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Whole transcriptome sequencing reveals genes involved in plastid/chloroplast division and development are regulated by the HP1/DDB1 at an early stage of tomato fruit development
The phenotype of tomato high pigment-1 (hp1) mutant is characterized by overproduction of pigments including chlorophyll and carotenoids during fruit development and ripening. Although the increased plastid compartment size has been thought to largely attribute to the enhanced pigmentation, the mole...
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Published in: | Planta 2013-11, Vol.238 (5), p.923-936 |
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creator | Tang, Xiaofeng Tang, Zizhi Huang, Shengxiong Liu, Jikai Liu, Jia Shi, Wei Tian, Xuefen Li, Yuxiang Zhang, Danfeng Yang, Jian Gao, Yongfeng Zeng, Deer Hou, Pei Niu, Xiangli Cao, Ying Li, Guangwei Li, Xiao Xiao, Fangming Liu, Yongsheng |
description | The phenotype of tomato high pigment-1 (hp1) mutant is characterized by overproduction of pigments including chlorophyll and carotenoids during fruit development and ripening. Although the increased plastid compartment size has been thought to largely attribute to the enhanced pigmentation, the molecular aspects of how the HP1/DDB1 gene manipulates plastid biogenesis and development are largely unknown. In the present study, we compared transcriptome profiles of immature fruit pericarp tissue between tomato cv. Ailsa Craig (WT) and its isogenic hp1 mutant. Over 20 million sequence reads, representing > 1.6 Gb sequence data per sample, were generated and assembled into 21,972 and 22,167 gene models in WT and hp1, respectively, accounting for over 60 % official gene models in both samples. Subsequent analyses revealed that 8,322 and 7,989 alternative splicing events, 8833 or 8510 extended 5′-UTRs, 8,263 or 8,939 extended 3′-UTRs, and 1,136 and 1,133 novel transcripts, exist in WT and hp1, respectively. Significant differences in expression level of 880 genes were detected between the WT and hp1, many of which are involved in signaling transduction, transcription regulation and biotic and abiotic stresses response. Distinctly, RNA-seq datasets, quantitative RT-PCR analyses demonstrate that, in hp1 mutant pericarp tissue at early developmental stage, an apparent expression alteration was found in several regulators directly involved in plastid division and development. These results provide a useful reference for a more accurate and more detailed characterization of the molecular process in the development and pigmentation of tomato fruits. |
doi_str_mv | 10.1007/s00425-013-1942-9 |
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Although the increased plastid compartment size has been thought to largely attribute to the enhanced pigmentation, the molecular aspects of how the HP1/DDB1 gene manipulates plastid biogenesis and development are largely unknown. In the present study, we compared transcriptome profiles of immature fruit pericarp tissue between tomato cv. Ailsa Craig (WT) and its isogenic hp1 mutant. Over 20 million sequence reads, representing > 1.6 Gb sequence data per sample, were generated and assembled into 21,972 and 22,167 gene models in WT and hp1, respectively, accounting for over 60 % official gene models in both samples. Subsequent analyses revealed that 8,322 and 7,989 alternative splicing events, 8833 or 8510 extended 5′-UTRs, 8,263 or 8,939 extended 3′-UTRs, and 1,136 and 1,133 novel transcripts, exist in WT and hp1, respectively. Significant differences in expression level of 880 genes were detected between the WT and hp1, many of which are involved in signaling transduction, transcription regulation and biotic and abiotic stresses response. Distinctly, RNA-seq datasets, quantitative RT-PCR analyses demonstrate that, in hp1 mutant pericarp tissue at early developmental stage, an apparent expression alteration was found in several regulators directly involved in plastid division and development. These results provide a useful reference for a more accurate and more detailed characterization of the molecular process in the development and pigmentation of tomato fruits.