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Communication between the maternal testa and the embryo and/or endosperm affect testa attributes in tomato

Two tomato (Lycopersicon esculentum) mutants with dark testae displaying poor germination rate and percentage on both water and 100 μM $\text{gibberellin}_{4+7}$ were recovered. The mutants were allelic (black seed1-1; bks1-1 and bks1-2), inherited in Mendelian fashion as a recessive gene residing o...

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Published in:Plant physiology (Bethesda) 2003-09, Vol.133 (1), p.145-160
Main Authors: Downie, A.B, Zhang, D, Dirk, L.M.A, Thacker, R.R, Pfeiffer, J.A, Drake, J.L, Levy, A.A, Butterfield, D.A, Buxton, J.W, Snyder, J.C
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cited_by cdi_FETCH-LOGICAL-c559t-ac502f9b63858c978c7ee3e0575a4cbe15b13f6de4ede37ac1eaded6589cf2793
cites cdi_FETCH-LOGICAL-c559t-ac502f9b63858c978c7ee3e0575a4cbe15b13f6de4ede37ac1eaded6589cf2793
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container_title Plant physiology (Bethesda)
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creator Downie, A.B
Zhang, D
Dirk, L.M.A
Thacker, R.R
Pfeiffer, J.A
Drake, J.L
Levy, A.A
Butterfield, D.A
Buxton, J.W
Snyder, J.C
description Two tomato (Lycopersicon esculentum) mutants with dark testae displaying poor germination rate and percentage on both water and 100 μM $\text{gibberellin}_{4+7}$ were recovered. The mutants were allelic (black seed1-1; bks1-1 and bks1-2), inherited in Mendelian fashion as a recessive gene residing on chromosome 11. They are not allelic to bs (brown seed) -1, -2, or -4, which impair seed germination and possess dark testae. The bks/bs mutants accumulated dark pigment in the cell layers of the testa above the endothelium, which itself accumulated proanthocyanidins similar to wild type. The poor germination performance of bks mutant seeds was because of impediment of the mutant testae to radicle egress. Imbibition on $\text{gibberellin}_{4+7}$ did not ameliorate germination percentage or rate. The toughening of the bks testa and associated poor germination were partially overcome when seeds were not dried before germination or were dried under N2. The seeds of the bks mutant have elevated activity of at least one enzyme responsible for the detoxification of reactive oxygen species. The bks mutant is epistatic to 12 anthocyaninless mutants of tomato. Bio- and physicochemical analysis of the bks testa determined that it accumulated a melanic substance. Inheritance of bks/bs mutations contrasts with that of the anthocyaninless mutants, which are inherited according to the genotype of the maternally derived testa. This suggests that the testa manufactures components before its demise that can maximize testa strength, whereas the endosperm/embryo produces factors that are conveyed to the testa, mitigating this process.
