The evolution of the SEPALLATA subfamily of MADS-box genes: A preangiosperm origin with multiple duplications throughout angiosperm history

Genetics

Volumn 169, Issue 4, 2005, Pages 2209-2223

  Zahn, Laura M ^a   Kong, Hongzhi ^a,b   Leebens Mack, James H ^a   Kim, Sangtae ^c   Soltis, Pamela S ^d   Landherr, Lena L ^a   Soltis, Douglas E ^c   DePamphilis, Claude W ^a   Ma, Hong ^a,e  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b INSTITUTE OF BOTANY   (China)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

^e PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MADS DOMAIN PROTEIN;

ANGIOSPERM; ARTICLE; CELL LINEAGE; FLOWER; FLOWER DEVELOPMENT; GENE; GENE DUPLICATION; GENE INTERACTION; GENE ISOLATION; GYMNOSPERM; MERISTEM; NONHUMAN; PLANT EVOLUTION; PRIORITY JOURNAL; SEP GENE;

ALGORITHMS; AMINO ACID SEQUENCE; ANGIOSPERMS; ARABIDOPSIS; DATABASES, GENETIC; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENES, PLANT; IN SITU HYBRIDIZATION; MADS DOMAIN PROTEINS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

GYMNOSPERMAE; LILIOPSIDA; MAGNOLIOPHYTA;

EID: 15944373717     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.037770     Document Type: Article

References (98)