</description><identifier>ISSN: 0032-0935</identifier><identifier>EISSN: 1432-2048</identifier><identifier>DOI: 10.1007/s00425-013-1942-9</identifier><identifier>PMID: 23948801</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer-Verlag</publisher><subject>3' Untranslated Regions - genetics ; 5' Untranslated Regions - genetics ; Agriculture ; alternative splicing ; Alternative Splicing - genetics ; Biomedical and Life Sciences ; Carotenoids ; chlorophyll ; Chlorophylls ; Chloroplasts ; data collection ; Developmental stages ; early development ; Ecology ; Exons ; Forestry ; Fruit - genetics ; Fruit - growth & development ; fruiting ; Fruits ; Gene Expression Regulation, Developmental ; Gene Expression Regulation, Plant ; Gene Ontology ; Genes ; Genes, Plant - genetics ; Genomes ; Life Sciences ; Lycopersicon esculentum ; Lycopersicon esculentum - genetics ; Lycopersicon esculentum - growth & development ; Molecular Sequence Annotation ; mutants ; Original Article ; pericarp ; phenotype ; Pigmentation ; pigments ; Plant cells ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Sciences ; Plants ; Plastids ; Plastids - genetics ; Reproducibility of Results ; Reverse Transcriptase Polymerase Chain Reaction ; ripening ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Sequence Analysis, RNA ; Tomatoes ; transcription (genetics) ; Transcription, Genetic ; transcriptome ; Transcriptome - genetics ; Untranslated regions</subject><ispartof>Planta, 2013-11, Vol.238 (5), p.923-936</ispartof><rights>Springer-Verlag Berlin Heidelberg 2013</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c451t-c92b5a0f4ff0c3581f968a85afb4a0323037d413a8c35b9d45d5548b6955c91e3</citedby><cites>FETCH-LOGICAL-c451t-c92b5a0f4ff0c3581f968a85afb4a0323037d413a8c35b9d45d5548b6955c91e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/43564027$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/43564027$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23948801$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tang, Xiaofeng</creatorcontrib><creatorcontrib>Tang, Zizhi</creatorcontrib><creatorcontrib>Huang, Shengxiong</creatorcontrib><creatorcontrib>Liu, Jikai</creatorcontrib><creatorcontrib>Liu, Jia</creatorcontrib><creatorcontrib>Shi, Wei</creatorcontrib><creatorcontrib>Tian, Xuefen</creatorcontrib><creatorcontrib>Li, Yuxiang</creatorcontrib><creatorcontrib>Zhang, Danfeng</creatorcontrib><creatorcontrib>Yang, Jian</creatorcontrib><creatorcontrib>Gao, Yongfeng</creatorcontrib><creatorcontrib>Zeng, Deer</creatorcontrib><creatorcontrib>Hou, Pei</creatorcontrib><creatorcontrib>Niu, Xiangli</creatorcontrib><creatorcontrib>Cao, Ying</creatorcontrib><creatorcontrib>Li, Guangwei</creatorcontrib><creatorcontrib>Li, Xiao</creatorcontrib><creatorcontrib>Xiao, Fangming</creatorcontrib><creatorcontrib>Liu, Yongsheng</creatorcontrib><title>Whole transcriptome sequencing reveals genes involved in plastid/chloroplast division and development are regulated by the HP1/DDB1 at an early stage of tomato fruit development</title><title>Planta</title><addtitle>Planta</addtitle><addtitle>Planta</addtitle><description>The phenotype of tomato high pigment-1 (hp1) mutant is characterized by overproduction of pigments including chlorophyll and carotenoids during fruit development and ripening. Although the increased plastid compartment size has been thought to largely attribute to the enhanced pigmentation, the molecular aspects of how the HP1/DDB1 gene manipulates plastid biogenesis and development are largely unknown. In the present study, we compared transcriptome profiles of immature fruit pericarp tissue between tomato cv. Ailsa Craig (WT) and its isogenic hp1 mutant. Over 20 million sequence reads, representing > 1.6 Gb sequence data per sample, were generated and assembled into 21,972 and 22,167 gene models in WT and hp1, respectively, accounting for over 60 % official gene models in both samples. Subsequent analyses revealed that 8,322 and 7,989 alternative splicing events, 8833 or 8510 extended 5′-UTRs, 8,263 or 8,939 extended 3′-UTRs, and 1,136 and 1,133 novel transcripts, exist in WT and hp1, respectively. Significant differences in expression level of 880 genes were detected between the WT and hp1, many of which are involved in signaling transduction, transcription regulation and biotic and abiotic stresses response. Distinctly, RNA-seq datasets, quantitative RT-PCR analyses demonstrate that, in hp1 mutant pericarp tissue at early developmental stage, an apparent expression alteration was found in several regulators directly involved in plastid division and development. These results provide a useful reference for a more accurate and more detailed characterization of the molecular process in the development and pigmentation of tomato fruits.