Petunia pp 157-177 | Cite as

Vegetative Branching in Petunia

  • Revel S.M. Drummond
  • Susan E. Ledger
  • Joanne L. Simons
  • Bart J. Janssen
  • Kimberley C. Snowden


Plant form is established by the response of the plant to endogenous and environmental cues. One architectural process for which genetic components have been identified is the decision for axillary buds to grow. In Petunia, a number of genes involved in the decision to branch have been identified and aspects of their functions are elucidated. The genes altered in the dad mutants appear to be involved in a single pathway that controls branching and to interact with auxin and cytokinins. These genes mediate the production and reception of hormones inducing and suppressing bud outgrowth. Among species there is a high degree of gene conservation in the pathway and the similarities and differences in gene functions have shown the power of using multiple plant systems. The understanding of developmental processes allows controlled modifications to be made, and the continuing research into axillary bud fate will have a significant impact on future improvements to crop species.


Shoot Apical Meristem Apical Dominance Plant Architecture Auxin Level Main Shoot 


  1. Adams, S., Pearson, S. and Hadley, P. (1997) The effects of temperature and photoperiod on the flowering and morphology of trailing petunias. Acta Hort. 435, 65–75.Google Scholar
  2. Aguilar-Martínez, J., Poza-Carrión, C. and Cubas, P. (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19, 458–472.CrossRefPubMedGoogle Scholar
  3. Apisitwanich, S., Swiecicki, W. and Wolko, B. (1992) A new ramosus gene on chromosome 5. Pisum Genetics 24, 14–15.Google Scholar
  4. Arite, T., Iwata, H., Ohshima, K., Maekawa, M., Nakajima, M., Kojima, M., Sakakibara, H. and Kyozuka, J. (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J. 51, 1019–1029.CrossRefPubMedGoogle Scholar
  5. Arumingtyas, E., Floyd, R., Gregory, M. and Murfet, I. (1992) Branching in Pisum: Inheritance and allelism tests with 17 ramosus mutants. Pisum Genet. 24, 17–31.Google Scholar
  6. Auldridge, M., Block, A., Vogel, J., Dabney-Smith, C., Mila, I., Bouzayen, M., Magallanes-Lundback, M., DellaPenna, D., McCarty, D. and Klee, H. (2006) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J. 45, 982–993.CrossRefPubMedGoogle Scholar
  7. Bennett, T., Sieberer, T., Willett, B., Booker, J., Luschnig, C. and Leyser, O. (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr. Biol.16, 553–563.CrossRefPubMedGoogle Scholar
  8. Beveridge, C., Ross, J. and Murfet, I. (1996) Branching in pea (action of genes Rms3 and Rms4). Plant Physiol. 110, 859–865.PubMedGoogle Scholar
  9. Beveridge, C., Symons, G., Murfet, I., Ross, J. and Rameau, C. (1997) The rms1 mutant of pea has elevated indole-3-acetic acid levels and reduced root-sap zeatin riboside content but increased branching controlled by graft-transmissible signal(s). Plant Physiol. 115, 1251–1258.Google Scholar
  10. Beveridge, C. (2000) Long-distance signalling and a mutational analysis of branching in pea. Plant Growth Reg. 32, 193–203.CrossRefGoogle Scholar
  11. Blixt, S. (1976) Linkage studies in Pisum. XV. Establishing the RMS-gene and the linkage of RMS and FAS in chromosome 3. Agri. Hort. Genet. 34, 83–87.Google Scholar
  12. Booker, J., van de Sande, K. and Leyser, H. (1999) max3, an Arabidopsis mutant with a modified pattern of aerial branching. Biol. Plantar. 42, S41.CrossRefGoogle Scholar
  13. Booker, J., Chatfield, S. and Leyser, O. (2003) Auxin acts in xylem-associated or medullary cells to mediate apical dominance. Plant Cell 15, 495–507.CrossRefPubMedGoogle Scholar
  14. Booker, J., Auldridge, M., Wills, S., McCarty, D., Klee, H. and Leyser, O. (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr. Biol. 14, 1232–1238.CrossRefPubMedGoogle Scholar
