Molecular mechanisms of plant competition: Neighbour detection and response strategies

Functional Ecology

Volumn 27, Issue 4, 2013, Pages 841-853

  Pierik, Ronald ^a   Mommer, Liesje ^b,c   Voesenek, Laurentius Acj ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Allelopathy; Competition; Foraging; Light; Nutrients; Phenotypic plasticity; Shade avoidance; Signalling

Indexed keywords

ALLELOPATHY; COMPETITIVE ABILITY; EXUDATION; INTERSPECIFIC COMPETITION; LIGHT AVAILABILITY; MOLECULAR ANALYSIS; NUTRITIONAL STATUS; PHENOTYPIC PLASTICITY; PLANT COMMUNITY; RESEARCH METHOD; ROOT SYSTEM; SIGNALING; SPECIES DIVERSITY; SPECIES RICHNESS; VOLATILE ORGANIC COMPOUND;

EID: 84880759839     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12010     Document Type: Article

References (145)

1. Abel, S. (2011) Phosphate sensing in root development. Current Opinion in Plant Biology, 14, 303-309.
2. Ahmad, M., Jarillo, J.A., Smirnova, O. & Cashmore, A.R. (1998) The CRY1 blue light photoreceptor of arabidopsis interacts with phytochrome A in vitro. Molecular Cell, 1, 939-948.
3. Badri, D.V. & Vivanco, J.M. (2009) Regulation and function of root exudates. Plant Cell and Environment, 32, 666-681.
4. Badri, D.V., Quintana, N., El Kassis, E.G., Kim, H.K., Choi, Y.H., Sugiyama, A., Verpoorte, R., Martinoia, E., Manter, D.K. & Vivanco, J.M. (2009) An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiology, 151, 2006-2017.
5. Bae, G. & Choi, G. (2008) Decoding of light signals by plant phytochromes and their interacting proteins RID C-1601-2011. Annual Review of Plant Biology, 59, 281-311.
6. Bais, H.P., Vepachedu, R., Gilroy, S., Callaway, R.M. & Vivanco, J.M. (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science, 301, 1377-1380.
7. Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S. & Vivanco, J.M. (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology, 57, 233-266.
8. Baldwin, I.T., Halitschke, R., Paschold, A., von Dahl, C.C. & Preston, C.A. (2006) Volatile signaling in plant-plant interactions: "talking trees" in the genomics era. Science, 311, 812-815.
9. Ballaré, C.L. (1999) Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. Trends in Plant Science, 4, 97-102.
10. Ballaré, C.L. & Scopel, A.L. (1997) Phytochrome signalling in plant canopies: testing its population-level implications with photoreceptor mutants of arabidopsis. Functional Ecology, 11, 441-450.
11. Ballaré, C.L., Scopel, A.L. & Sánchez, R.A. (1990) Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies. Science, 247, 329-331.
12. Ballaré, C.L., Mazza, C.A., Austin, A.T. & Pierik, R. (2012) Canopy light and plant health. Plant Physiology, 160, 145-155.
13. Bartholomew, B. (1970) Bare zone between Californian shrub and grassland communities: the role of animals. Science, 170, 1210-1212.
14. Bertin, C., Yang, X.H. & Weston, L.A. (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant and Soil, 256, 67-83.
15. Bertin, C., Weston, L.A., Huang, T., Jander, G., Owens, T., Meinwald, J. & Schroeder, F.C. (2007) Grass roots chemistry: meta-tyrosine, an herbicidal nonprotein amino acid. Proceedings of the National Academy of Sciences of the United States of America, 104, 16964-16969.
16. Biedrzycki, M.L. & Bais, H.P. (2010) Kin recognition in plants: a mysterious behaviour unsolved. Journal of Experimental Botany, 61, 4123-4128.
17. Bilbrough, C.J. & Caldwell, M.M. (1995) The effects of shading and N-status on root proliferation in nutrient patches by the perennial grass agropyron-desertorum in the field. Oecologia, 103, 10-16.
18. Blom, D., Fabbri, C., Connor, E.C., Schiestl, F.P., Klauser, D.R., Boller, T., Eberl, L. & Weisskopf, L. (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environmental Microbiology, 13, 3047-3058.
19. Caffaro, M.M., Vivanco, J.M., Gutierrez Boem, F.H. & Rubio, G. (2011) The effect of root exudates on root architecture in arabidopsis thaliana. Plant Growth Regulation, 64, 241-249.
20. Cahill, J.F. (2003) Lack of relationship between below-ground competition and allocation to roots in 10 grassland species. Journal of Ecology, 91, 532-540.
21. Cahill, J.F. Jr & McNickle, G.G. (2011) The behavioral ecology of nutrient foraging by plants. Annual Review of Ecology, Evolution, and Systematics, 42, 289-311.
22. Cahill, J.F. Jr, McNickle, G.G., Haag, J.J., Lamb, E.G., Nyanumba, S.M. & Clair Cassady St, C. (2010) Plants integrate information about nutrients and neighbors. Science, 328, 1657.
23. Callaway, R.M. & Aschehoug, E.T. (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science, 290, 521-523.
