MADS reloaded: Evolution of the AGAMOUS subfamily genes

New Phytologist

Volumn 201, Issue 3, 2014, Pages 717-732

  Dreni, Ludovico ^a   Kater, Martin M ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

AGAMOUS; Development; Evolution; Reproductive organ; Seed plants

Indexed keywords

EVOLUTIONARY BIOLOGY; PROTEIN; SEED;

SPERMATOPHYTA;

MADS DOMAIN PROTEIN;

AGAMOUS; DEVELOPMENT; EVOLUTION; FLOWER; FRUIT; GENETICS; GENITAL SYSTEM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; PLANT GENE; REVIEW; SEED PLANT;

AGAMOUS; DEVELOPMENT; EVOLUTION; REPRODUCTIVE ORGAN; SEED PLANTS;

EVOLUTION, MOLECULAR; FLOWERS; FRUIT; GENES, PLANT; MADS DOMAIN PROTEINS; PHYLOGENY;

EID: 84891901721     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12555     Document Type: Review

References (158)

1. Airoldi CA, Bergonzi S, Davies B. 2010. Single amino acid change alters the ability to specify male or female organ identity. Proceedings of the National Academy of Sciences, USA 107: 18898-18902.
2. Airoldi CA, Davies B. 2012. Gene duplication and the evolution of plant MADS-box transcription factors. Journal of Genetics and Genomics 39: 157-165.
3. Alvarez J, Smyth DR. 1999. CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126: 2377-2386.
4. Álvarez-Buylla ER, Ambrose BA, Flores-Sandoval E, Englund M, Garay-Arroyo A, García-Ponce B, de la Torre-Bárcena E, Espinosa-Matías S, Martínez E, Piñeyro-Nelson A et al. 2010. B-function expression in the flower center underlies the homeotic phenotype of Lacandonia schismatica (Triuridaceae). Plant Cell 22: 3543-3559.
5. Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ. 2000. Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Molecular Cell 5: 569-579.
6. Angenent GC, Franken J, Busscher M, van Dijken A, van Went JL, Dons HJ, van Tunen AJ. 1995. A novel class of MADS box genes is involved in ovule development in petunia. Plant Cell 7: 1569-1582.
7. Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S. 2007. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8: 242.
8. Barker EI, Ashton NW. 2013. A parsimonious model of lineage-specific expansion of MADS-box genes in Physcomitrella patens. Plant Cell Reports. 32: 1161-1177.
9. Baum SF, Eshed Y, Bowman JL. 2001. The Arabidopsis nectary is an ABC-independent floral structure. Development 128: 4657-4667.
10. Becker A, Theissen G. 2003. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Molecular Phylogenetics and Evolution 29: 464-489.
11. Boss PK, Sensi E, Hua C, Davies C, Thomas MR. 2002. Cloning and characterisation of grapevine (Vitis vinifera L.) MADS-box genes expressed during inflorescence and berry development. Plant Science 162: 887-895.
12. Bowman JL, Drews GN, Meyerowitz EM. 1991b. Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell 3: 749-758.
13. Bowman JL, Sakai H, Jack T, Weigel D, Mayer U, Meyerowitz EM. 1992. SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114: 599-615.
14. Bowman JL, Smyth DR. 1999. CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126: 2387-2396.
15. Bowman JL, Smyth DR, Meyerowitz EM. 1989. Genes directing flower development in Arabidopsis. Plant Cell 1: 37-52.
16. Bowman JL, Smyth DR, Meyerowitz EM. 1991a. Genetic interactions among floral homeotic genes of Arabidopsis. Development 112: 1-20.
17. Brambilla V, Battaglia R, Colombo M, Masiero S, Bencivenga S, Kater MM, Colombo L. 2007. Genetic and molecular interactions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell 19: 2544-2556.
18. Brunner AM, Rottmann WH, Sheppard LA, Krutovskii K, DiFazio SP, Leonardi S, Strauss SH. 2000. Structure and expression of duplicate AGAMOUS orthologues in poplar. Plant Molecular Biology 44: 619-634.
19. Busch MA, Bomblies K, Weigel D. 1999. Activation of a floral homeotic gene in Arabidopsis. Science 285: 585-587.
20. Causier B, Bradley D, Cook H, Davies B. 2009. Conserved intragenic elements were critical for the evolution of the floral C-function. Plant Journal 58: 41-52.
