Molecular and phylogenetic analyses of the MADS-box gene family in tomato

Molecular Biology and Evolution

Volumn 23, Issue 11, 2006, Pages 2245-2258

  Hileman, Lena C ^a,b   Sundstrom, Jens F ^a,c   Litt, Amy ^a,d   Chen, Meiqin ^a,e   Shumba, Takudzwa ^a   Irish, Vivian F ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF KANSAS   (United States)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^d NEW YORK BOTANICAL GARDEN   (United States)

^e PEKING UNIVERSITY   (China)

Author keywords

Gene duplication; Homeotic gene; MADS box gene; Solanaceae; Tomato

Indexed keywords

MADS DOMAIN PROTEIN;

ANGIOSPERM; ARABIDOPSIS; ARTICLE; COMPARATIVE GENOMIC HYBRIDIZATION; GENE; GENE DUPLICATION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC CODE; MADS BOX GENE; MIKC GENE; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT GENETICS; PROTEIN DOMAIN; TOMATO; TRANSCRIPTION REGULATION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; LYCOPERSICON ESCULENTUM; MAGNOLIOPHYTA; SOLANACEAE;

EID: 33749577815     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msl095     Document Type: Article

References (90)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-402.
2. Alvarez-Buylla ER, Liljegren SJ, Pelaz S, Gold SE, Burgeff C, Ditta GS, Vergara-Silva F, Yanofsky MF. 2000. MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J 24:457-66.
3. Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS, de Pouplana LR, Martinez-Castilla L, Yanofsky MF. 2000. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci USA 97:5328-33.
4. Ampomah-Dwamena C, Morris BA, Sutherland P, Veit B, Yao JL. 2002. Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol 130:605-17.
5. Baum DA, Doebley J, Irish VF, Kramer EM. 2002. Response: missing links: the genetic architecture of flower and floral diversification. Trends Plant Sci 7:31-4.
6. Becker A, Theissen G. 2003. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464-89.
7. Boss PK, Bastow RM, Mylne JS, Dean C. 2004. Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:S18-31.
8. Burgeff C, Liljegren SJ, Tapia-Lopez R, Yanofsky MF, Alvarez-Buylla ER. 2002. MADS-box gene expression in lateral primordia, meristems and differentiated tissues of Arabidopsis thaliana roots. Planta 214:365-72.
9. Busi MV, Bustamante C, D'Angelo C, Hidalgo-Cuevas M, Boggio SB, Valle EM, Zabaleta E. 2003. MADS-box genes expressed during tomato seed and fruit development. Plant Mol Biol 52:801-15.
10. Cannon SB, Crow JA, Heuer ML, et al. (22 co-authors). 2005. Databases and information integration for the Medicago truncatula genome and transcriptome. Plant Physiol 138:38-46.
11. Causier B, Castillo R, Zhou JL, Ingram R, Xue YB, Schwarz-Sommer Z, Davies B. 2005. Evolution in action: following function in duplicated floral homeotic genes. Curr Biol 15:1508-12.
12. Cho SC, Jang SH, Chae SJ, Chung KM, Moon YH, An GH, Jang SK. 1999. Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol Biol 40:419-29.
13. Davies B, EgeaCortines M, Silva ED, Saedler H, Sommer H. 1996. Multiple interactions amongst floral homeotic MADS box proteins. EMBO J 15:4330-43.
14. Davies B, Motte P, Keck E, Saedler H, Sommer H, Schwarz-Sommer Z. 1999. PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J 18:4023-34.
15. De Bodt S, Raes J, Van de Peer YV, Theissen G. 2003. And then there were many: MADS goes genomic. Trends Plant Sci 8:475-83.
16. De Bodt S, Theissen G, Van de Peer Y. 2006. Promoter analysis of MADS-box genes in Eudicots through phylogenetic footprinting. Mol Biol Evol 23:1293-1303.
17. de Martino G, Pan I, Emmanuel E, Levy AA, Irish VF. 2006. Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating flowering. Plant Cell 18:1833-1845.
18. Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF. 2004. The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935-40.
19. Egea-Cortines M, Saedler H, Sommer H. 1999. Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J 18:5370-9.
20. Fan HY, Hu Y, Tudor M, Ma H. 1997. Specific interactions between the K domains of AG and AGLs, members of the MADS domain family of DNA binding proteins. Plant J 12:999-1010.
21. Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky MF, Kater MM, Colombo L. 2003. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15:2603-11.
22. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-91.
23. Goto K, Meyerowitz EM. 1994. Function and regulation of the Arabidopsis floral homeotic gene pistillata. Genes Dev 8:1548-60.
24. Hartmann U, Hohmann S, Nettesheim K, Wisman E, Saedler H, Huijser P. 2000. Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351-60.