doi_str_mv 10.1104/pp.103.022632
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The mutants were allelic (black seed1-1; bks1-1 and bks1-2), inherited in Mendelian fashion as a recessive gene residing on chromosome 11. They are not allelic to bs (brown seed) -1, -2, or -4, which impair seed germination and possess dark testae. The bks/bs mutants accumulated dark pigment in the cell layers of the testa above the endothelium, which itself accumulated proanthocyanidins similar to wild type. The poor germination performance of bks mutant seeds was because of impediment of the mutant testae to radicle egress. Imbibition on $\text{gibberellin}_{4+7}$ did not ameliorate germination percentage or rate. The toughening of the bks testa and associated poor germination were partially overcome when seeds were not dried before germination or were dried under N2. The seeds of the bks mutant have elevated activity of at least one enzyme responsible for the detoxification of reactive oxygen species. The bks mutant is epistatic to 12 anthocyaninless mutants of tomato. Bio- and physicochemical analysis of the bks testa determined that it accumulated a melanic substance. Inheritance of bks/bs mutations contrasts with that of the anthocyaninless mutants, which are inherited according to the genotype of the maternally derived testa. This suggests that the testa manufactures components before its demise that can maximize testa strength, whereas the endosperm/embryo produces factors that are conveyed to the testa, mitigating this process.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.103.022632</identifier><identifier>PMID: 12970482</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>alleles ; anthocyanins ; Anthocyanins - biosynthesis ; Biological and medical sciences ; catalase ; Cell Communication - genetics ; Cell Communication - physiology ; Development and Hormone Action ; embryo (plant) ; endosperm ; Enzymes ; Enzymes - genetics ; Enzymes - metabolism ; epidermis (plant) ; Fructification and ripening ; Fruits ; Fundamental and applied biological sciences. Psychology ; Gene Expression Regulation, Enzymologic ; Gene Expression Regulation, Plant ; genetic complementation ; Genetic Complementation Test ; Genetic mutation ; Genotypes ; Germination ; Germination - drug effects ; Germination - physiology ; gibberellic acid ; Gibberellins - pharmacology ; Lycopersicon esculentum - genetics ; Lycopersicon esculentum - growth &amp; development ; Lycopersicon esculentum - metabolism ; melanin ; Melanins - biosynthesis ; mutants ; Mutation ; peroxidase ; pigmentation ; Pigments ; Pigments, Biological - biosynthesis ; Pigments, Biological - chemistry ; plant anatomy ; Plant Epidermis - genetics ; Plant Epidermis - growth &amp; development ; Plant Epidermis - metabolism ; Plant physiology and development ; plant proteins ; Plants ; Proanthocyanidins - biosynthesis ; reactive oxygen species ; Reactive Oxygen Species - metabolism ; Seed germination ; Seeds ; Seeds - genetics ; Seeds - growth &amp; development ; Seeds - metabolism ; Solanum lycopersicum var. lycopersicum ; superoxide dismutase ; Testa ; tomatoes ; vegetable crops ; Vegetative and sexual reproduction, floral biology, fructification</subject><ispartof>Plant physiology (Bethesda), 2003-09, Vol.133 (1), p.145-160</ispartof><rights>Copyright 2003 American Society of Plant Biologists</rights><rights>2003 INIST-CNRS</rights><rights>Copyright © 2003, The American Society for Plant Biologists 2003</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c559t-ac502f9b63858c978c7ee3e0575a4cbe15b13f6de4ede37ac1eaded6589cf2793</citedby><cites>FETCH-LOGICAL-c559t-ac502f9b63858c978c7ee3e0575a4cbe15b13f6de4ede37ac1eaded6589cf2793</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/4281325$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/4281325$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,885,27923,27924,58237,58470</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=15125732$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12970482$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Downie, A.B</creatorcontrib><creatorcontrib>Zhang, D</creatorcontrib><creatorcontrib>Dirk, L.M.A</creatorcontrib><creatorcontrib>Thacker, R.R</creatorcontrib><creatorcontrib>Pfeiffer, J.A</creatorcontrib><creatorcontrib>Drake, J.L</creatorcontrib><creatorcontrib>Levy, A.A</creatorcontrib><creatorcontrib>Butterfield, D.A</creatorcontrib><creatorcontrib>Buxton, J.W</creatorcontrib><creatorcontrib>Snyder, J.C</creatorcontrib><title>Communication