21. Causier B, Castillo R, Zhou J, Ingram R, Xue Y, Schwarz-Sommer Z, Davies B. 2005. Evolution in action: following function in duplicated floral homeotic genes. Current Biology 15: 1508-1512.
22. Coen ES, Meyerowitz EM. 1991. The war of the whorls: genetic interactions controlling flower development. Nature 353: 31-37.
23. Colombo L, Franken J, Koetje E, van Went J, Dons HJ, Angenent GC, van Tunen AJ. 1995. The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7: 1859-1868.
24. Colombo L, Franken J, Van der Krol AR, Wittich PE, Dons HJ, Angenent GC. 1997. Downregulation of ovule-specific MADS box genes from petunia results in maternally controlled defects in seed development. Plant Cell 9: 703-715.
25. Colombo L, Battaglia R, Kater MM. 2008. Arabidopsis ovule development and its evolutionary conservation. Trends in Plant Science 13: 444-450.
26. Colombo M, Brambilla V, Marcheselli R, Caporali E, Kater MM, Colombo L. 2010. A new role for the SHATTERPROOF genes during Arabidopsis gynoecium development. Developmental Biology 337: 294-302.
27. Cooper B, Clarke JD, Budworth P, Kreps J, Hutchison D, Park S, Guimil S, Dunn M, Luginbühl P, Ellero C et al. 2003. A network of rice genes associated with stress response and seed development. Proceedings of the National Academy of Sciences, USA 100: 4945-4950.
28. Cui R, Han J, Zhao S, Su K, Wu F, Du X, Xu Q, Chong K, Theissen G, Meng Z. 2010. Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa). Plant Journal 61: 767-781.
29. Davies B, Egea-Cortines M, de Andrade SilvaE, Saedler H, Sommer H. 1996. Multiple interactions amongst floral homeotic MADS box proteins. EMBO Journal 15: 4330-4343.
30. 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 Journal 18: 4023-4034.
31. Di Stilio VS, Kramer EM, Baum DA. 2005. Floral MADS box genes and homeotic gender dimorphism in Thalictrum dioicum (Ranunculaceae) - a new model for the study of dioecy. Plant Journal 41: 755-766.
32. Dinh TT, Girke T, Liu X, Yant L, Schmid M, Chen X. 2012. The floral homeotic protein APETALA2 recognizes and acts through an AT-rich sequence element. Development 139: 1978-1986.
33. Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF. 2004. The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Current Biology 14: 1935-1940.
34. Dreni L, Jacchia S, Fornara F, Fornari M, Ouwerkerk PB, An G, Colombo L, Kater MM. 2007. The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice. Plant Journal 52: 690-699.
35. Dreni L, Osnato M, Kater MM. 2013. The ins and outs of the rice AGAMOUS subfamily. Molecular Plant 6: 650-664.
36. Dreni L, Pilatone A, Yun D, Erreni S, Pajoro A, Caporali E, Zhang D, Kater MM. 2011. Functional analysis of all AGAMOUS subfamily members in rice reveals their roles in reproductive organ identity determination and meristem determinacy. Plant Cell 23: 2850-2863.
37. Drews GN, Bowman JL, Meyerowitz EM. 1991. Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65: 991-1002.
38. Elitzur T, Vrebalov J, Giovannoni JJ, Goldschmidt EE, Friedman H. 2010. The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene. Journal of Experimental Botany 61: 1523-1535.
39. Englund M, Carlsbecker A, Engström P, Vergara-Silva F. 2011. Morphological "primary homology" and expression of AG-subfamily MADS-box genes in pines, podocarps, and yews. Evolution & Development 13: 171-181.
40. Favaro R, Immink RG, Ferioli V, Bernasconi B, Byzova M, Angenent GC, Kater M, Colombo L. 2002. Ovule-specific MADS-box proteins have conserved protein-protein interactions in monocot and dicot plants. Molecular Genetics and Genomics 268: 152-159.
41. 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: 2603-2611.
42. Ferrario S, Immink RG, Shchennikova A, Busscher-Lange J, Angenent GC. 2003. The MADS box gene FBP2 is required for SEPALLATA function in petunia. Plant Cell 15: 914-925.
