Forbidden Fruit: Dominance Relationships and the Control of Shoot Architecture
Catriona H. Walker
School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, UK
Search for more papers by this authorTom Bennett
School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, UK
Search for more papers by this authorCatriona H. Walker
School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, UK
Search for more papers by this authorTom Bennett
School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, UK
Search for more papers by this authorAbstract
Plants continually integrate environmental information to make decisions about their development. Correlative controls, in which one part of the plant regulates the growth of another, form an important class of regulatory mechanism, but their study has been neglected, and their molecular basis remains unclear. In this article, we examine the role of negative correlative controls or ‘dominance’ phenomena in the regulation of shoot architecture. Apical dominance, in which actively growing shoot branches inhibit the growth of other branches, is perhaps the most famous example of this. We discuss the recent progress made in understanding the mechanistic basis for apical dominance and three plausible models for shoot branching control. We then use the apical dominance paradigm to explore other dominance phenomena, including seed–seed inhibition (carpic dominance), seed-to-meristem inhibition, and the control of maternal senescence by seeds. We propose that apical and carpic dominance may share a common mechanistic basis rooted in auxin transport canalisation. Conversely, we conclude that seed-to-meristem inhibition and seed-driven senescence may not be ‘true’ correlative controls, but rather more complex phenomena in which seed set plays a permissive rather than instructive role. Overall, we attempt to develop a coherent framework for understanding the developmental and regulatory mechanisms that control shoot architecture and provide new insights into the end of flowering, fruiting, and growth.
References
- Abruzzese, A., Mignani, I., and Cocucci, S.M. (1995). Nutritional status in apples and June drop. Journal of the American Society for Horticultural Science 120: 71–74.
- Adamowski, M. and Friml, J. (2015). PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27: 20–32.
- Aguilar-Martínez, J.A., Poza-Carrión, C., and Cubas, P. (2007). Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. The Plant Cell 19: 458–472.
- Arite, T., Iwata, H., Ohshima, K. et al. (2007). DWARF10, an RMS1/MAX4/DAD1 ortholog controls lateral bud outgrowth in rice. The Plant Journal 51: 1019–1029.
- Balla, J., Kalousek, P., Reinöhl, V. et al. (2011). Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth. The Plant Journal 65: 571–577.
- Balla, J., Medvedova, Z., Kalousek, P. et al. (2016). Auxin flow-mediated competition between axillary buds to restore apical dominance. Scientific Reports 6: 35955.
- Bangerth, F. (1989). Dominance among fruits/sinks and the search for a correlative signal. Physiologia Plantarum 76: 608–614.
- Bangerth, F. (2000). Abscission and thinning of young fruit and their regulation by plant hormones and bioregulators. Plant Growth Regulation 31: 43–59.
- Barbier, F.F., Lunn, J.E., and Beveridge, C.A. (2015a). Ready, steady, go! A sugar hit starts the race to shoot branching. Current Opinion in Plant Biology 25: 39–45.
- Barbier, F., Péron, T., Lecerf, M. et al. (2015b). Sucrose is an early modulator of the key hormonal mechanisms controlling bud outgrowth in Rosa hybrida . Journal of Experimental Biology 66: 2569–2582.
-
Bennett, T. and Leyser, O. (2014). The auxin question: a philosophical overview. In: Auxin and its Role in Plant Development (ed. E. Zažímalová, J. Petrasek and E. Benkova), 3–19. Berlin: Springer.
10.1007/978-3-7091-1526-8_1 Google Scholar
- Bennett, T., Sieberer, T., Willett, B. et al. (2006). The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Current Biology 16: 553–563.
- Bennett, T., Hines, G., and Leyser, O. (2014). Canalization: what the flux? Trends in Genetics 30: 41–48.
- Bennett, T., Hines, G., van Rongen, M. et al. (2016). Connective auxin transport in the shoot facilitates communication between shoot apices. PLoS Biology 14: e1002446.
- Bohner, J. and Bangerth, F. (1988). Effects of fruit set sequence and defoliation on cell number, cell size and hormone levels of tomato fruits (Lycopersicon esculentum mill.) within a truss. Journal of Plant Growth Regulation 7: 141–155.
- Booker, J., Chatfield, S., and Leyser, O. (2003). Auxin acts in xylem-associated or medullary cells to mediate apical dominance. The Plant Cell 15: 495–507.
- Braun, N., de Saint Germain, A., Pillot, J.-P. et al. (2012). The pea TCP transcription factor PsBRC1 acts downstream of Strigolactones to control shoot branching. Plant Physiology 158: 225–238.