between the maternal testa and the embryo and/or endosperm affect testa attributes in tomato</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Two tomato (Lycopersicon esculentum) mutants with dark testae displaying poor germination rate and percentage on both water and 100 μM $\text{gibberellin}_{4+7}$ were recovered. The mutants were allelic (black seed1-1; bks1-1 and bks1-2), inherited in Mendelian fashion as a recessive gene residing on chromosome 11. They are not allelic to bs (brown seed) -1, -2, or -4, which impair seed germination and possess dark testae. The bks/bs mutants accumulated dark pigment in the cell layers of the testa above the endothelium, which itself accumulated proanthocyanidins similar to wild type. The poor germination performance of bks mutant seeds was because of impediment of the mutant testae to radicle egress. Imbibition on $\text{gibberellin}_{4+7}$ did not ameliorate germination percentage or rate. The toughening of the bks testa and associated poor germination were partially overcome when seeds were not dried before germination or were dried under N2. The seeds of the bks mutant have elevated activity of at least one enzyme responsible for the detoxification of reactive oxygen species. The bks mutant is epistatic to 12 anthocyaninless mutants of tomato. Bio- and physicochemical analysis of the bks testa determined that it accumulated a melanic substance. Inheritance of bks/bs mutations contrasts with that of the anthocyaninless mutants, which are inherited according to the genotype of the maternally derived testa. This suggests that the testa manufactures components before its demise that can maximize testa strength, whereas the endosperm/embryo produces factors that are conveyed to the testa, mitigating this process.</description><subject>alleles</subject><subject>anthocyanins</subject><subject>Anthocyanins - biosynthesis</subject><subject>Biological and medical sciences</subject><subject>catalase</subject><subject>Cell Communication - genetics</subject><subject>Cell Communication - physiology</subject><subject>Development and Hormone Action</subject><subject>embryo (plant)</subject><subject>endosperm</subject><subject>Enzymes</subject><subject>Enzymes - genetics</subject><subject>Enzymes - metabolism</subject><subject>epidermis (plant)</subject><subject>Fructification and ripening</subject><subject>Fruits</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Regulation, Enzymologic</subject><subject>Gene Expression Regulation, Plant</subject><subject>genetic complementation</subject><subject>Genetic Complementation Test</subject><subject>Genetic mutation</subject><subject>Genotypes</subject><subject>Germination</subject><subject>Germination - drug effects</subject><subject>Germination - physiology</subject><subject>gibberellic acid</subject><subject>Gibberellins - pharmacology</subject><subject>Lycopersicon esculentum - genetics</subject><subject>Lycopersicon esculentum - growth &amp; development</subject><subject>Lycopersicon esculentum - metabolism</subject><subject>melanin</subject><subject>Melanins - biosynthesis</subject><subject>mutants</subject><subject>Mutation</subject><subject>peroxidase</subject><subject>pigmentation</subject><subject>Pigments</subject><subject>Pigments, Biological - biosynthesis</subject><subject>Pigments, Biological - chemistry</subject><subject>plant anatomy</subject><subject>Plant Epidermis - genetics</subject><subject>Plant Epidermis - growth &amp; development</subject><subject>Plant Epidermis - metabolism</subject><subject>Plant physiology and development</subject><subject>plant proteins</subject><subject>Plants</subject><subject>Proanthocyanidins - biosynthesis</subject><subject>reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Seed germination</subject><subject>Seeds</subject><subject>Seeds - genetics</subject><subject>Seeds - growth &amp; development</subject><subject>Seeds - metabolism</subject><subject>Solanum lycopersicum var. lycopersicum</subject><subject>superoxide dismutase</subject><subject>Testa</subject><subject>tomatoes</subject><subject>vegetable