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Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles
Gametophytic self-incompatibility in plants involves rejection of pollen when pistil and pollen share the same allele at the S locus. This locus is highly multiallelic, but the mechanism by which new functional S alleles are generated in nature has not been determined and remains one of the most int...
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Published in: | The Plant cell 1999-11, Vol.11 (11), p.2087-2097 |
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container_end_page | 2097 |
container_issue | 11 |
container_start_page | 2087 |
container_title | The Plant cell |
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creator | Matton, D.P Luu, D.T Xike, Q Laublin, G O'Brien, M Maes, O Morse, D Cappadocia, M |
description | Gametophytic self-incompatibility in plants involves rejection of pollen when pistil and pollen share the same allele at the S locus. This locus is highly multiallelic, but the mechanism by which new functional S alleles are generated in nature has not been determined and remains one of the most intriguing conceptual barriers to a full understanding of self-incompatibility. The S(11) and S(13) RNases of Solanum chacoense differ by only 10 amino acids, but they are phenotypically distinct (i.e., they reject either S(11) or S(13) pollen, respectively). These RNases are thus ideally suited for a dissection of the elements involved in recognition specificity. We have previously found that the modification of four amino acid residues in the S(11) RNase to match those in the S(13) RNase was sufficient to completely replace the S(11) phenotype with the S(13) phenotype. We now show that an S(11) RNase in which only three amino acid residues were modified to match those in the S(13) RNase displays the unprecedented property of dual specificity (i.e., the simultaneous rejection of both S(11) and S(13) pollen). Thus, S(12)S(14) plants expressing this hybrid S RNase rejected S(11), S(12), S(13), and S(14) pollen yet allowed S(15) pollen to pass freely. Surprisingly, only a single base pair differs between the dual-specific S allele and a monospecific S(13) allele. Dual-specific S RNases represent a previously unsuspected category of S alleles. We propose that dual-specific alleles play a critical role in establishing novel S alleles, because the plants harboring them could maintain their old recognition phenotype while acquiring a new one. |
doi_str_mv | 10.1105/tpc.11.11.2087 |
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This locus is highly multiallelic, but the mechanism by which new functional S alleles are generated in nature has not been determined and remains one of the most intriguing conceptual barriers to a full understanding of self-incompatibility. The S(11) and S(13) RNases of Solanum chacoense differ by only 10 amino acids, but they are phenotypically distinct (i.e., they reject either S(11) or S(13) pollen, respectively). These RNases are thus ideally suited for a dissection of the elements involved in recognition specificity. We have previously found that the modification of four amino acid residues in the S(11) RNase to match those in the S(13) RNase was sufficient to completely replace the S(11) phenotype with the S(13) phenotype. We now show that an S(11) RNase in which only three amino acid residues were modified to match those in the S(13) RNase displays the unprecedented property of dual specificity (i.e., the simultaneous rejection of both S(11) and S(13) pollen). Thus, S(12)S(14) plants expressing this hybrid S RNase rejected S(11), S(12), S(13), and S(14) pollen yet allowed S(15) pollen to pass freely. Surprisingly, only a single base pair differs between the dual-specific S allele and a monospecific S(13) allele. Dual-specific S RNases represent a previously unsuspected category of S alleles. We propose that dual-specific alleles play a critical role in establishing novel S alleles, because the plants harboring them could maintain their old recognition phenotype while acquiring a new one.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.11.11.2087</identifier><identifier>PMID: 10559436</identifier><language>eng</language><publisher>United States: American Society of Plant Physiologists</publisher><subject>Alleles ; Amino Acid Sequence ; amino acid sequences ; Amino acids ; Crosses, Genetic ; crossing ; Gels ; gene expression ; genes ; genotype ; growth ; inhibition ; messenger RNA ; Molecular Sequence Data ; Mutagenesis, Site-Directed ; Phenotype ; Phenotypes ; Plants ; Plants, Genetically Modified ; Pollen ; Pollen - physiology ; pollen tubes ; Pollination ; Recombinant Proteins - chemistry ; Recombinant Proteins - metabolism ; ribonucleases ; Ribonucleases - chemistry ; Ribonucleases - genetics ; Ribonucleases - metabolism ; RNA ; self incompatibility ; Solanaceae - enzymology ; Solanaceae - genetics ; Solanum chacoense ; styles ; Transgenes ; Transgenic plants</subject><ispartof>The Plant cell, 1999-11, Vol.11 (11), p.2087-2097</ispartof><rights>Copyright 1999 American Society of Plant Physiologists</rights><rights>Copyright American Society of Plant Physiologists Nov 