- Brewer, P.B., Dun, E.A., Ferguson, B.J. et al. (2009). Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiology 150: 482–493.
- Brewer, P.B., Dun, E.A., Gui, R. et al. (2015). Strigolactone inhibition of branching independent of polar auxin transport. Plant Physiology 168: 1820–1829.
- Brown, B.T., Foster, C., Phillips, J.N., and Rattigann, B.M. (1979). The indirect role of 2,4-D in the maintenance of apical dominance in decapitated sunflower seedlings (Helianthus annus L.). Planta 146: 475–480.
- Carbonell-Bejerano, P., Urbez, C., Granell, A. et al. (2011). Ethylene is involved in pistil fate by modulating the onset of ovule senescence and the GA mediated fruit set in Arabidopsis. BMC Plant Biology 11: 84.
- Chatfield, S.P., Stirnberg, P., Forde, B.G., and Leyser, O. (2000). The hormonal regulation of axillary bud growth in Arabidopsis . The Plant Journal 24: 159–169.
- Child, R.D., Chauvaux, N., John, K. et al. (1998). Ethylene biosynthesis in oilseed rape pods in relation to pod shatter. Journal of Experimental Botany 49: 829–838.
- Cline, M.G. (1997). Concepts and terminology of apical dominance. American Journal of Botany 84: 1064–1069.
- Crawford, S., Shinohara, N., Sieberer, T. et al. (2010). Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137: 2905–2913.
- Domagalska, M.A. and Leyser, O. (2011). Signal integration in the control of shoot branching. Nature Reviews. Molecular Cell Biology 12: 211–221.
- Dun, E.A., Ferguson, B.J., and Beveridge, C.A. (2006). Apical dominance and shoot branching. Divergent opinions or divergent mechanisms? Plant Physiology 142: 812–819.
- Dun, E.A., de Saint Germain, A., Rameau, C., and Beveridge, C.A. (2012). Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiology 158: 487–498.
- Dun, E.A., de Saint Germain, A., Rameau, C., and Beveridge, C.A. (2013). Dynamics of strigolactone function and shoot branching responses in Pisum sativum . Molecular Plant 6: 128–140.
- Everat-Bourbouloux, A. and Bonnemain, J.-L. (1980). Distribution of labelled auxin and derivatives in stem tissues of intact and decapitated broad-bean plants in relation to apical dominance. Physiologia Plantarum 50: 145–152.
- Finlayson, S.A., Krishnareddy, S.R., Kebrom, T.H., and Casal, J.J. (2010). Phytochrome regulation of branching in Arabidopsis. Plant Physiology 152: 1914–1927.
- Fisher, J.E. (1973). Developmental morphology of the inflorescence in hexaploid wheat cultivars with and without the cultivar Norin 10 in their ancestry. Canadian Journal of Plant Science 53: 7–15.
- Forde, B.G. (2014). Nitrogen signalling pathways shaping root system architecture: an update. Current Opinion in Plant Biology 21: 30–36.
- Franklin, K.A., Toledo-Ortiz, G., Pyott, D.E., and Halliday, K.J. (2014). Interaction of light and temperature signalling. Journal of Experimental Botany 65: 2859–2871.
-
de Freitas Lima, M., Eloy, N.B., de Siqueira, J.A.B. et al. (2017). Molecular mechanisms of biomass increase in plants. Biotechnology doi: 10.1016/j.biori.2017.08.001.
10.1016/j.biori.2017.08.001 Google Scholar
- Goetz, M., Vivian-Smith, A., Johnson, S.D., and Koltunow, A.M. (2006). AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. The Plant Cell 18: 1873–1886.
- Goetz, M., Hooper, L.C., Rodrigues, J.C.M. et al. (2007). Expression of aberrant forms of AUXIN RESPONSE FACTOR8 stimulates parthenocarpy in Arabidopsis and tomato. Plant Physiology 145: 351–366.
- Gomez-Roldan, V., Fermas, S., Brewer, P.B. et al. (2008). Strigolactone inhibition of shoot branching. Nature 455: 189–194.
- González-Grandío, E., Poza-Carríon, C., Sorzano, C.O.S., and Cubas, P. (2013). BRANCHED1 promotes axillary bud dormancy in response to shade in Arabidopsis . The Plant Cell 25: 834–850.
- Guan, J.C., Koch, K.E., Suzuki, M. et al. (2012). Diverse roles of strigolactone signaling in maize architecture and the uncoupling of a branching-specific subnetwork. Plant Physiology 160: 1303–1317.
