B- and C-class gene expression during corona development of the blue passionflower (Passiflora caerulea, Passifloraceae)

American Journal of Botany

Volumn 98, Issue 6, 2011, Pages 923-934

  Hemingway, Claire A ^a,b   Christensen, Ashley R ^a   Malcomber, Simon T ^a  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b Botanical Society of America   (United States)

Author keywords

ABC model; AGAMOUS(AG); Flower morphology; Heteranthery; Heterochrony; Heterotopy; Novel compound structures; Organ identity; PISTILLATA(PI); TOMATO MADS6(TM6)

Indexed keywords

MESSENGER RNA; VEGETABLE PROTEIN;

DICOTYLEDON; GENE EXPRESSION; HETEROCHRONY (ONTOGENY); HYBRIDIZATION; HYPOTHESIS TESTING; MITOCHONDRIAL DNA; POLYMERASE CHAIN REACTION; REAL TIME; SCANNING ELECTRON MICROSCOPY;

ARTICLE; BAYES THEOREM; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN SITU HYBRIDIZATION; METABOLISM; PASSIFLORA; PHYLOGENY; PLANT GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ULTRASTRUCTURE;

BAYES THEOREM; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; IN SITU HYBRIDIZATION; PASSIFLORA; PHYLOGENY; PLANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

PASSIFLORA; PASSIFLORA CAERULEA; PASSIFLORACEAE;

EID: 84858436919     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1100026     Document Type: Article

References (63)

