OsHXK3 encodes a hexokinase-like protein that positively regulates grain size in rice

Key message We report the map-based cloning and functional characterization of SNG1 , which encodes OsHXK3, a hexokinase-like protein that plays a pivotal role in controlling grain size in rice. Grain size is an important agronomic trait determining grain yield and appearance quality in rice. Here,...

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Veröffentlicht in:	Theoretical and applied genetics 2022-10, Vol.135 (10), p.3417-3431
Hauptverfasser:	Yun, Peng, Li, Yibo, Wu, Bian, Zhu, Yun, Wang, Kaiyue, Li, Pingbo, Gao, Guanjun, Zhang, Qinglu, Li, Xianghua, Li, Zefu, He, Yuqing
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Sprache:	eng
Schlagworte:	Agriculture Biochemistry Biological activity Biomedical and Life Sciences Biotechnology Cloning Crop yields Edible Grain - genetics Edible Grain - metabolism Environmental aspects Forecasts and trends Gene Expression Regulation, Plant Genetic aspects Gibberellins Gibberellins - metabolism Glucose - metabolism Grain Grain size Growth Health aspects Hexokinase Hexokinase - genetics Hexokinase - metabolism Homeostasis Life Sciences Measurement Mitochondria Mutants Original Article Oryza - genetics Oryza - metabolism Phenotypes Phosphorylation Plant Biochemistry Plant Breeding/Biotechnology Plant Genetics and Genomics Plant Proteins - genetics Plant Proteins - metabolism Proteins Protoplasts Rice Scanning electron microscopy
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container_title	Theoretical and applied genetics
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creator	Yun, Peng Li, Yibo Wu, Bian Zhu, Yun Wang, Kaiyue Li, Pingbo Gao, Guanjun Zhang, Qinglu Li, Xianghua Li, Zefu He, Yuqing
description	Key message We report the map-based cloning and functional characterization of SNG1 , which encodes OsHXK3, a hexokinase-like protein that plays a pivotal role in controlling grain size in rice. Grain size is an important agronomic trait determining grain yield and appearance quality in rice. Here, we report the discovery of rice mutant short and narrow grain1 ( sng1 ) with reduced grain length, width and weight. Map-based cloning revealed that the mutant phenotype was caused by loss of function of gene OsHXK3 that encodes a hexokinase-like (HKL) protein. OsHXK3 was associated with the mitochondria and was ubiquitously distributed in various organs, predominately in younger organs. Analysis of glucose (Glc) phosphorylation activities in young panicles and protoplasts showed that OsHXK3 was a non-catalytic hexokinase (HXK). Overexpression of OsHXK3 could not complement the Arabidopsis glucose insensitive2-1 ( gin2-1 ) mutant, indicating that OsHXK3 lacked Glc signaling activity. Scanning electron microscopy analysis revealed that OsHXK3 affects grain size by promoting spikelet husk cell expansion. Knockout of other nine OsHXK genes except OsHXK3 individually did not change grain size, indicating that functions of OsHXKs have differentiated in rice. OsHXK3 influences gibberellin (GA) biosynthesis and homeostasis. Compared with wild type, OsGA3ox2 was significantly up-regulated and OsGA2ox1 was significantly down-regulated in young panicle of sng1 , and concentrations of biologically active GAs were significantly decreased in young panicles of the mutants. The yield per plant of OsHXK3 overexpression lines (OE-4 and OE-35) was increased by 10.91% and 7.62%, respectively, compared to that of wild type. Our results provide evidence that an HXK lacking catalytic and sensory functions plays an important role in grain size and has the potential to increase yield in rice.
