A role for PHANTASTICA in medio-lateral regulation of adaxial domain development in tomato and tobacco leaves

• Background and Aims Diverse leaf forms in nature can be categorized into two groups: simple and compound. A simple leaf has a single blade unit, whilst a compound leaf is dissected into leaflets. For both simple and compound leaves, a MYB domain transcription factor PHANTASTICA (PHAN) plays an imp...

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Veröffentlicht in:Annals of botany 2012-02, Vol.109 (2), p.407-418
Hauptverfasser: Zoulias, Nicholas, Koenig, Daniel, Hamidi, Ashley, McCormick, Sheila, Kim, Minsung
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container_title Annals of botany
container_volume 109
creator Zoulias, Nicholas
Koenig, Daniel
Hamidi, Ashley
McCormick, Sheila
Kim, Minsung
description • Background and Aims Diverse leaf forms in nature can be categorized into two groups: simple and compound. A simple leaf has a single blade unit, whilst a compound leaf is dissected into leaflets. For both simple and compound leaves, a MYB domain transcription factor PHANTASTICA (PHAN) plays an important role in establishing the adaxial domain in the leaf. Absence of PHAN in arabidopsis and antirrhinum leaves supresses blade development, and in tomato suppresses leaflet development. However, in the rachis and petiole regions of tomato leaves where PHAN and the adaxial domain coexist, it has been unclear why leaf blade and leaflets are not formed. We hypothesized that PHAN regulates the medio-lateral extent of the adaxial domain, thereby determining compound leaf architecture. • Methods To test this hypothesis, we generated and analysed transgenic tomato plants expressing tomato PHAN (SIPHAN) under the Cauliflower mosaic virus (CaMV) 35S promoter in both sense and antisense orientations, and tobacco plants that over-express tomato SlPHAN. • Key Results Modulations in SlPHAN resulted in a variety of leaf morphologies such as simple, ternate and compound in either a peltate or non-peltate arrangement. Measurements of the extent of the adaxial domain along the wild-type tomato leaf axis showed that the adaxial domain is narrowed in the rachis and petiole in comparison with regions where laminar tissue arises. In antiSlPHAN transgenic leaves, no blade or leaflet was formed where the adaxial domain was medio-laterally narrowed, and KNOX gene expression was correlatively upregulated. CaMV35S::SlPHAN expression led to widening of the adaxial domain and ectopie blade outgrowth in the rachis of tomato and in the petiole of tobacco. Taken together, these results suggest that SlPHAN plays a role in medio-lateral extension of the adaxial domain and contributes to final leaf morphology in tomato. • Conclusions This study provides a novel insight into leaf architecture in tomato and highlights how changes in the expression domain of a master regulator gene such as SlPHAN can be translated into diverse final leaf morphologies.
doi_str_mv 10.1093/aob/mcr295
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A simple leaf has a single blade unit, whilst a compound leaf is dissected into leaflets. For both simple and compound leaves, a MYB domain transcription factor PHANTASTICA (PHAN) plays an important role in establishing the adaxial domain in the leaf. Absence of PHAN in arabidopsis and antirrhinum leaves supresses blade development, and in tomato suppresses leaflet development. However, in the rachis and petiole regions of tomato leaves where PHAN and the adaxial domain coexist, it has been unclear why leaf blade and leaflets are not formed. We hypothesized that PHAN regulates the medio-lateral extent of the adaxial domain, thereby determining compound leaf architecture. • Methods To test this hypothesis, we generated and analysed transgenic tomato plants expressing tomato PHAN (SIPHAN) under the Cauliflower mosaic virus (CaMV) 35S promoter in both sense and antisense orientations, and tobacco plants that over-express tomato SlPHAN. • Key Results Modulations in SlPHAN resulted in a variety of leaf morphologies such as simple, ternate and compound in either a peltate or non-peltate arrangement. Measurements of the extent of the adaxial domain along the wild-type tomato leaf axis showed that the adaxial domain is narrowed in the rachis and petiole in comparison with regions where laminar tissue arises. In antiSlPHAN transgenic leaves, no blade or leaflet was formed where the adaxial domain was medio-laterally narrowed, and KNOX gene expression was correlatively upregulated. CaMV35S::SlPHAN expression led to widening of the adaxial domain and ectopie blade outgrowth in the rachis of tomato and in the petiole of tobacco. Taken together, these results suggest that SlPHAN plays a role in medio-lateral extension of the adaxial domain and contributes to final leaf morphology in tomato. • Conclusions This study provides a novel insight into leaf architecture in tomato and highlights how changes in the expression domain of a master regulator gene such as SlPHAN can be translated into diverse final leaf morphologies.