1. Ackerman, C. M., Q. Yu, S. Kim, R. E. Paull, P. H. Moore, and R. Ming. 2008. B-class MADS-box genes in trioecious papaya: Two paleoAP3 paralogs, CpTM6-1 and CpTM6-2, and a PI ortholog CpPI. Planta 227: 741-753.
2. Amela Garcia, M. T., B. G. Galati, and P. S. Hoc. 2007. Ultrastructure of the corona of scented and scentless flowers of Passiflora spp. (Passifloraceae). Flora 202: 303-315.
3. Baum, D. A., and M. J. Donoghue. 2002. Transference of function, heterotopy and the evolution of plant development. In Q. C. B. Cronk, R. M. Bateman, and J. A. Hawkins [eds.], Developmental genetics and plant evolution, 52-69. Taylor and Francis, New York, New York, USA.
4. Becker, A., and G. Theissen. 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.
5. Bernhard, A. 1999. Flower structure, development, and systematics in Passifloraceae and in Abatia (Flacourtiaceae). International Journal of Plant Sciences 160: 135-150.
6. Bowman, J. L. 1997. Evolutionary conservation of angiosperm flower development at the molecular and genetic levels. Journal of Biosciences 22: 515-527.
7. Bowman, J. L., D. R. Smyth, and E. M. Meyerowitz. 1989. Genes directing flower development in Arabidopsis. Plant Cell 1: 37-52.
8. Bowman, J. L., D. R. Smyth, and E. M. Meyerowitz. 1991. Genetic interactions among floral homeotic genes of Arabidopsis. Development 112: 1-20.
9. Burch-Smith, T. M., J. C. Anderson, G. B. Martin, and S. P. Dinesh-Kumar. 2004. Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant Journal 39: 734-746.
10. Coen, E. S., and E. M. Meyerowitz. 1991. The war of the whorls: Genetic interactions controlling flower development. Nature 353: 31-37.
11. Colombo, L., J. Franken, E. Koetje, J. van Went, H. Dons, G. C. Angenent, and A. J. van Tunen. 1995. The Petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7: 1859-1868.
12. Constantin, G. D., B. N. Krath, S. A. MacFarlane, M. Nicolaisen, I. E. Johansen, and O. S. Lund. 2004. Virus-induced gene silencing as a tool for functional genomics in a legume species. Plant Journal 40: 622-631.
13. Cronquist, A. 1981. An integrated system of classification of flowering plants. Columbia University Press, New York, New York, USA. de Martino, G., I. Pan, E. Emmanuel, A. Levy, and V. F. Irish. 2006. Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell 18: 1833-1845.
14. De Wilde, W. J. J. O. 1974. The genera of tribe Passifloreae (Passifloraceae) with special reference to flower morphology. Blumea 22: 37-50.
15. Ditta, G., A. Pinyopich, P. Robles, S. Pelaz, and M. F. Yanofsky. 2004. The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Current Biology 14: 1935-1940.
16. Edgar, R. C. 2004. MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
17. Endress, P. 2006. Angiosperm floral evolution: Morphological developmental framework. In J. Leebens-Mack, D. E. Soltis, and P. S. Soltis [eds.], Developmental genetics of the flower, Advances in Botanical Research, vol. 44, 1-61. Elsevier, London, UK.
18. Endress, P. K. 1996. Diversity and evolutionary biology of tropical flowers, 2nd ed. Cambridge University Press, Cambridge, UK.
19. Endress, P. K., and M. L. Matthews. 2006. Elaborate petals and staminodes in eudicots: Diversity, function, and evolution. Organisms, Diversity & Evolution 6: 257-293.
20. Favaro, R., A. Pinyopich, R. Battaglia, M. Kooiker, L. Borghi, G. Ditta, M. F. Yanofsky, et al. 2003. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15: 2603-2611.
21. Feuillet, C., and J. M. MacDougal. 2007. Passifloraceae. In K. Kubitzki, C. Bayer, and P. F. Stevens [eds.], The families and genera of vascular plants, vol. 9, Flowering plants: Eudicots; Berberidopsidales, Buxales, Crossosomatales, Fabales p.p., Geraniales, Gunnerales, Myrtales p.p., Proteales, Saxifragales, Vitales, Zygophyllales, Clusiaceae Alliance, Passifloraceae Alliance, Dilleniaceae, Huaceae, Picramniaceae, Sabiaceae. Springer, New York, New York, USA.
22. Gadberry, M. D., S. T. Malcomber, A. N. Doust, and E. A. Kellogg. 2005. Primaclade-A flexible tool to find conserved PCR primers across multiple species. Bioinformatics 21: 1263-1264.
23. Hansen, A. K., L. E. Gilbert, B. B. Simpson, S. R. Downie, A. C. Aervi, and R. K. Jansen. 2006. Phylogenetic relationships and chromosome number evolution in Passiflora. Systematic Biology 31: 138-150.
24. Heard, J., and K. Dunn. 1995. Symbiotic induction of a MADS-box gene during development of alfalfa root nodules. Proceedings of the National Academy of Sciences, USA 92: 5273-5277.
25. Hicks, G. H. 1897. Passion flowers. Asa Gray Bulletin 5: 51-54.
26. Hileman, L. C., S. Drea, G. Martino, A. Litt, and V. F. Irish. 2005. Virus-induced gene silencing is an effective tool for assaying gene function in the basal eudicot species Papaver somniferum (opium poppy). Plant Journal 44: 334-341.
27. Janssen, B. J., A. Williams, J. J. Chen, J. Mathern, S. Hake, and N. Sinha. 1998. Isolation and characterization of two knotted-like homeobox genes from tomato. Plant Molecular Biology 36: 417-425.
28. Jaramillo, M. A., and E. M. Kramer. 2004. APETALA3 and PISTILLATA homologs exhibit novel expression patterns in the unique perianth of Aristolochia (Aristolochiaceae). Evolution & Development 6: 449-458.
29. Jaramillo, M. A., and E. M. Kramer. 2007. The role of developmental genetics in understanding homology and morphological evolution in plants. International Journal of Plant Sciences 168: 61-72.
30. Kellogg, E. A. 2000. The grasses: A case study in macroevolution. Annual Review of Ecology and Systematics 31: 217-238.
