genetics and Developmental Biology, the Chinese Academy of Sciences, Beijing 100101, China%National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, the Chinese Academy of Agricultural Sciences, Beijing 100081, China
AuthorAffiliation_xml – name: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research(Beijing), Institute of Genetics and Developmental Biology, the Chinese Academy of Sciences, Beijing 100101, China%National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, the Chinese Academy of Agricultural Sciences, Beijing 100081, China
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  givenname: Chengcai
  surname: Chu
  fullname: Chu, Chengcai
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30267474$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2018 Institute of Botany, Chinese Academy of Sciences
2018 Institute of Botany, Chinese Academy of Sciences.
2019 Institute of Botany, Chinese Academy of Sciences
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PublicationTitle Journal of integrative plant biology
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State Key Laboratory of Plant Genomics and National Center for Plant Gene Research(Beijing), Institute of Genetics and Developmental Biology, the Chinese Academy of Sciences, Beijing 100101, China%National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, the Chinese Academy of Agricultural Sciences, Beijing 100081, China
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References 2015; 38
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2005; 137
2005; 138
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Snippet Grain size is an important agronomic trait affecting grain yield, but the underlying molecular mechanisms remain to be elucidated. Here, we isolated a dominant...
Grain size is an important agronomic trait affecting grain yield,but the underlying molecular mechanisms remain to be elucidated.Here,we isolated a dominant...
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SubjectTerms agronomic traits
Agronomy
Biological Transport
Crop yield
Cytokinins
Cytokinins - metabolism
Edible Grain - genetics
Edible Grain - metabolism
Endoplasmic reticulum
Gene expression
Gene Expression Regulation, Plant - physiology
gene overexpression
genes
Grain size
grain yield
Homology
Localization
Molecular modelling
Mutants
Nucleobase Transport Proteins - genetics
Nucleobase Transport Proteins - metabolism
Oryza
Oryza - enzymology
Oryza - genetics
Oryza - metabolism
Particle size
Permease
phenotype
Phenotypes
Plant cells
Plant Proteins - genetics
Plant Proteins - metabolism
Plant Roots - genetics
Plant Roots - metabolism
Plant Shoots - genetics
Plant Shoots - metabolism
Plant tissues
plasma membrane
quantitative polymerase chain reaction
reverse transcriptase polymerase chain reaction
Reverse transcription
Rice
Roots
Shoots
Transport
transporters
Vascular tissue
vascular tissues
Title Big Grain3, encoding a purine permease, regulates grain size via modulating cytokinin transport in rice
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fjipb.12727
https://www.ncbi.nlm.nih.gov/pubmed/30267474
https://www.proquest.com/docview/2220151488
https://www.proquest.com/docview/2114697967
https://www.proquest.com/docview/2253241496
https://d.wanfangdata.com.cn/periodical/zwxb201905005
Volume 61
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