Single amino acid change alters the ability to specify male or female organ identity
The molecular mechanisms underlying the developmental processes that shape living organisms provide a basis to understand the evolution of biological complexity. Gene duplication allows biological functions to become separated, leading to increased complexity through subfunctionalization. Recently,...
Saved in:
Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 107; no. 44; pp. 18898 - 18902 |
---|---|
Main Authors | , , , |
Format | Journal Article |
Language | English |
Published |
United States
National Academy of Sciences
02.11.2010
National Acad Sciences |
Subjects | |
Online Access | Get full text |
ISSN | 0027-8424 1091-6490 1091-6490 |
DOI | 10.1073/pnas.1009050107 |
Cover
Abstract | The molecular mechanisms underlying the developmental processes that shape living organisms provide a basis to understand the evolution of biological complexity. Gene duplication allows biological functions to become separated, leading to increased complexity through subfunctionalization. Recently, the relative contributions to morphological evolution of changes to the regulatory and/or coding regions of duplicated genes have been the subject of debate. Duplication generated multiple copies of the MADS-box transcription factor genes that play essential roles in specifying organ identity in the flower, making this evolutionary novelty a good model to investigate the nature of the changes necessary to drive subfunctionalization. Here, we show that naturally occurring variation at a single amino acid in a MADS-box transcription factor switches its ability to specify male and female reproductive organs by altering its repertoire of protein–protein interactions. However, these different developmental fates are only manifest because of an underlying variation in the expression pattern of interacting proteins. This shows that the morphological outcomes of changes to protein sequence and gene expression must be interpreted in the context of the wider regulatory network. It also suggests an explanation for the surprisingly widespread duplications of some of the floral transcription factors. |
---|---|
AbstractList | The molecular mechanisms underlying the developmental processes that shape living organisms provide a basis to understand the evolution of biological complexity. Gene duplication allows biological functions to become separated, leading to increased complexity through subfunctionalization. Recently, the relative contributions to morphological evolution of changes to the regulatory and/or coding regions of duplicated genes have been the subject of debate. Duplication generated multiple copies of the MADS-box transcription factor genes that play essential roles in specifying organ identity in the flower, making this evolutionary novelty a good model to investigate the nature of the changes necessary to drive subfunctionalization. Here, we show that naturally occurring variation at a single amino acid in a MADS-box transcription factor switches its ability to specify male and female reproductive organs by altering its repertoire of protein-protein interactions. However, these different developmental fates are only manifest because of an underlying variation in the expression pattern of interacting proteins. This shows that the morphological outcomes of changes to protein sequence and gene expression must be interpreted in the context of