crops</subject><subject>Vegetative and sexual reproduction, floral biology, fructification</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><recordid>eNpVkctv1DAQxi1ERZfCkRuCXOCWrZ-Jc-CAVjwqVeIAPVsTZ9JmldjBdkD973E3Sx8nz_j7zTe2PkLeMLpljMrzed4yKraU80rwZ2TDlOAlV1I_JxtKc021bk7Jyxj3lFImmHxBThlvaio135D9zk_T4gYLafCuaDH9RXRFusFigoTBwVgkjAkKcN3hGqc23Pq79tyHAl3n44xhKqDv0ab_cEphaJfcFEN289nLvyInPYwRXx_PM3L19cuv3ffy8se3i93ny9Iq1aQSrKK8b9pKaKVtU2tbIwqkqlYgbYtMtUz0VYcSOxQ1WIbQYVcp3die1404I59W33lpJ-wsuhRgNHMYJgi3xsNgnipuuDHX_o9hTaUaluc_HueD_73k75hpiBbHERz6JZpaVFzKA1iuoA0-xoD9_Q5GzV04Zp5zKcwaTubfPX7YA31MIwMfjgBEC2MfwNkhPnCKcVUfjN6u3D4mH-51yTUTXGX5_Sr34A1ch2xx9ZPn7CmjWklZi3_eg62m</recordid><startdate>20030901</startdate><enddate>20030901</enddate><creator>Downie, A.B</creator><creator>Zhang, D</creator><creator>Dirk, L.M.A</creator><creator>Thacker, R.R</creator><creator>Pfeiffer, J.A</creator><creator>Drake, J.L</creator><creator>Levy, A.A</creator><creator>Butterfield, D.A</creator><creator>Buxton, J.W</creator><creator>Snyder, J.C</creator><general>American Society of Plant Biologists</general><general>American Society of Plant Physiologists</general><general>The American Society for Plant Biologists</general><scope>FBQ</scope><scope>IQODW</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20030901</creationdate><title>Communication between the maternal testa and the embryo and/or endosperm affect testa attributes in tomato</title><author>Downie, A.B ; Zhang, D ; Dirk, L.M.A ; Thacker, R.R ; Pfeiffer, J.A ; Drake, J.L ; Levy, A.A ; Butterfield, D.A ; Buxton, J.W ; Snyder, J.C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c559t-ac502f9b63858c978c7ee3e0575a4cbe15b13f6de4ede37ac1eaded6589cf2793</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>alleles</topic><topic>anthocyanins</topic><topic>Anthocyanins - biosynthesis</topic><topic>Biological and medical sciences</topic><topic>catalase</topic><topic>Cell Communication - genetics</topic><topic>Cell Communication - physiology</topic><topic>Development and Hormone Action</topic><topic>embryo (plant)</topic><topic>endosperm</topic><topic>Enzymes</topic><topic>Enzymes - genetics</topic><topic>Enzymes - metabolism</topic><topic>epidermis (plant)</topic><topic>Fructification and ripening</topic><topic>Fruits</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Regulation, Enzymologic</topic><topic>Gene Expression Regulation, Plant</topic><topic>genetic complementation</topic><topic>Genetic Complementation Test</topic><topic>Genetic mutation</topic><topic>Genotypes</topic><topic>Germination</topic><topic>Germination - drug effects</topic><topic>Germination - physiology</topic><topic>gibberellic acid</topic><topic>Gibberellins - pharmacology</topic><topic>Lycopersicon esculentum - genetics</topic><topic>Lycopersicon esculentum - growth &amp; development</topic><topic>Lycopersicon esculentum - metabolism</topic><topic>melanin</topic><topic>Melanins - biosynthesis</topic><topic>mutants</topic><topic>Mutation</topic><topic>peroxidase</topic><topic>pigmentation</topic><topic>Pigments</topic><topic>Pigments, Biological - biosynthesis</topic><topic>Pigments, Biological - chemistry</topic><topic>plant anatomy</topic><topic>Plant Epidermis - genetics</topic><topic>Plant Epidermis - growth &amp; development</topic><topic>Plant Epidermis - metabolism</topic><topic>Plant physiology and development</topic><topic>plant proteins</topic><topic>Plants</topic><topic>Proanthocyanidins - biosynthesis</topic><topic>reactive oxygen species</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Seed germination</topic><topic>Seeds</topic><topic>Seeds - genetics</topic><topic>Seeds - growth &amp; development</topic><topic>Seeds - metabolism</topic><topic>Solanum lycopersicum var. lycopersicum</topic><topic>superoxide dismutase</topic><topic>Testa</topic><topic>tomatoes</topic><topic>vegetable crops</topic><topic>Vegetative and sexual reproduction, floral