Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms

Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 101; no. 7; pp. 1910 - 1915
Main Authors Nam, J, Kim, J, Lee, S, An, G, Ma, H, Nei, M
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 17.02.2004
National Acad Sciences
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Abstract Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have a deeper insight into the evolutionary pattern of this gene family, we enumerated all available functional and nonfunctional (pseudogene) MADS-box genes from the Arabidopsis and rice genomes. Plant MADS-box genes can be classified into types I and II genes on the basis of phylogenetic analysis. Conducting extensive homology search and phylogenetic analysis, we found 64 presumed functional and 37 nonfunctional type I genes and 43 presumed functional and 4 nonfunctional type II genes in Arabidopsis. We also found 24 presumed functional and 6 nonfunctional type I genes and 47 presumed functional and 1 nonfunctional type II genes in rice. Our phylogenetic analysis indicated there were at least about four to eight type I genes and ≈ 15-20 type II genes in the most recent common ancestor of Arabidopsis and rice. It has also been suggested that type I genes have experienced a higher rate of birth-and-death evolution than type II genes in angiosperms. Furthermore, the higher rate of birth-and-death evolution in type I genes appeared partly due to a higher frequency of segmental gene duplication and weaker purifying selection in type I than in type II genes.
AbstractList Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have a deeper insight into the evolutionary pattern of this gene family, we enumerated all available functional and nonfunctional (pseudogene) MADS-box genes from the Arabidopsis and rice genomes. Plant MADS-box genes can be classified into types I and II genes on the basis of phylogenetic analysis. Conducting extensive homology search and phylogenetic analysis, we found 64 presumed functional and 37 nonfunctional type I genes and 43 presumed functional and 4 nonfunctional type II genes in Arabidopsis . We also found 24 presumed functional and 6 nonfunctional type I genes and 47 presumed functional and 1 nonfunctional type II genes in rice. Our phylogenetic analysis indicated there were at least about four to eight type I genes and ≈15–20 type II genes in the most recent common ancestor of Arabidopsis and rice. It has also been suggested that type I genes have experienced a higher rate of birth-and-death evolution than type II genes in angiosperms. Furthermore, the higher rate of birth-and-death evolution in type I genes appeared partly due to a higher frequency of segmental gene duplication and weaker purifying selection in type I than in type II genes.
Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have a deeper insight into the evolutionary pattern of this gene family, we enumerated all available functional and nonfunctional (pseudogene) MADS-box genes from the Arabidopsis and rice genomes. Plant MADS-box genes can be classified into types I and II genes on the basis of phylogenetic analysis. Conducting extensive homology search and phylogenetic analysis, we found 64 presumed functional and 37 nonfunctional type I genes and 43 presumed functional and 4 nonfunctional type II genes in Arabidopsis. We also found 24 presumed functional and 6 nonfunctional type I genes and 47 presumed functional and 1 nonfunctional type II genes in rice. Our phylogenetic analysis indicated there were at least about four to eight type I genes and ≈ 15-20 type II genes in the most recent common ancestor of Arabidopsis and rice. It has also been suggested that type I genes have experienced a higher rate of birth-and-death evolution than type II genes in angiosperms. Furthermore, the higher rate of birth-and-death evolution in type I genes appeared partly due to a higher frequency of segmental gene duplication and weaker purifying selection in type I than in type II genes.
Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have a deeper insight into the evolutionary pattern of this gene family, we enumerated all available functional and nonfunctional (pseudogene) MADS-box genes from the Arabidopsis and rice genomes. Plant MADS-box genes can be classified into types I and II genes on the basis of phylogenetic analysis. Conducting extensive homology search and phylogenetic analysis, we found 64 presumed functional and 37 nonfunctional type I genes and 43 presumed functional and 4 nonfunctional type II genes in Arabidopsis. We also found 24 presumed functional and 6 nonfunctional type I genes and 47 presumed functional and 1 nonfunctional type II genes in rice. Our phylogenetic analysis indicated there were at least about four to eight type I genes and about equal to 15-20 type II genes in the most recent common ancestor of Arabidopsis and rice. It has also been suggested that type I genes have experienced a higher rate of birth-and-death evolution than type II genes in angiosperms. Furthermore, the higher rate of birth-and-death evolution in type I genes appeared partly due to a higher frequency of segmental gene duplication and weaker purifying selection in type I than in type II genes. [PUBLICATION ABSTRACT]
Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have a deeper insight into the evolutionary pattern of this gene family, we enumerated all available functional and nonfunctional (pseudogene) MADS-box genes from the Arabidopsis and rice genomes. Plant MADS-box genes can be classified into types I and II genes on the basis of phylogenetic analysis. Conducting extensive homology search and phylogenetic analysis, we found 64 presumed functional and 37 nonfunctional type I genes and 43 presumed functional and 4 nonfunctional type II genes in Arabidopsis. We also found 24 presumed functional and 6 nonfunctional type I genes and 47 presumed functional and 1 nonfunctional type II genes in rice. Our phylogenetic analysis indicated there were at least about four to eight type I genes and approximately 15-20 type II genes in the most recent common ancestor of Arabidopsis and rice. It has also been suggested that type I genes have experienced a higher rate of birth-and-death evolution than type II genes in angiosperms. Furthermore, the higher rate of birth-and-death evolution in type I genes appeared partly due to a higher frequency of segmental gene duplication and weaker purifying selection in type I than in type II genes.Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have a deeper insight into the evolutionary pattern of this gene family, we enumerated all available functional and nonfunctional (pseudogene) MADS-box genes from the Arabidopsis and rice genomes. Plant MADS-box genes can be classified into types I and II genes on the basis of phylogenetic analysis. Conducting extensive homology search and phylogenetic analysis, we found 64 presumed functional and 37 nonfunctional type I genes and 43 presumed functional and 4 nonfunctional type II genes in Arabidopsis. We also found 24 presumed functional and 6 nonfunctional type I genes and 47 presumed functional and 1 nonfunctional type II genes in rice. Our phylogenetic analysis indicated there were at least about four to eight type I genes and approximately 15-20 type II genes in the most recent common ancestor of Arabidopsis and rice. It has also been suggested that type I genes have experienced a higher rate of birth-and-death evolution than type II genes in angiosperms. Furthermore, the higher rate of birth-and-death evolution in type I genes appeared partly due to a higher frequency of segmental gene duplication and weaker purifying selection in type I than in type II genes.
Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have a deeper insight into the evolutionary pattern of this gene family, we enumerated all available functional and nonfunctional (pseudogene) MADS-box genes from the Arabidopsis and rice genomes. Plant MADS-box genes can be classified into types I and II genes on the basis of phylogenetic analysis. Conducting extensive homology search and phylogenetic analysis, we found 64 presumed functional and 37 nonfunctional type I genes and 43 presumed functional and 4 nonfunctional type II genes in Arabidopsis. We also found 24 presumed functional and 6 nonfunctional type I genes and 47 presumed functional and 1 nonfunctional type II genes in rice. Our phylogenetic analysis indicated there were at least about four to eight type I genes and [approx]15-20 type II genes in the most recent common ancestor of Arabidopsis and rice. It has also been suggested that type I genes have experienced a higher rate of birth-and-death evolution than type II genes in angiosperms. Furthermore, the higher rate of birth-and-death evolution in type I genes appeared partly due to a higher frequency of segmental gene duplication and weaker purifying selection in type I than in type II genes.
Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have a deeper insight into the evolutionary pattern of this gene family, we enumerated all available functional and nonfunctional (pseudogene) MADS-box genes from the Arabidopsis and rice genomes. Plant MADS-box genes can be classified into types I and II genes on the basis of phylogenetic analysis. Conducting extensive homology search and phylogenetic analysis, we found 64 presumed functional and 37 nonfunctional type I genes and 43 presumed functional and 4 nonfunctional type II genes in Arabidopsis . We also found 24 presumed functional and 6 nonfunctional type I genes and 47 presumed functional and 1 nonfunctional type II genes in rice. Our phylogenetic analysis indicated there were at least about four to eight type I genes and ≈15–20 type II genes in the most recent common ancestor of Arabidopsis and rice. It has also been suggested that type I genes have experienced a higher rate of birth-and-death evolution than type II genes in angiosperms. Furthermore, the higher rate of birth-and-death evolution in type I genes appeared partly due to a higher frequency of segmental gene duplication and weaker purifying selection in type I than in type II genes.
Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have a deeper insight into the evolutionary pattern of this gene family, we enumerated all available functional and nonfunctional (pseudogene) MADS-box genes from the Arabidopsis and rice genomes. Plant MADS-box genes can be classified into types I and II genes on the basis of phylogenetic analysis. Conducting extensive homology search and phylogenetic analysis, we found 64 presumed functional and 37 nonfunctional type I genes and 43 presumed functional and 4 nonfunctional type II genes in Arabidopsis. We also found 24 presumed functional and 6 nonfunctional type I genes and 47 presumed functional and 1 nonfunctional type II genes in rice. Our phylogenetic analysis indicated there were at least about four to eight type I genes and approximately 15-20 type II genes in the most recent common ancestor of Arabidopsis and rice. It has also been suggested that type I genes have experienced a higher rate of birth-and-death evolution than type II genes in angiosperms. Furthermore, the higher rate of birth-and-death evolution in type I genes appeared partly due to a higher frequency of segmental gene duplication and weaker purifying selection in type I than in type II genes.
Author An, G
Ma, H
Kim, J
Lee, S
Nei, M
Nam, J
AuthorAffiliation Institute of Molecular Evolutionary Genetics and Department of Biology, Pennsylvania State University, University Park, PA 16802; and § National Research Laboratory of Plant Functional Genomics, Division of Molecular and Life Sciences, Pohang University of Science and Technology, Pohang 790-784, Korea
AuthorAffiliation_xml – name: Institute of Molecular Evolutionary Genetics and Department of Biology, Pennsylvania State University, University Park, PA 16802; and § National Research Laboratory of Plant Functional Genomics, Division of Molecular and Life Sciences, Pohang University of Science and Technology, Pohang 790-784, Korea
Author_xml – sequence: 1
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  fullname: Lee, S
– sequence: 4
  fullname: An, G
– sequence: 5
  fullname: Ma, H
– sequence: 6
  fullname: Nei, M
BackLink https://www.ncbi.nlm.nih.gov/pubmed/14764899$$D View this record in MEDLINE/PubMed
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Cites_doi 10.1038/35008089
10.1016/S0092-8674(02)00933-9
10.1073/pnas.0631708100
10.1093/oxfordjournals.molbev.a026408
10.1101/gad.5.3.484
10.1126/science.279.5349.407
10.1093/nar/gkg642
10.1038/221040a0
10.1023/A:1006051911291
10.1016/0092-8674(94)90291-7
10.1007/s00239-002-2426-x
10.1105/tpc.011544
10.1126/science.1068037
10.1007/s00239-003-0039-7
10.1016/S0378-1119(00)00243-2
10.1093/pcp/pcg156
10.1016/S1369-5266(00)00139-4
10.1093/molbev/msg152
10.1007/s00438-002-0781-3
10.1105/tpc.11.5.949
10.1073/pnas.94.15.7799
10.1016/S0092-8674(00)80618-2
10.1073/pnas.97.10.5328
10.1080/10635150390218213
10.1046/j.1365-313x.2000.00891.x
10.1093/oxfordjournals.molbev.a004137
10.1073/pnas.212646199
10.1093/molbev/msg216
10.1038/35012103
10.1016/S1055-7903(03)00207-0
10.1111/j.1432-1033.1995.tb20430.x
10.1093/nar/25.17.3389
10.1093/bioinformatics/17.12.1244
10.1007/s00438-001-0615-8
10.1016/S0092-8674(02)00932-7
ContentType Journal Article
Copyright Copyright 1993/2004 The National Academy of Sciences of the United States of America
Copyright National Academy of Sciences Feb 17, 2004
Copyright © 2004, The National Academy of Sciences 2004
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To whom correspondence should be addressed. E-mail: jyn101@psu.edu.