43. Ferrario S, Shchennikova AV, Franken J, Immink RG, Angenent GC. 2006. Control of floral meristem determinacy in petunia by MADS-box transcription factors. Plant Physiology 140: 890-898.
44. Flanagan CA, Hu Y, Ma H. 1996. Specific expression of the AGL1 MADS-box gene suggests regulatory functions in Arabidopsis gynoecium and ovule development. Plant Journal 10: 343-353.
45. Fourquin C, Del Cerro C, Victoria FC, Vialette-Guiraud A, de Oliveira AC, Ferrándiz C. 2013. A change in SHATTERPROOF protein lies at the origin of a fruit morphological novelty and a new strategy for seed dispersal in Medicago genus. Plant Physiology 162: 907-917.
46. Fourquin C, Ferrándiz C. 2012. Functional analyses of AGAMOUS family members in Nicotiana benthamiana clarify the evolution of early and late roles of C-function genes in eudicots. Plant Journal 71: 990-1001.
47. Garay-Arroyo A, Piñeyro-Nelson A, García-Ponce B, Sánchez Mde L, Álvarez-Buylla ER. 2012. When ABC becomes ACB. Journal of Experimental Botany 63: 2377-2395.
48. Giménez E, Pineda B, Capel J, Antón MT, Atarés A, Pérez-Martín F, García-Sogo B, Angosto T, Moreno V, Lozano R. 2010. Functional analysis of the Arlequin mutant corroborates the essential role of the Arlequin/TAGL1 gene during reproductive development of tomato. PLoS One 5: e14427.
49. Gómez-Mena C, de Folter S, Costa MM, Angenent GC, Sablowski R. 2005. Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132: 429-438.
50. Gramzow L, Ritz MS, Theissen G. 2010. On the origin of MADS-domain transcription factors. Trends in Genetics 26: 149-153.
51. Gramzow L, Barker E, Schulz C, Ambrose B, Ashton N, Theißen G, Litt A. 2012. Selaginella genome analysis - entering the "homoplasy heaven" of the MADS world. Frontiers in Plant Science 3: 214.
52. Gregis V, Sessa A, Colombo L, Kater MM. 2006. AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell 18: 1373-1382.
53. Gregis V, Sessa A, Dorca-Fornell C, Kater MM. 2009. The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes. Plant Journal 60: 626-637.
54. Hands P, Vosnakis N, Betts D, Irish VF, Drea S. 2011. Alternate transcripts of a floral developmental regulator have both distinct and redundant functions in opium poppy. Annals of Botany 107: 1557-1566.
55. Heijmans K, Ament K, Rijpkema AS, Zethof J, Wolters-Arts M, Gerats T, Vandenbussche M. 2012b. Redefining C and D in the petunia ABC. Plant Cell 24: 2305-2317.
56. Heijmans K, Morel P, Vandenbussche M. 2012a. MADS-box genes and floral development: the dark side. Journal of Experimental Botany 63: 5397-5404.
57. Hong RL, Hamaguchi L, Busch MA, Weigel D. 2003. Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing. Plant Cell 15: 1296-1309.
58. Honma T, Goto K. 2001. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409: 525-529.
59. Hu J, Zhang J, Shan H, Chen Z. 2012. Expression of floral MADS-box genes in Sinofranchetia chinensis (Lardizabalaceae): implications for the nature of the nectar leaves. Annals of Botany 110: 57-69.
60. Hu L, Liang W, Yin C, Cui X, Zong J, Wang X, Hu J, Zhang D. 2011. Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23: 515-533.
61. Ikeda K, Ito M, Nagasawa N, Kyozuka J, Nagato Y. 2007. Rice ABERRANT PANICLE ORGANIZATION 1, encoding an F-box protein, regulates meristem fate. Plant Journal 51: 1030-1040.
62. Ikeda K, Nagasawa N, Nagato Y. 2005. ABERRANTPANICLEORGANIZATION 1 temporally regulates meristem identity in rice. Developmental Biology 282: 349-360.
63. Ikeda M, Mitsuda N, Ohme-Takagi M. 2009. Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21: 3493-3505.
64. Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A. 2009. TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant Journal 60: 1081-1095.
65. Ito T, Ng KH, Lim TS, Yu H, Meyerowitz EM. 2007. The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell 19: 3516-3529.
66. Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann JL, Meyerowitz EM. 2004. The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430: 356-360.
67. Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK. 1994. Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6: 1211-1225.
68. Kang HG, Jang S, Chung JE, Cho YG, An G. 1997. Characterization of two rice MADS boxgenes that control flowering time. Molecules and Cells 7: 559-566.
69. Kater MM, Colombo L, Franken J, Busscher M, Masiero S, Van Lookeren Campagne MM, Angenent GC. 1998. Multiple AGAMOUS homologs from cucumber and petunia differ in their ability to induce reproductive organ fate. Plant Cell 10: 171-182.
70. Kaufmann K, Melzer R, Theissen G. 2005. MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347: 183-198.
71. Kaufmann K, Muiño JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC. 2009. Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biology 7: e1000090.
72. Kempin SA, Mandel MA, Yanofsky MF. 1993. Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic gene NAG1. Plant Physiology 103: 1041-1046.
73. Kooiker M, Airoldi CA, Losa A, Manzotti PS, Finzi L, Kater MM, Colombo L. 2005. BASIC PENTACYSTEINE1, a GA binding protein that induces conformational changes in the regulatory region of the homeotic Arabidopsis gene SEEDSTICK. Plant Cell 17: 722-729.
74. Koornneef M, de Bruine JH, Goettsch P. 1980. A provisional map of chromosome 4 of Arabidopsis. Arabidopsis Information Service 17: 11-18.
75. 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: 1011-1023.
76. Krogan NT, Hogan K, Long JA. 2012. APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 139: 4180-4190.
77. Lee JY, Baum SF, Alvarez J, Patel A, Chitwood DH, Bowman JL. 2005. Activation of CRABS CLAW in the nectaries and carpels of Arabidopsis. Plant Cell 17: 25-36.
78. Lenhard M, Bohnert A, Jürgens G, Laux T. 2001. Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105: 805-814.
79. Leseberg CH, Li A, Kang H, Duvall M, Mao L. 2006. Genome-wide analysis of the MADS-box gene family in Populus trichocarpa. Gene 378: 84-94.
80. Li H, Liang W, Hu Y, Zhu L, Yin C, Xu J, Dreni L, Kater MM, Zhang D. 2011b. Rice MADS6 interacts with the floral homeotic genes SUPERWOMAN1, MADS3, MADS58, MADS13, and DROOPING LEAF in specifying floral organ identities and meristem fate. Plant Cell 23: 2536-2552.
81. Li H, Liang W, Yin C, Zhu L, Zhang D. 2011a. Genetic interaction of OsMADS3, DROOPING LEAF, and OsMADS13 in specifying rice floral organ identities and meristem determinacy. Plant Physiology 156: 263-274.
82. Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF. 2000. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404: 766-770.
83. van der Linden CG, Vosman B, Smulders MJ. 2002. Cloning and characterization of four apple MADS box genes isolated from vegetative tissue. Journal of Experimental Botany 53: 1025-1036.
84. Linkies A, Graeber K, Knight C, Leubner-Metzger G. 2010. The evolution of seeds. New Phytologist 186: 817-831.
85. Liu J, Xu B, Hu L, Li M, Su W, Wu J, Yang J, Jin Z. 2009. Involvement of a banana MADS-box transcription factor gene in ethylene-induced fruit ripening. Plant Cell Reports 28: 103-111.
86. Liu JH, Zhang J, Jia CH, Zhang JB, Wang JS, Yang ZX, Xu BY, Jin ZQ. 2013. The interaction of banana MADS-box protein MuMADS1 and ubiquitin-activating enzyme E-MuUBA in post-harvest banana fruit. Plant Cell Reports 32: 129-137.
87. Liu X, Anderson J, Pijut P. 2010b. Cloning and characterization of Prunus serotina AGAMOUS, a putative flower homeotic gene. Plant Molecular Biology Reporter 28: 193-203.
88. Liu X, Kim YJ, Müller R, Yumul RE, Liu C, Pan Y, Cao X, Goodrich J, Chen X. 2011. AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb Group proteins. Plant Cell 23: 3654-3670.
89. Liu X, Zuo KJ, Xu JT, Li Y, Zhang F, Yao HY, Wang Y, Chen Y, Qiu CX, Sun XF, Tang KX. 2010a. Functional analysis of GbAGL1, a D-lineage gene from cotton (Gossypium barbadense). Journal of Experimental Botany 61: 1193-1203.
90. Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D. 2001. A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105: 793-803.
