DEF- and GLO-like proteins may have lost most of their interaction partners during angiosperm evolution

Annals of Botany

Volumn 114, Issue 7, 2014, Pages 1431-1443

  Melzer, Rainer ^a,b   Härter, Andrea ^a   Rümpler, Florian ^a   Kim, Sangtae ^c,e   Soltis, Pamela S ^d   Soltis, Douglas E ^c,d   Theißen, Günter ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

^e Sungshin Women's University   (South Korea)

Author keywords

APETALA3; basal angiosperms; character state evolution; DEFICIENS; early diverging angiosperms; EMSA; floral homeotic gene; Flower development; GLOBOSA; MADS domain protein; PISTILLATA; protein protein interaction; yeast two hybrid

Indexed keywords

ANGIOSPERM; FLOWER; PROTEIN; YEAST;

MAGNOLIOPHYTA;

DEFICIENS PROTEIN; GLOBOSA PROTEIN, PLANT; HOMEODOMAIN PROTEIN; MADS DOMAIN PROTEIN; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ANGIOSPERM; CLASSIFICATION; EVOLUTION; FLOWER; GENE EXPRESSION REGULATION; GENETICS; PHYLOGENY; PROTEIN MULTIMERIZATION; TWO HYBRID SYSTEM;

ANGIOSPERMS; BIOLOGICAL EVOLUTION; DEFICIENS PROTEIN; FLOWERS; GENE EXPRESSION REGULATION, PLANT; HOMEODOMAIN PROTEINS; MADS DOMAIN PROTEINS; PHYLOGENY; PLANT PROTEINS; PROTEIN MULTIMERIZATION; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84913590461     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcu094     Document Type: Review

References (73)