1. ALBERT, V. A., D. E. SOLTIS, J. E. CARLSON, W. G. FARMERIE, P. K. WALL et al., 2005 Floral gene resources from basal angiosperms for comparative genomics research. BMC Plant Biol. (in press).
2. AOKI, S., K. UEHARA, M. IMAFUKU, M. HASEBE and M. ITO, 2004 Phylogeny and divergence of basal angiosperms inferred from APETALA3-and PISTILLATA-like MADS-box genes. J. Plant Res. 117: 229-244.
3. ANGIOSPERM PHYLOGENY GROUP, 2003 An update of the Angio sperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot. J. Linn. Soc. 141: 399-436.
4. BARKMAN, T. J., G. CHENERY, J. R. MCNEAL, J. LYONS-WEILER, W. J. ELLISENS et al., 2000 Independent and combined analyses of sequences from all three genomic compartments converge on the root of flowering plant phylogeny. Proc. Natl. Acad. Sci. USA 97: 13166-13171.
5. BECKER, A., and G. THEISSEN, 2003 The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 29: 464-489.
6. BONHOMME, F., H. SOMMER, G. BERNIER and A. JACQMARD, 1997 Characterization of SaMADS D from Sinapis alba suggests a dual function of the gene: in inflorescence development and floral organogenesis. Plant Mol. Biol. 34: 573-582.
7. BONHOMME, F., B. KURZ, S. MELZER, G. BERNIER and A. JACQMARD, 2000 Cytokinin and gibberellin activate SaMADS A, a gene apparently involved in regulation of the floral transition in Sinapis alba. Plant J. 24: 103-111.
8. BOWERS, J. E., B. A. CHAPMAN, J. RONG and A. H. PATERSON, 2003 Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438.
9. BUZGO, M., D. E. SOLTIS, P. S. SOLTIS and H. MA, 2004 Towards a comprehensive integration or morphological and genetic studies of floral development. Trends Plant Sci. 9: 164-173.
10. COEN, E. S., and E. M. MEYEROWITZ, 1991 The war of the whorls: genetic interactions controlling flower development. Nature 353: 31-37.
11. DAVIES, B., and Z. SCHWARZ-SOMMER, 1994 Control of floral organ identity by homeotic MADS-box transcription factors. Results Probl. Cell Differ. 20: 235-258.
12. DAVIES, B., M. EGEA-CORTINES, E. DE ANDRADE SILVA, H. SAEDLER and H. SOMMER, 1996 Multiple interactions amongst floral homeotic MADS box proteins. EMBOJ. 15: 4330-4343.
13. DE BODT, S., J. RAES, Y. VAN DE PEER and G. THEISSEN, 2003 And then there were many: MADS goes genomic. Trends Plant Sci. 8: 475-483.
14. DITTA, G., A. PINYOPICH, P. ROBLES, S. PELAZ and M. F. YANOFSKY, 2004 The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr. Biol. 14: 1935-1940.
15. EDGAR, R. C., 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
16. EGEA-CORTINES, M., H. SAEDLER and H. SOMMER, 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: 5370-5379.
17. ERMOLAEVA, M. D., M. WU, J. A. EISEN and S. L. SALZBERG, 2003 The age of the Arabidopsis thaliana genome duplication. Plant Mol. Biol. 51: 859-866.
18. FAN, H. Y., Y. HU, M. TUDOR and H. MA, 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.
19. FAVARO, R., R. G. IMMINK, V. FERIOLI, B. BERNASCONI, M. BYZOVA et al., 2002 Ovule-specific MADS-box proteins have conserved protein-protein interactions in monocot and dicot plants. Mol. Genet. Genomics 268: 152-159.
20. FAVARO, R., A. PINYOPICH, R. BATTAGLIA, M. KOOIKER, L. BORGHI et al., 2003 MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15: 2603-2611.
21. FELSENSTEIN, J., 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
22. FERRARIO, S., R. G. IMMINK, A. SHCHENNIKOVA, J. BUSSCHER-LANGE and G. C. ANGENENT, 2003 The MADS box gene FBP2 is required for SEPALLATA function in petunia. Plant Cell 15: 914-925.
23. FLANAGAN, C. A., and H. MA, 1994 Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant Arabidopsis flowers. Plant Mol. Biol. 26: 581-595.
24. FORCE, A., M. LYNCH, F. B. PICKETT, A. AMORES, Y. L. YAN et al., 1999 Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