  15. Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P. and Leyser, O. (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Develop. Cell 8, 443–449.CrossRefGoogle Scholar
  16. Brunaud, A., Bognon, F. and Cornu, A. (1977) Analyse du port chez des Petunia. Bulletin de la société botanique de France 124, 307–327.Google Scholar
  17. Burnham, C (1959) Teosinte branched. Maize Genet. Coop. News. 33, 74.Google Scholar
  18. Cathey, H. and Campbell, L. (1984) Plant Physiol. In: K Sink (Ed.), Petunia: Monographs on Theoretical and Applied Genetics 9. Springer-Verlag, Berlin, pp. 208–230.Google Scholar
  19. Clark, D., Dervinis, C., Barret, J., Klee, H. and Jones, M. (2004) Drought-induced leaf senescence and horticultural performance of transgenic P-SAG12-IPT petunias. J. Amer. Soc. Hort. Sci. 129, 93–99.Google Scholar
  20. Cline, M. (1994) The role of hormones in apical dominance. New approaches to an old problem in plant development. Physiol. Plantar. 90, 230–237.CrossRefGoogle Scholar
  21. Cline, M. (1996) Exogenous auxin effects on lateral bud outgrowth in decapitated shoots. Ann. Bot. 78, 255–266.CrossRefGoogle Scholar
  22. Doebley, J., Stec, A. and Gustus, C. (1995) teosinte branched1 and the origin of maize: Evidence for epistasis and the evolution of dominance. Genetics 141, 333–346.PubMedGoogle Scholar
  23. Doebley, J., Stec, A. and Hubbard, L. (1997) The evolution of apical dominance in maize. Nature 386, 485–488.CrossRefPubMedGoogle Scholar
  24. Dun, E., Ferguson, B. and Beveridge, C. (2006) Apical dominance and shoot branching: Divergent opinions or divergent mechanisms? Plant Physiol. 142, 812–819.CrossRefPubMedGoogle Scholar
  25. Finlayson, S. (2007) Arabidopsis TEOSINTE BRANCHED1-LIKE 1 regulates axillary bud outgrowth and is homologous to monocot TEOSINTE BRANCHED1. Plant Cell Physiol. 48, 667–677.CrossRefPubMedGoogle Scholar
  26. Gao, M., Kieliszewski, M., Lamport, D. and Showalter, A. (1999) Isolation, characterization and immunolocalization of a novel, modular tomato arabinogalactan-protein corresponding to the LeAGP-1 gene. Plant J. 18, 43–55.CrossRefPubMedGoogle Scholar
  27. Haver, D. and Schuch, U. (2001) Influence of root restriction and ethylene exposure on apicaldominance of petunia (Petunia x hybrida Hort. Vilm.-Andr.). Plant Growth Reg. 35, 187–196.CrossRefGoogle Scholar
  28. Haver, D., Schuch, U. and Lovatt, C. (2003) Exposure of petunia seedlings to ethylene decreased apical dominance by reducing the ratio of auxin to cytokinin. J. Plant Growth Reg. 21, 459–468.CrossRefGoogle Scholar
  29. Ishikawa, S., Maekawa, M., Arite, T., Onishi, K., Takamure, I. and Kyozuka, J. (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol. 46, 79–86.CrossRefPubMedGoogle Scholar
  30. Johnson, X., Brcich, T., Dun, E., Goussot, M., Haurogné, K., Beveridge, C. and Rameau, C. (2006) Branching genes are conserved across species: Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol. 142, 1014–1026.CrossRefPubMedGoogle Scholar
  31. Kamoda, S. and Saburi, Y. (1993a) Cloning, expression and sequence analysis of a lignostilbene-α,β-dioxygenase gene from Pseudomonas paucimobilis TMY1009. Biosci. Biotech. Biochem. 57, 926–930.Google Scholar
  32. Kamoda, S. and Saburi, Y. (1993b) Structural and enzymatical comparison of lignostilbene-α,β-dioxygenase isozymes, I, II and III, from Pseudomonas paucimobilis TMY1009. Biosci. Biotech. Biochem. 57, 931–934.Google Scholar
  33. Kebrom, T., Burson, B. and Finlayson, S. (2006) Phytochrome B represses Teosinte Branched1 expression and induces sorghum axillary bud outgrowth in response to light signals. Plant Physiol. 140, 1109–1117.CrossRefPubMedGoogle Scholar
  34. Klee, H., Horsch, R., Hinchee, M., Hein, M. and Hoffmann, N. (1987) The effects of overproduction of two Agrobacterium tumefaciens T-DNA auxin biosynthetic gene products in transgenic petunia plants. Genes Devel. 1, 86–96.Google Scholar