1. Alvarez-Buylla ER, Ambrose BA, Flores-Sandoval E, et al. 2010. B-function expression in the flower center underlies the homeotic phenotype of Lacandonia schismatica (Triuridaceae). The Plant Cell 22: 3543-3559.
2. Amborella Genome Project. 2013. The Amborella genome and the evolution of flowering plants. Science 342: 11.
3. Aoki S, Uehara K, Imafuku M, Hasebe M, Ito M. 2004. Phylogeny and divergence of basal angiosperms inferred from APETALA3-and PISTILLATA-like MADS-box genes. Journal of Plant Research 117: 229-244.
4. APGIII. 2009. Anupdate of the Angiosperm Phylogeny Group classification for the orders and families offlowering plants:APGIII. Botanical Journal of the Linnean Society 161: 105-121.
5. Buzgo M, Soltis PS, Soltis DE. 2004. Floral developmental morphology of Amborella trichopoda (Amborellaceae). International Journal of Plant Sciences 165: 925-947.
6. ChangYY, KaoNH, LiJY, et al. 2010. Characterization of the possible roles for BclassMADSbox genes in regulation of perianth formation in orchid. Plant Physiology 152: 837-853.
7. Davies B, EgeaCortines M, Silva ED, Saedler H, Sommer H. 1996. Multiple interactions amongst floral homeotic MADS box proteins. EMBO Journal 15: 4330-4343.
8. Drea S, Hileman LC, De Martino G, Irish VF. 2007. Functional analyses of genetic pathways controlling petal specification in poppy. Development 134: 4157-4166.
9. de Folter S, Immink RGH, Kieffer M, et al. 2005. Comprehensive interaction map of the ArabidopsisMADSbox transcription factors. The Plant Cell 17: 1424-1433.
10. Geuten K, Becker A, Kaufmann K, et al. 2006. Petaloidy and petal identity MADS-box genes in the balsaminoid genera Impatiens and Marcgravia. The Plant Journal 47: 501-518.
11. Goto K, Meyerowitz EM. 1994. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes and Development 8: 1548-1560.
12. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27: 221-224.
13. Gregis V, Sessa A, Dorca-Fornell C, Kater MM. 2009. The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress classBandC floral homeotic genes. The Plant Journal 60: 626-637.
14. Hernandez-Hernandez T, Martinez-Castilla LP, Alvarez-Buylla ER. 2007. Functional diversification of B MADS-box homeotic regulators of flower development: adaptive evolution in protein-protein interaction domains after major gene duplication events. Molecular Biology and Evolution 24: 465-481.
15. Honma T, Goto K. 2001. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409: 525-529.
16. Hsu HF, Yang CH. 2002. An orchid (Oncidium Gower Ramsey) AP3-like MADS gene regulates floral formation and initiation. Plant and Cell Physiology 43: 1198-1209.
17. Hu JC. 2000. A guided tour in protein interaction space: coiled coils from the yeast proteome. Proceedings of the National Academy of Sciences, USA 97: 12935-12936.
18. Huang H, Tudor M, Su T, Zhang Y, Hu Y, Ma H. 1996. DNA binding properties of two Arabidopsis MADS domain proteins: binding consensus and dimer formation. The Plant Cell 8: 81-94.
19. Immink RGH, Ferrario S, Busscher-Lange J, et al. 2003. Analysis of the petunia MADS-box transcription factor family. Molecular Genetics and Genomics 268: 598-606.
20. Immink RG, Tonaco IA, de Folter S, et al. 2009. SEPALLATA3: the 'glue' for MADS box transcription factor complex formation. Genome Biology 10: R24.
21. ImminkRG,Kaufmann K, Angenent GC.2010. The 'ABC' ofMADSdomain protein behaviour and interactions. Seminars in Cell and Developmental Biology 21: 87-93.
22. Kanno A, Saeki H, Kameya T, Saedler H, Theißen G. 2003. Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Molecular Biology 52: 831-841.
23. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772-780.
24. 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.
25. Kaufmann K, Pajoro A, Angenent GC. 2010. Regulation of transcription in plants: mechanisms controlling developmental switches. Nature Reviews Genetics 11: 830-842.
26. Kim ST, Yoo MJ, AlbertVA, Farris JS, Soltis PS, Soltis DE. 2004. Phylogeny and diversification of B-function MADS-box genes in angiosperms: evolutionary and functional implications of a 260-million-year-old duplication. American Journal of Botany 91: 2102-2118.
27. Kim S, Koh J, Yoo MJ, et al. 2005. Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. The Plant Journal 43: 724-744.
28. Kim S, Soltis PS, Soltis DE. 2013. AGL6-like MADS-box genes are sister to AGL2-like MADS-box genes. Journal of Plant Biology 56: 315-325.
29. 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: 765-783.
30. Kramer EM, Holappa L, Gould B, Jaramillo MA, Setnikov D, Santiago PM. 2007. Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia. The Plant Cell 19: 750-766.
31. Lee HL, Irish VF. 2011. Gene duplication and loss in a MADS box gene transcription factor circuit. Molecular Biology and Evolution 28: 3367-3380.
32. Lenser T, Theissen G, Dittrich P. 2009. Developmental robustness by obligate interaction of class B floral homeotic genes and proteins. PLoS Computational Biology 5: e1000264.
33. Leseberg CH, Eissler CL, Wang X, Johns MA, Duvall MR, Mao L. 2008. Interaction study of MADS-domain proteins in tomato. Journal of Experimental Botany 59: 2253-2265.
34. Litt A,KramerEM.2010. TheABCmodel and the diversification of floral organ identity. Seminars in Cell and Developmental Biology 21: 129-137.
35. Liu CJ, Zhang JA, Zhang N, et al. 2010. Interactions among proteins of floral MADS-box genes in basal eudicots: implications for evolution of the regulatory network for flower development. Molecular Biology and Evolution 27: 1598-1611.
36. MaddisonWP, MaddisonDR. 2011. Mesquite: a modular system for evolutionary analysis. Version 2.75 http://mesquiteproject.org.
37. MalcomberST, KelloggEA.2005.SEPALLATAgene diversification: brave new whorls. Trends in Plant Science 10: 427-4335.
38. Marquez-Guzman J,EnglemanM,Martinez-MenaA,MartinezE,Ramos C. 1989. Reproductive anatomy of Lacandonia schismatica (Lacandoniaceae). Annals of the Missouri Botanical Garden 76: 124-127.