the wider regulatory network. It also suggests an explanation for the surprisingly widespread duplications of some of the floral transcription factors.The molecular mechanisms underlying the developmental processes that shape living organisms provide a basis to understand the evolution of biological complexity. Gene duplication allows biological functions to become separated, leading to increased complexity through subfunctionalization. Recently, the relative contributions to morphological evolution of changes to the regulatory and/or coding regions of duplicated genes have been the subject of debate. Duplication generated multiple copies of the MADS-box transcription factor genes that play essential roles in specifying organ identity in the flower, making this evolutionary novelty a good model to investigate the nature of the changes necessary to drive subfunctionalization. Here, we show that naturally occurring variation at a single amino acid in a MADS-box transcription factor switches its ability to specify male and female reproductive organs by altering its repertoire of protein-protein interactions. However, these different developmental fates are only manifest because of an underlying variation in the expression pattern of interacting proteins. This shows that the morphological outcomes of changes to protein sequence and gene expression must be interpreted in the context of the wider regulatory network. It also suggests an explanation for the surprisingly widespread duplications of some of the floral transcription factors. The molecular mechanisms underlying the developmental processes that shape living organisms provide a basis to understand the evolution of biological complexity. Gene duplication allows biological functions to become separated, leading to increased complexity through subfunctionalization. Recently, the relative contributions to morphological evolution of changes to the regulatory and/or coding regions of duplicated genes have been the subject of debate. Duplication generated multiple copies of the MADS-box transcription factor genes that play essential roles in specifying organ identity in the flower, making this evolutionary novelty a good model to investigate the nature of the changes necessary to drive subfunctionalization. Here, we show that naturally occurring variation at a single amino acid in a MADS-box transcription factor switches its ability to specify male and female reproductive organs by altering its repertoire of protein-protein interactions. However, these different developmental fates are only manifest because of an underlying variation in the expression pattern of interacting proteins. This shows that the morphological outcomes of changes to protein sequence and gene expression must be interpreted in the context of the wider regulatory network. It also suggests an explanation for the surprisingly widespread duplications of some of the floral transcription factors. The molecular mechanisms underlying the developmental processes that shape living organisms provide a basis to understand the evolution of biological complexity. Gene duplication allows biological functions to become separated, leading to increased complexity through subfunctionalization. Recently, the relative contributions to morphological evolution of changes to the regulatory and/or coding regions of duplicated genes have been the subject of debate. Duplication generated multiple copies of the MADS-box