25. Hecht V, Foucher F, Ferrandiz C, et al. (11 co-authors). 2005. Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol 137:1420-34.
26. Henschel K, Kofuji R, Hasebe M, Saedler H, Munster T, Theissen G. 2002. Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol Biol Evol 19:801-14.
27. Honma T, Goto K. 2001. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525-9.
28. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754-5.
29. Initiative AG. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815.
30. Irish VF. 2003. The evolution of floral homeotic gene function. Bioessays 25:637-46.
31. Irish VF, Litt A. 2005. Flower development and evolution: gene duplication, diversification and redeployment. Curr Opin Genet Dev 15:454-60.
32. Jack T. 2001. Relearning our ABCs: new twists on an old model. Trends Plant Sci 6:310-6.
33. Jack T. 2004. Molecular and genetic mechanisms of floral control. Plant Cell 16:S1-17.
34. Jack T, Brockman LL, Meyerowitz EM. 1992. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68:683-97.
35. Kaufmann K, Melzer R, Theissen G. 2005. MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347:183-98.
36. Kofuji R, Sumikawa N, Yamasaki M, Kondo K, Ueda K, Ito M, Hasebe M. 2003. Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses. Mol Biol Evol 20:1963-77.
37. Kohler C, Hennig L, Spillane C, Pien S, Gruissem W, Grossniklaus U. 2003. The polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev 17:1540-53.
38. Kohler C, Page DR, Gagliardini V, Grossniklaus U. 2005. The Arabidopsis thaliana MEDEA polycomb group protein controls expression of PHERES1 by parental imprinting. Nat Genet 37:28-30.
39. Kramer EM, Dorit RL, Irish VF. 1998. Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149:765-83.
40. Kramer EM, Irish VF. 1999. Evolution of genetic mechanisms controlling petal development. Nature 399:144-8.
41. Kramer EM, Jaramillo MA, Di Stilio VS. 2004. Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166:1011-23.
42. Krizek BA, Meyerowitz EM. 1996. Mapping the protein regions responsible for the functional specificities of the Arabidopsis MADS domain organ-identity proteins. Proc Natl Acad Sci USA 93:4063-70.
43. Krizek BA, Riechmann JL, Meyerowitz EM. 1999. Use of the APETALA1 promoter to assay the in vivo function of chimeric MADS box genes. Sex Plant Reprod 12:14-26.
44. Lamb RS, Irish VF. 2003. Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc Natl Acad Sci USA 100:6558-63.
45. Litt A, Irish VF. 2003. Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165:821-33.
46. Ma H, Yanofsky MF, Meyerowitz EM. 1991. Agl1-Agl6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5:484-95.
47. Ma L, Sun N, Liu X, Jiao Y, Zhao H, Deng XW. 2005. Organspecific expression of Arabidopsis genome during development. Plant Physiol 138:80-91.
48. Maddison WP, Maddison DR. 2000. MacClade: analysis of phylogeny and character evolution. Version 4.0. Sunderland, MA: Sinauer Associates.
49. Mao L, Begum D, Chuang HW, Budiman MA, Szymkowiak EJ, Irish EE, Wing RA. 2000. JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development. Nature 406:910-3.
50. Martienssen R, Irish V. 1999. Copying out our ABCs-the role of gene redundancy in interpreting genetic hierarchies. Trends Genet 15:435-7.
51. Messenguy F, Dubois E. 2003. Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316:1-21.
52. Michaels SD, Amasino RM. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949-56.
53. Michaels SD, Ditta G, Gustafson-Brown C, Pelaz S, Yanofsky MF, Amasino RM. 2003. AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J 33:867-74.
54. Mo Y, Ho W, Johnston K, Marmorstein R. 2001. Crystal structure of a ternary SAP-1/SRF/c-fos SIRE DNA complex. J Mol Biol 314:495-506.
55. Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I. 2003. The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613-23.
56. Moore RC, Purugganan MD. 2005. The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122-8.
57. Nam J, Kim J, Lee S, An GH, Ma H, Nei MS. 2004. Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms. Proc Natl Acad Sci USA 101:1910-5.
58. Nawy T, Lee JY, Colinas J, Wang JY, Thongrod SC, Malamy JE, Birnbaum K, Benfey PN. 2005. Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell 17:1908-25.
59. Nesi N, Debeaujon I, Jond C, Stewart AJ, Jenkins GI, Caboche M, Lepiniec L. 2002. The TRANSPARENT TESTA16 locus encodes the Arabidopsis B sister MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14:2463-79.
60. Parenicova L, de Folter S, Kieffer M, et al. (12 co-authors). 2003. Molecular and phylogenetic analyses of the complete MADSbox transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15:1538-51.
61. Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF. 2000. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200-3.
62. Pelaz S, Gustafson-Brown C, Kohalmi SE, Crosby WL, Yanofsky MF. 2001. APETALA1 and SEPALLATA3 interact to promote flower development. Plant J 26:385-94.
63. Pellegrini L, Song T, Richmond TJ. 1995. Structure of serum response factor core bound to DNA. Nature 376:490-8.
64. Pnueli L, Abuabeid M, Zamir D, Nacken W, Schwarzsommer Z, Lifschitz E. 1991. The Mads box gene family in tomato-temporal expression during floral development, conserved secondary structures and homology with homeotic genes from antirrhinum and Arabidopsis. Plant J 1:255-66.
65. Pnueli L, Hareven D, Broday L, Hurwitz C, Lifschitz E. 1994. The Tm5 Mads box gene mediates organ differentiation in the 3 inner whorls of tomato flowers. Plant Cell 6:175-86.
66. Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E. 1994. Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6:163-73.
67. Prasad K, Sriram P, Kumar CS, Kushalappa K, Vijayraghavan U. 2001. Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals. Dev Genes Evol 211:281-90.
68. Project IRGS. 2005. The map-based sequence of the rice genome. Nature 436:793-800.
69. Riechmann JL, Krizek BA, Meyerowitz EM. 1996. Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci USA 93:4793-8.
70. Riechmann JL, Meyerowitz EM. 1997. Determination of floral organ identity by Arabidopsis MADS domain homeotic proteins AP1, AP3, PI, and AG is independent of their DNA-binding specificity. Mol Biol Cell 8:1243-59.
71. Ronquist F, Huelsenbeck JP. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-4.
72. Rounsley SD, Ditta GS, Yanofsky MF. 1995. Diverse roles for Mads box genes in Arabidopsis development. Plant Cell 7:1259-69.
73. Santelli E, Richmond TJ. 2000. Crystal structure of MEF2A core bound to DNA at 1.5 angstrom resolution. J Mol Biol 297:437-49.
74. Shore P, Sharrocks D. 1995. The Mads-box family of transcription factors. Eur J Biochem 229:1-13.
75. Soltis DE, Soltis PS, Albert VA, Oppenheimer DG, dePamphilis CW, Ma H, Frohlich MW, Theissen G. 2002. Missing links: the genetic architecture of flower and floral diversification. Trends Plant Sci 7:22-31.
76. Sonnhammer ELL, Koonin EV. 2002. Orthology, paralogy and proposed classification for paralog subtypes. Trends Genet 18:619-20.
77. Stellari GM, Jaramillo MA, Kramer EM. 2004. Evolution of the APETALA3 and PISTILLATA lineages of MADS-box-containing genes in the basal angiosperms. Mol Biol Evol 21:506-19.
78. Sung S, Amasino RM. 2005. Remembering winter: toward a molecular understanding of vernalization. Annu Rev Plant Biol 56:491-508.
79. Svensson ME, Johannesson H, Engstrom P. 2000. The LAMB1 gene from the clubmoss, Lycopodium annotinum, is a divergent MADS-box gene, expressed specifically in sporogenic structures. Gene 253:31-43.
80. Swofford DL. 2002. PAUP* 4.0: phylogenetic analysis using parsimony (*and other methods). Sunderland, MA: Sinauer Associates.
81. Tan S, Richmond TJ. 1998. Crystal structure of the yeast MAT alpha 2/MCM1/DNA ternary complex. Nature 391:660-6.
82. Uimari A, Kotilainen M, Elomaa P, Yu D, Albert VA, Teeri TH. 2004. Integration of reproductive meristem fates by a SEPALLATA-like MADS-box gene. Proc Natl Acad Sci USA 101:15817-22.
83. Vandenbussche M, Theissen G, Van de Peer Y, Gerats T. 2003. Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acids Res 31:4401-9.
84. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J. 2002. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus. Science 296:343-6.
85. Yalovsky S, Rodriguez-Concepcion M, Bracha K, Toledo-Ortiz G, Gruissem W. 2000. Prenylation of the floral transcription factor APETALA1 modulates its function. Plant Cell 12:1257-66.
86. Yu H, Xu Y, Tan EL, Kumar PP. 2002. AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proc Natl Acad Sci USA 99:16336-41.
87. Yu JJ, Wang W, Lin S, et al. (117 co-authors). 2005. The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38.
88. Zachgo S, Saedler H, SchwarzSommer Z. 1997. Pollen-specific expression of DEFH125, a MADS-box transcription factor in Antirrhinum with unusual features. Plant J 11:1043-50.
89. Zahn LM, King HZ, Leebens-Mack JH, Kim S, Soltis PS, Landherr LL, Soltis DE, dePamphilis CW, Ma H. 2005. The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169:2209-23.
90. Zhang H, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407-9.