- Guan, P., Ripoll, J.-J., Wang, R. et al. (2017). Interacting TCP and NLP transcription factors control plant responses to nitrate availability. Proceedings of the National Academy of Sciences 114: 2419–2424.
- Hall, S.M. and Hillman, J.R. (1975). Correlative inhibition of lateral bud growth in Phaseolus vulgaris L. timing of bud growth following decapitation. Planta 123: 137–143.
- Hempel, F.D. and Feldman, L.J. (1994). Bi-directional inflorescence development in Arabidopsis Thaliana: acropetal initiation of flowers and basipetal initiation of paraclade. Planta 192: 276–286.
- Hensel, L.L., Grbic, V., Baumgarten, D.B., and Bleecker, A.B. (1993). Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis . Plant Cell 5: 553–564.
- Hensel, L.L., Nelson, M.A., Richmond, T.A., and Bleeker, A.B. (1994). The fate of inflorescence meristems is controlled by developing fruits in Arabidopsis . Plant Physiology 106: 863–876.
- Heuvelink, E. and Korner, O. (2001). Parthenocarpic fruit growth reduces yield fluctuation and blossom-end rot in sweet pepper. Annals of Botany 88: 69–74.
- Hildebrand, F. (1881). Die lebensdauer und vegetationsweise der pflanzen, ihre ursache und ihre entwicklung. Botanische Jahrbücher fur Systematik 2: 51–135.
- de Jong, M., George, G., Ongaro, V. et al. (2014). Auxin and Strigolactone signaling are required for modulation of Arabidopsis shoot branching by nitrogen supply. Plant Physiology 166: 384–395.
- Karasov, T., Chae, E., Herman, J. et al. (2017). Mechanisms to mitigate the tradeoff between growth and defense. The Plant Cell doi: 10.1105/tpc.16.00931.
- Kebrom, T.H., Burson, B.L., and Finlayson, S.A. (2006). Phytochrome B represses Teosinte Branched1 expression and induces sorghum axillary bud outgrowth in response to light signals. Plant Physiology 140: 1109–1117.
- Kebrom, T.H., Brutnell, T.P., and Finlayson, S.A. (2010). Suppression of sorghum axillary bud outgrowth by shade, phyB and defoliation signalling pathways. Plant, Cell and Environment 33: 48–58.
- Kim, I.S., Okubo, H., and Fujieda, K. (1992). Endogenous levels of IAA in relation to parthenocarpy in cucumber (Cucumis sativus L.). Scientia Horticulturae 52: 1–8.
- Kohlen, W., Charnikhova, T., Liu, Q. et al. (2011). Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis . Plant Physiology 155: 972–987.
- Krapp, A., David, L.C., Chardin, C. et al. (2014). Nitrate transport and signalling in Arabidopsis. Journal of Experimental Botany 65: 789–798.
- Lastdrager, J., Hanson, J., and Smeekens, S. (2014). Sugar signals and the control of plant growth and development. Journal of Experimental Botany 65: 799–807.
- Lenser, T., Graeber, K., Cevik, Ö.S. et al. (2016). Developmental control and plasticity of fruit and seed dimorphism in Aethionema arabicum . Plant Physiology 172: 1691–1707.
- Leopold, A.C., Niedergang-Kamien, E., and Janick, J. (1959). Experimental modification of plant senescence. Plant Physiology 34: 570–573.
- Leyser, O. (2011). Auxin, self-organisation, and the colonial nature of plants. Current Biology 21: 331–337.
- Li, C.-J. and Bangerth, F. (1999). Autoinhibition of indoleacetic acid transport in the shoots of two-branched pea (Pisum sativum) plants and its relationship to correlative dominance. Physiologia Plantarum 106: 415–420.
- Li, H., Ma, Q., Li, H. et al. (2014). Root morphological responses to localised nutrient supply differ among crop species with contrasting root traits. Plant and Soil 376: 151–163.
- López-Ráez, J.A., Charnikhova, T., Gómez-Roldán, V. et al. (2008). Tomato Strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytologist 178: 863–874.
- Marhavy, P., Duclercg, J., and Weller, B. (2014). Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Current Biology 24: 1031–1037.
- Martínez, C., Manzano, S., Megías, Z. et al. (2013). Involvement of ethylene biosynthesis and signalling in fruit set and early fruit development in zucchini squash (Cucurbita pepo L.). BMC Plant Biology 13: 139.
