Divergences of MPF2-like MADS-domain proteins have an association with the evolution of the inflated calyx syndrome within Solanaceae

Planta

Volumn 236, Issue 4, 2012, Pages 1247-1260

  Zhang, Jisi ^a,b   Khan, Muhammad Ramzan ^c,d   Tian, Ying ^a   Li, Zhichao ^a,b   Riss, Simone ^c,e   He, Chaoying ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^d NATIONAL AGRICULTURAL RESEARCH CENTRE   (Pakistan)

^e ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

Functional evolution; Heterotopic expression; Inflated calyx syndrome; MADS box gene; Protein protein interaction; Solanaceae

Indexed keywords

ARABIDOPSIS; SOLANACEAE;

EID: 84866931181     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-012-1684-0     Document Type: Article

References (62)

1. 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: 605-617.
2. Blazquez MA, Ferrandiz C, Madueno F, Parcy F (2006) How floral meristems are built. Plant Mol Biol 60: 855-870.
3. Bracha-Drori K, Shichrur K, Katz A, Oliva M, Angelovici R, Yalovsky S, Ohad N (2004) Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J 40: 419-427.
4. Carroll SB, Grenier JK, Weatherbee SD (2001) From DNA to diversity: molecular genetics and the evolution of animal design. Blackwell Science, Malden, ISBN 0-632-04511-6.
5. Cho S, Jang S, Chae S, Chung KM, Moon Y-H, An G, Jang SK (1999) Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol Biol 40: 419-429.
6. Clough SJ, Bent A (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
7. Cong B, Barrero LS, Tanksley SD (2008) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat Genet 40: 800-804.
8. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
9. de Folter S, Immink RG, Kieffer M, Parenicová L, Henz SR, Weigel D, Busscher 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. Doebley JF, Lukens L (1998) Transcriptional regulators and the evolution of plant form. Plant Cell 10: 1075-1082.
11. Duttweiler HM (1996) A highly sensitive and non-lethal β-galactosidase plate assay for yeast. Trends Genet 12: 340-341.
12. Ema M, Hirota K, Mimura J, Abe H, Yodoi J, Sogawa K, Poellinger L, Fujii-Kuriyama Y (1999) Molecular mechanisms of transcription activation by HLF and HIF1α in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J 18: 1905-1914.
13. Fornara F, Gregis V, Pelucchi N, Colombo L, Kater M (2008) The rice StMADS11-like genes OsMADS22 and OsMADS47 cause floral reversions in Arabidopsis without complementing the svp and agl24 mutants. J Exp Bot 59: 2181-2190.
14. Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2. 2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289: 85-88.
15. Gregis V, Sessa A, Colombo L, Kater M (2006) AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell 18: 1373-1382.
16. Hackbusch J, Richter K, Muller J, Salamini F, Uhrig JF (2005) A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. Proc Natl Acad Sci USA 102: 4908-4912.
17. 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: 351-360.
18. He CY, Saedler H (2005) Heterotopic expression of MPF2 is the key to the evolution of the Chinese lantern of Physalis, a morphological novelty in Solanaceae. Proc Natl Acad Sci USA 102: 5779-5784.
19. He CY, Saedler H (2007) Hormonal control of the inflated calyx syndrome, a morphological novelty, in Physalis. Plant J 49: 935-946.
20. He CY, Münster T, Saedler H (2004) On the origin of floral morphological novelties. FEBS Lett 567: 147-151.
21. He CY, Sommer H, Grosardt B, Huijser P, Saedler H (2007) PFMAGO, a MAGO NASHI-like factor, interacts with the MADS-domain protein MPF2 from Physalis floridana. Mol Biol Evol 24: 1229-1241.
22. He CY, Tian Y, Saedler R, Efremova N, Riss S, Khan MR, Yephremov A, Saedler H (2010) The MADS-domain protein MPF1 of Physalis floridana controls plant architecture, seed development and flowering time. Planta 231: 767-777.
23. Hiratsu K, Mitsuda N, Matsui K, Ohme-Takagi M (2004) Identification of the minimal repression domain of SUPERMAN shows that the DLELRL hexapeptide is both necessary and sufficient for repression of transcription in Arabidopsis. Biochem Biophys Res Commun 321: 172-178.
24. Hu J, Saedler H (2007) Evolution of the inflated calyx syndrome in Solanaceae. Mol Biol Evol 24: 2443-2453.
25. Huelsenbeck JP, Ronquist FR (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
26. Huelsenbeck JP, Ronquist FR, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310-2314.
27. Immink RG, Ferrario S, Busscher-Lange J, Kooiker M, Busscher M, Angenent GC (2003) Analysis of the Petunia MADS-box transcription factor family. Mol Genet Genomics 268: 598-606.
28. Immink RG, Kaufmann K, Angenent GC (2010) The 'ABC' of MADS domain protein behaviour and interactions. Semin Cell Dev Biol 21: 87-93.
29. Irish VF, Litt A (2005) Flower development and evolution: gene duplication, diversification and redeployment. Curr Opin Genet Dev 15: 454-460.
