Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia

Plant Cell

Volumn 19, Issue 3, 2007, Pages 750-766

  Kramer, Elena M ^a   Holappa, Lynn ^a   Gould, Billie ^a   Jaramillo, M Alejandra ^a,b   Setnikov, Dimitriy ^a,c   Santiago, Philip M ^a,d  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMERS; PLANTS (BOTANY); PROTEINS;

GENE SILENCING; HOMEOTIC MUTANT LINES; PETALOID ORGANS;

GENES;

DIMERS; GENES; PLANTS; PROTEINS;

AQUILEGIA;

EID: 34250173782     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.107.050385     Document Type: Article

References (73)

1. Aagaard, J.E., Olmstead, R.G., Willis, J.H., and Phillips, P.C. (2005). Duplication of floral regulatory genes in the Lamiales. Am. J. Bot. 92: 1284-1293.
2. Albert, V.A., Gustafsson, M.H.G., and Di Laurenzio, L. (1998). Ontogenetic systematics, molecular developmental genetics, and the angiosperm petal. In Molecular Systematics of Plants, Vol. II, D. Soltis, P. Soltis, and J.J. Doyle, eds (New York: Chapman and Hall), pp. 349-374.
3. Ambrose, B.A., Lerner, D.R., Ciceri, P., Padilla, C.M., Yanofsky, M.F., and Schmidt, R.J. (2000). Molecular and genetic analyses of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell 5: 569-579.
4. Aoki, S., Uehara, K., Imafuku, M., Hasebe, M., and Ito, M. (2004). Phylogeny and divergence of basal angiosperms inferred from APETALA3-and PISTILLATA-like MADS-box genes. J. Plant Res. 117: 229-244.
5. Becker, A., and 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.
6. Bowman, J.L., Smyth, D.R., and Meyerowitz, E.M. (1989). Genes directing flower development in Arabidopsis. Plant Cell 1: 37-52.
7. Burch-Smith, T.M., Anderson, J.C., Martin, G.B., and Dinesh-Kumar, S.P. (2004). Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J. 39: 734-746.
8. Buzgo, M., Soltis, P.S., and Soltis, D.E. (2004). Floral developmental morphology of Amborella trichopoda (Amborellaceae). Int. J. Plant Sci. 165: 925-947.
9. Carpenter, R., and Coen, E.S. (1990). Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev. 4: 1483-1493.
10. Chen, J.C., Jiang, C.Z., Gookin, T.E., Hunter, D.A., Clark, D.G., and Reid, M.S. (2004). Chalcone synthase as a reporter in virus-induced gene silencing studies of flower senescence. Plant Mol. Biol. 55: 521-530.
11. Christensen, K.I., and Hansen, H.V. (1998). SEM studies of epidermal patterns of petals in the angiosperms. Opera Bot. 135: 5-91.
12. Coen, E.S., and Meyerowitz, E.M. (1991). The war of the whorls: Genetic interactions controlling flower development. Nature 353: 31-37.
13. Cubas, P. (2002). Role of TCP genes in the evolution of morphological characters in angiosperms. In Developmental Genetics and Plant Evolution, Q.C.B. Cronk, R.M. Bateman, and J.A. Hawkins, eds (London: Taylor and Hawkins), pp. 247-266.
14. de Martino, G., Pan, I., Emmanuel, E., Levy, A., and Irish, V. (2006). Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell 18: 1833-1845.
15. Dinesh-Kumar, S.P., Anandalakshmi, R., Marathe, R., Schiff, M., and Liu, Y. (2003). Virus-induced gene silencing. In Plant Functional Genomics, E. Grotewold, ed (Totowa, NJ: Humana Press), pp. 287-293.
16. Endress, P.K. (1994). Diversity and Evolutionary Biology of Tropical Flowers. (Cambridge, UK: Cambridge University Press).
17. Erbar, C., Kusma, S., and Leins, P. (1998). Development and interpretation of nectary organs in Ranunculaceae. Flora 194: 317-332.
18. Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.-L., and Postlethwait, J. (1999). Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
19. Geuten, K., Becker, A., Kaufmann, K., Caris, P., Janssens, S., Viaene, T., Theissen, G., and Smets, E. (2006). Petaloidy and petal identity MADS-box genes in the balsaminoid genera Impatiens and Marcgravia. Plant J. 47: 501-518
20. Goto, K., and Meyerowitz, E.M. (1994). Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8: 1548-1560.
21. Hileman, L.C., Drea, S., de Martino, G., Litt, A., and Irish, V.F. (2005). Virus-induced gene silencing is an effective tool for assaying gene function in the basal eudicot species Papaver somniferum (opium poppy). Plant J. 44: 334-341.
22. Hill, T., Day, C.D., Zondlo, S.C., Thackeray, A.G., and Irish, V.F. (1998). Discrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3. Development 125: 1711-1721.
23. Honma, T., and Goto, K. (2000). The Arabidopsis floral homeotic gene PISTILLATA is regulated by discrete cis-elements responsive to induction and maintenance signals. Development 127: 2021-2030.
24. Hoot, S.B. (1995). Phylogeny of the Ranunculaceae based on preliminary atpB, rbcL and 18S nuclear ribosomal DNA sequence data. Plant Syst. Evol. Suppl. 9: 241-251.
25. Jack, T., Brockman, L.L., and Meyerowitz, E.M. (1992). The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68: 683-697.
26. Jack, T., Fox, G.L., and Meyerowitz, E.M. (1994). Arabidopsis homeotic gene APETALA3 ectopic expression: Transcriptional and post-transcriptional regulation determine floral organ identity. Cell 76: 703-716.
27. Jaramillo, M.A., and Kramer, E.M. (2004). APETALA3 and PISTILLATA homologs exhibit novel expression patterns in the unique perianth in Aristolochia (Aristolochiaceae). Evol. Dev. 6: 449-458.
28. Jaramillo, M.A., and Kramer, E.M. (2007). The role of developmental genetics in understanding homology and morphological evolution in plants. Int. J. Plant Sci. 168: 61-72.
29. Jenik, P.D., and Irish, V.F. (2001). The Arabidopsis floral homeotic gene APETALA3 differentially regulates intercellular signaling required for petal and stamen development. Development 128: 13-23.
30. Kanno, A., Saeki, H., Kameya, T., Saedler, H., and Theissen, G. (2003). Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Mol. Biol. 52: 831-841.
31. Kim, S., Koh, J., Yoo, M.J., Kong, H.Z., Hu, Y., Ma, H., Soltis, P.S., and Soltis, D.E. (2005). Expression of floral MADS-box genes in basal angiosperms: Implications for the evolution of floral regulators. Plant J. 43: 724-744.
32. Kim, S., Yoo, M., Albert, V.A., Farris, J.S., Soltis, P.S., and Soltis, D.E. (2004). Phylogeny and diversification of B-function genes in angiosperms: Evolutionary and functional implications of a 260-million year old duplication. Am. J. Bot. 91: 2102-2118.
33. Kosuge, K. (1994). Petal evolution in Ranunculaceae. Plant Syst. Evol. Suppl. 8: 185-191.
34. Kramer, E.M. (2005a). Floral architecture: Regulation and diversity of floral shape and pattern. In Plant Architecture and Its Manipulation, C.G.N. Turnbull, ed (Oxford, UK: Blackwell Publishing), pp. 120-147.
35. Kramer, E.M. (2005b). Methods for studying the evolution of plant reproductive structures: Comparative gene expression techniques. In Molecular Evolution: Producing the Biochemical Data, E.A. Zimmer and E.H. Roalson, eds (San Diego, CA: Elsevier Academic Press), pp. 617-635.
