Flower development of Phalaenopsis orchid involves functionally divergent SEPALLATA-like genes

New Phytologist

Volumn 202, Issue 3, 2014, Pages 1024-1042

  Pan, Zhao Jun ^a   Chen, You Yi ^a   Du, Jian Syun ^a   Chen, Yun Yu ^b   Chung, Mei Chu ^c   Tsai, Wen Chieh ^a   Wang, Chun Neng ^b   Chen, Hong Hwa ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

Author keywords

Complex formation; Divergence; Flower development; Orchid; Phalaenopsis; SEPALLATA

Indexed keywords

DEVELOPMENTAL BIOLOGY; FLOWERING; GENE EXPRESSION; HERB; PIGMENT; PLANT ARCHITECTURE; PROTEIN; VIRUS;

ORCHIDACEAE; PHALAENOPSIS;

MADS DOMAIN PROTEIN; PROTEIN BINDING; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ANTIBODY SPECIFICITY; BIOLOGICAL MODEL; CELL SHAPE; CHEMISTRY; CYTOLOGY; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; ORCHIDACEAE; ORGANOGENESIS; PHENOTYPE; PHYLOGENY; PLANT EPIDERMIS; PLANT GENE; PROMOTER REGION; TRANSGENIC PLANT; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; CELL SHAPE; CLONING, MOLECULAR; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENE SILENCING; GENES, PLANT; MADS DOMAIN PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; ORCHIDACEAE; ORGAN SPECIFICITY; ORGANOGENESIS; PHENOTYPE; PHYLOGENY; PLANT EPIDERMIS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEIN BINDING;

EID: 84898033837     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12723     Document Type: Article

References (62)