31. Kramer, E. M., and M. A. Jaramillo. 2005. Genetic basis for innovations in floral organ identity. Journal of Experimental Zoology, B, Molecular and Developmental Evolution 304B: 526-535.
32. Kramer, E. M., M. A. Jaramillo, and V. S. Di Stilio. 2004. Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166: 1011-1023.
33. Krizek, B. A., and E. M. Meyerowitz. 1996. The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122: 11-22.
34. Krosnick, S. E., E. M. Harris, and J. V. Freudenstein. 2006. Patterns of anomalous floral development in the Asian Passiflora (subgenus Decaloba: supersection Disemma). American Journal of Botany 93: 620-636.
35. Li, P., and M. Johnston. 2000. Heterochrony in plant evolutionary studies through the twentieth century. Botanical Review 66: 57-88.
36. Linnaeus, C. 1753. Species plantarum. L. Salvius, Stockholm, Sweden.
37. Liu, Y., N. Nakayama, M. Schiff, A. Litt, V. F. Irish, and S. P. Dinesh-Kumar. 2004. Virus induced gene silencing of a DEFICIENS ortholog in Nicotiana benthamiana. Plant Molecular Biology 54: 701-711.
38. Maddison, D. R., and W. P. Maddison. 2003. MacClade: Analysis of phylogeny and character evolution, version 4.06. Sinauer, Sunderland, Massachusetts, USA
39. Malcomber, S. T., and E. A. Kellogg. 2004. Heterogeneous expression patterns and separate roles of the SEPALLATA gene LEAFY HULL STERILE1 in grasses. Plant Cell 16: 1692-1706.
40. Manders, G., W. Otoni, F. d' Utra Vaz, N. Blackball, J. Power, and M. Davey. 1994. Transformation of passionfruit (Passiflora edulis fv flavicarpa Degener.) using Agrobacterium tumefaciens. Plant Cell Reports 13: 697-702.
41. Masters, M. T. 1871. Contributions to the natural history of Passifloraceae. Transactions of the Linnean Society of London 27: 593-645.
42. Mazzucato, A., I. Olimpieri, F. Siligato, M. E. Picarella, and G. P. Soressi. 2008. Characterization of genes controlling stamen identity and development in a parthenocarpic tomato mutant indicates a role for the DEFICIENS ortholog in the control of fruit set. Physiologia Plantarum 132: 526-537.
43. Moncur, M. W. 1988. Floral development of tropical and subtropical fruit and nut species. Commonwealth Scientific and Industrial Research Organization, Collingwood, Australia.
44. Pelaz, S., G. S. Ditta, E. Baumann, E. Wisman, and M. F. Yanofsky. 2000. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405: 200-203.
45. Pinyopich, A., G. S. Ditta, B. Savidge, S. J. Liljegren, E. Baumann, E. Wisman, and M. F. Yanofsky. 2003. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424: 85-88.
46. Poupin, M. J., F. Federici, C. Medina, J. T. Matus, T. Timmermann, and P. Arce-Johnson. 2007. Isolation of the three grape sublineages of B-class MADS-box TM6, PISTILLATA and APETALA3 genes which are differentially expressed during flower and fruit development. Gene 404: 10-24.
47. Preston, J. C., A. Christensen, S. T. Malcomber, and E. A. Kellogg. 2009. MADS-box gene expression and implications for developmental origins of the grass spikelet. American Journal of Botany 96: 1419-1429.
48. Puri, V. 1948. Studies in floral anatomy, V. On the structure and nature of the corona in certain species of the Passifloraceae. Journal of the Indian Botanical Society 27: 130-149.
49. Riechmann, J. L., B. A. Krizek, and E. M. Meyerowitz. 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.
50. Riechmann, J. L., M. Wang, and E. M. Meyerowitz. 1996b. DNAbinding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Research 24: 3134-3141.
51. Robertson, D. 2004. VIGS vectors for gene silencing: Many targets, many tools. Annual Review of Plant Biology 55: 495-519.
52. Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
53. Ronse Decraene, L. P. 2007. Are petals sterile stamens or bracts? The origin and evolution of petals in the core eudicots. Annals of Botany 100: 621-630.
54. Sajo, M. das G., R. de Mello-Silva, and P. J. Rudall. 2010. Homologies of floral structures in Velloziaceae with particular reference to the corona. International Journal of Plant Sciences 171: 595-606.
55. Stevens, P. F. 2001 onward. Angiosperm Phylogeny Website, version 9, June 2008 [and more or less continuously updated], website http:/www.mobot.org/MOBOT/research/APweb/.
56. Theissen, G. 2001. Genetics of identity. Nature 414: 491.
57. Ulmer, T., and J. M. MacDougal. 2004. Passiflora: Passionflowers of the world. Timber Press, Portland, Oregon, USA.
58. Vanderplank, J. 1991. Passion flowers and passion fruit. 1st ed. MIT Press, Cambridge, Massachusetts, USA.
59. Whipple, C. J., M. J. Zanis, E. A. Kellogg, and R. J. Schmidt. 2007. Conservation of B class gene expression in the second whorl of a basal grass and outgroups links the origin of lodicules and petals. Proceedings of the National Academy of Sciences, USA 104: 1081-1086.
60. Yockteng, R., and S. Nadot. 2004. Phylogenetic relationships among Passiflora species based on the glutamine synthetase nuclear gene expressed in chloroplast (ncpGS). Molecular Phylogenetics and Evolution 31: 379-396.
61. Yu, D., M. Kotilainen, E. Pollanen, M. Mehto, P. Elomaa, Y. Helariutta, V. A. Albert, et al. 1999. Organ identity genes and modified patterns of flower development in Gerbera hybrida (Asteraceae). Plant Journal 17: 51-62.
62. Zahn, L. M., J. H. Leebens-Mack, J. M. Arrington, Y. Hu, L. L. Landherr, C. W. dePamphilis, A. Becker, et al. 2006. Conservation and divergence in the AGAMOUS subfamily of MADSbox genes: Evidence of independent sub-and neofunctionalization events. Evolution & Development 8: 30-45.
63. Zahn, L. M., J. Leebens-Mack, C. W. dePamphilis, H. Ma, and G. Theissen. 2005. To B 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.