Contributed by Masatoshi Nei, December 22, 2003
Abbreviations: M-domain, MADS-domain; MRCA, most recent common ancestor.
Present address: Michigan State University–Department of Energy Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824.
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References e_1_3_2_26_2
e_1_3_2_29_2
(e_1_3_2_27_2) 2002; 15
e_1_3_2_41_2
e_1_3_2_40_2
e_1_3_2_20_2
e_1_3_2_21_2
e_1_3_2_42_2
e_1_3_2_22_2
e_1_3_2_23_2
e_1_3_2_24_2
e_1_3_2_25_2
e_1_3_2_9_2
e_1_3_2_15_2
e_1_3_2_38_2
e_1_3_2_8_2
e_1_3_2_16_2
e_1_3_2_7_2
e_1_3_2_17_2
e_1_3_2_6_2
e_1_3_2_18_2
e_1_3_2_39_2
e_1_3_2_19_2
e_1_3_2_1_2
e_1_3_2_30_2
e_1_3_2_32_2
e_1_3_2_10_2
e_1_3_2_31_2
e_1_3_2_5_2
(e_1_3_2_11_2) 2002; 47
e_1_3_2_34_2
e_1_3_2_4_2
e_1_3_2_12_2
e_1_3_2_33_2
(e_1_3_2_37_2) 2003; 12
e_1_3_2_3_2
e_1_3_2_13_2
e_1_3_2_36_2
e_1_3_2_2_2
e_1_3_2_14_2
e_1_3_2_35_2
(e_1_3_2_28_2) 1987; 4
10821278 - Nature. 2000 May 11;405(6783):200-3
12815071 - Genes Dev. 2003 Jun 15;17(12):1540-53
5782607 - Nature. 1969 Jan 4;221(5175):40-2
12949148 - Mol Biol Evol. 2003 Dec;20(12):1963-77
7744019 - Eur J Biochem. 1995 Apr 1;229(1):1-13
10783890 - Nature. 2000 Apr 13;404(6779):766-70
10805792 - Proc Natl Acad Sci U S A. 2000 May 9;97(10):5328-33
11751241 - Bioinformatics. 2001 Dec;17(12):1244-5
3447015 - Mol Biol Evol. 1987 Jul;4(4):406-25
7913881 - Cell. 1994 Jul 29;78(2):203-9
11862488 - Mol Genet Genomics. 2002 Feb;266(6):942-50
12837945 - Plant Cell. 2003 Jul;15(7):1538-51
12297045 - Cell. 2002 Sep 20;110(6):713-23
14615187 - Mol Phylogenet Evol. 2003 Dec;29(3):464-89
10925200 - Gene. 2000 Jul 25;253(1):31-43
12297046 - Cell. 2002 Sep 20;110(6):725-35
10908645 - Mol Biol Evol. 2000 Aug;17(8):1251-8
12698294 - J Mol Evol. 2003 May;56(5):573-86
9254694 - Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
9430595 - Science. 1998 Jan 16;279(5349):407-9
11163172 - Curr Opin Plant Biol. 2001 Feb;4(1):75-85
9869408 - Plant Mol Biol. 1998 Dec;38(6):1021-9
12888499 - Nucleic Acids Res. 2003 Aug 1;31(15):4401-9
12136088 - Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
10330478 - Plant Cell. 1999 May;11(5):949-56
11935017 - Science. 2002 Apr 5;296(5565):79-92
14701936 - Plant Cell Physiol. 2003 Dec;44(12):1403-11
11115127 - Plant J. 2000 Nov;24(4):457-66
12777513 - Mol Biol Evol. 2003 Sep;20(9):1435-47
1672119 - Genes Dev. 1991 Mar;5(3):484-95
15008427 - J Mol Evol. 2003;57 Suppl 1:S290-6
10778850 - Cell. 2000 Mar 31;101(1):5-8
12746493 - Proc Natl Acad Sci U S A. 2003 May 27;100(11):6558-63
9223266 - Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7799-806
12032236 - Mol Biol Evol. 2002 Jun;19(6):801-14
12451182 - Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16138-43
12857639 - Syst Biol. 2003 Aug;52(4):477-87
12589434 - Mol Genet Genomics. 2003 Feb;268(5):598-606
References_xml – ident: e_1_3_2_17_2
  doi: 10.1038/35008089
– ident: e_1_3_2_36_2
  doi: 10.1016/S0092-8674(02)00933-9
– ident: e_1_3_2_1_2
– ident: e_1_3_2_39_2
  doi: 10.1073/pnas.0631708100
– ident: e_1_3_2_42_2
  doi: 10.1093/oxfordjournals.molbev.a026408
– ident: e_1_3_2_7_2
  doi: 10.1101/gad.5.3.484
– ident: e_1_3_2_14_2
  doi: 10.1126/science.279.5349.407
– ident: e_1_3_2_41_2
  doi: 10.1093/nar/gkg642
– ident: e_1_3_2_21_2
  doi: 10.1038/221040a0
– volume: 12
  start-page: 1540
  year: 2003
  ident: e_1_3_2_37_2
  publication-title: Genes Dev.
– ident: e_1_3_2_19_2
  doi: 10.1023/A:1006051911291
– ident: e_1_3_2_12_2
  doi: 10.1016/0092-8674(94)90291-7
– ident: e_1_3_2_23_2
  doi: 10.1007/s00239-002-2426-x
– ident: e_1_3_2_4_2
  doi: 10.1105/tpc.011544
– ident: e_1_3_2_26_2
– ident: e_1_3_2_25_2
  doi: 10.1126/science.1068037
– ident: e_1_3_2_33_2
  doi: 10.1007/s00239-003-0039-7
– ident: e_1_3_2_10_2
  doi: 10.1016/S0378-1119(00)00243-2
– ident: e_1_3_2_6_2
  doi: 10.1093/pcp/pcg156
– ident: e_1_3_2_13_2
  doi: 10.1016/S1369-5266(00)00139-4
– ident: e_1_3_2_20_2
  doi: 10.1093/molbev/msg152
– ident: e_1_3_2_40_2
  doi: 10.1007/s00438-002-0781-3
– ident: e_1_3_2_15_2
  doi: 10.1105/tpc.11.5.949
– ident: e_1_3_2_22_2
  doi: 10.1073/pnas.94.15.7799
– ident: e_1_3_2_30_2
– volume: 47
  start-page: 287
  year: 2002
  ident: e_1_3_2_11_2
  publication-title: Maydica
– ident: e_1_3_2_18_2
  doi: 10.1016/S0092-8674(00)80618-2
– ident: e_1_3_2_3_2
  doi: 10.1073/pnas.97.10.5328
– ident: e_1_3_2_32_2
  doi: 10.1080/10635150390218213
– ident: e_1_3_2_16_2
  doi: 10.1046/j.1365-313x.2000.00891.x
– volume: 4
  start-page: 406
  year: 1987
  ident: e_1_3_2_28_2
  publication-title: Mol. Biol. Evol.
– ident: e_1_3_2_8_2
  doi: 10.1093/oxfordjournals.molbev.a004137
– ident: e_1_3_2_31_2
  doi: 10.1073/pnas.212646199
– ident: e_1_3_2_5_2
  doi: 10.1093/molbev/msg216
– ident: e_1_3_2_38_2
  doi: 10.1038/35012103
– ident: e_1_3_2_9_2
  doi: 10.1016/S1055-7903(03)00207-0
– ident: e_1_3_2_2_2
  doi: 10.1111/j.1432-1033.1995.tb20430.x
– ident: e_1_3_2_24_2
  doi: 10.1093/nar/25.17.3389
– ident: e_1_3_2_29_2
  doi: 10.1093/bioinformatics/17.12.1244
– ident: e_1_3_2_34_2
  doi: 10.1007/s00438-001-0615-8
– ident: e_1_3_2_35_2
  doi: 10.1016/S0092-8674(02)00932-7
– volume: 15
  start-page: 3059
  year: 2002
  ident: e_1_3_2_27_2
  publication-title: Nucleic Acids Res.
– reference: 12297046 - Cell. 2002 Sep 20;110(6):725-35
– reference: 1672119 - Genes Dev. 1991 Mar;5(3):484-95
– reference: 10778850 - Cell. 2000 Mar 31;101(1):5-8
– reference: 10821278 - Nature. 2000 May 11;405(6783):200-3
– reference: 12589434 - Mol Genet Genomics. 2003 Feb;268(5):598-606
– reference: 12032236 - Mol Biol Evol. 2002 Jun;19(6):801-14
– reference: 12698294 - J Mol Evol. 2003 May;56(5):573-86
– reference: 10925200 - Gene. 2000 Jul 25;253(1):31-43
– reference: 12888499 - Nucleic Acids Res. 2003 Aug 1;31(15):4401-9
– reference: 12857639 - Syst Biol. 2003 Aug;52(4):477-87
– reference: 10783890 - Nature. 2000 Apr 13;404(6779):766-70
– reference: 12815071 - Genes Dev. 2003 Jun 15;17(12):1540-53
– reference: 11115127 - Plant J. 2000 Nov;24(4):457-66
– reference: 12746493 - Proc Natl Acad Sci U S A. 2003 May 27;100(11):6558-63
– reference: 9223266 - Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7799-806
– reference: 12297045 - Cell. 2002 Sep 20;110(6):713-23
– reference: 11163172 - Curr Opin Plant Biol. 2001 Feb;4(1):75-85
– reference: 12136088 - Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
– reference: 12451182 - Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16138-43
– reference: 7913881 - Cell. 1994 Jul 29;78(2):203-9
– reference: 12837945 - Plant Cell. 2003 Jul;15(7):1538-51
– reference: 12777513 - Mol Biol Evol. 2003 Sep;20(9):1435-47
– reference: 14701936 - Plant Cell Physiol. 2003 Dec;44(12):1403-11
– reference: 15008427 - J Mol Evol. 2003;57 Suppl 1:S290-6
– reference: 3447015 - Mol Biol Evol. 1987 Jul;4(4):406-25
– reference: 10330478 - Plant Cell. 1999 May;11(5):949-56
– reference: 11862488 - Mol Genet Genomics. 2002 Feb;266(6):942-50
– reference: 7744019 - Eur J Biochem. 1995 Apr 1;229(1):1-13
– reference: 10908645 - Mol Biol Evol. 2000 Aug;17(8):1251-8
– reference: 12949148 - Mol Biol Evol. 2003 Dec;20(12):1963-77
– reference: 11751241 - Bioinformatics. 2001 Dec;17(12):1244-5
– reference: 11935017 - Science. 2002 Apr 5;296(5565):79-92
– reference: 10805792 - Proc Natl Acad Sci U S A. 2000 May 9;97(10):5328-33
– reference: 9254694 - Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
– reference: 9430595 - Science. 1998 Jan 16;279(5349):407-9
– reference: 9869408 - Plant Mol Biol. 1998 Dec;38(6):1021-9
– reference: 5782607 - Nature. 1969 Jan 4;221(5175):40-2
– reference: 14615187 - Mol Phylogenet Evol. 2003 Dec;29(3):464-89
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SubjectTerms Angiosperms
Arabidopsis - genetics
Arabidopsis thaliana
Biological Sciences
Birth rate
Datasets
Evolution
Evolution, Molecular
Flowers & plants
Genes
Genes, Plant - genetics
Genome, Plant
Genomes
Genomics
MADS box
MADS Domain Proteins - genetics
Magnoliopsida - genetics
Mortality
Oryza - genetics
Oryza sativa
Phylogenetics
Phylogeny
Plant Proteins - genetics
Plants
Protein Structure, Tertiary
Pseudogenes
Pseudogenes - genetics
Rice
Title Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms
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