FLOURY ENDOSPERM24, a heat shock protein 101 (HSP101), is required for starch biosynthesis and endosperm development in rice
Summary Endosperm is the main storage organ in cereal grain and determines grain yield and quality. The molecular mechanisms of heat shock proteins in regulating starch biosynthesis and endosperm development remain obscure. Here, we report a rice floury endosperm mutant flo24 that develops abnormal...
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| creator | Wu, Hongming Ren, Yulong Dong, Hui Xie, Chen Zhao, Lei Wang, Xin Zhang, Fulin Zhang, Binglei Jiang, Xiaokang Huang, Yunshuai Jing, Ruonan Wang, Jian Miao, Rong Bao, Xiuhao Yu, Mingzhou Nguyen, Thanhliem Mou, Changling Wang, Yunlong Wang, Yihua Lei, Cailin Cheng, Zhijun Jiang, Ling Wan, Jianmin |
| description | Summary
Endosperm is the main storage organ in cereal grain and determines grain yield and quality. The molecular mechanisms of heat shock proteins in regulating starch biosynthesis and endosperm development remain obscure.
Here, we report a rice floury endosperm mutant flo24 that develops abnormal starch grains in the central starchy endosperm cells. Map‐based cloning and complementation test showed that FLO24 encodes a heat shock protein HSP101, which is localized in plastids. The mutated protein FLO24T296I dramatically lost its ability to hydrolyze ATP and to rescue the thermotolerance defects of the yeast hsp104 mutant.
The flo24 mutant develops more severe floury endosperm when grown under high‐temperature conditions than normal conditions. And the FLO24 protein was dramatically induced at high temperature. FLO24 physically interacts with several key enzymes required for starch biosynthesis, including AGPL1, AGPL3 and PHO1. Combined biochemical and genetic evidence suggests that FLO24 acts cooperatively with HSP70cp‐2 to regulate starch biosynthesis and endosperm development in rice.
Our results reveal that FLO24 acts as an important regulator of endosperm development, which might function in maintaining the activities of enzymes involved in starch biosynthesis in rice. |
| doi_str_mv | 10.1111/nph.19761 |
| format | Article |
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Endosperm is the main storage organ in cereal grain and determines grain yield and quality. The molecular mechanisms of heat shock proteins in regulating starch biosynthesis and endosperm development remain obscure.
Here, we report a rice floury endosperm mutant flo24 that develops abnormal starch grains in the central starchy endosperm cells. Map‐based cloning and complementation test showed that FLO24 encodes a heat shock protein HSP101, which is localized in plastids. The mutated protein FLO24T296I dramatically lost its ability to hydrolyze ATP and to rescue the thermotolerance defects of the yeast hsp104 mutant.
The flo24 mutant develops more severe floury endosperm when grown under high‐temperature conditions than normal conditions. And the FLO24 protein was dramatically induced at high temperature. FLO24 physically interacts with several key enzymes required for starch biosynthesis, including AGPL1, AGPL3 and PHO1. Combined biochemical and genetic evidence suggests that FLO24 acts cooperatively with HSP70cp‐2 to regulate starch biosynthesis and endosperm development in rice.