36. Kramer, E.M., Di Stilio, V.S., and Schluter, P. (2003). Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. Int. J. Plant Sci. 164: 1-11.
37. Kramer, E.M., Dorit, R.L., and Irish, V.F. (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.
38. Kramer, E.M., and Irish, V.F. (2000). Evolution of the petal and stamen developmental programs: Evidence from comparative studies of the lower eudicots and basal angiosperms. Int. J. Plant Sci. 161: S29-S40.
39. Kramer, E.M., and Jaramillo, M.A. (2005). The genetic basis for innovations in floral organ identity. J. Exp. Zool. 304B: 526-535.
40. Lamb, R.S., and Irish, V.F. (2003). Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc. Natl. Acad. Sci. USA 100: 6558-6563.
41. Lee, J.Y., Baum, S.F., Oh, S.H., Jiang, C.Z., Chen, J.C., and Bowman, J.L. (2005). Recruitment of CRABS CLAW to promote nectary development within the eudicot clade. Development 132: 5021-5032.
42. Lee, S., Jeon, J.-S., An, K., Moon, Y.-H., Lee, S., Chung, Y.-Y., and An, G. (2003). Alteration of floral organ identity in rice through ectopic expression of OsMADS16. Planta 217: 904-911.
43. Liu, Y., Nakayama, N., Schiff, M., Litt, A., Irish, V.F., and Dinesh-Kumar, S.P. (2004). Virus induced gene silencing of a DEFICIENS ortholog in Nicotiana benthamiana. Plant Mol. Biol. 54: 701-711.
44. Luo, D., Carpenter, R., Copsey, L., Vincent, C., Clark, J., and Coen, E. (1999). Control of organ asymmetry in flowers of Antirrhinum. Cell 99: 367-376.
45. Martin, C., Bhatt, K., Baumann, E., Jin, H., Zachgo, S., Roberts, K., Schwarz-Sommer, Z., Glover, B., and Perez-Rodrigues, M. (2002). The mechanics of cell fate determination in petals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357: 809-813.
46. McGonigle, B., Bouhidel, K., and Irish, V.F. (1996). Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. Genes Dev. 10: 1812-1821.
47. Munz, P.A. (1946). Aquilegia: The cultivated and wild columbines. Gentes Herb. 7: 1-150.
48. Nagasawa, N., Miyoshi, M., Sano, Y., Satoh, H., Hirano, H., Sakai, H., and Nagato, Y. (2003). SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130: 705-718.
49. Nakamura, T., Fukuda, T., Nakano, M., Hasebe, M., Kameya, T., and Kanno, A. (2005). The modified ABC model explains the development of the petaloid perianth of Agapanthus praecox ssp. orientalis (Agapanthaceae) flowers. Plant Mol. Biol. 58: 435-445.
50. Park, J.-H., Ishikawa, Y., Ochiai, H., Kanno, A., and Kameya, T. (2004). Two GLOBOSA-like genes are expressed in second and third whorls of homochlamydeous flowers in Asparagus officinalis L. Plant Cell Physiol. 45: 325-332.
51. Park, J.-H., Ishikawa, Y., Yoshida, R., Kanno, A., and Kameya, T. (2003). Expression of AODEF, a B-functional MADS-box gene, in stamens and inner petals of the dioecious species Asparagus officinalis L. Plant Mol. Biol. 51: 867-875.
52. Prantl, K. (1887). Beitrage zur Morphologie und Systematik der Ranunculacean. Bot. Jahrb. Syst. 9: 225-273.
53. Ratcliff, F., Martin-Hernandez, A.M., and Baulcombe, D.C. (2001). Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J. 25: 237-245.
54. Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., and Bartel, D.P. (2002). Prediction of plant microRNA targets. Cell 110: 513-520.
55. Riechmann, J.L., Krizek, B.A., and Meyerowitz, E.M. (1996). Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc. Natl. Acad. Sci. USA 93: 4793-4798.