transcription factor genes that play essential roles in specifying organ identity in the flower, making this evolutionary novelty a good model to investigate the nature of the changes necessary to drive subfunctionalization. Here, we show that naturally occurring variation at a single amino acid in a MADS-box transcription factor switches its ability to specify male and female reproductive organs by altering its repertoire of protein - protein interactions. However, these different developmental fates are only manifest because of an underlying variation in the expression pattern of interacting proteins. This shows that the morphological outcomes of changes to protein sequence and gene expression must be interpreted in the context of the wider regulatory network. It also suggests an explanation for the surprisingly widespread duplications of some of the floral transcription factors. [PUBLICATION ABSTRACT] |
Author | Coen, Enrico Sandro Airoldi, Chiara A. Bergonzi, Sara Davies, Brendan |
Author_xml | – sequence: 1 givenname: Chiara A. surname: Airoldi fullname: Airoldi, Chiara A. – sequence: 2 givenname: Sara surname: Bergonzi fullname: Bergonzi, Sara – sequence: 3 givenname: Brendan surname: Davies fullname: Davies, Brendan – sequence: 4 givenname: Enrico Sandro surname: Coen fullname: Coen, Enrico Sandro |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20956314$$D View this record in MEDLINE/PubMed |
BookMark | eNp9ksFvFCEUxompsdvq2ZOG9FIvY4FhBriYNI1VkyY9WM-EYZhdNjOwAmuy_71vsltXm9gD4YX3ex_fg3eGTkIMDqG3lHykRNRXm2AyRESRhsDBC7SgRNGq5YqcoAUhTFSSM36KznJeE-AaSV6hUwZBW1O-QA_ffViODpvJh4iN9T22KxOWcDIWlzIuKwg7P_qywyXivHHWDzs8GSiKCQ_uEC1NwL53oQD4Gr0czJjdm8N-jn7cfn64-Vrd3X_5dnN9V1muVKmstU5wNojeODIv3jhjZNP1VEFzvKbMtEow1w1sYP0A2W4wnTLS8obTuj5Hn_a6m203ud7C7cmMepP8ZNJOR-P1v5ngV3oZf2mmRC0lAYHLg0CKP7cuFz35bN04muDiNmvRMi4IIzP54VmSSgaWWkI4oBdP0HXcpgAPMesJymWrAHr_t_U_nh9_BoBmD9gUc05u0NYXU3ycO_GjpkTPE6DnCdDHCYC6qyd1j9L_r8AHK3PiSAvNOfQllQTk3R5Z5xLT0WwjuGxUXf8G55DIEA |
CitedBy_id | crossref_primary_10_1038_s41438_020_00459_x crossref_primary_10_1093_jxb_erx479 crossref_primary_10_1371_journal_pone_0030524 crossref_primary_10_3389_fpls_2015_00734 crossref_primary_10_5713_ab_22_0051 crossref_primary_10_1093_icb_icx067 crossref_primary_10_1186_s13227_015_0002_x crossref_primary_10_1371_journal_pone_0103770 crossref_primary_10_1111_nph_12078 crossref_primary_10_1093_jxb_ert479 crossref_primary_10_1016_j_jgg_2012_02_008 crossref_primary_10_1186_s12870_015_0569_3 crossref_primary_10_1111_nph_12555 crossref_primary_10_3389_fpls_2015_01193 crossref_primary_10_1038_s41477_023_01351_x crossref_primary_10_1242_dev_067215 crossref_primary_10_1104_pp_113_217570 crossref_primary_10_1002_dvdy_24268 crossref_primary_10_1186_s12870_018_1574_0 crossref_primary_10_1016_j_ydbio_2021_12_018 crossref_primary_10_1093_molbev_msw031 crossref_primary_10_1186_1471_2164_15_1125 crossref_primary_10_1080_11263504_2013_877531 crossref_primary_10_1242_dev_074674 crossref_primary_10_1093_jxb_ers233 crossref_primary_10_1093_plphys_kiac571 crossref_primary_10_1016_j_tplants_2012_06_001 crossref_primary_10_1111_ede_12125 crossref_primary_10_1007_s00344_022_10815_x crossref_primary_10_1093_treephys_tpz091 crossref_primary_10_1093_nar_gkx267 crossref_primary_10_1111_j_1365_313X_2012_05046_x crossref_primary_10_1111_rssc_12003 crossref_primary_10_1073_pnas_1203686109 crossref_primary_10_1016_j_plantsci_2018_08_021 crossref_primary_10_3389_fpls_2020_00637 crossref_primary_10_1016_j_plaphy_2025_109512 crossref_primary_10_1098_rstb_2011_0252 |