</description><subject>3' Untranslated Regions - genetics</subject><subject>5' Untranslated Regions - genetics</subject><subject>Agriculture</subject><subject>alternative splicing</subject><subject>Alternative Splicing - genetics</subject><subject>Biomedical and Life Sciences</subject><subject>Carotenoids</subject><subject>chlorophyll</subject><subject>Chlorophylls</subject><subject>Chloroplasts</subject><subject>data collection</subject><subject>Developmental stages</subject><subject>early development</subject><subject>Ecology</subject><subject>Exons</subject><subject>Forestry</subject><subject>Fruit - genetics</subject><subject>Fruit - growth & development</subject><subject>fruiting</subject><subject>Fruits</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Ontology</subject><subject>Genes</subject><subject>Genes, Plant - genetics</subject><subject>Genomes</subject><subject>Life Sciences</subject><subject>Lycopersicon esculentum</subject><subject>Lycopersicon esculentum - genetics</subject><subject>Lycopersicon esculentum - growth & development</subject><subject>Molecular Sequence Annotation</subject><subject>mutants</subject><subject>Original Article</subject><subject>pericarp</subject><subject>phenotype</subject><subject>Pigmentation</subject><subject>pigments</subject><subject>Plant cells</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Sciences</subject><subject>Plants</subject><subject>Plastids</subject><subject>Plastids - genetics</subject><subject>Reproducibility of Results</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>ripening</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Sequence Analysis, RNA</subject><subject>Tomatoes</subject><subject>transcription (genetics)</subject><subject>Transcription, Genetic</subject><subject>transcriptome</subject><subject>Transcriptome - genetics</subject><subject>Untranslated regions</subject><issn>0032-0935</issn><issn>1432-2048</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNqNktFuFCEUhidGY7fVB_BCJfHGm3FhgFm41FatSRNNtPGSMDNnZtnMwhaYTfaxfMOedWrTeGHkBsj5_p8DP0XxgtF3jNLVMlEqKllSxkumRVXqR8WCCV6VFRXqcbGgFNdUc3lSnKa0oRSLq9XT4qTiWihF2aL49XMdRiA5Wp_a6HY5bIEkuJnAt84PJMIe7JjIAB4ScX4fxj10uCC70absumW7HkMMv3ekc3uXXPDE-o50KB3Dbgs-ExsBrYZptBnVzYHkNZDLb2x5cfGBEYuAJ2DjeCAp2wFI6Al2YnMgfZxcfuj1rHjSY0fw_G4-K64_ffxxflleff385fz9VdkKyXLZ6qqRlvai72nLpWK9rpVV0vaNsPgunPJVJxi3CquN7oTspBSqqbWUrWbAz4q3s-8uBnyOlM3WpRbG0XoIUzJM1IpLrbT8D1RIzWquV4i--QvdhCl6vMiREgr70gIpNlNtDClF6M0uuq2NB8OoOUZv5ugNRm-O0RuNmld3zlOzhe5e8SdrBKoZSFjyA8QHR__D9eUs2qQc4r2p4LIWtDre5_Vc720wdogumevvFX40ikNyWvNb4I7NyA</recordid><startdate>20131101</startdate><enddate>20131101</enddate><creator>Tang, Xiaofeng</creator><creator>Tang, Zizhi</creator><creator>Huang, Shengxiong</creator><creator>Liu, Jikai</creator><creator>Liu, Jia</creator><creator>Shi, Wei</creator><creator>Tian, Xuefen</creator><creator>Li, Yuxiang</creator><creator>Zhang, Danfeng</creator><creator>Yang, Jian</creator><creator>Gao, Yongfeng</creator><creator>Zeng, Deer</creator><creator>Hou, Pei</creator><creator>Niu, Xiangli</creator><creator>Cao, Ying</creator><creator>Li, Guangwei</creator><creator>Li, Xiao</creator><creator>Xiao, Fangming</creator><creator>Liu, Yongsheng</creator><general>Springer-Verlag</general><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>FBQ</scope><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>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>7X2</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>ATCPS</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>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20131101</creationdate><title>Whole transcriptome sequencing reveals genes involved in plastid/chloroplast division and development are regulated by the HP1/DDB1 at an early stage of tomato fruit development</title><author>Tang, Xiaofeng ; Tang, Zizhi ; Huang, Shengxiong ; Liu, Jikai ; Liu, Jia ; Shi, Wei ; Tian, Xuefen ; Li, Yuxiang ; Zhang, Danfeng ; Yang, Jian ; Gao, Yongfeng ; Zeng, Deer ; Hou, Pei ; Niu, Xiangli ; Cao, Ying ; Li, Guangwei ; Li, Xiao ; Xiao, Fangming ; Liu, Yongsheng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c451t-c92b5a0f4ff0c3581f968a85afb4a0323037d413a8c35b9d45d5548b6955c91e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>3' Untranslated Regions - 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genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Sciences</topic><topic>Plants</topic><topic>Plastids</topic><topic>Plastids - genetics</topic><topic>Reproducibility of Results</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>ripening</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Sequence Analysis, RNA</topic><topic>Tomatoes</topic><topic>transcription (genetics)</topic><topic>Transcription, Genetic</topic><topic>transcriptome</topic><topic>Transcriptome - genetics</topic><topic>Untranslated regions</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tang, Xiaofeng</creatorcontrib><creatorcontrib>Tang, Zizhi</creatorcontrib><creatorcontrib>Huang, Shengxiong</creatorcontrib><creatorcontrib>Liu, Jikai</creatorcontrib><creatorcontrib>Liu, Jia</creatorcontrib><creatorcontrib>Shi, Wei</creatorcontrib><creatorcontrib>Tian, Xuefen</creatorcontrib><creatorcontrib>Li, Yuxiang</creatorcontrib><creatorcontrib>Zhang, Danfeng</creatorcontrib><creatorcontrib>Yang, Jian</creatorcontrib><creatorcontrib>Gao, Yongfeng</creatorcontrib><creatorcontrib>Zeng, Deer</creatorcontrib><creatorcontrib>Hou, Pei</creatorcontrib><creatorcontrib>Niu, Xiangli</creatorcontrib><creatorcontrib>Cao, Ying</creatorcontrib><creatorcontrib>Li, Guangwei</creatorcontrib><creatorcontrib>Li, Xiao</creatorcontrib><creatorcontrib>Xiao, Fangming</creatorcontrib><creatorcontrib>Liu, Yongsheng</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Agricultural