doi_str_mv	10.1007/s00122-022-04189-7
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Grain size is an important agronomic trait determining grain yield and appearance quality in rice. Here, we report the discovery of rice mutant short and narrow grain1 ( sng1 ) with reduced grain length, width and weight. Map-based cloning revealed that the mutant phenotype was caused by loss of function of gene OsHXK3 that encodes a hexokinase-like (HKL) protein. OsHXK3 was associated with the mitochondria and was ubiquitously distributed in various organs, predominately in younger organs. Analysis of glucose (Glc) phosphorylation activities in young panicles and protoplasts showed that OsHXK3 was a non-catalytic hexokinase (HXK). Overexpression of OsHXK3 could not complement the Arabidopsis glucose insensitive2-1 ( gin2-1 ) mutant, indicating that OsHXK3 lacked Glc signaling activity. Scanning electron microscopy analysis revealed that OsHXK3 affects grain size by promoting spikelet husk cell expansion. Knockout of other nine OsHXK genes except OsHXK3 individually did not change grain size, indicating that functions of OsHXKs have differentiated in rice. OsHXK3 influences gibberellin (GA) biosynthesis and homeostasis. Compared with wild type, OsGA3ox2 was significantly up-regulated and OsGA2ox1 was significantly down-regulated in young panicle of sng1 , and concentrations of biologically active GAs were significantly decreased in young panicles of the mutants. The yield per plant of OsHXK3 overexpression lines (OE-4 and OE-35) was increased by 10.91% and 7.62%, respectively, compared to that of wild type. Our results provide evidence that an HXK lacking catalytic and sensory functions plays an important role in grain size and has the potential to increase yield in rice.</description><identifier>ISSN: 0040-5752</identifier><identifier>EISSN: 1432-2242</identifier><identifier>DOI: 10.1007/s00122-022-04189-7</identifier><identifier>PMID: 35941236</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Agriculture ; Biochemistry ; Biological activity ; Biomedical and Life Sciences ; Biotechnology ; Cloning ; Crop yields ; Edible Grain - genetics ; Edible Grain - metabolism ; Environmental aspects ; Forecasts and trends ; Gene Expression Regulation, Plant ; Genetic aspects ; Gibberellins ; Gibberellins - metabolism ; Glucose - metabolism ; Grain ; Grain size ; Growth ; Health aspects ; Hexokinase ; Hexokinase - genetics ; Hexokinase - metabolism ; Homeostasis ; Life Sciences ; Measurement ; Mitochondria ; Mutants ; Original Article ; Oryza - genetics ; Oryza - metabolism ; Phenotypes ; Phosphorylation ; Plant Biochemistry ; Plant Breeding/Biotechnology ; Plant Genetics and Genomics ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Proteins ; Protoplasts ; Rice ; Scanning electron microscopy</subject><ispartof>Theoretical and applied genetics, 2022-10, Vol.135 (10), p.3417-3431</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022. 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The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.</rights><rights>COPYRIGHT 2022 Springer</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c476t-96e1fe37f98ef92fb673b3fd694dcb17049b5ae15e633c9f08065dbc5fb3a8a73</citedby><cites>FETCH-LOGICAL-c476t-96e1fe37f98ef92fb673b3fd694dcb17049b5ae15e633c9f08065dbc5fb3a8a73</cites><orcidid>0000-0002-4855-5991</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00122-022-04189-7$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00122-022-04189-7$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>315,781,785,27926,27927,41490,42559,51321</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35941236$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yun, Peng</creatorcontrib><creatorcontrib>Li, Yibo</creatorcontrib><creatorcontrib>Wu, Bian</creatorcontrib><creatorcontrib>Zhu, Yun</creatorcontrib><creatorcontrib>Wang, Kaiyue</creatorcontrib><creatorcontrib>Li, Pingbo</creatorcontrib><creatorcontrib>Gao, Guanjun</creatorcontrib><creatorcontrib>Zhang, Qinglu</creatorcontrib><creatorcontrib>Li, Xianghua</creatorcontrib><creatorcontrib>Li, Zefu</creatorcontrib><creatorcontrib>He, Yuqing</creatorcontrib><title>OsHXK3 encodes a hexokinase-like protein that positively regulates grain size in rice</title><title>Theoretical and applied genetics</title><addtitle>Theor Appl Genet</addtitle><addtitle>Theor Appl Genet</addtitle><description>Key message We report the map-based cloning and functional characterization of SNG1 , which encodes OsHXK3, a hexokinase-like protein that plays a pivotal role in controlling grain size in rice. Grain size is an important agronomic trait determining grain yield and appearance quality in rice. Here, we report the discovery of rice mutant short and narrow grain1 ( sng1 ) with reduced grain length, width and weight. Map-based cloning revealed that the mutant phenotype was caused by loss of function of gene OsHXK3 that encodes a hexokinase-like (HKL) protein. OsHXK3 was associated with the