Cites_doi | 10.1016/S0076-6879(02)50957-5 10.1093/emboj/18.14.4023 10.1038/35012103 10.1007/978-3-642-86659-3 10.1007/s11103-004-0416-7 10.1007/s00497-002-0151-7 10.1002/bies.10292 10.1038/353031a0 10.1105/tpc.105.031831 10.1038/35008089 10.1105/tpc.105.039107 10.1111/j.1558-5646.2007.00105.x 10.1016/j.cub.2005.07.063 10.1534/genetics.104.037770 10.1046/j.0960-7412.2003.01473.x 10.1046/j.1365-313x.1998.00343.x 10.1093/nar/gkp129 10.1371/journal.pbio.1000090 10.1038/35054083 10.1016/j.cell.2008.06.030 10.1016/j.cub.2004.10.028 10.1093/nar/gkn900 10.1101/gad.5.3.484 10.1002/j.1460-2075.1996.tb00807.x 10.1016/S1369-5266(00)00139-4 10.1016/j.tplants.2007.06.012 10.1105/tpc.015123 10.1046/j.1365-313X.2003.01896.x 10.1093/nar/17.16.6747 10.1038/nrg2063 10.1186/gb-2009-10-2-r24 |
ContentType | Journal Article |
Copyright | Copyright National Academy of Sciences Nov 2, 2010 |
Copyright_xml | – notice: Copyright National Academy of Sciences Nov 2, 2010 |
DBID | AAYXX CITATION CGR CUY CVF ECM EIF NPM 7QG 7QL 7QP 7QR 7SN 7SS 7T5 7TK 7TM 7TO 7U9 8FD C1K FR3 H94 M7N P64 RC3 7S9 L.6 7X8 5PM |
DOI | 10.1073/pnas.1009050107 |
DatabaseName | CrossRef Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed Animal Behavior Abstracts Bacteriology Abstracts (Microbiology B) Calcium & Calcified Tissue Abstracts Chemoreception Abstracts Ecology Abstracts Entomology Abstracts (Full archive) Immunology Abstracts Neurosciences Abstracts Nucleic Acids Abstracts Oncogenes and Growth Factors Abstracts Virology and AIDS Abstracts Technology Research Database Environmental Sciences and Pollution Management Engineering Research Database AIDS and Cancer Research Abstracts Algology Mycology and Protozoology Abstracts (Microbiology C) Biotechnology and BioEngineering Abstracts Genetics Abstracts AGRICOLA AGRICOLA - Academic MEDLINE - Academic PubMed Central (Full Participant titles) |
DatabaseTitle | CrossRef MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) Virology and AIDS Abstracts Oncogenes and Growth Factors Abstracts Technology Research Database Nucleic Acids Abstracts Ecology Abstracts Neurosciences Abstracts Biotechnology and BioEngineering Abstracts Environmental Sciences and Pollution Management Entomology Abstracts Genetics Abstracts Animal Behavior Abstracts Bacteriology Abstracts (Microbiology B) Algology Mycology and Protozoology Abstracts (Microbiology C) AIDS and Cancer Research Abstracts Chemoreception Abstracts Immunology Abstracts Engineering Research Database Calcium & Calcified Tissue Abstracts AGRICOLA AGRICOLA - Academic MEDLINE - Academic |
DatabaseTitleList | MEDLINE - Academic MEDLINE Virology and AIDS Abstracts CrossRef AGRICOLA |
Database_xml | – sequence: 1 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Sciences (General) |
EISSN | 1091-6490 |
EndPage | 18902 |
ExternalDocumentID | PMC2973880 2183043161 20956314 10_1073_pnas_1009050107 107_44_18898 25748593 |
Genre | Research Support, Non-U.S. Gov't Journal Article Feature |
GrantInformation_xml | – fundername: Biotechnology and Biological Sciences Research Council grantid: BB/G024995/1 |