- Mason, M.G., Ross, J.J., Babst, B.A. et al. (2014). Sugar demand, not auxin, is the initial regulator of apical dominance. Proceedings of the National Academy of Sciences 111: 6092–6097.
- Medici, A. and Krouk, G. (2014). The primary nitrate response: a multifaceted signalling pathway. Journal of Experimental Botany 65: 5567–5576.
- Minakuchi, K., Kameoka, H., Yasuno, N. et al. (2010). FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant and Cell Physiology 51: 1127–1135.
- Molisch, H. (1929). Die Lebensdauer der Pflanze. Germany: Verlag von Gustav Fischer.
- Morris, D.A. (1977). Transport of exogenous auxin in two-branched dwarf pea seedlings (Pisum sativum L.): some implications for polarity and apical dominance. Planta 136: 91–96.
- Morris, S.E., Cox, M.C., Ross, J.J. et al. (2005). Auxin dynamics after decapitation are not correlated with the initial growth of axillary buds. Plant Physiology 138: 1665–1672.
- Muller, D., Waldie, T., Miyawaki, K. et al. (2015). Cytokinin is required for escape but not release from auxin mediated apical dominance. The Plant Journal 82: 874–886.
- Nooden, L.D. (1984). Integration of soybean pod development and monocarpic senescence. Physiologia Plantarum 62: 273–284.
- Nooden, L.D. and Penney, J.P. (2001). Correlative controls of senescence and plant death in Arabidopsis Thaliana (Brassicaceae). Journal of Experimental Botany 52: 2151–2159.
- Nordstrom, A., Tarkowski, P., Tarkowska, D. et al. (2004). Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proceedings of the National Academy of Sciences 101: 8039–8044.
- Ojehomon, O.O. (1970). Effects of continuous removal of open flowers on the seed yield of two varieties of cowpea (V. unguiculata). Journal of Agricultural Science 74: 375–381.
- Ongaro, V., Bainbridge, K., Williamson, L., and Leyser, O. (2008). Interactions between axillary branches of Arabidopsis . Molecular Plant 1: 388–400.
-
Ostergaard, L. (2009). Annual Plant Reviews, Fruit Development and Seed Dispersal. Sussex: Wiley-Blackwell.
10.1002/9781444314557 Google Scholar
- Pandolfini, T. (2009). Seedless fruit production by hormonal regulation of fruit set. Nutrients 168–177.
- Pechan, P.A. and Morgan, D.G. (1985). Defoliation and its effects on pod and seed development in oil seed rape (Brassica napus L.). Journal of Experimental Botany 36: 458–468.
- Pomares-Viciana, T., Die, J., Del Rio-Celestino, M. et al. (2017). Auxin signalling regulation during induced and parthenocarpic fruit set in zucchini. Molecular Breeding doi: 10.1007/s11032-017-0661-5.
- Prasad, T.K., Li, X., Abdel-Rahman, A.M. et al. (1993). Does auxin play a role in the release of apical dominance by shoot inversion in Ipomoea nil? Annals of Botany 71: 223–229.
- Prusinkiewicz, P., Crawford, S., Smith, R.S. et al. (2009). Control of bud activation by as auxin transport switch. Proceedings of the National Academy of Sciences 106: 17431–17436.
- Raven, J.A. (1975). Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytologist 74: 163–172.
- Roychoudhry, S., Del Bianco, M., Kieffer, M., and Kepinski, S. (2013). Auxin controls gravitropic setpoint angle in higher plant lateral branches. Current Biology 23: 1497–1504.
- Rubery, P.H. and Sheldrake, A.R. (1974). Carrier-mediated auxin transport. Planta 118: 101–121.
- Sachs, T. (1969). Polarity and the induction of organised vascular tissues. Annals of Botany 33: 263–275.
- Sachs, T. (1981). The control of patterned differentiation of vascular tissues. Advances in Botanical Research 9: 151–262.
- Sachs, T. and Thimann, K.V. (1964). Release of lateral buds from apical dominance. Nature 201: 939–940.
- Sauer, M., Balla, J., and Luschnig, C. (2006). Canalization of auxin flow by aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes and Development 20: 2902–2911.
- Scarpella, E., Marcos, D., Friml, J., and Berleth, T. (2006). Control of leaf vascular patterning by polar auxin transport. Genes and Development 20: 1015–1027.
- Seale, M., Bennett, T., and Leyser, O. (2017). BRC1 expression regulates bud activation potential but is not necessary or sufficient for bud growth inhibition in Arabidopsis . Development 144: 1661–1673.