  35. Klee, H. (2003) Hormones are in the air. Proc. Natl. Acad. Sci., USA 100, 10144–10145.CrossRefPubMedGoogle Scholar
  36. Lukens, L. and Doebley, J. (2001) Molecular evolution of the teosinte branched gene among maize and related grasses. Molec. Biol. Evol. 18, 627–638.PubMedGoogle Scholar
  37. Moiseyev, G., Chen, Y., Takahashi, Y., Wu, B.X. and Ma, J.-X. (2005) RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc. Natl. Acad. Sci., USA 102, 12413–12418.CrossRefPubMedGoogle Scholar
  38. Morris, S., Turnbull, C., Murfet, I. and Beveridge, C. (2001) Mutational analysis of branching in pea. Evidence that Rms1 and Rms5 regulate the same novel signal. Plant Physiol. 126, 1205–1213.CrossRefPubMedGoogle Scholar
  39. Morris, S.E., Beveridge, C.A., Murfet, I.C., Prioul, S. and Rameau, C. (2003) The basal-branching pea mutant rms7-1. Pisum Genet. 35, 10–14.Google Scholar
  40. Nakagawa, H., Jiang, C.J., Sakakibara, H., Kojima, M., Honda, I., Ajisaka, H., Nishijima, T., Koshioka, M., Homma, T., Mander, L.N. and Takatsuji, H. (2005) Overexpression of a petunia zinc-finger gene alters cytokinin metabolism and plant forms. Plant Journal 41, 512–523.CrossRefPubMedGoogle Scholar
  41. Napoli, C. (1996) Highly branched phenotype of the petunia dad1-1 mutant is reversed by grafting. Plant Physiol. 111, 27–37.PubMedGoogle Scholar
  42. Napoli, C.A. and Ruehle, J. (1996) New mutations affecting meristem growth and potential in Petunia hybridaVilm. J. Hered. 87, 371–377.Google Scholar
  43. Napoli, C.A., Beveridge, C.A. and Snowden, K.C. (1999) Reevaluating concepts of apical dominance and the control of axillary bud outgrowth. Curr. Topics Develop. Biol. 44, 127–169.CrossRefGoogle Scholar
  44. Nelson, D.R., Schuler, M.A., Paquette, S.M., Werck-Reichhart, D. and Bak, S. (2004) Comparative genomics of rice and Arabidopsis. Analysis of 727 Cytochrome P450 genes and pseudogenes from a monocot and a dicot. Plant Physiol. 135, 756–772.CrossRefPubMedGoogle Scholar
  45. Nordström, A., Tarkowski, P., Tarkowska, D., Norbaek, R., Åstot, C., Dolezal, K. and Sandberg, G. (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: A factor of potential importance for auxin-cytokinin-regulated development. Proc. Natl. Acad. Sci., USA 101, 8039–8044.CrossRefPubMedGoogle Scholar
  46. Oh, S.A., Park, J.-H., Lee, G.I., Paek, K.H., Park, S.K. and Nam, H.G. (1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J. 12, 527–535.CrossRefPubMedGoogle Scholar
  47. Pillay, I. and Railton, I.D. (1983) Complete release of axillary buds from apical dominance in intact, light-grown seedlings of Pisum sativum L. following a single application of cytokinin. Plant Physiol. 71, 972–974.CrossRefPubMedGoogle Scholar
  48. Prinsen, E., Redig, P., Van Onckelen, H., Van Dongen, W. and Esmans, E. (1995) Quantitative analysis of cytokinins by electrospray tandem mass spectrometry. Rapid Comm. Mass Spec. 9, 948–953.Google Scholar
  49. Rameau, C., Murfet, I., Laucou, V., Floyd, R., Morris, S. and Beveridge, C. (2002) Pea rms6 mutants exhibit increased basal branching. Physiol. Plantar. 115, 458–467.CrossRefGoogle Scholar
  50. Ross, J. (1998) Effects of auxin transport inhibitors on gibberellins in pea. J. Plant Growth Reg. 17, 141–146.CrossRefGoogle Scholar
  51. Schwartz, S.H., Tan, B.C., Gage, D.A., Zeevaart, J.A.D. and McCarty, D.R. (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276, 1872–1874.CrossRefPubMedGoogle Scholar
  52. Schwartz, S., Qin, X. and Loewen, M. (2004) The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J. Biol. Chem. 279, 46940–46945.CrossRefPubMedGoogle Scholar
  53. Simons, J., Napoli, C., Janssen, B., Plummer, K. and Snowden, K. (2007) Analysis of the DECREASED APICAL DOMINANCE genes of petunia in the control of axillary branching. Plant Physiol. 143, 697–706.CrossRefPubMedGoogle Scholar