GroupedDBID | --- -DZ -~X .55 0R~ 123 29P 2AX 2FS 2WC 4.4 53G 5RE 5VS 85S AACGO AAFWJ AANCE AAYJJ ABBHK ABOCM ABPLY ABPPZ ABTLG ABXSQ ABZEH ACGOD ACHIC ACIWK ACNCT ACPRK ADQXQ ADULT ADXHL AENEX AEUPB AEXZC AFFNX AFOSN AFRAH ALMA_UNASSIGNED_HOLDINGS AQVQM AS~ BKOMP CS3 D0L DCCCD DIK DU5 E3Z EBS EJD F5P FRP GX1 H13 HH5 HQ3 HTVGU HYE IPSME JAAYA JBMMH JENOY JHFFW JKQEH JLS JLXEF JPM JSG JST KQ8 L7B LU7 MVM N9A N~3 O9- OK1 P-O PNE PQQKQ R.V RHI RNA RNS RPM RXW SA0 SJN TAE TN5 UKR W8F WH7 WOQ WOW X7M XSW Y6R YBH YKV YSK ZCA ~02 ~KM - 02 0R 1AW 55 AAPBV ABFLS ABPTK ADACO ADZLD AJYGW AS ASUFR DNJUQ DOOOF DWIUU DZ F20 JSODD KM PQEST RHF VQA X XHC ZA5 AAYXX CITATION CGR CUY CVF ECM EIF NPM 7QG 7QL 7QP 7QR 7SN 7SS 7T5 7TK 7TM 7TO 7U9 8FD C1K FR3 H94 M7N P64 RC3 7S9 L.6 7X8 5PM |
ID | FETCH-LOGICAL-c499t-ccce742f7dae0dae045eaa85bd190734312a6972ebf2f2df5eabfab9a8c454133 |
ISSN | 0027-8424 1091-6490 |
IngestDate | Thu Aug 21 18:32:29 EDT 2025 Thu Sep 04 23:09:51 EDT 2025 Fri Sep 05 05:01:07 EDT 2025 Sat Aug 16 22:23:22 EDT 2025 Sat May 31 02:08:34 EDT 2025 Thu Apr 24 22:51:45 EDT 2025 Tue Jul 01 00:47:01 EDT 2025 Wed Nov 11 00:30:52 EST 2020 Thu May 29 08:40:39 EDT 2025 |
IsDoiOpenAccess | false |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Issue | 44 |
Language | English |
License | Freely available online through the PNAS open access option. |
LinkModel | OpenURL |
MergedId | FETCHMERGED-LOGICAL-c499t-ccce742f7dae0dae045eaa85bd190734312a6972ebf2f2df5eabfab9a8c454133 |
Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 Author contributions: C.A.A. and B.D. designed research; C.A.A. and S.B. performed research; C.A.A. and B.D. analyzed data; and C.A.A. and B.D. wrote the paper. Edited by Enrico Sandro Coen, John Innes Centre, Norwich, United Kingdom, and approved September 21, 2010 (received for review June 24, 2010) 1Present address: Department of Developmental Biology, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany. |
OpenAccessLink | http://doi.org/10.1073/pnas.1009050107 |
PMID | 20956314 |
PQID | 762714869 |
PQPubID | 42026 |
PageCount | 5 |
ParticipantIDs | crossref_primary_10_1073_pnas_1009050107 proquest_journals_762714869 crossref_citationtrail_10_1073_pnas_1009050107 pubmed_primary_20956314 jstor_primary_25748593 pubmedcentral_primary_oai_pubmedcentral_nih_gov_2973880 proquest_miscellaneous_1825416004 proquest_miscellaneous_762470200 pnas_primary_107_44_18898 |
ProviderPackageCode | RNA PNE CITATION AAYXX |
PublicationCentury | 2000 |
PublicationDate | 2010-11-02 |
PublicationDateYYYYMMDD | 2010-11-02 |
PublicationDate_xml | – month: 11 year: 2010 text: 2010-11-02 day: 02 |
PublicationDecade | 2010 |
PublicationPlace | United States |
PublicationPlace_xml | – name: United States – name: Washington |
PublicationTitle | Proceedings of the National Academy of Sciences - PNAS |
PublicationTitleAlternate | Proc Natl Acad Sci U S A |
PublicationYear | 2010 |
Publisher | National Academy of Sciences National Acad Sciences |
Publisher_xml | – name: National Academy of Sciences – name: National Acad Sciences |
References | Forest F (e_1_3_3_34_2) 2009 Darwin F (e_1_3_3_1_2) 1903 e_1_3_3_17_2 e_1_3_3_16_2 e_1_3_3_19_2 e_1_3_3_18_2 e_1_3_3_13_2 e_1_3_3_12_2 e_1_3_3_15_2 e_1_3_3_14_2 e_1_3_3_32_2 e_1_3_3_33_2 e_1_3_3_11_2 e_1_3_3_30_2 e_1_3_3_10_2 e_1_3_3_31_2 Dillon PJ (e_1_3_3_25_2) 1990; 9 e_1_3_3_6_2 e_1_3_3_5_2 e_1_3_3_8_2 e_1_3_3_7_2 e_1_3_3_28_2 e_1_3_3_9_2 e_1_3_3_27_2 e_1_3_3_29_2 e_1_3_3_24_2 e_1_3_3_23_2 e_1_3_3_26_2 e_1_3_3_2_2 e_1_3_3_20_2 e_1_3_3_4_2 e_1_3_3_22_2 e_1_3_3_3_2 e_1_3_3_21_2 |