25. GASCUEL, O., 1997 BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol. Biol. Evol. 14: 685-695.
26. GRAHAM, S. W., and R. G. OLMSTEAD, 2000 Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. Am. J. Bot. 87: 1712-1730.
27. GUINDON, S., and O. GASCUEL, 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704.
28. HONMA, T., and K. GOTO, 2000 The Arabidopsis floral homeotic gene PISTILLATA is regulated by discrete cis-elements responsive to induction and maintenance signals. Development 127: 2021-2030.
29. HONMA, T., and K. GOTO, 2001 Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409: 525-529.
30. HSU, H. F., and C. H. YANG, 2002 An orchid (Oncidium Gower Ramsey) AP3-like MADS gene regulates floral formation and initiation. Plant Cell Physiol. 43: 1198-1209.
31. HUANG, H., M. TUDOR, C. A. WEISS, Y. HU and H. MA, 1995 The Arabidopsis MADS-box gene AGL3 is widely expressed and encodes a sequence-specific DNA-binding protein. Plant Mol. Biol. 28: 549-567.
32. IMMINK, R. G., T. W. GADELLA, JR., S. FERRARIO, M. BUSSCHER and G. C. ANGENENT, 2002 Analysis of MADS box protein-protein interactions in living plant cells. Proc. Natl. Acad. Sci. USA 99: 2416-2421.
33. IMMINK, R. G., S. FERRARIO, J. BUSSCHER-LANGE, M. KOOIKER, M. BUSSCHER et al., 2003 Analysis of the petunia MADS-box transcription factor family. Mol. Genet. Genomics 268: 598-606.
34. IRISH, V. F., 2003 The evolution of floral homeotic gene function. BioEssays 25: 637-646.
35. IRISH, V. F., and I. M. SUSSEX, 1990 Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2: 741-753.
36. JACK, T., 2004 Molecular and genetic mechanisms of floral control. Plant Cell 16: S1-S17.
37. JOHANSEN, B., L. B. PEDERSEN, M. SKIPPER and S. FREDERIKSEN, 2002 MADS-box gene evolution-structure and transcription patterns. Mol. Phylogenet. Evol. 23: 458-480.
38. KANNO, A., H. SAEKI, T. KAMEYA, H. SAEDLER and G. THEISSEN, 2003 Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Mol. Biol. 52: 831-841.
39. KIM, S., M.-J. Yoo, V. A. ALBERT, J. S. FARRIS, P. S. SOLTIS et al., 2004 Phylogeny and diversification of B-function MADS-box genes in angiosperms: evolutionary and functional implications of a 260-million-year-old duplication. Am. J. Bot. 91: 2102-2118.
40. KIM, S., J. KOH, H. MA, Y. HU, P. K. ENDRESS et al., 2005 Sequence and expression studies of A-, B-, and E-class MADS-box genes in Eupomatia (Eupomatiaceae): support for the bracteate origin of the calyptra. Int. J. Plant Sci. 166: 185-198.
41. KOTILAINEN, M., P. ELOMAA, A. UIMARI, V. A. ALBERT, D. YU et al., 2000 GRCD1, an AGL2-like MADS box gene, participates in the C function during stamen development in Gerbera hybrida. Plant Cell 12: 1893-1902.
42. KRAMER, E. M., R. L. DORIT and V. F. IRISH, 1998 Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149: 765-783.
43. KRAMER, E. M., V. S. DI STILIO and P. M. SCHLUTER, 2003 Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. Int. J. Plant Sci. 164: 1-11.
44. KRAMER, E. M., M. A. JARAMILLO and V. S. DI STILIO, 2004 Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166: 1011-1023.
45. KU, H. M., T. VISION, J. LIU and S. D. TANKSLEY, 2000 Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny. Proc. Natl. Acad. Sci. USA 97: 9121-9126.
46. LAMB, R. S., and V. F. IRISH, 2003 Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc. Natl. Acad. Sci. USA 100: 6558-6563.
47. LAWTON-RAUH, A. L., E. R. ALVAREZ-BUYLLA and M. D. PURUGGANAN, 2000 Molecular evolution of flower development. Trends Ecol. Evol. 15: 144-149.
48. LEMMETYINEN, J., M. HASSINEN, A. ELO, I. PORALI, K. KEINONEN et al., 2004 Functional characterization of SEPALLATA3 and AGAMOUS orthologues in silver birch. Physiol. Plant 121: 149-162.
49. LITT, A., and V. F. IRISH, 2003 Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165: 821-833.