  54. Snowden, K. and Napoli, C. (2003) A quantitative study of lateral branching in petunia. Funct. Plant Biol. 30, 987–994.CrossRefGoogle Scholar
  55. Snowden, K., Simkin, A., Janssen, B., Templeton, K., Loucas, H., Simons, J., Karunairetnam, S., Gleave, A., Clark, D. and Klee, H. (2005) The decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17, 746–759.CrossRefPubMedGoogle Scholar
  56. Sorefan, K., Booker, J., Haurogne, K., Goussot, M., Bainbridge, K., Foo, E., Chatfield, S., Ward, S., Beveridge, C., Rameau, C. and Leyser, O. (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Devel. 17, 1469–1474.CrossRefPubMedGoogle Scholar
  57. Souer, E., van der Krol, A., Kloos, D., Spelt, C., Bliek, M., Mol, J. and Koes, R. (1998) Genetic control of branching pattern and floral identity during Petunia inflorescence development. Development 125, 733–742.PubMedGoogle Scholar
  58. Steeves, T. and Sussex, I. (1989) Patterns in Plant Development, 2nd edn. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  59. Stirnberg, P., van de Sande, K. and Leyser, H. (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Devel. 129, 1131–1141.Google Scholar
  60. Symons, G., Murfet, I., Ross, J., Sherriff, L. and Watkentin, T. (1999) bushy, a dominant pea mutant characterised by short, thin stems, tiny leaves, and a major reduction in apical dominance. Physiol. Plantar. 107, 346–352.CrossRefGoogle Scholar
  61. Synková, H., Wilhelmová, N., Šesták, Z. and Pospíšilová, J. (1997) Photosyntesis in transgenic plants with elevated cytokinin contents. In: M. Pessarakli (Ed.), Handbook of Photosynthesis. Marcel Dekker, NY, pp. 541–552.Google Scholar
  62. Takeda, T., Suwa, Y., Suzuki, M., Kitano, H., Ueguchi-Tanaka, M., Ashikari, M., Matsuoka, M. and Ueguchi, C. (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J. 33, 513–520.CrossRefPubMedGoogle Scholar
  63. Tanaka, M., Takei, K., Kojima, M., Sakakibara, H. and Mori, H. (2006) Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J. 45, 1028–1036.CrossRefPubMedGoogle Scholar
  64. Thomas, R. and Hay, M. (2007) Cumulative activation of axillary buds by nodal roots in Trifolium repens L. J. Exper. Bot. 58, 2069–2078.CrossRefGoogle Scholar
  65. Turnbull, C., Raymond, M., Dodd, I. and Morris, S. (1997) Rapid increases in cytokinin concentration in lateral buds of chickpea (Cicer arietinum L.) during release of apical dominance. Planta 202, 271–276.CrossRefGoogle Scholar
  66. Turnbull, C., Booker, J. and Leyser, H. (2002) Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J. 32, 255–262.CrossRefPubMedGoogle Scholar
  67. von Lintig, J. and Vogt, K. (2000) Filling the Gap in Vitamin A Research: Molecular identification of an enzyme cleaving β-carotene to retinal. J. Biol. Chem. 275, 11915–11920.CrossRefGoogle Scholar
  68. Woo, H., Chung, K., Park, J.-H., Oh, S., Ahn, T., Hong, S., Jang, S. and Nam, H. (2001) ORE9, an F-Box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13, 1779–1790.CrossRefPubMedGoogle Scholar
  69. Zou, J., Chen, Z., Zhang, S., Zhang, W., Jiang, G., Zhao, X., Zhai, W., Pan, X. and Zhu, L. (2005) Characterizations and fine mapping of a mutant gene for high tillering and dwarfing in rice (Oryza sativa L.). Planta 222, 604–612.CrossRefPubMedGoogle Scholar
  70. Zubko, E., Adams, C., Machaekova, I., Malbeck, J., Scollan, C. and Meyer, P. (2002) Activation tagging identifies a gene from Petunia hybrida responsible for the production of active cytokinins in plants. Plant J. 29, 797–808.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Revel S.M. Drummond
    • 1
  • Susan E. Ledger
  • Joanne L. Simons
  • Bart J. Janssen
  • Kimberley C. Snowden
  1. 1.HortResearchPrivate BagAucklandNew Zealand

Personalised recommendations