AGL6-like MADS-box genes are sister to AGL2-like MADS-box genes

Journal of Plant Biology

Volumn 56, Issue 5, 2013, Pages 315-325

  Kim, Sangtae ^a   Soltis, Pamela S ^b   Soltis, Douglas E ^b,c  

^a Korea Basic Science Institute (KBSI)   (South Korea)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

AGL2; AGL6; Gene phylogeny; MADS box; SQUA

Indexed keywords

EID: 84884752003     PISSN: 12269239     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12374-013-0147-x     Document Type: Article

References (74)

1. 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: 457-466.
2. APGIII (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161: 105-121.
3. 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: 464-489.
4. 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.
5. Chanderbali AS, Kim S, Buzgo M, Zheng Z, Oppenheimer DG, Soltis DE, Soltist PS (2006) Genetic footprints of stamen ancestors guide perianth evolution in Persea (Lauraceae). Int J Plant Sci 167: 1075-1089.
6. Coen ES, Meyerowitz EM (1991) The war of the whorls - genetic interactions controlling flower development. Nature 353: 31-37.
7. Colombo L, Franken J, Koetje E, Vanwent J, Dons HJM, Angenent GC, Vantunen AJ (1995) The Petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7: 1859-1868.
8. De Bodt S, Raes J, van de Peer YV, Theissen G (2003) And then there were many: MADS goes genomic. Trends Plant Sci 8: 475-483.
9. de Folter S, Immink RGH, Kieffer M, Paenicová L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17: 1424-1433.
10. 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: 1935-1940.
11. Donoghue MJ (2010) An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proc Natl Acad Sci USA 107: 5897-5902.
12. Doyle JA (2012) Molecular and fossil evidence on the origin of angiosperms. Annu Rev Earth Planet Sci 40: 301-326.
13. Fan J, Li W, Dong X, Guo W, Shu H (2007) Ectopic expression of a hyacinth AGL6 homolog caused earlier flowering and homeotic conversion in Arabidopsis. Sci China C Life Sci 50: 676-689.
14. Felsenstein J (1981) Evolutionary trees from DNA-sequences: a maximum-likelihood approach. J Mol Evol 17: 368-376.
15. Felsenstein J (1985) Confidence limits on phylogenies - an approach using the bootstrap. Evolution 39: 783-791.
16. Feng Q, Zhang Y, Hao P, Wang S, Fu G, Huang Y, Li Y, Zhu J, Liu Y, Hu X, Jia P, Zhao Q, Ying K, Yu S, Tang Y, Weng Q, Zhang L, Lu Y, Mu J, Zhang LS, Yu Z, Fan D, Liu X, Lu T, Li C, Wu Y, Sun T, Lei H, Li T, Hu H, Guan J, Wu M, Zhang R, Zhou B, Chen Z, Chen L, Jin Z, Wang R, Yin H, Cai Z, Ren S, Lv G, Gu W, Zhu G, Tu Y, Jia J, Chen J, Kang H, Chen X, Shao C, Sun Y, Hu Q, Zhang X, Zhang W, Wang L, Ding C, Sheng H, Gu J, Chen S, Ni L, Zhu F, Chen W, Lan L, Lai Y, Cheng Z, Gu M, Jiang J, Li J, Hong G, Xue Y, Han B (2002) Sequence and analysis of rice chromosome 4. Nature 420: 316-320.
17. 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.
18. 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. Front Plant Sci 3: 214.
19. Gu Q, Ferrandiz C, Yanofsky MF, Martienssen R (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125: 1509-1517.
20. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
21. Gustafsonbrown C, Savidge B, Yanofsky MF (1994) Regulation of the Arabidopsis floral homeotic gene APETALA1. Cell 76: 131-143.
22. Hecht V, Foucher F, Ferrandiz C, Macknight R, Navarro C, Morin J, Vardy ME, Ellis N, Beltran JP, Rameau C, Weller JL (2005) Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol 137: 1420-1434.
23. 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: 801-814.
24. Hileman LC, Sundstrom JF, Litt A, Chen M, Shumba T, Irish VF (2006) Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Mol Biol Evol 23: 2245-2258.