1999</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c501t-f3f7b42408f9c5d649b441df2503bbfd57a93f9bc995f7e204c6ff3060364ccf3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/3871011$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/3871011$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,881,27903,27904,58216,58449</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/10559436$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Matton, D.P</creatorcontrib><creatorcontrib>Luu, D.T</creatorcontrib><creatorcontrib>Xike, Q</creatorcontrib><creatorcontrib>Laublin, G</creatorcontrib><creatorcontrib>O'Brien, M</creatorcontrib><creatorcontrib>Maes, O</creatorcontrib><creatorcontrib>Morse, D</creatorcontrib><creatorcontrib>Cappadocia, M</creatorcontrib><title>Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Gametophytic self-incompatibility in plants involves rejection of pollen when pistil and pollen share the same allele at the S locus. This locus is highly multiallelic, but the mechanism by which new functional S alleles are generated in nature has not been determined and remains one of the most intriguing conceptual barriers to a full understanding of self-incompatibility. The S(11) and S(13) RNases of Solanum chacoense differ by only 10 amino acids, but they are phenotypically distinct (i.e., they reject either S(11) or S(13) pollen, respectively). These RNases are thus ideally suited for a dissection of the elements involved in recognition specificity. We have previously found that the modification of four amino acid residues in the S(11) RNase to match those in the S(13) RNase was sufficient to completely replace the S(11) phenotype with the S(13) phenotype. We now show that an S(11) RNase in which only three amino acid residues were modified to match those in the S(13) RNase displays the unprecedented property of dual specificity (i.e., the simultaneous rejection of both S(11) and S(13) pollen). Thus, S(12)S(14) plants expressing this hybrid S RNase rejected S(11), S(12), S(13), and S(14) pollen yet allowed S(15) pollen to pass freely. Surprisingly, only a single base pair differs between the dual-specific S allele and a monospecific S(13) allele. Dual-specific S RNases represent a previously unsuspected category of S alleles. We propose that dual-specific alleles play a critical role in establishing novel S alleles, because the plants harboring them could maintain their old recognition phenotype while acquiring a new one.</description><subject>Alleles</subject><subject>Amino Acid Sequence</subject><subject>amino acid sequences</subject><subject>Amino acids</subject><subject>Crosses, Genetic</subject><subject>crossing</subject><subject>Gels</subject><subject>gene expression</subject><subject>genes</subject><subject>genotype</subject><subject>growth</subject><subject>inhibition</subject><subject>messenger RNA</subject><subject>Molecular Sequence Data</subject><subject>Mutagenesis, Site-Directed</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Plants</subject><subject>Plants, Genetically Modified</subject><subject>Pollen</subject><subject>Pollen - physiology</subject><subject>pollen tubes</subject><subject>Pollination</subject><subject>Recombinant Proteins - chemistry</subject><subject>Recombinant Proteins - metabolism</subject><subject>ribonucleases</subject><subject>Ribonucleases - chemistry</subject><subject>Ribonucleases - genetics</subject><subject>Ribonucleases - metabolism</subject><subject>RNA</subject><subject>self incompatibility</subject><subject>Solanaceae - enzymology</subject><subject>Solanaceae - genetics</subject><subject>Solanum chacoense</subject><subject>styles</subject><subject>Transgenes</subject><subject>Transgenic plants</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1999</creationdate><recordtype>article</recordtype><recordid>eNpVkU1rFTEYhQex2FrdutQgbqd98zWZLFxI8QuKFWvBXchkkrm5TCfTJNNy_725TC1XCORAnnPyJqeq3mA4wxj4eZ5NEftFoBXPqhPMKamJbP88LxoY1Kzh-Lh6mdIWALDA8kV1XJxcMtqcVNPPGPrFZB8mFBzSE7pGv37oZNGDzxvUL3pEabbGO2983qG0DINNOSGNpnBvR7TZzSFvbPIJuRBRkWiwk436X-RkH0qmHkc72vSqOnJ6TPb1435a3Xz5_PviW3159fX7xafL2nDAuXbUiY4RBq2ThvcNkx1juHeEA-0613OhJXWyM1JyJywBZhrnKDRAG2aMo6fVxzV3Xrpb2xs75ahHNUd_q-NOBe3V_yeT36gh3Ctc7iG8-N8_-mO4W8qD1TYscSojK4JbwaWQUKCzFTIxpBSte8rHoPbtqNJOEfu1b6cY3h5OdYCvdRTgwwpsUw7xMI5QEIq2AgPGBXu3Yk4HpYfok7q5JoApEMlFUz7pL81Boe4</recordid><startdate>19991101</startdate><enddate>19991101</enddate><creator>Matton, D.P</creator><creator>Luu, D.T</creator><creator>Xike, Q</creator><creator>Laublin, G</creator><creator>O'Brien, M</creator><creator>Maes, O</creator><creator>Morse, D</creator><creator>Cappadocia, M</creator><general>American Society of Plant Physiologists</general><general>American Society of Plant Biologists</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>4T-</scope><scope>7QO</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AF</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>AEUYN</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>M2P</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>S0X</scope><scope>5PM</scope></search><sort><creationdate>19991101</creationdate><title>Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles</title><author>Matton, D.P ; Luu, D.T ; Xike, Q ; Laublin, G ; O'Brien, M ; Maes, O ; Morse, D ; Cappadocia, M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c501t-f3f7b42408f9c5d649b441df2503bbfd57a93f9bc995f7e204c6ff3060364ccf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1999</creationdate><topic>Alleles</topic><topic>Amino Acid Sequence</topic><topic>amino acid sequences</topic><topic>Amino acids</topic><topic>Crosses, Genetic</topic><topic>crossing</topic><topic>Gels</topic><topic>gene expression</topic><topic>genes</topic><topic>genotype</topic><topic>growth</topic><topic>inhibition</topic><topic>messenger RNA</topic><topic>Molecular Sequence Data</topic><topic>Mutagenesis, Site-Directed</topic><topic>Phenotype</topic><topic>Phenotypes</topic><topic>Plants</topic><topic>Plants, Genetically Modified</topic><topic>Pollen</topic><topic>Pollen - physiology</topic><topic>pollen tubes</topic><topic>Pollination</topic><topic>Recombinant Proteins - chemistry</topic><topic>Recombinant Proteins - metabolism</topic><topic>ribonucleases</topic><topic>Ribonucleases - chemistry</topic><topic>Ribonucleases - genetics</topic><topic>Ribonucleases - metabolism</topic><topic>RNA</topic><topic>self incompatibility</topic><topic>Solanaceae - enzymology</topic><topic>Solanaceae - genetics</topic><topic>Solanum chacoense</topic><topic>styles</topic><topic>Transgenes</topic><topic>Transgenic plants</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Matton, D.P</creatorcontrib><creatorcontrib>Luu, D.T</creatorcontrib><creatorcontrib>Xike, Q</creatorcontrib><creatorcontrib>Laublin, G</creatorcontrib><creatorcontrib>O'Brien, M</creatorcontrib><creatorcontrib>Maes, O</creatorcontrib><creatorcontrib>Morse, D</creatorcontrib><creatorcontrib>Cappadocia, M</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>Docstoc</collection><collection>Biotechnology Research 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>Science Database (Alumni Edition)</collection><collection>STEM Database</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 One Sustainability</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</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>Biological Sciences</collection><collection>Agriculture Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</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>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>SIRS Editorial</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>Matton, D.P</au><au>Luu, D.T</au><au>Xike, Q</au><au>Laublin, G</au><au>O'Brien, M</au><au>Maes, O</au><au>Morse, D</au><au>Cappadocia, M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>1999-11-01</date><risdate>1999</risdate><volume>11</volume><issue>11</issue><spage>2087</spage><epage>2097</epage><pages>2087-2097</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><abstract>Gametophytic self-incompatibility in plants involves rejection of pollen when pistil and pollen share the same allele at the S locus. This locus is highly multiallelic, but the mechanism by which new functional S alleles are generated in nature has not been determined and remains one of the most intriguing conceptual barriers to a full understanding of self-incompatibility. The S(11) and S(13) RNases of Solanum chacoense differ by only 10 amino acids, but they are phenotypically distinct (i.e., they reject either S(11) or S(13) pollen, respectively). These RNases are thus ideally suited for a dissection of the elements involved in recognition specificity. We have previously found that the modification of four amino acid residues in the S(11) RNase to match those in the S(13) RNase was sufficient to completely replace the S(11) phenotype with the S(13) phenotype. We now show that an S(11) RNase in which only three amino acid residues were modified to match those in the S(13) RNase displays the unprecedented property of dual specificity (i.e., the simultaneous rejection of both S(11) and S(13) pollen). Thus, S(12)S(14) plants expressing this hybrid S RNase rejected S(11), S(12), S(13), and S(14) pollen yet allowed S(15) pollen to pass freely. Surprisingly, only a single base pair differs between the dual-specific S allele and a monospecific S(13) allele. Dual-specific S RNases represent a previously unsuspected category of S alleles. We propose that dual-specific alleles play a critical role in establishing novel S alleles, because the plants harboring them could maintain their old recognition phenotype while acquiring a new one.</abstract><cop>United States</cop><pub>American Society of Plant Physiologists</pub><pmid>10559436</pmid><doi>10.1105/tpc.11.11.2087</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Alleles Amino Acid Sequence amino acid sequences Amino acids Crosses, Genetic crossing Gels gene expression genes genotype growth inhibition messenger RNA Molecular Sequence Data Mutagenesis, Site-Directed Phenotype Phenotypes Plants Plants, Genetically Modified Pollen Pollen - physiology pollen tubes Pollination Recombinant Proteins - chemistry Recombinant Proteins - metabolism ribonucleases Ribonucleases - chemistry Ribonucleases - genetics Ribonucleases - metabolism RNA self incompatibility Solanaceae - enzymology Solanaceae - genetics Solanum chacoense styles Transgenes Transgenic plants |
title | Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles |
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