39. McGonigle B, Bouhidel K, Irish VF. 1996. Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. Genes and Development 10: 1812-1821.
40. 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.
41. Melzer R,Wang YQ, Theissen G. 2010. The naked and the dead: the ABCs of gymnosperm reproduction and the origin of the angiosperm flower. Seminars in Cell and Developmental Biology 21: 118-128.
42. Mondragon-Palomino M, Hiese L, Harter A, Koch MA, Theissen G. 2009. Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses. BMC Evolutionary Biology 9: 81.
43. Mooers AO, Schluter D. 1999. Reconstructing ancestor states with maximum likelihood: support for one-and two-rate models. Systematic Biology 48: 623-633.
44. Münster T, Wingen LU, Faigl W, Werth S, Saedler H, Theißen G. 2001. Characterization of three GLOBOSA-like MADS-box genes from maize: evidence for ancient paralogy in one class of floral homeotic B-function genes of grasses. Gene 262: 1-13.
45. NagasawaN,MiyoshiM,SanoY, et al. 2003.SUPERWOMAN1andDROOPING LEAFgenes control floral organ identity in rice.Development 130: 705-718.
46. Newman JR,Wolf E, Kim PS. 2000. A computationally directed screen identifying interacting coiled coils from Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, USA 97: 13203-13208.
47. Riechmann JL, Krizek BA, Meyerowitz EM. 1996a. Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proceedings of the National Academy of Sciences, USA 93: 4793-4798.
48. RiechmannJL,WangMQ,MeyerowitzEM.1996b.DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Research 24: 3134-3141.
49. RijpkemaAS, Zethof J, GeratsT,VandenbusscheM.2009. The petuniaAGL6 gene has a SEPALLATA-like function in floral patterning. The Plant Journal 60: 1-9.
50. Ronai Z,WangY, Khandurina J, et al. 2003.Transcription factor binding study by capillary zone electrophoretic mobility shift assay. Electrophoresis 24: 96-100.
51. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
52. Rudall PJ,RemizowaMV,Prenner G, Prychid CJ,TuckettRE, SokoloffDD. 2009. Nonflowers near the base of extant angiosperms? Spatiotemporal arrangement of organs in reproductive units of Hydatellaceae and its bearing on the origin of the flower. American Journal of Botany 96: 67-82.
53. Schwarz-Sommer Z, Hue I, Huijser P, et al. 1992. Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens-evidence for DNA-binding and autoregulation of its persistent expression throughout flower development. EMBO Journal 11: 251-263.
54. Smaczniak C, Immink RG, Angenent GC, Kaufmann K. 2012. Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139: 3081-3098.
55. Smirnova E, Shurland DL, Newman-Smith ED, Pishvaee B, van der Bliek AM. 1999. A model for dynamin self-assembly based on binding between three different protein domains. Journal of Biological Chemistry 274: 14942-14947.
56. Soltis PS, Soltis DE, Kim S, Chanderbali A, Buzgo M. 2006. Expression of floral regulators in basal angiosperms and the origin and evolution of ABC-function. Advances in Botanical Research 44: 483-506.
57. Soltis DE, Chanderbali AS,KimS, BuzgoM, Soltis PS. 2007. TheABCmodel and its applicability to basal angiosperms. Annals of Botany 100: 155-163.
58. Soltis PS, Brockington SF, Yoo MJ, et al. 2009. Floral variation and floral genetics in basal angiosperms. American Journal of Botany, 96: 110-128.
59. Sundström J, Engström P. 2002. Conifer reproductive development involves B-type MADS-box genes with distinct and different activities in male organ primordia. The Plant Journal 31: 161-169.
60. Theißen G. 2001. Development of floral organ identity: stories from the MADS house. Current Opinion in Plant Biology 4: 75-85.
61. Theißen G, Melzer R. 2007. Molecular mechanisms underlying origin and diversification of the angiosperm flower. Annals of Botany 100: 603-619.
62. Theißen G, Saedler H. 2001. Plant biology. Floral quartets. Nature 409: 469-471.
63. Thompson BE, Bartling L, Whipple C, et al. 2009. bearded-ear encodes a MADS box transcription factor critical for maize floral development. The Plant Cell 21: 2578-2590.
64. Vandenbussche M, Zethof J, Royaert S, Weterings K, Gerats T. 2004. The duplicated B-class heterodimer model: whorl-specific effects and complex genetic interactions in Petunia hybrida flower development. The Plant Cell 16: 741-754.
65. Wang YQ, Melzer R, Theissen G. 2010. Molecular interactions of orthologues of floral homeotic proteins fromthe gymnosperm Gnetumgnemonprovide a clue to the evolutionary origin of 'floral quartets'. The Plant Journal 64: 177-190.
66. Whipple CJ, Schmidt RJ. 2006. Genetics of grass flower development. Advances in Botanical Research 44: 385-424.
67. Whipple CJ, Ciceri P, Padilla CM, Ambrose BA, Bandong SL, Schmidt RJ. 2004.Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development 131: 6083-6091.
68. Winter KU, Saedler H, Theißen G. 2002a. On the origin of classBfloral homeotic genes: functional substitution and dominant inhibition in Arabidopsis by expression of an orthologue from the gymnosperm Gnetum. The Plant Journal 31: 457-475.
69. Winter KU,Weiser C, Kaufmann K, et al. 2002b. Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerization. Molecular Biology and Evolution 19: 587-596.
70. Yang YZ, Fanning L, JackT. 2003. TheKdomain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. The Plant Journal 33: 47-59.
71. Yao SG, Ohmori S, Kimizu M,Yoshida H. 2008. Unequal genetic redundancy of rice PISTILLATA orthologs, OsMADS2 and OsMADS4, in lodicule and stamen development. Plant and Cell Physiology 49: 853-857.
72. Zahn LM, King HZ, Leebens-Mack JH, et al. 2005a. The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169: 2209-2223.
73. ZahnLM,Leebens-MackJ,DepamphilisCW,MaH, Theißen G. 2005b.ToB or not to B a flower: the role of DEFICIENS and GLOBOSA orthologs in the evolution of the angiosperms. Journal of Heredity 96: 225-240.