References_xml | – ident: e_1_3_3_32_2 doi: 10.1016/S0076-6879(02)50957-5 – ident: e_1_3_3_14_2 doi: 10.1093/emboj/18.14.4023 – ident: e_1_3_3_24_2 doi: 10.1038/35012103 – ident: e_1_3_3_5_2 doi: 10.1007/978-3-642-86659-3 – ident: e_1_3_3_15_2 doi: 10.1007/s11103-004-0416-7 – ident: e_1_3_3_33_2 doi: 10.1007/s00497-002-0151-7 – volume-title: The Timetree of Life year: 2009 ident: e_1_3_3_34_2 – ident: e_1_3_3_3_2 doi: 10.1002/bies.10292 – ident: e_1_3_3_9_2 doi: 10.1038/353031a0 – ident: e_1_3_3_17_2 doi: 10.1105/tpc.105.031831 – ident: e_1_3_3_19_2 doi: 10.1038/35008089 – ident: e_1_3_3_29_2 doi: 10.1105/tpc.105.039107 – volume-title: More Letters of Charles Darwin year: 1903 ident: e_1_3_3_1_2 – ident: e_1_3_3_8_2 doi: 10.1111/j.1558-5646.2007.00105.x – ident: e_1_3_3_13_2 doi: 10.1016/j.cub.2005.07.063 – ident: e_1_3_3_2_2 doi: 10.1534/genetics.104.037770 – ident: e_1_3_3_21_2 doi: 10.1046/j.0960-7412.2003.01473.x – ident: e_1_3_3_27_2 doi: 10.1046/j.1365-313x.1998.00343.x – ident: e_1_3_3_12_2 doi: 10.1093/nar/gkp129 – ident: e_1_3_3_28_2 doi: 10.1371/journal.pbio.1000090 – ident: e_1_3_3_10_2 doi: 10.1038/35054083 – ident: e_1_3_3_7_2 doi: 10.1016/j.cell.2008.06.030 – ident: e_1_3_3_30_2 doi: 10.1016/j.cub.2004.10.028 – ident: e_1_3_3_22_2 doi: 10.1093/nar/gkn900 – ident: e_1_3_3_16_2 doi: 10.1101/gad.5.3.484 – ident: e_1_3_3_23_2 doi: 10.1002/j.1460-2075.1996.tb00807.x – ident: e_1_3_3_11_2 doi: 10.1016/S1369-5266(00)00139-4 – ident: e_1_3_3_4_2 doi: 10.1016/j.tplants.2007.06.012 – ident: e_1_3_3_31_2 doi: 10.1105/tpc.015123 – ident: e_1_3_3_20_2 doi: 10.1046/j.1365-313X.2003.01896.x – ident: e_1_3_3_26_2 doi: 10.1093/nar/17.16.6747 – ident: e_1_3_3_6_2 doi: 10.1038/nrg2063 – ident: e_1_3_3_18_2 doi: 10.1186/gb-2009-10-2-r24 – volume: 9 start-page: 298 year: 1990 ident: e_1_3_3_25_2 article-title: A rapid method for the construction of synthetic genes using the polymerase chain reaction publication-title: Biotechniques |
SSID | ssj0009580 |
Score | 2.218474 |
Snippet | The molecular mechanisms underlying the developmental processes that shape living organisms provide a basis to understand the evolution of biological... |
SourceID | pubmedcentral proquest pubmed crossref pnas jstor |
SourceType | Open Access Repository Aggregation Database Index Database Enrichment Source Publisher |
StartPage | 18898 |
SubjectTerms | Amino Acid Substitution Amino acids Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Biological Sciences Carpels Evolution Evolution, Molecular Females Flowers gene duplication Gene expression Gene Expression Regulation, Plant - physiology Genes MADS Domain Proteins males Models, Genetic Morphology nucleotide sequences Ovule - genetics Ovule - metabolism Petals Plants Pollen - genetics Pollen - metabolism protein-protein interactions Proteins Stamens Transcription factors Yeasts |
Title | Single amino acid change alters the ability to specify male or female organ identity |
URI | https://www.jstor.org/stable/25748593 http://www.pnas.org/content/107/44/18898.abstract https://www.ncbi.nlm.nih.gov/pubmed/20956314 https://www.proquest.com/docview/762714869 https://www.proquest.com/docview/1825416004 https://www.proquest.com/docview/762470200 https://pubmed.ncbi.nlm.nih.gov/PMC2973880 |
Volume | 107 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