1. Aceto S, Gaudio L. 2011. The MADS and the beauty: genes involved in the development of orchid flowers. Current Genomics 12: 342-356.
2. Ampomah-Dwamena C, Morris BA, Sutherland P, Veit B, Yao JL. 2002. Down-regulation of TM29, a tomato SEPALLATA homolog, causes partheno-carpic fruit development and floral reversion. Plant Physiology 130: 605-617.
3. 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.
4. Buchner P, Boutin JP. 1998. A MADS box transcription factor of the AP1/AGL9 subfamily is also expressed in the seed coat of pea (Pisum sativum) during development. Plant Molecular Biology 38: 1253-1255.
5. Chang YY, Chiu YF, Wu JW, Yang CH. 2009. Four orchid (Oncidium Gower Ramsey) AP1/AGL9-like MADS box genes show novel expression patterns and cause different effects on floral transition and formation in Arabidopsis thaliana. Plant and Cell Physiology 50: 1425-1438.
6. Chen YY, Lee PF, Hsiao YY, Wu WL, Pan ZJ, Lee YI, Liu KW, Chen LJ, Liu ZJ, Tsai WC. 2012. C- and D-class MADS-box genes from Phalaenopsis equestris (Orchidaceae) display functions in gynostemium and ovule development. Plant and Cell Physiology 53: 1053-1067.
7. Chung YY, Kim SR, Finkel D, Yanofsky MF, An G. 1994. Early flowering and reduced apical dominance result from ectopic expression of a rice MADS box gene. Plant Molecular Biology 26: 657-665.
8. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16: 735-743.
9. Cozzolino S, Widmer A. 2005. Orchid diversity: an evolutionary consequence of deception? Trends in Ecology & Evolution 20: 487-494.
10. 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.
11. Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.
12. Darwin C. 1885. The various contrivances by which orchids are fertilized by insects. London, UK: University of Chicago Press.
13. 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.
14. Dressler RL. 1993. Phylogeny and classification of the orchid family. Portland, OR, USA: Dioscorides Press.
15. 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.
16. 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.
17. Fujisawa M, Nakano T, Ito Y. 2011. Identification of potential target genes for the tomato fruit-ripening regulator RIN by chromatin immunoprecipitation. BMC Plant Biology 11: 26.
18. Fujisawa M, Shima Y, Higuchi N, Nakano T, Koyama Y, Kasumi T, Ito Y. 2012. Direct targets of the tomato-ripening regulator RIN identified by transcriptome and chromatin immunoprecipitation analyses. Planta 235: 1107-1122.
19. Hsiao YY, Huang TH, Fu CH, Huang SC, Chen YJ, Huang YM, Chen WH, Tsai WC, Chen HH. 2012. Transcriptomic analysis of floral organs from Phalaenopsis orchid by using oligonucleotide microarray. Gene 518: 91-100.
20. Hsieh MH, Lu HC, Pan ZJ, Yeh HH, Wang SS, Chen WH, Chen HH. 2013a. Optimizing virus-induced gene silencing efficiency with Cymbidium mosaic virus in Phalaenopsis flower. Plant Science 201-202: 25-41.
21. Hsieh MH, Pan ZJ, Lai PH, Lu HC, Yeh HH, Hsu CC, Wu WL, Chung MC, Wang SS, Chen WH et al. 2013b. Virus-induced gene silencing unravels multiple transcription factors involved in floral growth and development in Phalaenopsis orchids. Journal of Experimental Botany 64: 3869-3884.
22. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310-2314.
23. Immink RG, Tonaco IA, de Folter S, Shchennikova A, van Dijk AD, Busscher-Lange J, Borst JW, Angenent GC. 2009. SEPALLATA3: the 'glue' for MADS box transcription factor complex formation. Genome Biology 10: R24.
24. Ireland HS, Yao JL, Tomes S, Sutherland PW, Nieuwenhuizen N, Gunaseelan K, Winz RA, David KM, Schaffer RJ. 2013. Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. Plant Journal 73: 1044-1056.
25. Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, Yasuda J, Ito H, Inakuma T, Hiroi S, Kasumi T. 2008. DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant Journal 55: 212-223.
26. Kaufmann K, Muino 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.
27. Koch K, Bhushanb B, Barthlott W. 2008. Diversity of structure, morphology and wetting of plant surfaces. Soft Matter 4: 1943-1963.
28. Kramer EM, Hall JC. 2005. Evolutionary dynamics of genes controlling floral development. Current Opinion in Plant Biology 8: 13-18.
29. Krizek BA, Anderson JT. 2013. Control of flower size. Journal of Experimental Botany 64: 1427-1437.
30. Lid SE, Meeley RB, Min Z, Nichols S, Olsen OA. 2004. Knock-out mutants of two members of the AGL2 subfamily of MADS-box genes expressed during maize kernel development. Plant Science 167: 575-582.
31. Lu HC, Chen HH, Tsai WC, Chen WH, Su HJ, Chang DC, Yeh HH. 2007. Strategies for functional validation of genes involved in reproductive stages of orchids. Plant Physiology 143: 558-569.
32. Lu HC, Hsieh MH, Chen CE, Chen HH, Wang HI, Yeh HH. 2012. A high-throughput virus-induced gene-silencing vector for screening transcription factors in virus-induced plant defense response in orchid. Molecular Plant-Microbe Interactions 25: 738-746.
33. Lu ZX, Wu M, Loh CS, Yeong CY, Goh CJ. 1993. Nucleotide sequence of a flower-specific MADS box cDNA clone from orchid. Plant Molecular Biology 23: 901-904.