25. Hsu HF, Huang CH, Chou LT, Yang CH (2003) Ectopic expression of an orchid (Oncidium Gower Ramsey) AGL6-like gene promotes flowering by activating flowering time genes in Arabidopsis thaliana. Plant Cell Physiol 44: 783-794.
26. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
27. Kim S, Koh J, Yoo MJ, Kong HZ, Hu Y, Ma H, Soltis PS, Soltis DE (2005a) Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. Plant J 43: 724-744.
28. Kim S, Koh J, Ma H, Hu Y, Endress PK, Hauser BA, Buzgo M, Soltis PS, Soltis DE (2005b) Sequence and expression studies of A-, B-, and E-class MADS-box homologues in Eupomatia (Eupomatiaceae): support for the bracteate origin of the calyptra. Intl J Plant Sci 166: 185-198.
29. Koo SC, Bracko O, Park MS, Schwab R, Chun HJ, Park KM, Seo JS, Grbic V, Balasubramanian S, Schmid M, Godard F, Yun DJ, Lee SY, Cho MJ, Weigel D, Kim MC (2010) Control of lateral organ development and flowering time by the Arabidopsis thaliana MADS-box gene AGAMOUS-LIKE6. Plant J 62: 807-816.
30. Kotilainen M, Elomaa P, Uimari A, Albert VA, Yu D, Teeri TH (2000) GRCD1, an AGL2-like MADS box gene, participates in the C function during stamen development in Gerbera hybrida. Plant Cell 12: 1893-1902.
31. Kramer EM, Dorit RL, Irish VF (1999) Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 151: 915-915.
32. Kwantes M, Liebsch D, Verelst W (2012) How MIKC* MADS-box genes originated and evidence for their conserved function throughout the evolution of vascular plant gametophytes. Mol Biol Evol 29: 293-302.
33. Li H, Liang W, Jia R, Yin C, Zong J, Kong H, Zhang D (2010) The AGL6-like gene OsMADS6 regulates floral organ and meristem identities in rice. Cell Res 20: 299-313.
34. 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: 821-833.
35. 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: 484-495.
36. Magallon S (2010) Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Syst Biol 59: 384-399.
37. Mapes G, Rothwell GW (1984) Premineralized ovulate cones of Lebachia from the late Palaeozoic limestones of Kansas. Paleontology 27: 69-94.
38. Mapes G, Rothwell GW (1991) Structure and relationships of primitive conifers. Neues Jahrbuch für Geologie and Paläontologie-Abhandulungen 183: 269-287.
39. Mena M, Mandel MA, Lerner DR, Yanofsky MF, Schmidt RJ (1995) A characterization of the MADS-box gene family in maize. Plant J 8: 845-854.
40. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956.
41. Moon YH, Kang HG, Jung JY, Jeon JS, Sung SK, An G (1999) Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiol 120: 1193-1204.
42. Munster T, Pahnke J, DiRosa A, Kim JT, Martin W, Saedler H, Theissen G (1997) Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants. Proc Natl Acad Sci USA 94: 2415-2420.
43. Nam J, dePamphilis CW, Ma H, Nei M (2003) Antiquity and evolution of the MADS-box gene family controlling flower development in plants. Mol Biol Evol 20: 1435-1447.
44. Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2: 186-195.
45. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A, Vicedomini R, Sahlin K, Sherwood E, Elfstrand M, Gramzow L, Holmberg K, Hallman J, Keech O, Klasson L, Koriabine M, Kucukoglu M, Kaller M, Luthman J, Lysholm F, Niittyla T, Olson A, Rilakovic N, Ritland C, Rossello JA, Sena J, Svensson T, Talavera-Lopez C, Theissen G, Tuominen H, Vanneste K, Wu ZQ, Zhang B, Zerbe P, Arvestad L, Bhalerao R, Bohlmann J, Bousquet J, Garcia Gil R, Hvidsten TR, de Jong P, MacKay J, Morgante M, Ritland K, Sundberg B, Thompson SL, van de Peer Y, Andersson B, Nilsson O, Ingvarsson PK, Lundeberg J, Jansson S (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497: 579-584.
46. Ohmori S, Kimizu M, Sugita M, Miyao A, Hirochika H, Uchida E, Nagato Y, Yoshida H (2009) MOSAIC FLORAL ORGANS1, an AGL6-like MADS box gene, regulates floral organ identity and meristem fate in rice. Plant Cell 21: 3008-3025.