</description><identifier>ISSN: 0305-7364</identifier><identifier>EISSN: 1095-8290</identifier><identifier>DOI: 10.1093/aob/mcr295</identifier><identifier>PMID: 22184618</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Cauliflower mosaic virus ; Down regulation ; Epidermal cells ; gene expression ; Gene Expression Regulation, Plant ; Genes, Plant ; genetics ; growth &amp; development ; Leaf blade ; Leaf development ; Leaves ; Morphogenesis ; Morphogenesis - genetics ; Nicotiana - genetics ; Nicotiana - growth &amp; development ; Original ; Petioles ; Phenotypes ; Plant Leaves ; Plant Leaves - genetics ; Plant Leaves - growth &amp; development ; Plant morphology ; Plant Proteins ; Plant Proteins - genetics ; Plants ; Plants, Genetically Modified ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - growth &amp; development ; regulator genes ; Solanum lycopersicum ; Solanum lycopersicum - genetics ; Solanum lycopersicum - growth &amp; development ; tobacco ; tomatoes ; transcription factors ; Transcription Factors - genetics ; Transgenic plants</subject><ispartof>Annals of botany, 2012-02, Vol.109 (2), p.407-418</ispartof><rights>Annals of Botany Company 2012</rights><rights>The Author 2011. 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For Permissions, please email: journals.permissions@oup.com 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c528t-a9667ad17f3f354cf4984df42ca188046fe96a61a4a6d0183eabb260a7a7e1673</citedby><cites>FETCH-LOGICAL-c528t-a9667ad17f3f354cf4984df42ca188046fe96a61a4a6d0183eabb260a7a7e1673</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/43579404$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/43579404$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,1578,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22184618$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zoulias, Nicholas</creatorcontrib><creatorcontrib>Koenig, Daniel</creatorcontrib><creatorcontrib>Hamidi, Ashley</creatorcontrib><creatorcontrib>McCormick, Sheila</creatorcontrib><creatorcontrib>Kim, Minsung</creatorcontrib><title>A role for PHANTASTICA in medio-lateral regulation of adaxial domain development in tomato and tobacco leaves</title><title>Annals of botany</title><addtitle>Ann Bot</addtitle><description>• Background and Aims Diverse leaf forms in nature can be categorized into two groups: simple and compound. 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development</subject><subject>Plant morphology</subject><subject>Plant Proteins</subject><subject>Plant Proteins - genetics</subject><subject>Plants</subject><subject>Plants, Genetically Modified</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - growth &amp; development</subject><subject>regulator genes</subject><subject>Solanum lycopersicum</subject><subject>Solanum lycopersicum - genetics</subject><subject>Solanum lycopersicum - growth &amp; development</subject><subject>tobacco</subject><subject>tomatoes</subject><subject>transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transgenic plants</subject><issn>0305-7364</issn><issn>1095-8290</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kc1rFTEUxUNR2mftpnslm6IIY_M9yabwKGqF0go-1-FOJqlTZiavycxD_3tTpj5001UuJ7-c3MNB6JSSj5QYfg6xOR9cYkYeoFVRZKWZIS_QinAiq5orcYRe5XxPCGHK0EN0xBjVQlG9QsMap9h7HGLC367WN5v1983XyzXuRjz4totVD5NP0OPk7-Yyd3HEMWBo4VdX1DYOUNDW73wft4Mfp8eXU1GniGFsy9iAcxH3HnY-v0YvA_TZnzydx-jH50-by6vq-vZL-fW6cpLpqQKjVA0trQMPXAoXhNGiDYI5oFoToYI3ChQFAaolVHMPTcMUgRpqT1XNj9HF4rudmxLDlb1KBrtN3QDpt43Q2f9vxu6nvYs7y5nSUpBi8O7JIMWH2efJDl12vu9h9HHO1lDDmKwJK-T7Z0nKlSRMGKIK-mFBXYo5Jx_2C1FiH5u0pUm7NFngt_9G2KN_qyvA2QLEefu80ZuFu89TTHtScFkbQQT_A9IlsUQ</recordid><startdate>20120201</startdate><enddate>20120201</enddate><creator>Zoulias, Nicholas</creator><creator>Koenig, Daniel</creator><creator>Hamidi, Ashley</creator><creator>McCormick, Sheila</creator><creator>Kim, Minsung</creator><general>Oxford University Press</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>7S9</scope><scope>L.6</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20120201</creationdate><title>A role for PHANTASTICA in medio-lateral regulation of adaxial domain development in tomato and tobacco leaves</title><author>Zoulias, Nicholas ; 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development</topic><topic>Plant morphology</topic><topic>Plant Proteins</topic><topic>Plant Proteins - genetics</topic><topic>Plants</topic><topic>Plants, Genetically