mitochondria and was ubiquitously distributed in various organs, predominately in younger organs. Analysis of glucose (Glc) phosphorylation activities in young panicles and protoplasts showed that OsHXK3 was a non-catalytic hexokinase (HXK). Overexpression of OsHXK3 could not complement the Arabidopsis glucose insensitive2-1 ( gin2-1 ) mutant, indicating that OsHXK3 lacked Glc signaling activity. Scanning electron microscopy analysis revealed that OsHXK3 affects grain size by promoting spikelet husk cell expansion. Knockout of other nine OsHXK genes except OsHXK3 individually did not change grain size, indicating that functions of OsHXKs have differentiated in rice. OsHXK3 influences gibberellin (GA) biosynthesis and homeostasis. Compared with wild type, OsGA3ox2 was significantly up-regulated and OsGA2ox1 was significantly down-regulated in young panicle of sng1 , and concentrations of biologically active GAs were significantly decreased in young panicles of the mutants. The yield per plant of OsHXK3 overexpression lines (OE-4 and OE-35) was increased by 10.91% and 7.62%, respectively, compared to that of wild type. Our results provide evidence that an HXK lacking catalytic and sensory functions plays an important role in grain size and has the potential to increase yield in rice.</description><subject>Agriculture</subject><subject>Biochemistry</subject><subject>Biological activity</subject><subject>Biomedical and Life Sciences</subject><subject>Biotechnology</subject><subject>Cloning</subject><subject>Crop yields</subject><subject>Edible Grain - genetics</subject><subject>Edible Grain - metabolism</subject><subject>Environmental aspects</subject><subject>Forecasts and trends</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genetic aspects</subject><subject>Gibberellins</subject><subject>Gibberellins - metabolism</subject><subject>Glucose - metabolism</subject><subject>Grain</subject><subject>Grain size</subject><subject>Growth</subject><subject>Health aspects</subject><subject>Hexokinase</subject><subject>Hexokinase - genetics</subject><subject>Hexokinase - metabolism</subject><subject>Homeostasis</subject><subject>Life Sciences</subject><subject>Measurement</subject><subject>Mitochondria</subject><subject>Mutants</subject><subject>Original Article</subject><subject>Oryza - genetics</subject><subject>Oryza - metabolism</subject><subject>Phenotypes</subject><subject>Phosphorylation</subject><subject>Plant Biochemistry</subject><subject>Plant Breeding/Biotechnology</subject><subject>Plant Genetics and Genomics</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Proteins</subject><subject>Protoplasts</subject><subject>Rice</subject><subject>Scanning electron microscopy</subject><issn>0040-5752</issn><issn>1432-2242</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kdFq1UAQhhex2GP1BbyQgDd6kTq7k2STy1KsLRYKasG7ZbOZTbfNSY67m9L69G441XKKyDIMzHz_MLM_Y284HHIA-TEAcCFyWKLgdZPLZ2zFCxS5EIV4zlYABeSlLMU-exnCNQCIEvAF28eyKbjAasUuL8Lpjy-Y0WimjkKmsyu6m27cqAPlg7uhbOOnSG7M4pWO2WYKLrpbGu4zT_086Jg0vdepH9wvylL2ztArtmf1EOj1Qz5glyefvh-f5ucXn8-Oj85zU8gq5k1F3BJK29RkG2HbSmKLtquaojMtl1A0bamJl1QhmsZCDVXZtaa0LepaSzxg77dz05I_ZwpRrV0wNAx6pGkOSkgA5JiOTei7J-j1NPsxbZcoXstCcBSPVK8HUm60U_TaLEPVkRTAUSLWiTr8B5VeR2tnppGsS_UdwYcdQWIi3cVezyGos29fd1mxZY2fQvBk1ca7tfb3ioNafFdb3xUssfiulo94-3Dd3K6p-yv5Y3QCcAuE1Bp78o_n_2fsb-I0tSQ</recordid><startdate>20221001</startdate><enddate>20221001</enddate><creator>Yun, Peng</creator><creator>Li, Yibo</creator><creator>Wu, Bian</creator><creator>Zhu, Yun</creator><creator>Wang, Kaiyue</creator><creator>Li, Pingbo</creator><creator>Gao, Guanjun</creator><creator>Zhang, Qinglu</creator><creator>Li, Xianghua</creator><creator>Li, Zefu</creator><creator>He, Yuqing</creator><general>Springer Berlin Heidelberg</general><general>Springer</general><general>Springer Nature B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISR</scope><scope>3V.</scope><scope>7SS</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-4855-5991</orcidid></search><sort><creationdate>20221001</creationdate><title>OsHXK3 encodes a hexokinase-like protein that positively regulates grain size in rice</title><author>Yun, Peng ; Li, Yibo ; Wu, Bian ; Zhu, Yun ; Wang, Kaiyue ; Li, Pingbo ; Gao, Guanjun ; Zhang, Qinglu ; Li, Xianghua ; Li, Zefu ; He, Yuqing</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c476t-96e1fe37f98ef92fb673b3fd694dcb17049b5ae15e633c9f08065dbc5fb3a8a73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Agriculture</topic><topic>Biochemistry</topic><topic>Biological activity</topic><topic>Biomedical and Life Sciences</topic><topic>Biotechnology</topic><topic>Cloning</topic><topic>Crop yields</topic><topic>Edible Grain - genetics</topic><topic>Edible Grain - metabolism</topic><topic>Environmental aspects</topic><topic>Forecasts and trends</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genetic aspects</topic><topic>Gibberellins</topic><topic>Gibberellins - metabolism</topic><topic>Glucose - metabolism</topic><topic>Grain</topic><topic>Grain