Our results reveal that FLO24 acts as an important regulator of endosperm development, which might function in maintaining the activities of enzymes involved in starch biosynthesis in rice.</description><identifier>ISSN: 0028-646X</identifier><identifier>ISSN: 1469-8137</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19761</identifier><identifier>PMID: 38634187</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>ATP ; Biosynthesis ; Cloning ; Complementation ; Crop yield ; Crystal defects ; Endosperm ; endosperm development ; Enzymes ; FLO24 ; grain yield ; Heat ; Heat shock ; Heat shock proteins ; heat stress ; heat tolerance ; High temperature ; Molecular modelling ; Mutants ; plastid ; plastids ; Proteins ; Rice ; Starch ; starch biosynthesis ; Starch grains ; Storage organs ; temperature ; Temperature requirements ; Temperature tolerance ; Yeasts</subject><ispartof>The New phytologist, 2024-06, Vol.242 (6), p.2635-2651</ispartof><rights>2024 The Authors © 2024 New Phytologist Foundation</rights><rights>2024 The Authors. New Phytologist © 2024 New Phytologist Foundation.</rights><rights>Copyright © 2024 New Phytologist Trust</rights><rights>2024 The Authors New Phytologist © 2024 New Phytologist Foundation.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3861-260df16a85c67f097cae64641e793e688aa6c0f58beb2fb1d31f5c1274cce1433</citedby><cites>FETCH-LOGICAL-c3861-260df16a85c67f097cae64641e793e688aa6c0f58beb2fb1d31f5c1274cce1433</cites><orcidid>0000-0002-0017-8760 ; 0000-0002-7813-4362 ; 0000-0002-8473-1948 ; 0000-0002-9032-3529 ; 0000-0003-1464-5881</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fnph.19761$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.19761$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38634187$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wu, Hongming</creatorcontrib><creatorcontrib>Ren, Yulong</creatorcontrib><creatorcontrib>Dong, Hui</creatorcontrib><creatorcontrib>Xie, Chen</creatorcontrib><creatorcontrib>Zhao, Lei</creatorcontrib><creatorcontrib>Wang, Xin</creatorcontrib><creatorcontrib>Zhang, Fulin</creatorcontrib><creatorcontrib>Zhang, Binglei</creatorcontrib><creatorcontrib>Jiang, Xiaokang</creatorcontrib><creatorcontrib>Huang, Yunshuai</creatorcontrib><creatorcontrib>Jing, Ruonan</creatorcontrib><creatorcontrib>Wang, Jian</creatorcontrib><creatorcontrib>Miao, Rong</creatorcontrib><creatorcontrib>Bao, Xiuhao</creatorcontrib><creatorcontrib>Yu, Mingzhou</creatorcontrib><creatorcontrib>Nguyen, Thanhliem</creatorcontrib><creatorcontrib>Mou, Changling</creatorcontrib><creatorcontrib>Wang, Yunlong</creatorcontrib><creatorcontrib>Wang, Yihua</creatorcontrib><creatorcontrib>Lei, Cailin</creatorcontrib><creatorcontrib>Cheng, Zhijun</creatorcontrib><creatorcontrib>Jiang, Ling</creatorcontrib><creatorcontrib>Wan, Jianmin</creatorcontrib><title>FLOURY ENDOSPERM24, a heat shock protein 101 (HSP101), is required for starch biosynthesis and endosperm development in rice</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Endosperm is the main storage organ in cereal grain and determines grain yield and quality. The molecular mechanisms of heat shock proteins in regulating starch biosynthesis and endosperm development remain obscure.
Here, we report a rice floury endosperm mutant flo24 that develops abnormal starch grains in the central starchy endosperm cells. Map‐based cloning and complementation test showed that FLO24 encodes a heat shock protein HSP101, which is localized in plastids. The mutated protein FLO24T296I dramatically lost its ability to hydrolyze ATP and to rescue the thermotolerance defects of the yeast hsp104 mutant.
The flo24 mutant develops more severe floury endosperm when grown under high‐temperature conditions than normal conditions. And the FLO24 protein was dramatically induced at high temperature. FLO24 physically interacts with several key enzymes required for starch biosynthesis, including AGPL1, AGPL3 and PHO1. Combined biochemical and genetic evidence suggests that FLO24 acts cooperatively with HSP70cp‐2 to regulate starch biosynthesis and endosperm development in rice.