Modified</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Plants, Genetically Modified - growth &amp; development</topic><topic>regulator genes</topic><topic>Solanum lycopersicum</topic><topic>Solanum lycopersicum - genetics</topic><topic>Solanum lycopersicum - growth &amp; development</topic><topic>tobacco</topic><topic>tomatoes</topic><topic>transcription factors</topic><topic>Transcription Factors - genetics</topic><topic>Transgenic plants</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zoulias, Nicholas</creatorcontrib><creatorcontrib>Koenig, Daniel</creatorcontrib><creatorcontrib>Hamidi, Ashley</creatorcontrib><creatorcontrib>McCormick, Sheila</creatorcontrib><creatorcontrib>Kim, Minsung</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Annals of botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zoulias, Nicholas</au><au>Koenig, Daniel</au><au>Hamidi, Ashley</au><au>McCormick, Sheila</au><au>Kim, Minsung</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A role for PHANTASTICA in medio-lateral regulation of adaxial domain development in tomato and tobacco leaves</atitle><jtitle>Annals of botany</jtitle><addtitle>Ann Bot</addtitle><date>2012-02-01</date><risdate>2012</risdate><volume>109</volume><issue>2</issue><spage>407</spage><epage>418</epage><pages>407-418</pages><issn>0305-7364</issn><eissn>1095-8290</eissn><abstract>• Background and Aims Diverse leaf forms in nature can be categorized into two groups: simple and compound. A simple leaf has a single blade unit, whilst a compound leaf is dissected into leaflets. For both simple and compound leaves, a MYB domain transcription factor PHANTASTICA (PHAN) plays an important role in establishing the adaxial domain in the leaf. Absence of PHAN in arabidopsis and antirrhinum leaves supresses blade development, and in tomato suppresses leaflet development. However, in the rachis and petiole regions of tomato leaves where PHAN and the adaxial domain coexist, it has been unclear why leaf blade and leaflets are not formed. We hypothesized that PHAN regulates the medio-lateral extent of the adaxial domain, thereby determining compound leaf architecture. • Methods To test this hypothesis, we generated and analysed transgenic tomato plants expressing tomato PHAN (SIPHAN) under the Cauliflower mosaic virus (CaMV) 35S promoter in both sense and antisense orientations, and tobacco plants that over-express tomato SlPHAN. • Key Results Modulations in SlPHAN resulted in a variety of leaf morphologies such as simple, ternate and compound in either a peltate or non-peltate arrangement. Measurements of the extent of the adaxial domain along the wild-type tomato leaf axis showed that the adaxial domain is narrowed in the rachis and petiole in comparison with regions where laminar tissue arises. In antiSlPHAN transgenic leaves, no blade or leaflet was formed where the adaxial domain was medio-laterally narrowed, and KNOX gene expression was correlatively upregulated. CaMV35S::SlPHAN expression led to widening of the adaxial domain and ectopie blade outgrowth in the rachis of tomato and in the petiole of tobacco. Taken together, these results suggest that SlPHAN plays a role in medio-lateral extension of the adaxial domain and contributes to final leaf morphology in tomato. • Conclusions This study provides a novel insight into leaf architecture in tomato and highlights how changes in the expression domain of a master regulator gene such as SlPHAN can be translated into diverse final leaf morphologies.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>22184618</pmid><doi>10.1093/aob/mcr295</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record>
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source PubMed (Medline); MEDLINE; JSTOR; EZB Electronic Journals Library; Oxford Journals
subjects Cauliflower mosaic virus
Down regulation
Epidermal cells
gene expression
Gene Expression Regulation, Plant
Genes, Plant
genetics
growth & development
Leaf blade
Leaf development
Leaves
Morphogenesis
Morphogenesis - genetics
Nicotiana - genetics
Nicotiana - growth & development
Original
Petioles
Phenotypes
Plant Leaves
Plant Leaves - genetics
Plant Leaves - growth & development
Plant morphology
Plant Proteins
Plant Proteins - genetics
Plants
Plants, Genetically Modified
Plants, Genetically Modified - genetics
Plants, Genetically Modified - growth & development
regulator genes
Solanum lycopersicum
Solanum lycopersicum - genetics
Solanum lycopersicum - growth & development
tobacco
tomatoes
transcription factors
Transcription Factors - genetics
Transgenic plants
title A role for PHANTASTICA in medio-lateral regulation of adaxial domain development in tomato and tobacco leaves
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