biology, fructification</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Downie, A.B</creatorcontrib><creatorcontrib>Zhang, D</creatorcontrib><creatorcontrib>Dirk, L.M.A</creatorcontrib><creatorcontrib>Thacker, R.R</creatorcontrib><creatorcontrib>Pfeiffer, J.A</creatorcontrib><creatorcontrib>Drake, J.L</creatorcontrib><creatorcontrib>Levy, A.A</creatorcontrib><creatorcontrib>Butterfield, D.A</creatorcontrib><creatorcontrib>Buxton, J.W</creatorcontrib><creatorcontrib>Snyder, J.C</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><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><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Downie, A.B</au><au>Zhang, D</au><au>Dirk, L.M.A</au><au>Thacker, R.R</au><au>Pfeiffer, J.A</au><au>Drake, J.L</au><au>Levy, A.A</au><au>Butterfield, D.A</au><au>Buxton, J.W</au><au>Snyder, J.C</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Communication between the maternal testa and the embryo and/or endosperm affect testa attributes in tomato</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2003-09-01</date><risdate>2003</risdate><volume>133</volume><issue>1</issue><spage>145</spage><epage>160</epage><pages>145-160</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Two tomato (Lycopersicon esculentum) mutants with dark testae displaying poor germination rate and percentage on both water and 100 μM $\text{gibberellin}_{4+7}$ were recovered. The mutants were allelic (black seed1-1; bks1-1 and bks1-2), inherited in Mendelian fashion as a recessive gene residing on chromosome 11. They are not allelic to bs (brown seed) -1, -2, or -4, which impair seed germination and possess dark testae. The bks/bs mutants accumulated dark pigment in the cell layers of the testa above the endothelium, which itself accumulated proanthocyanidins similar to wild type. The poor germination performance of bks mutant seeds was because of impediment of the mutant testae to radicle egress. Imbibition on $\text{gibberellin}_{4+7}$ did not ameliorate germination percentage or rate. The toughening of the bks testa and associated poor germination were partially overcome when seeds were not dried before germination or were dried under N2. The seeds of the bks mutant have elevated activity of at least one enzyme responsible for the detoxification of reactive oxygen species. The bks mutant is epistatic to 12 anthocyaninless mutants of tomato. Bio- and physicochemical analysis of the bks testa determined that it accumulated a melanic substance. Inheritance of bks/bs mutations contrasts with that of the anthocyaninless mutants, which are inherited according to the genotype of the maternally derived testa. This suggests that the testa manufactures components before its demise that can maximize testa strength, whereas the endosperm/embryo produces factors that are conveyed to the testa, mitigating this process.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>12970482</pmid><doi>10.1104/pp.103.022632</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record>
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source JSTOR Archival Journals and Primary Sources Collection; Oxford Journals Online
subjects alleles
anthocyanins
Anthocyanins - biosynthesis
Biological and medical sciences
catalase
Cell Communication - genetics
Cell Communication - physiology
Development and Hormone Action
embryo (plant)
endosperm
Enzymes
Enzymes - genetics
Enzymes - metabolism
epidermis (plant)
Fructification and ripening
Fruits
Fundamental and applied biological sciences. Psychology
Gene Expression Regulation, Enzymologic
Gene Expression Regulation, Plant
genetic complementation
Genetic Complementation Test
Genetic mutation
Genotypes
Germination
Germination - drug effects
Germination - physiology
gibberellic acid
Gibberellins - pharmacology
Lycopersicon esculentum - genetics
Lycopersicon esculentum - growth & development
Lycopersicon esculentum - metabolism
melanin
Melanins - biosynthesis
mutants
Mutation
peroxidase
pigmentation
Pigments
Pigments, Biological - biosynthesis
Pigments, Biological - chemistry
plant anatomy
Plant Epidermis - genetics
Plant Epidermis - growth & development
Plant Epidermis - metabolism
Plant physiology and development
plant proteins
Plants
Proanthocyanidins - biosynthesis
reactive oxygen species
Reactive Oxygen Species - metabolism
Seed germination
Seeds
Seeds - genetics
Seeds - growth & development
Seeds - metabolism
Solanum lycopersicum var. lycopersicum
superoxide dismutase
Testa
tomatoes
vegetable crops
Vegetative and sexual reproduction, floral biology, fructification
title Communication between the maternal testa and the embryo and/or endosperm affect testa attributes in tomato
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