Our results reveal that FLO24 acts as an important regulator of endosperm development, which might function in maintaining the activities of enzymes involved in starch biosynthesis in rice.</description><subject>ATP</subject><subject>Biosynthesis</subject><subject>Cloning</subject><subject>Complementation</subject><subject>Crop yield</subject><subject>Crystal defects</subject><subject>Endosperm</subject><subject>endosperm development</subject><subject>Enzymes</subject><subject>FLO24</subject><subject>grain yield</subject><subject>Heat</subject><subject>Heat shock</subject><subject>Heat shock proteins</subject><subject>heat stress</subject><subject>heat tolerance</subject><subject>High temperature</subject><subject>Molecular modelling</subject><subject>Mutants</subject><subject>plastid</subject><subject>plastids</subject><subject>Proteins</subject><subject>Rice</subject><subject>Starch</subject><subject>starch biosynthesis</subject><subject>Starch grains</subject><subject>Storage organs</subject><subject>temperature</subject><subject>Temperature requirements</subject><subject>Temperature tolerance</subject><subject>Yeasts</subject><issn>0028-646X</issn><issn>1469-8137</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqF0VFr1TAYBuAgijtOL_wDEvBmg3XL16RJejnmmUc47hw2B3pV0vQr7WybLmmVA_54M8_0QhBz8908vOTlJeQ1sFOI72wYm1PIlYQnZAFC5okGrp6SBWOpTqSQnw_IixDuGGN5JtPn5IBryQVotSA_Lteb2-svdHn1bnOzXV5_TMUJNbRBM9HQOPuVjt5N2A4UGNCj1c023uMT2gbq8X5uPVa0dp6GyXjb0LJ1YTdMDYYIzFBRHCoXRvQ9rfAbdm7scZhojPOtxZfkWW26gK8e7yG5vVx-ulgl6837Dxfn68TGj0KSSlbVII3OrFQ1y5U1GFsJQJVzlFobIy2rM11imdYlVBzqzEKqhLUIgvNDcrTPjV3uZwxT0bfBYteZAd0cCg4Zz4TKJfs_ZQJSDorLSN_-Re_c7IdYJKpMc82lelDHe2W9C8FjXYy-7Y3fFcCKh_WKuF7xa71o3zwmzmWP1R_5e64Izvbge9vh7t9JxdV2tY_8CaQSoEg</recordid><startdate>202406</startdate><enddate>202406</enddate><creator>Wu, Hongming</creator><creator>Ren, Yulong</creator><creator>Dong, Hui</creator><creator>Xie, Chen</creator><creator>Zhao, Lei</creator><creator>Wang, Xin</creator><creator>Zhang, Fulin</creator><creator>Zhang, Binglei</creator><creator>Jiang, Xiaokang</creator><creator>Huang, Yunshuai</creator><creator>Jing, Ruonan</creator><creator>Wang, Jian</creator><creator>Miao, Rong</creator><creator>Bao, Xiuhao</creator><creator>Yu, Mingzhou</creator><creator>Nguyen, Thanhliem</creator><creator>Mou, Changling</creator><creator>Wang, Yunlong</creator><creator>Wang, Yihua</creator><creator>Lei, Cailin</creator><creator>Cheng, Zhijun</creator><creator>Jiang, Ling</creator><creator>Wan, Jianmin</creator><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-0017-8760</orcidid><orcidid>https://orcid.org/0000-0002-7813-4362</orcidid><orcidid>https://orcid.org/0000-0002-8473-1948</orcidid><orcidid>https://orcid.org/0000-0002-9032-3529</orcidid><orcidid>https://orcid.org/0000-0003-1464-5881</orcidid></search><sort><creationdate>202406</creationdate><title>FLOURY ENDOSPERM24, a heat shock protein 101 (HSP101), is required for starch biosynthesis and endosperm development in rice</title><author>Wu, Hongming ; Ren, Yulong ; Dong, Hui ; Xie, Chen ; Zhao, Lei ; Wang, Xin ; Zhang, Fulin ; Zhang, Binglei ; Jiang, Xiaokang ; Huang, Yunshuai ; Jing, Ruonan ; Wang, Jian ; Miao, Rong ; Bao, Xiuhao ; Yu, Mingzhou ; Nguyen, Thanhliem ; Mou, Changling ; Wang, Yunlong ; Wang, Yihua ; Lei, Cailin ; Cheng, Zhijun ; Jiang, Ling ; Wan, Jianmin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3861-260df16a85c67f097cae64641e793e688aa6c0f58beb2fb1d31f5c1274cce1433</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>ATP</topic><topic>Biosynthesis</topic><topic>Cloning</topic><topic>Complementation</topic><topic>Crop yield</topic><topic>Crystal defects</topic><topic>Endosperm</topic><topic>endosperm development</topic><topic>Enzymes</topic><topic>FLO24</topic><topic>grain yield</topic><topic>Heat</topic><topic>Heat shock</topic><topic>Heat shock proteins</topic><topic>heat stress</topic><topic>heat tolerance</topic><topic>High temperature</topic><topic>Molecular modelling</topic><topic>Mutants</topic><topic>plastid</topic><topic>plastids</topic><topic>Proteins</topic><topic>Rice</topic><topic>Starch</topic><topic>starch biosynthesis</topic><topic>Starch grains</topic><topic>Storage organs</topic><topic>temperature</topic><topic>Temperature requirements</topic><topic>Temperature