size</topic><topic>Growth</topic><topic>Health aspects</topic><topic>Hexokinase</topic><topic>Hexokinase - genetics</topic><topic>Hexokinase - metabolism</topic><topic>Homeostasis</topic><topic>Life Sciences</topic><topic>Measurement</topic><topic>Mitochondria</topic><topic>Mutants</topic><topic>Original Article</topic><topic>Oryza - genetics</topic><topic>Oryza - metabolism</topic><topic>Phenotypes</topic><topic>Phosphorylation</topic><topic>Plant Biochemistry</topic><topic>Plant Breeding/Biotechnology</topic><topic>Plant Genetics and Genomics</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Proteins</topic><topic>Protoplasts</topic><topic>Rice</topic><topic>Scanning electron microscopy</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yun, Peng</creatorcontrib><creatorcontrib>Li, Yibo</creatorcontrib><creatorcontrib>Wu, Bian</creatorcontrib><creatorcontrib>Zhu, Yun</creatorcontrib><creatorcontrib>Wang, Kaiyue</creatorcontrib><creatorcontrib>Li, Pingbo</creatorcontrib><creatorcontrib>Gao, Guanjun</creatorcontrib><creatorcontrib>Zhang, Qinglu</creatorcontrib><creatorcontrib>Li, Xianghua</creatorcontrib><creatorcontrib>Li, Zefu</creatorcontrib><creatorcontrib>He, Yuqing</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Theoretical and applied genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yun, Peng</au><au>Li, Yibo</au><au>Wu, Bian</au><au>Zhu, Yun</au><au>Wang, Kaiyue</au><au>Li, Pingbo</au><au>Gao, Guanjun</au><au>Zhang, Qinglu</au><au>Li, Xianghua</au><au>Li, Zefu</au><au>He, Yuqing</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>OsHXK3 encodes a hexokinase-like protein that positively regulates grain size in rice</atitle><jtitle>Theoretical and applied genetics</jtitle><stitle>Theor Appl Genet</stitle><addtitle>Theor Appl Genet</addtitle><date>2022-10-01</date><risdate>2022</risdate><volume>135</volume><issue>10</issue><spage>3417</spage><epage>3431</epage><pages>3417-3431</pages><issn>0040-5752</issn><eissn>1432-2242</eissn><abstract>Key message We report the map-based cloning and functional characterization of SNG1 , which encodes OsHXK3, a hexokinase-like protein that plays a pivotal role in controlling grain size in rice. Grain size is an important agronomic trait determining grain yield and appearance quality in rice. Here, we report the discovery of rice mutant short and narrow grain1 ( sng1 ) with reduced grain length, width and weight. Map-based cloning revealed that the mutant phenotype was caused by loss of function of gene OsHXK3 that encodes a hexokinase-like (HKL) protein. OsHXK3 was associated with the mitochondria and was ubiquitously distributed in various organs, predominately in younger organs. Analysis of glucose (Glc) phosphorylation activities in young panicles and protoplasts showed that OsHXK3 was a non-catalytic hexokinase (HXK). Overexpression of OsHXK3 could not complement the Arabidopsis glucose insensitive2-1 ( gin2-1 ) mutant, indicating that OsHXK3 lacked Glc signaling activity. Scanning electron microscopy analysis revealed that OsHXK3 affects grain size by promoting spikelet husk cell expansion. Knockout of other nine OsHXK genes except OsHXK3 individually did not change grain size, indicating that functions of OsHXKs have differentiated in rice. OsHXK3 influences gibberellin (GA) biosynthesis and homeostasis. Compared with wild type, OsGA3ox2 was significantly up-regulated and OsGA2ox1 was significantly down-regulated in young panicle of sng1 , and concentrations of biologically active GAs were significantly decreased in young panicles of the mutants. The yield per plant of OsHXK3 overexpression lines (OE-4 and OE-35) was increased by 10.91% and 7.62%, respectively, compared to that of wild type. Our results provide evidence that an HXK lacking catalytic and sensory functions plays an important role in grain size and has the potential to increase yield in rice.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>35941236</pmid><doi>10.1007/s00122-022-04189-7</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-4855-5991</orcidid></addata></record>
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subjects	Agriculture Biochemistry Biological activity Biomedical and Life Sciences Biotechnology Cloning Crop yields Edible Grain - genetics Edible Grain - metabolism Environmental aspects Forecasts and trends Gene Expression Regulation, Plant Genetic aspects Gibberellins Gibberellins - metabolism Glucose - metabolism Grain Grain size Growth Health aspects Hexokinase Hexokinase - genetics Hexokinase - metabolism Homeostasis Life Sciences Measurement Mitochondria Mutants Original Article Oryza - genetics Oryza - metabolism Phenotypes Phosphorylation Plant Biochemistry Plant Breeding/Biotechnology Plant Genetics and Genomics Plant Proteins - genetics Plant Proteins - metabolism Proteins Protoplasts Rice Scanning electron microscopy
title	OsHXK3 encodes a hexokinase-like protein that positively regulates grain size in rice
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