56. Rijpkema, A.S., Royaert, S., Zethof, J., van der Weerden, G., Gerats, T., and Vandenbussche, M. (2006). Functional divergence within the DEF/AP3 lineage: An analysis of PhTM6 in Petunia hybrida. Plant Cell 18: 1819-1832.
57. Sakai, H., Medrano, L.J., and Meyerowitz, E.M. (1995). Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378: 199-201.
58. Sommer, H., Nacken, W., Beltran, P., Huijser, R., Pape, H., Hansen, R., Flor, P., Saedler, H., and Schwarz-Sommer, Z. (1991). Properties of deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus. Dev. Suppl. 1: 169-175.
59. Stellari, G.M., Jaramillo, M.A., and Kramer, E.M. (2004). Evolution of the APETALA3 and PISTILLATA lineages of MADS-box containing genes in basal angiosperms. Mol. Biol. Evol. 21: 506-519.
60. Takhtajan, A. (1991). Evolutionary Trends in Flowering Plants. (New York: Columbia University Press).
61. Tamura, M. (1965). Morphology, ecology, and phylogeny of the Ranunculaceae. IV. Sci. Rep. Osaka Univ. 14: 53-71.
62. Trobner, W., Ramirez, L., Motte, P., Hue, I., Huijser, P., Lonnig, W.E., Saedler, H., Sommer, H., and Schwarz-Sommer, Z. (1992). Globosa - A homeotic gene which interacts with deficiens in the control of Antirrhinum floral organogenesis. EMBO J. 11: 4693-4704.
63. Tsai, W.C., Kuoh, C.S., Chuang, M.H., Chen, W.H., and Chen, H.H. (2004). Four DEF-like MADS box genes displayed distinct floral morphogenetic roles in Phalaenopsis orchid. Plant Cell Physiol. 45: 831-844.
64. Tucker, S.C., and Hodges, S.A. (2005). Floral ontogeny of Aquilegia, Semiaquilegia, and Isopyrum (Ranunculaceae). Int. J. Plant Sci. 166: 557-574.
65. Tzeng, T.Y., and Yang, C.H. (2001). A MADS box gene from lily (Lilium longiflorum) is sufficient to generate dominant negative mutation by interacting with PISTILLATA (PI) in Arabidopsis thaliana. Plant Cell Physiol. 42: 1156-1168.
66. Vandenbussche, M., Zethof, J., Royaert, S., Weterings, K., and Gerats, T. (2004). The duplicated B-class heterodimer model: Whorl-specific effects and complex genetic interactions in Petunia hybrida flower development. Plant Cell 16: 741-754.
67. Walker-Larsen, J., and Harder, L.D. (2000). The evolution of staminodes in angiosperms: Patterns of stamen reduction, loss, and functional re-invention. Am. J. Bot. 87: 1367-1384.
68. Whipple, C.J., Ciceri, P., Padilla, C.M., Ambrose, B.A., Bandong, S.L., and Schmidt, R.J. (2004). Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development 131: 6083-6091.
69. Winter, K.U., Weiser, C., Kaufmann, K., Bohne, A., Kirchner, C., Kanno, A., Saedler, H., and Theissen, G. (2002). Evolution of class B floral homeotic proteins: Obligate heterodimerization originated from homodimerization. Mol. Biol. Evol. 19: 587-596.
70. Worsdell, W.C. (1903). The origin of the perianth of flowers, with special reference to the Ranunculaceae. New Phytol. 2: 42-48.
71. Zachgo, S., de Andrade Silva, E., Motte, P., Trobner, W., Saedler, H., and Schwarz-Sommer, Z. (1995). Functional analysis of the Antirrhinum floral homeotic Deficiens gene in vivo and in vitro by using a temperature-sensitive mutant. Development 121: 2861-2875.
72. Zahn, L.M., Leebens-Mack, J., dePamphilis, C.W., Ma, H., and Theissen, G. (2005). To B or not to B a flower: The role of DEFICIENS and GLOBOSA orthologs in the evolution of the angiosperms. J. Hered. 96: 225-240.
73. Zanis, M., Soltis, P.S., Qiu, Y.-L., Zimmer, E.A., and Soltis, D.E. (2003). Phylogenetic analyses and perianth evolution in basal angiosperms. Ann. Mo. Bot. Gard. 90: 129-150.