journalDatabaseRights | – providerCode: PRVFSB databaseName: Free Full-Text Journals in Chemistry customDbUrl: eissn: 1091-6490 dateEnd: 20250401 omitProxy: true ssIdentifier: ssj0009580 issn: 0027-8424 databaseCode: HH5 dateStart: 19150101 isFulltext: true titleUrlDefault: http://abc-chemistry.org/ providerName: ABC ChemistRy – providerCode: PRVAFT databaseName: Open Access Digital Library customDbUrl: eissn: 1091-6490 dateEnd: 99991231 omitProxy: true ssIdentifier: ssj0009580 issn: 0027-8424 databaseCode: KQ8 dateStart: 19150101 isFulltext: true titleUrlDefault: http://grweb.coalliance.org/oadl/oadl.html providerName: Colorado Alliance of Research Libraries – providerCode: PRVAFT databaseName: Open Access Digital Library customDbUrl: eissn: 1091-6490 dateEnd: 99991231 omitProxy: true ssIdentifier: ssj0009580 issn: 0027-8424 databaseCode: KQ8 dateStart: 19150115 isFulltext: true titleUrlDefault: http://grweb.coalliance.org/oadl/oadl.html providerName: Colorado Alliance of Research Libraries – providerCode: PRVBFR databaseName: Free Medical Journals customDbUrl: eissn: 1091-6490 dateEnd: 99991231 omitProxy: true ssIdentifier: ssj0009580 issn: 0027-8424 databaseCode: DIK dateStart: 19150101 isFulltext: true titleUrlDefault: http://www.freemedicaljournals.com providerName: Flying Publisher – providerCode: PRVFQY databaseName: GFMER Free Medical Journals customDbUrl: eissn: 1091-6490 dateEnd: 99991231 omitProxy: true ssIdentifier: ssj0009580 issn: 0027-8424 databaseCode: GX1 dateStart: 0 isFulltext: true titleUrlDefault: http://www.gfmer.ch/Medical_journals/Free_medical.php providerName: Geneva Foundation for Medical Education and Research – providerCode: PRVAQN databaseName: PubMed Central customDbUrl: eissn: 1091-6490 dateEnd: 20250401 omitProxy: true ssIdentifier: ssj0009580 issn: 0027-8424 databaseCode: RPM dateStart: 19150101 isFulltext: true titleUrlDefault: https://www.ncbi.nlm.nih.gov/pmc/ providerName: National Library of Medicine |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3Nb9MwFLfKuHBBDBiEATISh6EoJXGcODlWCJiQqCbRSbtFduKMSFuCmvbA_g7-YN6LnaStWmlwaFQljpvm_fw-_L4IeY_93v1YSY_lsMi5ksJTYRp4sLYiFrMcjrgP-X0en1_yb1fR1WTyZyNqab1S0_xub17J_1AVzgFdMUv2Hyg7TAon4DvQF45AYTjei8Y_QO7caFfeVnXjyrwqbB6v2_nA206pNHW4Ox0Tsyqr8rd7KzGicOmW2n67hkVemYzdLS_vxSDd2j6WYN5vHs7GVBTLH1rXcy_mY2PjWbVE15Zx6ldyKd3ZdLD-9fK6qe-qflN63DAHOd0a0Om6sNC1uxIY4RF4_uZGJZi7XsJNfvRUG-YKuokXc9MedOC-pumthRnnG8w0SBLTodpK5gB9onvZPvAp7FVcyxajPlI_8vtptwps7wi-IRyxc8SLMMMJsnGCB-QhE3GMfTG-XgUbpZwTk9hk_2FfMEqEH3eeYEvXMeGuWEMXBu2zZ3bDcjf0nMUT8tgaKHRm0HZMJrp-So57EtMzW6f8wzOyMPCjHfwowo8a-FEDPwp4oRZ-dNVQCz-KoKPNkhr40Q5-tIffc3L55fPi07lnm3R4ORjLKy_Pcy04K0UhtY8fHmkpk0gVoGqKEPRTJuNUMK1KVrKihKuqlCqVSc4j0KDCE3JUN7V-SWihfMV5zvJCK6whlKQxK1LpS5-lAWPSIdP-dWa5rWCPjVRusgMEdMjZcMMvU7zl8NCTjj7DOBBlHGsBOsTpho73i4zzrMOmQ057KmaWLbQZaBci4EmcOuTdcBV4NjriZK2bNfwsbssEYGpwh9ADY2AaLsCW8x3ywsBifDQsHhoGcLPYAswwAEvGb1-pq59d6XjsVAcS-9X9X8wpeTSu79fkaLVc6zegh6_U225Z_AWX5dp- |
linkProvider | Geneva Foundation for Medical Education and Research |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Single+amino+acid+change+alters+the+ability+to+specify+male+or+female+organ+identity&rft.jtitle=Proceedings+of+the+National+Academy+of+Sciences+-+PNAS&rft.au=Airoldi%2C+Chiara+A.&rft.au=Bergonzi%2C+Sara&rft.au=Davies%2C+Brendan&rft.date=2010-11-02&rft.issn=0027-8424&rft.eissn=1091-6490&rft.volume=107&rft.issue=44&rft.spage=18898&rft.epage=18902&rft_id=info:doi/10.1073%2Fpnas.1009050107&rft.externalDBID=n%2Fa&rft.externalDocID=10_1073_pnas_1009050107 |
thumbnail_m | http://utb.summon.serialssolutions.com/2.0.0/image/custom?url=http%3A%2F%2Fwww.pnas.org%2Fcontent%2F107%2F44.cover.gif |
thumbnail_s | http://utb.summon.serialssolutions.com/2.0.0/image/custom?url=http%3A%2F%2Fwww.pnas.org%2Fcontent%2F107%2F44.cover.gif |