91. Lovisetto A, Guzzo F, Tadiello A, Toffali K, Favretto A, Casadoro G. 2012. Molecular analyses of MADS-box genes trace back to Gymnosperms the invention of fleshy fruits. Molecular Biology and Evolution 29: 409-419.
92. Ma H, Yanofsky MF, Meyerowitz EM. 1991. AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes & Development 5: 484-495.
93. Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y. 2005. Modeling gene and genome duplications in eukaryotes. Proceedings of the National Academy of Sciences, USA 102: 5454-5459.
94. Malcomber ST, Kellogg EA. 2005. SEPALLATA gene diversification: brave new whorls. Trends in Plant Science 10: 427-435.
95. Mandel MA, Bowman JL, Kempin SA, Ma H, Meyerowitz EM, Yanofsky MF. 1992. Manipulation of flower structure in transgenic tobacco. Cell 71: 133-143.
96. Matias-Hernandez L, Battaglia R, Galbiati F, Rubes M, Eichenberger C, Grossniklaus U, Kater MM, Colombo L. 2010. VERDANDI is a direct target of the MADS domain ovule identity complex and affects embryo sac differentiation in Arabidopsis. Plant Cell 22: 1702-1715.
97. Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T. 1998. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95: 805-815.
98. Mejía N, Soto B, Guerrero M, Casanueva X, Houel C, Miccono Mde L, Ramos R, Le Cunff L, Boursiquot JM, Hinrichsen P et al. 2011. Molecular, genetic and transcriptional evidence for a role of VvAGL11 in stenospermocarpic seedlessness in grapevine. BMC Plant Biology 11: 57.
99. Melzer R, Theissen G. 2009. Reconstitution of 'floral quartets' in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Research 37: 2723-2736.
100. Melzer R, Verelst W, Theissen G. 2009. The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in 'floral quartet'-like complexes in vitro. Nucleic Acids Research 37: 144-157.
101. Mena M, Ambrose BA, Meeley RB, Briggs SP, Yanofsky MF, Schmidt RJ. 1996. Diversification of C-function activity in maize flower development. Science 274: 1537-1540.
102. Mendes MA, Guerra RF, Berns MC, Manzo C, Masiero S, Finzi L, Kater MM, Colombo L. 2013. MADS domain transcription factors mediate short-range DNA looping that is essential for target gene expression in Arabidopsis. Plant Cell 25: 2560-2572.
103. Meyerowitz EM, Bowman JL, Brockman LL, Drews GN, Jack T, Sieburth LE, Weigel D. 1991. A genetic and molecular model for flower development in Arabidopsis thaliana. Development Supplement 1: 157-167.
104. Mizukami Y, Ma H. 1995. Separation of AG function in floral meristem determinacy from that in reproductive organ identity by expressing antisense AG RNA. Plant Molecular Biology 28: 767-784.
105. Mizzotti C, Mendes MA, Caporali E, Schnittger A, Kater MM, Battaglia R, Colombo L. 2012. The MADS box genes SEEDSTICK and ARABIDOPSIS Bsister play a maternal role in fertilization and seed development. Plant Journal 70: 409-420.
106. Monfared MM, Carles CC, Rossignol P, Pires HR, Fletcher JC. 2013. The ULT1 and ULT2 trxG genes play overlapping roles in Arabidopsis development and gene regulation. Molecular Plant 6: 1564-1579.
107. Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN. 2010. Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329: 1306-1311.
108. Münster T, Deleu W, Wingen LU, Ouzunova M, Cacharrón J, Faigl W, Werth S, Kim JTT, Saedler H, Theissen G. 2002. Maize MADS-box genes galore. Maydica 47: 287-301.
109. Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H, Sakai H, Nagato Y. 2003. SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130: 705-718.
110. Nesi N, Debeaujon I, Jond C, Stewart AJ, Jenkins GI, Caboche M, Lepiniec L. 2002. The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14: 2463-2479.
111. O'Maoiléidigh DS, Wuest SE, Rae L, Raganelli A, Ryan PT, Kwasniewska K, Das P, Lohan AJ, Loftus B, Graciet E et al. 2013. Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS. Plant Cell 25: 2482-2503.