Science Collection</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)</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest 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>Agriculture Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Biological Science Journals</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>Genetics Abstracts</collection><collection>MEDLINE - 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Although the increased plastid compartment size has been thought to largely attribute to the enhanced pigmentation, the molecular aspects of how the HP1/DDB1 gene manipulates plastid biogenesis and development are largely unknown. In the present study, we compared transcriptome profiles of immature fruit pericarp tissue between tomato cv. Ailsa Craig (WT) and its isogenic hp1 mutant. Over 20 million sequence reads, representing > 1.6 Gb sequence data per sample, were generated and assembled into 21,972 and 22,167 gene models in WT and hp1, respectively, accounting for over 60 % official gene models in both samples. Subsequent analyses revealed that 8,322 and 7,989 alternative splicing events, 8833 or 8510 extended 5′-UTRs, 8,263 or 8,939 extended 3′-UTRs, and 1,136 and 1,133 novel transcripts, exist in WT and hp1, respectively. Significant differences in expression level of 880 genes were detected between the WT and hp1, many of which are involved in signaling transduction, transcription regulation and biotic and abiotic stresses response. Distinctly, RNA-seq datasets, quantitative RT-PCR analyses demonstrate that, in hp1 mutant pericarp tissue at early developmental stage, an apparent expression alteration was found in several regulators directly involved in plastid division and development. These results provide a useful reference for a more accurate and more detailed characterization of the molecular process in the development and pigmentation of tomato fruits.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer-Verlag</pub><pmid>23948801</pmid><doi>10.1007/s00425-013-1942-9</doi><tpages>14</tpages></addata></record> |
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source | JSTOR Archival Journals and Primary Sources Collection; Springer Nature |
subjects | 3' Untranslated Regions - genetics 5' Untranslated Regions - genetics Agriculture alternative splicing Alternative Splicing - genetics Biomedical and Life Sciences Carotenoids chlorophyll Chlorophylls Chloroplasts data collection Developmental stages early development Ecology Exons Forestry Fruit - genetics Fruit - growth & development fruiting Fruits Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Gene Ontology Genes Genes, Plant - genetics Genomes Life Sciences Lycopersicon esculentum Lycopersicon esculentum - genetics Lycopersicon esculentum - growth & development Molecular Sequence Annotation mutants Original Article pericarp phenotype Pigmentation pigments Plant cells Plant Proteins - genetics Plant Proteins - metabolism Plant Sciences Plants Plastids Plastids - genetics Reproducibility of Results Reverse Transcriptase Polymerase Chain Reaction ripening RNA, Messenger - genetics RNA, Messenger - metabolism Sequence Analysis, RNA Tomatoes transcription (genetics) Transcription, Genetic transcriptome Transcriptome - genetics Untranslated regions |
title | Whole transcriptome sequencing reveals genes involved in plastid/chloroplast division and development are regulated by the HP1/DDB1 at an early stage of tomato fruit development |
url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-30T20%3A09%3A59IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Whole%20transcriptome%20sequencing%20reveals%20genes%20involved%20in%20plastid/chloroplast%20division%20and%20development%20are%20regulated%20by%20the%20HP1/DDB1%20at%20an%20early%20stage%20of%20tomato%20fruit%20development&rft.jtitle=Planta&rft.au=Tang,%20Xiaofeng&rft.date=2013-11-01&rft.volume=238&rft.issue=5&rft.spage=923&rft.epage=936&rft.pages=923-936&rft.issn=0032-0935&rft.eissn=1432-2048&rft_id=info:doi/10.1007/s00425-013-1942-9&rft_dat=%3Cjstor_proqu%3E43564027%3C/jstor_proqu%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c451t-c92b5a0f4ff0c3581f968a85afb4a0323037d413a8c35b9d45d5548b6955c91e3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1444823094&rft_id=info:pmid/23948801&rft_jstor_id=43564027&rfr_iscdi=true |