50. LYNCH, M., and A. FORCE, 2000 The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459-473.
51. MA, H., 1994 The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Dev. 8: 745-756.
52. MA, H., and C. DEPAMPHILIS, 2000 The ABCs of floral evolution. Cell 101: 5-8.
53. MA, H., M. F. YANOFSKY and E. M. MEYEROWITZ, 1991 AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev. 5: 484-495.
54. MADDISON, W. P., and D. R. MADDISON, 1989 Interactive analysis of phylogeny and character evolution using the computer program MacClade. Folia Primatol. 53: 190-202.
55. MALCOMBER, S. T., and E. A. KELLOGG, 2004 Heterogeneous expression patterns and separate roles of the SEPALLATA gene LEAFY HULL STERILE1 in grasses. Plant Cell 16: 1692-1706.
56. MANDEL, M. A., and M. F. YANOFSKY, 1998 The Arabidopsis AGL9 MADS box gene is expressed in young flower primordia. Sex. Plant Reprod. 11: 22-28.
57. MARTINEZ-CASTILLA, L. P., and E. R. ALVAREZ-BUYLLA, 2003 Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny. Proc. Natl. Acad. Sci. USA 100: 13407-13412.
58. MATHEWS, S., and M. J. DONOGHUE, 1999 The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286: 947-950.
59. MOURADOV, A., T. V. GLASSICK, B. A. HAMDORF, L. C. MURPHY, S. S. MARLA et al., 1998 Family of MADS-Box genes expressed early in male and female reproductive structures of monterey pine. Plant Physiol. 117: 55-62.
60. NAM, J., C. W. DEPAMPHILIS, H. MA and M. NEI, 2003 Antiquity and evolution of the MADS-box gene family controlling flower development in plants. Mol. Biol. Evol. 20: 1435-1447.
61. NAM, J., J. KIM, S. LEE, G. AN, H. MA et al., 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: 1910-1915.
62. NICHOLAS, K. B., H. B. NICHOLAS, JR, and D. W. DEERFIELD, II, 1997 GeneDoc: analysis and visualization of genetic variation. EMB-NEW.NEWS 4: 14.
63. PARENICOVA, L., S. DE FOLTER, M. KIEFFER, D. S. HORNER, C. FAVALLI el al., 2003 Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15: 1538-1551.
64. PELAZ, S., G. S. DITTA, E. BAUMANN, E. WISMAN and M. F. YANOFSKY, 2000 B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405: 200-203.
65. PELAZ, S., C. GUSTAFSON-BROWN, S. E. KOHALMI, W. L. CROSBY and M. F. YANOFSKY, 2001a APETALA1 and SEPALLATA3 interact to promote flower development. Plant J. 26: 385-394.
66. PELAZ, S., R. TAPIA-LOPEZ, E. R. ALVAREZ-BUYLLA and M. F. YANOFSKY, 2001b Conversion of leaves into petals in Arabidopsis. Curr. Biol. 11: 182-184.
67. POSADA, D., and K. A. CRANDALL, 1998 MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
68. PURUGGANAN, M. D., 1998 The molecular evolution of development. BioEssays 20: 700-711.
69. QIU, Y. L., J. LEE, F. BERNASCONI-QUADRONI, D. E. SOLTIS, P. S. SOLTIS et al., 1999 The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402: 404-407.
70. RIECHMANN, J. L., and E. M. MEYEROWITZ, 1997 Determination of floral organ identity by Arabidopsis MADS domain homeotic proteins API, AP3, PI, and AG is independent of their DNA-binding specificity. Mol. Biol. Cell 8: 1243-1259.
71. SAVIDGE, B., S. D. ROUNSLEY and M. F. YANOFSKY, 1995 Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7: 721-733.
72. SHANNON, S., and D. R. MEEKS-WAGNER, 1993 Genetic interactions that regulate inflorescence development in Arabidopsis. Plant Cell 5: 639-655.
73. SHCHENNIKOVA, A. V., O. A. SHULGA, R. IMMINK, K. G. SKRYABIN and G. C. ANGENENT, 2004 Identification and characterization of four chrysanthemum MADS-box genes, belonging to the APETALA1/FRUITFULL and SEPALLATA3 subfamilies. Plant Physiol. 134:1632-1641.
74. SMYTH, D. R., J. L. BOWMAN and E. M. MEYEROWITZ, 1990 Early flower development in Arabidopsis. Plant Cell 2: 755-767.
75. SOLTIS, P. S., D. E. SOLTIS and M. W. CHASE, 1999 Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402: 402-404.