34. Malcomber ST, Kellogg EA. 2005. SEPALLATA gene diversification: brave new whorls. Trends in Plant Science 10: 427-435.
35. Manchado-Rojo M, Delgado-Benarroch L, Roca MJ, Weiss J, Egea-Cortines M. 2012. Quantitative levels of Deficiens and Globosa during late petal development show a complex transcriptional network topology of B function. Plant Journal 72: 294-307.
36. Matsubara K, Shimamura K, Kodama H, Kokubun H, Watanabe H, Basualdo IL, Ando T. 2008. Green corolla segments in a wild Petunia species caused by a mutation in FBP2, a SEPALLATA-like MADS box gene. Planta 228: 401-409.
37. Mondragon-Palomino M. 2013. Perspectives on MADS-box expression during orchid flower evolution and development. Frontiers in Plant Science 4: 377.
38. Mondragon-Palomino M, Theissen G. 2011. Conserved differential expression of paralogous DEFICIENS- and GLOBOSA-like MADS-box genes in the flowers of Orchidaceae: refining the 'orchid code'. Plant Journal 66: 1008-1019.
39. Noda K, Glover BJ, Linstead P, Martin C. 1994. Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature 369: 661-664.
40. Oshima Y, Shikata M, Koyama T, Ohtsubo N, Mitsuda N, Ohme-Takagi M. 2013. MIXTA-like transcription factors and WAX INDUCER1/SHINE1 coordinately regulate cuticle development in Arabidopsis and Torenia fournieri. Plant Cell 25: 1609-1624.
41. Pan ZJ, Cheng CC, Tsai WC, Chung MC, Chen WH, Hu JM, Chen HH. 2011. The duplicated B-class MADS-box genes display dualistic characters in orchid floral organ identity and growth. Plant and Cell Physiology 52: 1515-1531.
42. 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.
43. Perez-Rodriguez M, Jaffe FW, Butelli E, Glover BJ, Martin C. 2005. Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development 132: 359-370.
44. Rijpkema AS, Zethof J, Gerats T, Vandenbussche M. 2009. The petunia AGL6 gene has a SEPALLATA-like function in floral patterning. Plant Journal 60: 1-9.
45. Rudall PJ, Bateman RM. 2002. Roles of synorganisation, zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots. Biological Reviews of the Cambridge Philosophical Society 77: 403-441.
46. Ruokolainen S, Ng YP, Albert VA, Elomaa P, Teeri TH. 2010. Large scale interaction analysis predicts that the Gerbera hybrida floral E function is provided both by general and specialized proteins. BMC Plant Biology 10: 129.
47. Seymour GB, Ryder CD, Cevik V, Hammond JP, Popovich A, King GJ, Vrebalov J, Giovannoni JJ, Manning K. 2010. A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria x ananassa Duch.) fruit, a non-climacteric tissue. Journal of Experimental Botany 62: 1179-1188.
48. Smaczniak C, Immink RG, Muino JM, Blanvillain R, Busscher M, Busscher-Lange J, Dinh QD, Liu S, Westphal AH, Boeren S et al. 2012. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proceedings of the National Academy of Sciences, USA 109: 1560-1565.
49. Stellari GM, Jaramillo MA, Kramer EM. 2004. Evolution of the APETALA3 and PISTILLATA lineages of MADS-box-containing genes in the basal angiosperms. Molecular Biology and Evolution 21: 506-519.
50. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
51. Tsai WC, Chen HH. 2006. The orchid MADS-box genes controlling floral morphogenesis. Scientific World Journal 6: 1933-1944.
52. Tsai WC, Kuoh CS, Chuang MH, Chen WH, Chen HH. 2004. Four DEF-like MADS box genes displayed distinct floral morphogenetic roles in Phalaenopsis orchid. Plant and Cell Physiology 45: 831-844.
53. Tsai WC, Lee PF, Chen HI, Hsiao YY, Wei WJ, Pan ZJ, Chuang MH, Kuoh CS, Chen WH, Chen HH. 2005. PeMADS6, a GLOBOSA/PISTILLATA-like gene in Phalaenopsis equestris involved in petaloid formation, and correlated with flower longevity and ovary development. Plant and Cell Physiology 46: 1125-1139.
54. Tsai WC, Pan ZJ, Hsiao YY, Jeng MF, Wu TF, Chen WH, Chen HH. 2008. Interactions of B-class complex proteins involved in tepal development in Phalaenopsis orchid. Plant and Cell Physiology 49: 814-824.
55. Uimari A, Kotilainen M, Elomaa P, Yu D, Albert VA, Teeri TH. 2004. Integration of reproductive meristem fates by a SEPALLATA-like MADS-box gene. Proceedings of the National Academy of Sciences, USA 101: 15817-15822.
56. 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.
57. Vignolini S, Davey MP, Bateman RM, Rudall PJ, Moyroud E, Tratt J, Malmgren S, Steiner U, Glover BJ. 2012. The mirror crack'd: both pigment and structure contribute to the glossy blue appearance of the mirror orchid, Ophrys speculum. New Phytologist 196: 1038-1047.
58. Whitney HM, Bennett KM, Dorling M, Sandbach L, Prince D, Chittka L, Glover BJ. 2011. Why do so many petals have conical epidermal cells? Annals of Botany 108: 609-616.
59. Xu Y, Teo LL, Zhou J, Kumar PP, Yu H. 2006. Floral organ identity genes in the orchid Dendrobium crumenatum. Plant Journal 46: 54-68.
60. Yu H, Goh CJ. 2000. Identification and characterization of three orchid MADS-box genes of the AP1/AGL9 subfamily during floral transition. Plant Physiology 123: 1325-1336.
61. 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.
62. Zwickl DJ. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Austin, TX, USA: The University of Texas.