47. Paenicová L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (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.
48. 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.
49. Petersen K, Didion T, Andersen CH, Nielsen KK (2004) MADS-box genes from perennial ryegrass differentially expressed during transition from vegetative to reproductive growth. J Plant Physiol 161: 439-447.
50. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
51. Prakash AP, Kumar PP (2002) PkMADS1 is a novel MADS box gene regulating adventitious shoot induction and vegetative shoot development in Paulownia kawakamii. Plant J 29: 141-151.
52. Reinheimer R, Kellogg EA (2009) Evolution of AGL6-like MADS box genes in grasses (Poaceae): ovule expression is ancient and palea expression is new. Plant Cell 21: 2591-2605.
53. 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: 1243-1259.
54. Rijpkema AS, Zethof J, Gerats T, Vandenbussche M (2009) The petunia AGL6 gene has a SEPALLATA-like function in floral patterning. Plant J 60: 1-9.
55. Rounsley SD, Ditta GS, Yanofsky MF (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7: 1259-1269.
56. Shindo S, Ito M, Ueda K, Kato M, Hasebe M (1999) Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evol Dev 1: 180-190.
57. Shore P, Sharrocks AD (1995) The MADS-Box family of transcription factors. Eur J Biochem 229: 1-13.
58. Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M, Swensen SM, Prince LM, Kress WJ, Nixon KC, Farris JS (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133: 381-461.
59. Soltis DE, Soltis PS, Endress P, K., Chase MW (2005) Phylogeny and evolution of angiosperms, Sinauer, Sunderland Soltis PS, Soltis DE, Chase MW (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402: 402-404.
60. Swofford DL (2001) PAUP* 4. 0b10: phylogenetic analysis using parsimony (*and other methods), Sinauer, Sunderland.
61. Tandre K, Albert VA, Sundas A, Engstrom P (1995) Conifer homologues to genes that control floral development in angiosperms. Plant Mol Biol 27: 69-78.
62. Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4: 75-85.
63. Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Munster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42: 115-149.
64. 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. J Mol Evol 43: 484-516.
65. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
66. Tsuchimoto S, Mayama T, van der Krol A, Ohtsubo E (2000) The whorl-specific action of a petunia class B floral homeotic gene. Genes Cells 5: 89-99.
67. Viaene T, Vekemans D, Becker A, Melzer S, Geuten K (2010) Expression divergence of the AGL6 MADS domain transcription factor lineage after a core eudicot duplication suggests functional diversification. BMC Plant Biol 10: 148.
68. West AG, Sharrocks AD (1999) MADS-box transcription factors adopt alternative mechanisms for bending DNA. J Mol Biol 286: 1311-1323.
69. Winter KU, Becker A, Munster T, Kim JT, Saedler H, Theissen G (1999) MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proc Natl Acad Sci USA 96: 7342-7347.
70. Yao J-L, Dong Y-H, Kvarnheden A, Morris B (1999) Seven MADSbox genes in apple areexpressed in different parts of the fruit. J Am Soc Hortic Sci 124: 8-13.
71. Yoo SK, Hong SM, Lee JS, Ahn JH (2011) A genetic screen for leaf movement mutants identifies a potential role for AGAMOUSLIKE 6 (AGL6) in circadian-clock control. Mol Cells 31: 281-287.
72. Yoo SK, Wu X, Lee JS, Ahn JH (2011) AGAMOUS-LIKE 6 is a floral promoter that negatively regulates the FLC/MAF clade genes and positively regulates FT in Arabidopsis. Plant J 65: 62-76.
73. 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: 2209-2223.
74. Zhang HM, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51: 51-59.