- Shinohara, N., Taylor, C., and Leyser, O. (2013). Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biology 11: e1001474.
- Simaskova, M., O'Brien, J.A., Khan, M. et al. (2014). Cytokinin response factors regulate PIN-FORMED auxin transporters. Nature Communications 6: 8717.
- Sjut, V. and Bangerth, F. (1984). Induced parthenocarpy – a way of manipulating levels of endogenous hormones in tomato fruit (Lycopersicon esculentum mill.) 2. Diffusible hormones. Journal of Plant Growth Regulation 2: 49–56.
- Snow, R. (1929). The transmission of inhibition through dead stretches of stem. Annals of Botany 43: 261–267.
- Snow, R. (1931). Experiments on growth inhibition. Part II: new phenomena of inhibition. Proceedings of the Royal Society B 108: 305–316.
- Song, X., Lu, Z., Yu, H. et al. (2017). IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signalling in rice. Cell Research 27: 1128–1141.
- de Stigter, H.C.M. (1969). Growth relations between individual fruits, and between fruits and roots in cucumber. Journal of Experimental Botany 27: 87–97.
- Sylvester-Bradley, R., Berry, P., Blake, J. et al. (2015). Wheat Growth Guide. Stoneleigh: Agriculture and Horticulture Development Board.
- Takei, K., Takahashi, T., Sugiyama, T. et al. (2002). Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. Journal of Experimental Biology 53: 971–977.
- Tanaka, M., Takei, K., Kojima, M. et al. (2006). Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. The Plant Journal 45: 1028–1036.
- Tayo, T.O. and Morgan, D.G. (1975). Quantitative analysis of the growth, development and distribution of flowers and pods in oil seed rape (Brassica napus L.). The Journal of Agricultural Science 85: 103–110.
-
Thimann, K. and Skoog, F. (1934). On the inhibition of bud development and other functions of growth substance in Vicia faba
. Proceedings of the Royal Society B doi: 10.1098/rspb.1934.0010.
10.1098/rspb.1934.0010 Google Scholar
- Troughton, A. (1977). The effect of phosphorus nutrition upon the growth and morphology of young plants of Lolium perenne L. Annals of Botany 41: 85–92.
- Umehara, M., Hanada, A., Yoshida, S. et al. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195–200.
- Wang, R., Farrona, S., Vincent, C. et al. (2009). PEP1 regulates perennial flowering in Arabis alpina . Nature 459: 423–428.
- Waters, M.T., Gutjahr, C., Bennett, T., and Nelson, D.C. (2017). Strigolactone signaling and evolution. Annual Review of Plant Biology 68: 8.1–8.31.
- Went, F.W. (1938). Specific factors other than auxin affecting growth and root formation. Plant Physiology 13: 55–80.
- Went, F.W. and Thimann, K.V. (1937). Phytohormones. New York: The Macmillan Company.
- Wickson, M. and Thimann, K.V. (1958). The antagonism of auxin and kinetin in apical dominance. Physiologia Plantarum 11: 62–74.
- Wingler, A. (2011). Interactions between flowering and senescence regulation and the influence of low temperature in Arabidopsis and crop plants. Annals of Applied Biology 159: 320–338.
- Woolhouse, H.W. (1983). Hormonal control of senescence allied to reproduction in plants. In: Beltsville Symposia in Agricultural Research: Strategies of Plant Reproduction (ed. W.J. Meudt), 201–236. London: Allanheld and Osmun.
- Wuest, S.E., Philipp, M.A., Guthorl, D. et al. (2016). Seed production affects maternal growth and senescence in Arabidopsis. Plant Physiology 171: 392–404.
- Yamada, Y. and Umehara, M. (2015). Possible roles of Strigolactones during leaf senescence. Plants 4: 664–677.
- Yoneyama, K., Yoneyama, K., Takeuchi, Y., and Sekimoto, H. (2007). Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225: 1013–1038.
- Yu, S.M., Lo, S.F., and Ho, T.H. (2015). Source-sink communication: regulated by hormone, nutrient, and stress cross-Signaling. Trends in Plant Science 20: 844–857.
- Zazímalová, E., Murphy, A.S., Yang, H. et al. (2010). Auxin transporters—why so many? Cold Spring Harbor Perspectives in Biology 2: a001552. doi: 10.1101/cshperspect.a001552.
- Zwack, P.J. and Rashotte, A.M. (2013). Cytokinin inhibition of leaf senescence. Plant Signaling and Behaviour 8: e24737.
Citing Literature
Browse other articles of this reference work: