Mutations in eIF5B Confer Thermosensitive and Pleiotropic Phenotypes via Translation Defects in Arabidopsis thaliana
The conserved eukaryotic translation initiation factor 5B, eIF5B, is a GTPase that acts late in translation initiation. We found that an Arabidopsis thaliana mutant sensitive to hot temperatures 3 (hot3-1), which behaves as the wild type in the absence of stress but is unable to acclimate to high te...
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| Veröffentlicht in: | The Plant cell 2017-08, Vol.29 (8), p.1952-1969 |
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| container_end_page | 1969 |
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| container_issue | 8 |
| container_start_page | 1952 |
| container_title | The Plant cell |
| container_volume | 29 |
| creator | Zhang, Liyuan Liu, Xinye Gaikwad, Kishor Kou, Xiaoxia Wang, Fei Tian, Xuejun Xin, Mingming Ni, Zhongfu Sun, Qixin Peng, Huiru Vierling, Elizabeth |
| description | The conserved eukaryotic translation initiation factor 5B, eIF5B, is a GTPase that acts late in translation initiation. We found that an Arabidopsis thaliana mutant sensitive to hot temperatures 3 (hot3-1), which behaves as the wild type in the absence of stress but is unable to acclimate to high temperature, carries a missense mutation in the eIF5B1 gene (At1g76810), producing a temperature sensitive protein. A more severe, T-DNA insertion allele (hot3-2) causes pleiotropic developmental phenotypes. Surprisingly, Arabidopsis has three other eIF5B genes that do not substitute for eIF5B1; two of these appear to be in the process of pseudogenization. Polysome profiling and RNA-seq analysis of hot3-1 plants show delayed recovery of polysomes after heat stress and reduced translational efficiency (TE) of a subset of stress protective proteins, demonstrating the critical role of translational control early in heat acclimation. Plants carrying the severe hot3-2 allele show decreased TE of auxin-regulated, ribosome-related, and electron transport genes, even under optimal growth conditions. The hot3-2 data suggest that disrupting specific eIF5B interactions on the ribosome can, directly or indirectly, differentially affect translation. Thus, modulating eIF5B interactions could be another mechanism of gene-specific translational control. |
| doi_str_mv | 10.1105/tpc.16.00808 |
| format | Article |
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We found that an Arabidopsis thaliana mutant sensitive to hot temperatures 3 (hot3-1), which behaves as the wild type in the absence of stress but is unable to acclimate to high temperature, carries a missense mutation in the eIF5B1 gene (At1g76810), producing a temperature sensitive protein. A more severe, T-DNA insertion allele (hot3-2) causes pleiotropic developmental phenotypes. Surprisingly, Arabidopsis has three other eIF5B genes that do not substitute for eIF5B1; two of these appear to be in the process of pseudogenization. Polysome profiling and RNA-seq analysis of hot3-1 plants show delayed recovery of polysomes after heat stress and reduced translational efficiency (TE) of a subset of stress protective proteins, demonstrating the critical role of translational control early in heat acclimation. Plants carrying the severe hot3-2 allele show decreased TE of auxin-regulated, ribosome-related, and electron transport genes, even under optimal growth conditions. The hot3-2 data suggest that disrupting specific eIF5B interactions on the ribosome can, directly or indirectly, differentially affect translation. Thus, modulating eIF5B interactions could be another mechanism of gene-specific translational control.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.16.00808</identifier><identifier>PMID: 28808135</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Acclimation ; Acclimatization ; Alleles ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Deoxyribonucleic acid ; DNA ; DNA, Bacterial - genetics ; Electron transport ; Electron Transport - genetics ; Eukaryotic Initiation Factors - genetics ; Eukaryotic Initiation Factors - metabolism ; Gene Expression Regulation, Plant ; Genes ; Genetic Complementation Test ; Genetic Pleiotropy ; Growth conditions ; Guanosine triphosphatases ; Heat ; Heat stress ; Heat tolerance ; Heat-Shock Response - genetics ; High temperature ; Indoleacetic Acids - metabolism ; Initiation factor eIF-5B ; Missense mutation ; mRNA ; Mutagenesis, Insertional ; Mutation ; Mutation - genetics ; Phenotype ; Phylogeny ; Plant Development ; Polyribosomes ; Polyribosomes - metabolism ; Protein Biosynthesis - genetics ; Proteins ; Ribonucleic acid ; RNA ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Sequence Homology, Amino Acid ; T-DNA ; Temperature ; Thermotolerance ; Time Factors</subject><ispartof>The Plant cell, 2017-08, Vol.29 (8), p.1952-1969</ispartof><rights>2017 American Society of Plant Biologists</rights><rights>2017 American Society of Plant Biologists. All rights reserved.</rights><rights>Copyright American Society of Plant Biologists Aug 2017</rights><rights>2017 American Society of Plant Biologists. All rights reserved. 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c434t-189b90c013c4d2502e5c7ab64080942349a8440ef11052b43f2b7e745538bcee3</citedby><orcidid>0000-0002-3591-4852 ; 0000-0002-6475-1554 ; 0000-0003-0189-4440 ; 0000-0002-0484-3844 ; 0000-0001-7811-8437 ; 0000-0002-0066-4881 ; 0000-0002-3751-7746 ; 0000-0002-7339-7374</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/90012853$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/90012853$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,803,885,27924,27925,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28808135$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Liyuan</creatorcontrib><creatorcontrib>Liu, Xinye</creatorcontrib><creatorcontrib>Gaikwad, Kishor</creatorcontrib><creatorcontrib>Kou, Xiaoxia</creatorcontrib><creatorcontrib>Wang, Fei</creatorcontrib><creatorcontrib>Tian, Xuejun</creatorcontrib><creatorcontrib>Xin, Mingming</creatorcontrib><creatorcontrib>Ni, Zhongfu</creatorcontrib><creatorcontrib>Sun, Qixin</creatorcontrib><creatorcontrib>Peng, Huiru</creatorcontrib><creatorcontrib>Vierling, Elizabeth</creatorcontrib><title>Mutations in eIF5B Confer Thermosensitive and Pleiotropic Phenotypes via Translation Defects in Arabidopsis thaliana</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>The conserved eukaryotic translation initiation factor 5B, eIF5B, is a GTPase that acts late in translation initiation. We found that an Arabidopsis thaliana mutant sensitive to hot temperatures 3 (hot3-1), which behaves as the wild type in the absence of stress but is unable to acclimate to high temperature, carries a missense mutation in the eIF5B1 gene (At1g76810), producing a temperature sensitive protein. A more severe, T-DNA insertion allele (hot3-2) causes pleiotropic developmental phenotypes. Surprisingly, Arabidopsis has three other eIF5B genes that do not substitute for eIF5B1; two of these appear to be in the process of pseudogenization. Polysome profiling and RNA-seq analysis of hot3-1 plants show delayed recovery of polysomes after heat stress and reduced translational efficiency (TE) of a subset of stress protective proteins, demonstrating the critical role of translational control early in heat acclimation. Plants carrying the severe hot3-2 allele show decreased TE of auxin-regulated, ribosome-related, and electron transport genes, even under optimal growth conditions. The hot3-2 data suggest that disrupting specific eIF5B interactions on the ribosome can, directly or indirectly, differentially affect translation. Thus, modulating eIF5B interactions could be another mechanism of gene-specific translational control.</description><subject>Acclimation</subject><subject>Acclimatization</subject><subject>Alleles</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA, Bacterial - genetics</subject><subject>Electron transport</subject><subject>Electron Transport - genetics</subject><subject>Eukaryotic Initiation Factors - genetics</subject><subject>Eukaryotic Initiation Factors - metabolism</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Genetic Complementation Test</subject><subject>Genetic Pleiotropy</subject><subject>Growth conditions</subject><subject>Guanosine triphosphatases</subject><subject>Heat</subject><subject>Heat stress</subject><subject>Heat tolerance</subject><subject>Heat-Shock Response - genetics</subject><subject>High temperature</subject><subject>Indoleacetic Acids - metabolism</subject><subject>Initiation factor eIF-5B</subject><subject>Missense mutation</subject><subject>mRNA</subject><subject>Mutagenesis, Insertional</subject><subject>Mutation</subject><subject>Mutation - genetics</subject><subject>Phenotype</subject><subject>Phylogeny</subject><subject>Plant Development</subject><subject>Polyribosomes</subject><subject>Polyribosomes - metabolism</subject><subject>Protein Biosynthesis - genetics</subject><subject>Proteins</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Sequence Homology, Amino Acid</subject><subject>T-DNA</subject><subject>Temperature</subject><subject>Thermotolerance</subject><subject>Time Factors</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc9v0zAYhiMEYr-4cQVZ4sJhKZ8dO4kvSKMwmDS0HYrEzXLcL9RVame2U2n__bx2q4CTLX2PHn-v36J4S2FGKYhPaTQzWs8AWmhfFMdUVKxksv39Mt-BQ8lrQY-KkxjXAEAbKl8XR6zNMK3EcZF-Tkkn610k1hG8uhRfyNy7HgNZrDBsfEQXbbJbJNotye2A1qfgR2vI7QqdT_cjRrK1miyCdnHYuchX7NGknfIi6M4u_RhtJGmlB6udPite9XqI-ObpPC1-XX5bzH-U1zffr-YX16XhFU8lbWUnwQCtDF8yAQyFaXRX8xxVclZxqVvOAfvHf2Adr3rWNdhwIaq2M4jVafF57x2nboNLgy4FPagx2I0O98prq_6dOLtSf_xWCSGBS5YFH58Ewd9NGJPa2GhwGLRDP0VFJZP5bdmKjH74D137KbgcTzGAWoJsWp6p8z1lgo8xYH9YhoJ6jKFynYrWaldnxt__HeAAP_eXgXd7YB2TD4e5zE2zvFT1ALDfpf0</recordid><startdate>20170801</startdate><enddate>20170801</enddate><creator>Zhang, Liyuan</creator><creator>Liu, Xinye</creator><creator>Gaikwad, Kishor</creator><creator>Kou, Xiaoxia</creator><creator>Wang, Fei</creator><creator>Tian, Xuejun</creator><creator>Xin, Mingming</creator><creator>Ni, Zhongfu</creator><creator>Sun, Qixin</creator><creator>Peng, Huiru</creator><creator>Vierling, Elizabeth</creator><general>American Society of Plant Biologists</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>4T-</scope><scope>7QO</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-3591-4852</orcidid><orcidid>https://orcid.org/0000-0002-6475-1554</orcidid><orcidid>https://orcid.org/0000-0003-0189-4440</orcidid><orcidid>https://orcid.org/0000-0002-0484-3844</orcidid><orcidid>https://orcid.org/0000-0001-7811-8437</orcidid><orcidid>https://orcid.org/0000-0002-0066-4881</orcidid><orcidid>https://orcid.org/0000-0002-3751-7746</orcidid><orcidid>https://orcid.org/0000-0002-7339-7374</orcidid></search><sort><creationdate>20170801</creationdate><title>Mutations in eIF5B Confer Thermosensitive and Pleiotropic Phenotypes via Translation Defects in Arabidopsis thaliana</title><author>Zhang, Liyuan ; Liu, Xinye ; Gaikwad, Kishor ; Kou, Xiaoxia ; Wang, Fei ; Tian, Xuejun ; Xin, Mingming ; Ni, Zhongfu ; Sun, Qixin ; Peng, Huiru ; Vierling, Elizabeth</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c434t-189b90c013c4d2502e5c7ab64080942349a8440ef11052b43f2b7e745538bcee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Acclimation</topic><topic>Acclimatization</topic><topic>Alleles</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA, Bacterial - genetics</topic><topic>Electron transport</topic><topic>Electron Transport - genetics</topic><topic>Eukaryotic Initiation Factors - genetics</topic><topic>Eukaryotic Initiation Factors - metabolism</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>Genetic Complementation Test</topic><topic>Genetic Pleiotropy</topic><topic>Growth conditions</topic><topic>Guanosine triphosphatases</topic><topic>Heat</topic><topic>Heat stress</topic><topic>Heat tolerance</topic><topic>Heat-Shock Response - genetics</topic><topic>High temperature</topic><topic>Indoleacetic Acids - metabolism</topic><topic>Initiation factor eIF-5B</topic><topic>Missense mutation</topic><topic>mRNA</topic><topic>Mutagenesis, Insertional</topic><topic>Mutation</topic><topic>Mutation - genetics</topic><topic>Phenotype</topic><topic>Phylogeny</topic><topic>Plant Development</topic><topic>Polyribosomes</topic><topic>Polyribosomes - metabolism</topic><topic>Protein Biosynthesis - genetics</topic><topic>Proteins</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Sequence Homology, Amino Acid</topic><topic>T-DNA</topic><topic>Temperature</topic><topic>Thermotolerance</topic><topic>Time Factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Liyuan</creatorcontrib><creatorcontrib>Liu, Xinye</creatorcontrib><creatorcontrib>Gaikwad, Kishor</creatorcontrib><creatorcontrib>Kou, Xiaoxia</creatorcontrib><creatorcontrib>Wang, Fei</creatorcontrib><creatorcontrib>Tian, Xuejun</creatorcontrib><creatorcontrib>Xin, Mingming</creatorcontrib><creatorcontrib>Ni, Zhongfu</creatorcontrib><creatorcontrib>Sun, Qixin</creatorcontrib><creatorcontrib>Peng, Huiru</creatorcontrib><creatorcontrib>Vierling, Elizabeth</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Docstoc</collection><collection>Biotechnology Research Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Liyuan</au><au>Liu, Xinye</au><au>Gaikwad, Kishor</au><au>Kou, Xiaoxia</au><au>Wang, Fei</au><au>Tian, Xuejun</au><au>Xin, Mingming</au><au>Ni, Zhongfu</au><au>Sun, Qixin</au><au>Peng, Huiru</au><au>Vierling, Elizabeth</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mutations in eIF5B Confer Thermosensitive and Pleiotropic Phenotypes via Translation Defects in Arabidopsis thaliana</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2017-08-01</date><risdate>2017</risdate><volume>29</volume><issue>8</issue><spage>1952</spage><epage>1969</epage><pages>1952-1969</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><abstract>The conserved eukaryotic translation initiation factor 5B, eIF5B, is a GTPase that acts late in translation initiation. We found that an Arabidopsis thaliana mutant sensitive to hot temperatures 3 (hot3-1), which behaves as the wild type in the absence of stress but is unable to acclimate to high temperature, carries a missense mutation in the eIF5B1 gene (At1g76810), producing a temperature sensitive protein. A more severe, T-DNA insertion allele (hot3-2) causes pleiotropic developmental phenotypes. Surprisingly, Arabidopsis has three other eIF5B genes that do not substitute for eIF5B1; two of these appear to be in the process of pseudogenization. Polysome profiling and RNA-seq analysis of hot3-1 plants show delayed recovery of polysomes after heat stress and reduced translational efficiency (TE) of a subset of stress protective proteins, demonstrating the critical role of translational control early in heat acclimation. Plants carrying the severe hot3-2 allele show decreased TE of auxin-regulated, ribosome-related, and electron transport genes, even under optimal growth conditions. The hot3-2 data suggest that disrupting specific eIF5B interactions on the ribosome can, directly or indirectly, differentially affect translation. Thus, modulating eIF5B interactions could be another mechanism of gene-specific translational control.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>28808135</pmid><doi>10.1105/tpc.16.00808</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-3591-4852</orcidid><orcidid>https://orcid.org/0000-0002-6475-1554</orcidid><orcidid>https://orcid.org/0000-0003-0189-4440</orcidid><orcidid>https://orcid.org/0000-0002-0484-3844</orcidid><orcidid>https://orcid.org/0000-0001-7811-8437</orcidid><orcidid>https://orcid.org/0000-0002-0066-4881</orcidid><orcidid>https://orcid.org/0000-0002-3751-7746</orcidid><orcidid>https://orcid.org/0000-0002-7339-7374</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | The Plant cell, 2017-08, Vol.29 (8), p.1952-1969 |
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| source | MEDLINE; JSTOR Archive Collection A-Z Listing; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals |
| subjects | Acclimation Acclimatization Alleles Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Deoxyribonucleic acid DNA DNA, Bacterial - genetics Electron transport Electron Transport - genetics Eukaryotic Initiation Factors - genetics Eukaryotic Initiation Factors - metabolism Gene Expression Regulation, Plant Genes Genetic Complementation Test Genetic Pleiotropy Growth conditions Guanosine triphosphatases Heat Heat stress Heat tolerance Heat-Shock Response - genetics High temperature Indoleacetic Acids - metabolism Initiation factor eIF-5B Missense mutation mRNA Mutagenesis, Insertional Mutation Mutation - genetics Phenotype Phylogeny Plant Development Polyribosomes Polyribosomes - metabolism Protein Biosynthesis - genetics Proteins Ribonucleic acid RNA RNA, Messenger - genetics RNA, Messenger - metabolism Sequence Homology, Amino Acid T-DNA Temperature Thermotolerance Time Factors |
| title | Mutations in eIF5B Confer Thermosensitive and Pleiotropic Phenotypes via Translation Defects in Arabidopsis thaliana |
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