30. Janssens SB, Viaene T, Huysmans S, Smets EF, Geuten KP (2008) Selection on length mutations after frameshift can explain the origin and retention of the AP3/DEF-like paralogues in Impatiens. J Mol Evol 66: 424-435.
31. Kane NA, Danyluk J, Tardif G, Ouellet F, Laliberté J-F, Limin AE, Fowler DB, Sarhan F (2005) TaVRT-2, a member of the StMADS-11 clade of flowering repressors, is regulated by vernalization and photoperiod in wheat. Plant Physiol 138: 2354-2363.
32. Khan MR, Hu J, Riss S, He CY, Saedler H (2009) MPF2-like-A MADS-box genes control the inflated calyx syndrome in Withania (Solanaceae): roles of Darwinian's selection. Mol Biol Evol 26: 2463-2473.
33. Knapp S (2002) Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. J Exp Bot 53: 2001-2022.
34. Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol Gene Genet 204: 383-396.
35. Kramer EM, Su HJ, Wu CC, Hu JM (2006) A simplified explanation for the frameshift mutation that created a novel C-terminal motif in the APETALA3 gene lineage. BMC Evol Biol 6: 30.
36. 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: 4063-4070.
37. Leseberg CH, Eissler CL, Wang X, Johns MA, Duvall MR, Mao L (2008) Interaction study of MADS-domain proteins in tomato. J Exp Bot 59: 2253-2265.
38. Li C, Zhou A, Sang T (2006) Rice domestication by reducing shattering. Science 311: 1936-1939.
39. Malcomber ST, Kellogg EA (2005) SEPALLATA gene diversification: brave new whorls. Trends Plant Sci 10: 427-435.
40. Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360: 273-277.
41. Masiero S, Li MA, Will I, Hartmann U, Saedler H, Huijser P, Schwarz-Sommer Z, Sommer H (2004) INCOMPOSITA: a MADS-box gene controlling prophyll development and floral meristem identity in Antirrhinum. Development 131: 5981-5990.
42. Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8: 122-128.
43. Olmstead RG, Bohs L, Migid HA, Santiago-Valentin E, Garcia VF, Collier SM (2008) A molecular phylogeny of the Solanaceae. Taxon 57: 1159-1181.
44. Piwarzyk E, Yang Y, Jack T (2007) Conserved C-terminal motifs of the Arabidopsis proteins APETALA3 and PISTILLATA are dispensable for floral organ identity function. Plant Physiol 145: 1495-1505.
45. Rijpkema AS, Gerats T, Vandenbussche M (2007) Evolutionary complexity of MADS complexes. Cur Opin Plant Biol 10: 32-38.
46. Riss S (2009) Isolation and analysis of MPF2-like MADS-box genes from Physaleae and characterization of their cis-regulatory regions. PhD thesis, Universität zu Köln.
47. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765-768.
48. Sentoku N, Kato H, Kitano H, Imai R (2005) OsMADS22, an STMADS11-like MADS-box gene of rice, is expressed in non-vegetative tissues and its ectopic expression induces spikelet meristem indeterminacy. Mol Genet Genomics 273: 1-9.
49. Shan H, Zahn L, Guindon S, Wall PK, Kong H, Ma H, dePamphilis CW, Leebens-Mack J (2009) Evolution of plant MADS box transcription factors: evidence for shifts in selection associated with early angiosperm diversification and concerted gene duplications. Mol Biol Evol 26: 2229-2244.
50. Su K, Zhao S, Shan H, Kong H, Lu W, Theissen G, Chen Z, Meng Z (2008) The MIK region rather than the C-terminal domain of AP3-like class B floral homeotic proteins determines functional specificity in the development and evolution of petals. New Phytol 178: 544-558.
51. Szymkowiak EJ, Irish EE (2006) JOINTLESS suppresses sympodial identity in inflorescence meristems of tomato. Planta 223: 646-658.
52. Trevaskis B, Tadege M, Hemming MN, Peacock WJ, Dennis ES, Sheldon C (2007) SVP-like MADS-box genes inhibit floral meristem identity in barley. Plant Physiol 143: 225-235.
53. 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: 4401-4409.
54. Voinnet O, Rivas R, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33: 949-956.
55. Wang RL, Stec A, Hey J, Lukens L, Doebley JF (1999) The limits of selection during maize domestication. Nature 398: 236-239.
56. Wang H, Nussbaum-Wagler T, Li BL, Zhao Q, Vigouroux Y, Faller M, Bomblies K, Lukens L, Doebley JF (2005) The origin of the naked grains of maize. Nature 436: 714-719.
57. Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
58. Yang Y, Jack T (2004) Defining subdomains of the K domain important for protein-protein interactions of plant MADS proteins. Plant Mol Biol 55: 45-59.
59. Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov chain Monte Carlo method. Mol Biol Evol 14: 717-724.
60. Yang Y, Fanning L, Jack T (2003) The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J 33: 47-59.
61. Yang Z, Wong W, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107-1118.
62. Yu H, Ito T, Wellmer F, Meyerowitz EM (2004) Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nat Genet 36: 157-161.