tolerance</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Hongming</creatorcontrib><creatorcontrib>Ren, Yulong</creatorcontrib><creatorcontrib>Dong, Hui</creatorcontrib><creatorcontrib>Xie, Chen</creatorcontrib><creatorcontrib>Zhao, Lei</creatorcontrib><creatorcontrib>Wang, Xin</creatorcontrib><creatorcontrib>Zhang, Fulin</creatorcontrib><creatorcontrib>Zhang, Binglei</creatorcontrib><creatorcontrib>Jiang, Xiaokang</creatorcontrib><creatorcontrib>Huang, Yunshuai</creatorcontrib><creatorcontrib>Jing, Ruonan</creatorcontrib><creatorcontrib>Wang, Jian</creatorcontrib><creatorcontrib>Miao, Rong</creatorcontrib><creatorcontrib>Bao, Xiuhao</creatorcontrib><creatorcontrib>Yu, Mingzhou</creatorcontrib><creatorcontrib>Nguyen, Thanhliem</creatorcontrib><creatorcontrib>Mou, Changling</creatorcontrib><creatorcontrib>Wang, Yunlong</creatorcontrib><creatorcontrib>Wang, Yihua</creatorcontrib><creatorcontrib>Lei, Cailin</creatorcontrib><creatorcontrib>Cheng, Zhijun</creatorcontrib><creatorcontrib>Jiang, Ling</creatorcontrib><creatorcontrib>Wan, Jianmin</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wu, Hongming</au><au>Ren, Yulong</au><au>Dong, Hui</au><au>Xie, Chen</au><au>Zhao, Lei</au><au>Wang, Xin</au><au>Zhang, Fulin</au><au>Zhang, Binglei</au><au>Jiang, Xiaokang</au><au>Huang, Yunshuai</au><au>Jing, Ruonan</au><au>Wang, Jian</au><au>Miao, Rong</au><au>Bao, Xiuhao</au><au>Yu, Mingzhou</au><au>Nguyen, Thanhliem</au><au>Mou, Changling</au><au>Wang, Yunlong</au><au>Wang, Yihua</au><au>Lei, Cailin</au><au>Cheng, Zhijun</au><au>Jiang, Ling</au><au>Wan, Jianmin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>FLOURY ENDOSPERM24, a heat shock protein 101 (HSP101), is required for starch biosynthesis and endosperm development in rice</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2024-06</date><risdate>2024</risdate><volume>242</volume><issue>6</issue><spage>2635</spage><epage>2651</epage><pages>2635-2651</pages><issn>0028-646X</issn><issn>1469-8137</issn><eissn>1469-8137</eissn><abstract>Summary
Endosperm is the main storage organ in cereal grain and determines grain yield and quality. The molecular mechanisms of heat shock proteins in regulating starch biosynthesis and endosperm development remain obscure.
Here, we report a rice floury endosperm mutant flo24 that develops abnormal starch grains in the central starchy endosperm cells. Map‐based cloning and complementation test showed that FLO24 encodes a heat shock protein HSP101, which is localized in plastids. The mutated protein FLO24T296I dramatically lost its ability to hydrolyze ATP and to rescue the thermotolerance defects of the yeast hsp104 mutant.
The flo24 mutant develops more severe floury endosperm when grown under high‐temperature conditions than normal conditions. And the FLO24 protein was dramatically induced at high temperature. FLO24 physically interacts with several key enzymes required for starch biosynthesis, including AGPL1, AGPL3 and PHO1. Combined biochemical and genetic evidence suggests that FLO24 acts cooperatively with HSP70cp‐2 to regulate starch biosynthesis and endosperm development in rice.
Our results reveal that FLO24 acts as an important regulator of endosperm development, which might function in maintaining the activities of enzymes involved in starch biosynthesis in rice.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>38634187</pmid><doi>10.1111/nph.19761</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-0017-8760</orcidid><orcidid>https://orcid.org/0000-0002-7813-4362</orcidid><orcidid>https://orcid.org/0000-0002-8473-1948</orcidid><orcidid>https://orcid.org/0000-0002-9032-3529</orcidid><orcidid>https://orcid.org/0000-0003-1464-5881</orcidid></addata></record> |
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| ispartof | The New phytologist, 2024-06, Vol.242 (6), p.2635-2651 |
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| source | Wiley Online Library Journals Frontfile Complete |
| subjects | ATP Biosynthesis Cloning Complementation Crop yield Crystal defects Endosperm endosperm development Enzymes FLO24 grain yield Heat Heat shock Heat shock proteins heat stress heat tolerance High temperature Molecular modelling Mutants plastid plastids Proteins Rice Starch starch biosynthesis Starch grains Storage organs temperature Temperature requirements Temperature tolerance Yeasts |
| title | FLOURY ENDOSPERM24, a heat shock protein 101 (HSP101), is required for starch biosynthesis and endosperm development in rice |
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