112. Pabón-Mora N, Litt A. 2011. Comparative anatomical and developmental analysis of dry and fleshy fruits of Solanaceae. American Journal of Botany 98: 1415-1436.
113. Pan IL, McQuinn R, Giovannoni JJ, Irish VF. 2010. Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. Journal of Experimental Botany 61: 1795-1806.
114. Parenicová L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B et 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.
115. 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: 200-203.
116. Pelaz S, Tapia-López R, Alvarez-Buylla ER, Yanofsky MF. 2001. Conversion of leaves into petals in Arabidopsis. Current Biology 11: 182-184.
117. Perl-Treves R, Kahana A, Rosenman N, Xiang Y, Silberstein L. 1998. Expression of multiple AGAMOUS-like genes in male and female flowers of cucumber (Cucumis sativus L.). Plant and Cell Physiology 39: 701-710.
118. Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF. 2003. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424: 85-88.
119. 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: 163-173.
120. Rosin FMA, Aharoni A, Salentijn EMJ, Schaart JG, Boone MJ, Hannapel DJ. 2003. Expression Patterns of a putative homolog of AGAMOUS, STAG1, from Strawberry. Plant Science 165: 959-968.
121. Rounsley SD, Ditta GS, Yanofsky MF. 1995. Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7: 1259-1269.
122. Roy Choudhury S, Roy S, Nag A, Singh SK, Sengupta DN. 2012. Characterization of an AGAMOUS-like MADS box protein, a probable constituent of flowering and fruit ripening regulatory system in banana. PLoS One 7: e44361.
123. Sakai H, Krizek BA, Jacobsen SE, Meyerowitz EM. 2000. Regulation of SUP expression identifies multiple regulators involved in Arabidopsis floral meristem development. Plant Cell 12: 1607-1618.
124. Sakai H, Medrano LJ, Meyerowitz EM. 1995. Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378: 199-203.
125. Samach A, Klenz JE, Kohalmi SE, Risseeuw E, Haughn GW, Crosby WL. 1999. The UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-box protein required for normal patterning and growth in the floral meristem. Plant Journal 20: 433-445.
126. Sang X, Li Y, Luo Z, Ren D, Fang L, Wang N, Zhao F, Ling Y, Yang Z, Liu Y, He G. 2012. CHIMERIC FLORAL ORGANS1, encoding a monocot-specific MADS box protein, regulates floral organ identity in rice. Plant Physiology 160: 788-807.
127. Savidge B, Rounsley SD, Yanofsky MF. 1995. Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7: 721-733.
128. Schmidt RJ, Veit B, Mandel MA, Mena M, Hake S, Yanofsky MF. 1993. Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell 5: 729-737.
129. Schultz EA, Pickett FB, Haughn GW. 1991. The FLO10 gene product regulates the expression domain of homeotic genes AP3 and PI in Arabidopsis flowers. Plant Cell 3: 1221-1237.
130. Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H. 1990. Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250: 931-936.
131. Sieburth LE, Running MP, Meyerowitz EM. 1995. Genetic separation of third and fourth whorl functions of AGAMOUS. Plant Cell 7: 1249-1258.
132. Simonini S, Roig-Villanova I, Gregis V, Colombo B, Colombo L, Kater MM. 2012. Basic pentacysteine proteins mediate MADS domain complex binding to the DNA for tissue-specific expression of target genes in Arabidopsis. Plant Cell 24: 4163-4172.
133. Singh R, Low ET, Ooi LC, Ong-Abdullah M, Ting NC, Nagappan J, Nookiah R, Amiruddin MD, Rosli R, Manaf MA et al. 2013. The oil palm SHELL gene controls oil yield and encodes a homologue of SEEDSTICK. Nature 500: 340-344.
134. Smaczniak C, Immink RG, Angenent GC, Kaufmann K. 2012a. Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139: 3081-3098.
135. Smaczniak C, Immink RG, Muiño JM, Blanvillain R, Busscher M, Busscher-Lange J, Dinh QD, Liu S, Westphal AH, Boeren S. 2012b. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proceedings of the National Academy of Sciences, USA 109: 1560-1565.
136. Sridhar VV, Surendrarao A, Gonzalez D, Conlan RS, Liu Z. 2004. Transcriptional repression of target genes by LEUNIG and SEUSS, two interacting regulatory proteins for Arabidopsis flower development. Proceedings of the National Academy of Sciences, USA 101: 11494-11499.
137. Sridhar VV, Surendrarao A, Liu Z. 2006. APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133: 3159-3166. Erratum in: Development 133: 3496.
138. Sun B, Xu Y, Ng KH, Ito T. 2009. A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes & Development 23: 1791-1804.
139. Tadiello A, Pavanello A, Zanin D, Caporali E, Colombo L, Rotino GL, Trainotti L, Casadoro G. 2009. A PLENA-like gene of peach is involved in carpel formation and subsequent transformation into a fleshy fruit. Journal of Experimental Botany 60: 651-661.
140. Tani E, Polidoros AN, Tsaftaris AS. 2007. Characterization and expression analysis of FRUITFULL- and SHATTERPROOF-like genes from peach (Prunus persica) and their role in split-pit formation. Tree Physiology 27: 649-659.
141. Theissen G. 2001. Development of floral organ identity: stories from the MADS house. Current Opinion in Plant Biology 4: 75-85.
142. Theissen G, Kim JT, Saedler H. 1996. Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. Journal of Molecular Evolution 43: 484-516.
143. Theissen G, Saedler H. 2001. Plant biology. Floral quartets. Nature 409: 469-471.
144. Theissen G, Strater T, Fischer A, Saedler H. 1995. Structural characterization, chromosomal localization and phylogenetic evaluation of two pairs of AGAMOUS-like MADS-box genes from maize. Gene 156: 155-166.
145. Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig WE, Saedler H, Sommer H, Schwarz-Sommer Z. 1992. GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO Journal 11: 4693-4704.
146. Tsuchimoto S, van der Krol AR, Chua NH. 1993. Ectopic expression of pMADS3 in transgenic petunia phenocopies the petunia blind mutant. Plant Cell 5: 843-853.
147. Vandenbussche M, Zethof J, Souer E, Koes R, Tornielli GB, Pezzotti M, Ferrario S, Angenent GC, Gerats T. 2003. 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.
148. Vrebalov J, Pan IL, Arroyo AJ, McQuinn R, Chung M, Poole M, Rose J, Seymour G, Grandillo S, Giovannoni J, Irish VF. 2009. Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell 21: 3041-3062.
149. Wang ZF, Ren Y. 2008. Ovule morphogenesis in Ranunculaceae and its systematic significance. Annals of Botany 101: 447-462.
150. Western TL, Haughn GW. 1999. BELL1 and AGAMOUS genes promote ovule identity in Arabidopsis thaliana. Plant Journal 18: 329-336.
151. Wuest SE, O'Maoileidigh DS, Rae L, Kwasniewska K, Raganelli A, Hanczaryk K, Lohan AJ, Loftus B, Graciet E, Wellmer F. 2012. Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proceedings of the National Academy of Sciences, USA 109: 13452-13457.
152. Yamaguchi T, Lee DY, Miyao A, Hirochika H, An G, Hirano HY. 2006. Functional diversification of the two C-class MADS box genes OSMADS3 and OSMADS58 in Oryza sativa. Plant Cell 18: 15-28.
153. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM. 1990. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346: 35-39.
154. Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen X, Schmid M. 2010. Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22: 2156-2170.
155. Yellina AL, Orashakova S, Lange S, Erdmann R, Leebens-Mack J, Becker A. 2010. Floral homeotic C function genes repress specific B function genes in the carpel whorl of the basal eudicot California poppy (Eschscholzia californica). Evodevo 1: 13.
156. Yun D, Liang W, Dreni L, Yin C, Zhou Z, Kater MM, Zhang D. 2013. OsMADS16 genetically interacts with OsMADS3 and OsMADS58 in specifying floral patterning in rice. Molecular Plant 6: 743-756.
157. Zahn LM, Kong H, 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: 2209-2223.
158. Zahn LM, Leebens-Mack JH, Arrington JM, Hu Y, Landherr LL, dePamphilis CW, Becker A, Theissen G, Ma H. 2006. Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evolution & Development 8: 30-45.