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Aberrant Stamen Development is Associated with Parthenocarpic Fruit Set Through Up-Regulation of Gibberellin Biosynthesis in Tomato
Abstract Parthenocarpy, a process in which fruit set occurs without fertilization, leads to the production of seedless fruit. A number of floral homeotic mutants with abnormal stamen development exhibit parthenocarpic fruit set. Flower development is thought to repress ovary growth before anthesis....
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Published in: | Plant and cell physiology 2019-01, Vol.60 (1), p.38-51 |
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creator | Okabe, Yoshihiro Yamaoka, Tatsuya Ariizumi, Tohru Ushijima, Koichiro Kojima, Mikiko Takebayashi, Yumiko Sakakibara, Hitoshi Kusano, Miyako Shinozaki, Yoshihito Pulungan, Sri Imriani Kubo, Yasutaka Nakano, Ryohei Ezura, Hiroshi |
description | Abstract
Parthenocarpy, a process in which fruit set occurs without fertilization, leads to the production of seedless fruit. A number of floral homeotic mutants with abnormal stamen development exhibit parthenocarpic fruit set. Flower development is thought to repress ovary growth before anthesis. However, the mechanism of parthenocarpic fruit development caused by aberrant flower formation is poorly understood. To investigate the molecular mechanism of parthenocarpic fruit development in floral homeotic mutants, we performed functional analysis of Tomato APETALA3 (TAP3) by loss-of-function approaches. Organ-specific promoter was used to induce organ-specific loss of function in stamen and ovary/fruit. We observed increased cell expansion in tap3 mutants and TAP3-RNAi lines during parthenocarpic fruit growth. These were predominantly accompanied by the up-regulation of GA biosynthesis genes, including SlGA20ox1, SlGA20ox2, and SlGA20ox3, as well as reduced expression of the GA-inactivating gene SlGA2ox1 and the auxin signaling gene SlARF7 involved in a crosstalk between GA and auxin. These transcriptional profiles are in agreement with the GA levels in these lines. These results suggest that stamen development negatively regulates fruit set by repressing the GA biosynthesis. |
doi_str_mv | 10.1093/pcp/pcy184 |
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Parthenocarpy, a process in which fruit set occurs without fertilization, leads to the production of seedless fruit. A number of floral homeotic mutants with abnormal stamen development exhibit parthenocarpic fruit set. Flower development is thought to repress ovary growth before anthesis. However, the mechanism of parthenocarpic fruit development caused by aberrant flower formation is poorly understood. To investigate the molecular mechanism of parthenocarpic fruit development in floral homeotic mutants, we performed functional analysis of Tomato APETALA3 (TAP3) by loss-of-function approaches. Organ-specific promoter was used to induce organ-specific loss of function in stamen and ovary/fruit. We observed increased cell expansion in tap3 mutants and TAP3-RNAi lines during parthenocarpic fruit growth. These were predominantly accompanied by the up-regulation of GA biosynthesis genes, including SlGA20ox1, SlGA20ox2, and SlGA20ox3, as well as reduced expression of the GA-inactivating gene SlGA2ox1 and the auxin signaling gene SlARF7 involved in a crosstalk between GA and auxin. These transcriptional profiles are in agreement with the GA levels in these lines. These results suggest that stamen development negatively regulates fruit set by repressing the GA biosynthesis.</description><identifier>ISSN: 0032-0781</identifier><identifier>EISSN: 1471-9053</identifier><identifier>DOI: 10.1093/pcp/pcy184</identifier><identifier>PMID: 30192961</identifier><language>eng</language><publisher>Japan: Oxford University Press</publisher><subject>Base Sequence ; Biosynthetic Pathways - genetics ; Flowers - genetics ; Flowers - growth & development ; Fruit - genetics ; Fruit - growth & development ; Gene Expression Regulation, Plant ; Gibberellins - biosynthesis ; Lycopersicon esculentum - genetics ; Lycopersicon esculentum - growth & development ; Mutagenesis - genetics ; Mutation - genetics ; Organ Specificity - genetics ; Parthenogenesis - genetics ; Phenotype ; Plant Growth Regulators - metabolism ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants, Genetically Modified ; Promoter Regions, Genetic - genetics ; RNA Interference ; Signal Transduction ; Transcription, Genetic ; Up-Regulation - genetics</subject><ispartof>Plant and cell physiology, 2019-01, Vol.60 (1), p.38-51</ispartof><rights>The Author(s) 2018. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c353t-f768a9e90c0ef8dca0579258e77e629e8c6d6ca67c7442fb6289155d2af0a6ba3</citedby><cites>FETCH-LOGICAL-c353t-f768a9e90c0ef8dca0579258e77e629e8c6d6ca67c7442fb6289155d2af0a6ba3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30192961$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Okabe, Yoshihiro</creatorcontrib><creatorcontrib>Yamaoka, Tatsuya</creatorcontrib><creatorcontrib>Ariizumi, Tohru</creatorcontrib><creatorcontrib>Ushijima, Koichiro</creatorcontrib><creatorcontrib>Kojima, Mikiko</creatorcontrib><creatorcontrib>Takebayashi, Yumiko</creatorcontrib><creatorcontrib>Sakakibara, Hitoshi</creatorcontrib><creatorcontrib>Kusano, Miyako</creatorcontrib><creatorcontrib>Shinozaki, Yoshihito</creatorcontrib><creatorcontrib>Pulungan, Sri Imriani</creatorcontrib><creatorcontrib>Kubo, Yasutaka</creatorcontrib><creatorcontrib>Nakano, Ryohei</creatorcontrib><creatorcontrib>Ezura, Hiroshi</creatorcontrib><title>Aberrant Stamen Development is Associated with Parthenocarpic Fruit Set Through Up-Regulation of Gibberellin Biosynthesis in Tomato</title><title>Plant and cell physiology</title><addtitle>Plant Cell Physiol</addtitle><description>Abstract
Parthenocarpy, a process in which fruit set occurs without fertilization, leads to the production of seedless fruit. A number of floral homeotic mutants with abnormal stamen development exhibit parthenocarpic fruit set. Flower development is thought to repress ovary growth before anthesis. However, the mechanism of parthenocarpic fruit development caused by aberrant flower formation is poorly understood. To investigate the molecular mechanism of parthenocarpic fruit development in floral homeotic mutants, we performed functional analysis of Tomato APETALA3 (TAP3) by loss-of-function approaches. Organ-specific promoter was used to induce organ-specific loss of function in stamen and ovary/fruit. We observed increased cell expansion in tap3 mutants and TAP3-RNAi lines during parthenocarpic fruit growth. These were predominantly accompanied by the up-regulation of GA biosynthesis genes, including SlGA20ox1, SlGA20ox2, and SlGA20ox3, as well as reduced expression of the GA-inactivating gene SlGA2ox1 and the auxin signaling gene SlARF7 involved in a crosstalk between GA and auxin. These transcriptional profiles are in agreement with the GA levels in these lines. These results suggest that stamen development negatively regulates fruit set by repressing the GA biosynthesis.</description><subject>Base Sequence</subject><subject>Biosynthetic Pathways - genetics</subject><subject>Flowers - genetics</subject><subject>Flowers - growth & development</subject><subject>Fruit - genetics</subject><subject>Fruit - growth & development</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gibberellins - biosynthesis</subject><subject>Lycopersicon esculentum - genetics</subject><subject>Lycopersicon esculentum - growth & development</subject><subject>Mutagenesis - genetics</subject><subject>Mutation - genetics</subject><subject>Organ Specificity - genetics</subject><subject>Parthenogenesis - genetics</subject><subject>Phenotype</subject><subject>Plant Growth Regulators - metabolism</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>RNA Interference</subject><subject>Signal Transduction</subject><subject>Transcription, Genetic</subject><subject>Up-Regulation - genetics</subject><issn>0032-0781</issn><issn>1471-9053</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNp9kM1q3DAURkVpaSY_mz5A0aZQAm6uZFuylpM0SQMDCcnM2sjydUbFtlxJTph1Xjwqk3aZhdAnODr38hHyhcEPBio_m8yUzo5VxQeyYIVkmYIy_0gWADnPQFbsgByG8Bsg5Rw-k4McmOJKsAV5WTbovR4jfYh6wJH-xCfs3ZRipDbQZQjOWB2xpc82bumd9nGLozPaT9bQKz_b9BUjXW-9mx-3dDNl9_g49zpaN1LX0WvbpBHY93ak59aF3ZgEIanTe-0GHd0x-dTpPuDJ231ENleX64tf2er2-uZiucpMXuYx66SotEIFBrCrWqOhlIqXFUqJgiusjGiF0UIaWRS8awSvFCvLlusOtGh0fkS-772Td39mDLEebDBpMz2im0PNGTAuZAVFQk_3qPEuBI9dPXk7aL-rGdR_S69T6fW-9AR_ffPOzYDtf_Rfywn4tgfcPL0negWaA40v</recordid><startdate>20190101</startdate><enddate>20190101</enddate><creator>Okabe, Yoshihiro</creator><creator>Yamaoka, Tatsuya</creator><creator>Ariizumi, Tohru</creator><creator>Ushijima, Koichiro</creator><creator>Kojima, Mikiko</creator><creator>Takebayashi, Yumiko</creator><creator>Sakakibara, Hitoshi</creator><creator>Kusano, Miyako</creator><creator>Shinozaki, Yoshihito</creator><creator>Pulungan, Sri Imriani</creator><creator>Kubo, Yasutaka</creator><creator>Nakano, Ryohei</creator><creator>Ezura, Hiroshi</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>7X8</scope></search><sort><creationdate>20190101</creationdate><title>Aberrant Stamen Development is Associated with Parthenocarpic Fruit Set Through Up-Regulation of Gibberellin Biosynthesis in Tomato</title><author>Okabe, Yoshihiro ; Yamaoka, Tatsuya ; Ariizumi, Tohru ; Ushijima, Koichiro ; Kojima, Mikiko ; Takebayashi, Yumiko ; Sakakibara, Hitoshi ; Kusano, Miyako ; Shinozaki, Yoshihito ; Pulungan, Sri Imriani ; Kubo, Yasutaka ; Nakano, Ryohei ; Ezura, Hiroshi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c353t-f768a9e90c0ef8dca0579258e77e629e8c6d6ca67c7442fb6289155d2af0a6ba3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Base Sequence</topic><topic>Biosynthetic Pathways - genetics</topic><topic>Flowers - genetics</topic><topic>Flowers - growth & development</topic><topic>Fruit - genetics</topic><topic>Fruit - growth & development</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gibberellins - biosynthesis</topic><topic>Lycopersicon esculentum - genetics</topic><topic>Lycopersicon esculentum - growth & development</topic><topic>Mutagenesis - genetics</topic><topic>Mutation - genetics</topic><topic>Organ Specificity - genetics</topic><topic>Parthenogenesis - genetics</topic><topic>Phenotype</topic><topic>Plant Growth Regulators - metabolism</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants, Genetically Modified</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>RNA Interference</topic><topic>Signal Transduction</topic><topic>Transcription, Genetic</topic><topic>Up-Regulation - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Okabe, Yoshihiro</creatorcontrib><creatorcontrib>Yamaoka, Tatsuya</creatorcontrib><creatorcontrib>Ariizumi, Tohru</creatorcontrib><creatorcontrib>Ushijima, Koichiro</creatorcontrib><creatorcontrib>Kojima, Mikiko</creatorcontrib><creatorcontrib>Takebayashi, Yumiko</creatorcontrib><creatorcontrib>Sakakibara, Hitoshi</creatorcontrib><creatorcontrib>Kusano, Miyako</creatorcontrib><creatorcontrib>Shinozaki, Yoshihito</creatorcontrib><creatorcontrib>Pulungan, Sri Imriani</creatorcontrib><creatorcontrib>Kubo, Yasutaka</creatorcontrib><creatorcontrib>Nakano, Ryohei</creatorcontrib><creatorcontrib>Ezura, Hiroshi</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Plant and cell physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Okabe, Yoshihiro</au><au>Yamaoka, Tatsuya</au><au>Ariizumi, Tohru</au><au>Ushijima, Koichiro</au><au>Kojima, Mikiko</au><au>Takebayashi, Yumiko</au><au>Sakakibara, Hitoshi</au><au>Kusano, Miyako</au><au>Shinozaki, Yoshihito</au><au>Pulungan, Sri Imriani</au><au>Kubo, Yasutaka</au><au>Nakano, Ryohei</au><au>Ezura, Hiroshi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Aberrant Stamen Development is Associated with Parthenocarpic Fruit Set Through Up-Regulation of Gibberellin Biosynthesis in Tomato</atitle><jtitle>Plant and cell physiology</jtitle><addtitle>Plant Cell Physiol</addtitle><date>2019-01-01</date><risdate>2019</risdate><volume>60</volume><issue>1</issue><spage>38</spage><epage>51</epage><pages>38-51</pages><issn>0032-0781</issn><eissn>1471-9053</eissn><abstract>Abstract
Parthenocarpy, a process in which fruit set occurs without fertilization, leads to the production of seedless fruit. A number of floral homeotic mutants with abnormal stamen development exhibit parthenocarpic fruit set. Flower development is thought to repress ovary growth before anthesis. However, the mechanism of parthenocarpic fruit development caused by aberrant flower formation is poorly understood. To investigate the molecular mechanism of parthenocarpic fruit development in floral homeotic mutants, we performed functional analysis of Tomato APETALA3 (TAP3) by loss-of-function approaches. Organ-specific promoter was used to induce organ-specific loss of function in stamen and ovary/fruit. We observed increased cell expansion in tap3 mutants and TAP3-RNAi lines during parthenocarpic fruit growth. These were predominantly accompanied by the up-regulation of GA biosynthesis genes, including SlGA20ox1, SlGA20ox2, and SlGA20ox3, as well as reduced expression of the GA-inactivating gene SlGA2ox1 and the auxin signaling gene SlARF7 involved in a crosstalk between GA and auxin. These transcriptional profiles are in agreement with the GA levels in these lines. These results suggest that stamen development negatively regulates fruit set by repressing the GA biosynthesis.</abstract><cop>Japan</cop><pub>Oxford University Press</pub><pmid>30192961</pmid><doi>10.1093/pcp/pcy184</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Base Sequence Biosynthetic Pathways - genetics Flowers - genetics Flowers - growth & development Fruit - genetics Fruit - growth & development Gene Expression Regulation, Plant Gibberellins - biosynthesis Lycopersicon esculentum - genetics Lycopersicon esculentum - growth & development Mutagenesis - genetics Mutation - genetics Organ Specificity - genetics Parthenogenesis - genetics Phenotype Plant Growth Regulators - metabolism Plant Proteins - genetics Plant Proteins - metabolism Plants, Genetically Modified Promoter Regions, Genetic - genetics RNA Interference Signal Transduction Transcription, Genetic Up-Regulation - genetics |
title | Aberrant Stamen Development is Associated with Parthenocarpic Fruit Set Through Up-Regulation of Gibberellin Biosynthesis in Tomato |
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