76. SOLTIS, D. E., P. S. SOLTIS, M. W. CHASE, M. E. MORT, D. C. ALBACH et al., 2000 Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. 133: 381-461.
77. SOLTIS, D. E., P. S. SOLTIS, V. A. ALBERT, D. G. OPPENHEIMER, C. W. DEPAMPHILIS et al., 2002 Missing links: the genetic architecture of flowers and floral diversification. Trends Plant Sci. 7: 22-31.
78. SOLTIS, D. E., V. A. ALBERT, S. KIM, M.-J. YOO, P. S. SOLTIS et al., 2005 Evolution of the flower, pp. 165-200 in Diversity and Evolution of Plants, edited by R. HENRY. CABI Publishers, Wallingford, UK.
79. SPOONER, D. M., G. J. ANDERSON and R. K. JANSEN, 1993 Chloroplast DNA evidence for the interrelationships of tomatoes, potatoes, and pepinos (Solanaceae). Am. J. Bot. 80: 676-688.
80. STELLARI, G. M., M. A. JARAMILLO and E. M. KRAMER, 2004 Evolution of the APETALA3 and PISTILLATA lineages of MADS-box-containing genes in the basal angiosperms. Mol. Biol. Evol. 21: 506-519.
81. SUNG, S. K., G. H. YU, J. NAM, D. H. JEONG and G. AN, 2000 Developmentally regulated expression of two MADS-box genes, MdMADS3 and MdMADS4, in the morphogenesis of flower buds and fruits in apple. Planta 210: 519-528.
82. SWOFFORD, D. L., 1993 PAUP: a computer program for phylogenetic inference using maximum parsimony. J. Gen. Physiol. 102: A9.
83. TANDRE, K., V. A. ALBERT, A. SUNDAS and P. ENGSTROM, 1995 Conifer homologues to genes that control floral development in angiosperms. Plant Mol. Biol. 27: 69-78.
84. THEISSEN, G., 2001 Development of floral organ identity: stories from the MADS house. Curr. Opin. Plant Biol. 4: 75-85.
85. THEISSEN, G., and H. SAEDLER, 2001 Plant biology. Floral quartets. Nature 409: 469-471.
86. THEISSEN, G., J. T. KIM and H. SAEDLER, 1996 Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J. Mol. Evol. 43: 484-516.
87. THEISSEN, G., A. BECKER, A. DI ROSA, A. KANNO, J. T. KIM et al., 2000 A short history of MADS-box genes in plants. Plant Mol. Biol. 42: 115-149.
88. UIMARI, A., M. KOTILAINEN, P. ELOMAA, D. YU, V. A. ALBERT et al., 2004 Integration of reproductive meristem fates by a SEPALLATA-like MADS-box gene. Proc. Natl. Acad. Sci. USA 101: 15817-15822.
89. VANDENBUSSCHE, M., G. THEISSEN, Y. VAN DE PEER and T. GERATS, 2003a Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acids Res. 31: 4401-4409.
90. VANDENBUSSCHE, M., J. ZETHOF, E. SOUER, R. KOES, G. B. TORNIELLI et al., 2003b Toward the analysis of the petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C, and D floral organ identity functions require SEPALLATA-like MADS box genes in petunia. Plant Cell 15: 2680-2693.
91. WEIGEL, D., and E. M. MEYEROWITZ, 1994 The ABCs of floral homeotic genes. Cell 78: 203-209.
92. WINTER, K. U., C. WEISER, K. KAUFMANN, A. BOHNE, C. KIRCHNER et al., 2002 Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerization. Mol. Biol. Evol. 19: 587-596.
93. YANG, Y., L. FANNING and T. JACK, 2003 The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J. 33: 47-59.
94. YANG, Z., 1994 Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J. Mol. Evol. 39: 306-314.
95. YU, H., and C. J. GOH, 2000 Identification and characterization of three orchid MADS-box genes of the AP1/AGL9 subfamily during floral transition. Plant Physiol. 123: 1325-1336.
96. ZANIS, M. J., D. E. SOLTIS, P. S. SOLTIS, S. MATHEWS and M. J. DONOGHUE, 2002 The root of the angiosperms revisited. Proc. Natl. Acad. Sci. USA 99: 6848-6853.
97. ZHANG, L. Q., S. K. POND and B. S. GAUT, 2001 A survey of the molecular evolutionary dynamics of twenty-five multigene families from four grass taxa. J. Mol. Evol. 52: 144-156.
98. ZHAO, D., Q. YU, C. CHEN and H. MA, 2001 Genetic control of reproductive meristems, pp. 89-142 in Meristematic Tissues in Plant Growth and Development, edited by M. T. MCMANUS and B. VEIT. Sheffield Academic Press, Sheffield, UK.