24. Callaway, R.M., DeLuca, T.H. & Belliveau, W.M. (1999) Biological-control herbivores may increase competitive ability of the noxious weed centaurea maculosa. Ecology, 80, 1196-1201.
25. Casal, J.J. & Mazzella, M.A. (1998) Conditional synergism between cryptochrome 1 and phytochrome B is shown by the analysis of phyA, phyB, and hy4 simple, double, and triple mutants in arabidopsis. Plant Physiology, 118, 19-25.
26. Casper, B.B., Schenk, H.J. & Jackson, R.B. (2003) Defining a plant's belowground zone of influence. Ecology, 84, 2313-2321.
27. Cerrudo, I., Keller, M.M., Cargnel, M.D., Demkura, P.V., de Wit, M., Patitucci, M.S., Pierik, R., Pieterse, C.M.J. & Ballare, C.L. (2012) Low red:far-red ratios reduce arabidopsis resistance to botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism. Plant Physiology, 158, 2042-2052.
28. Cipollini, D. (2004) Stretching the limits of plasticity: can a plant defend against both competitors and herbivores? Ecology, 85, 28-37.
29. Dakora, F.D. & Phillips, D.A. (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil, 245, 35-47.
30. Dennis, P.G., Miller, A.J. & Hirsch, P.R. (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiology Ecology, 72, 313-327.
31. Dicke, M. (2009) Behavioural and community ecology of plants that cry for help. Plant Cell and Environment, 32, 654-665.
32. Dicke, M. & Baldwin, I.T. (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'. Trends in Plant Science, 15, 167-175.
33. Ding, Z., Galván-Ampudia, C.S., Demarsy, E., Langowski, L., Kleine-Vehn, J., Fan, Y., Morita, M.T., Tasaka, M., Fankhauser, C., Offringa, R. & Friml, J. (2011) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in arabidopsis. Nature Cell Biology, 13, 447-452
34. Djakovic-Petrovic, T., de Wit, M., Voesenek, L.A.C.J. & Pierik, R. (2007) DELLA protein regulation in growth responses to canopy signals. The Plant Journal, 51, 117-126.
35. Drew, M.C. & Saker, L.R. (1975) Nutrient supply and growth of seminal root system in barley.2. localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of root system. Journal of Experimental Botany, 26, 79-90.
36. Ens, E.J., Bremner, J.B., French, K. & Korth, J. (2009) Identification of volatile compounds released by roots of an invasive plant, bitou bush (chrysanthemoides monilifera spp. rotundata), and their inhibition of native seedling growth. Biological Invasions, 11, 275-287.
37. Fargione, J. & Tilman, D. (2006) Plant species traits and capacity for resource reduction predict yield and abundance under competition in nitrogen-limited grassland. Functional Ecology, 20, 533-540.
38. Feng, S.H., Martinez, C., Gusmaroli, G., Wang, Y., Zhou, J.L., Wang, F., Chen, L.Y., Yu, L., Iglesias-Pedraz, J.M., Kircher, S., Schafer, E., Fu, X.D., Fan, L.M. & Deng, X.W. (2008) Coordinated regulation of arabidopsis thaliana development by light and gibberellins. Nature, 451, 475-479.
39. Fitter, A., Williamson, L., Linkohr, B. & Leyser, O. (2002) Root system architecture determines fitness in an arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proceedings of the Royal Society of London Series B-Biological Sciences, 269, 2017-2022.
40. Foo, E., Ross, J.J., Davies, N.W., Reid, J.B. & Weller, J.L. (2006) A role for ethylene in the phytochrome-mediated control of vegetative development. Plant Journal, 46, 911-921.
41. Forde, B.G. (2002) Local and long-range signalling pathways regulating plant responses to nitrate. Annual Reviews in Plant Biology, 53, 203-224.
42. Franklin, K.A. (2008) Shade avoidance. New Phytologist, 179, 930-944.
43. Franklin, K., Larner, V. & Whitelam, G. (2005) The signal transducing photoreceptors of plants. International Journal of Developmental Biology, 49, 653-664.
44. Franklin, K.A., Lee, S.H., Patel, D., Kumar, S.V., Spartz, A.K., Gu, C., Ye, S., Yu, P., Breen, G., Cohen, J.D., Wigge, P.A. & Gray, W.M. (2011) Phytochrome-Interacting Factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proceedings of the National Academy of Sciences of the United States of America, 108, 20231-20235.
45. Gagliano, M., Mancuso, S. & Robert, D. (2012) Towards understanding plant bioacoustics. Trends in Plant Science, 17, 323-325.
46. Galstyan, A., Cifuentes-Esquivel, N., Bou-Torrent, J. & Martinez-Garcia, J.F. (2011) The shade avoidance syndrome in arabidopsis: a fundamental role for atypical basic helix-loop-helix proteins as transcriptional cofactors. Plant Journal, 66, 258-267.
47. Gao, X., Zhang, F. & Hoffland, E. (2009) Malate exudation by six aerobic rice genotypes varying in zinc uptake efficiency. Journal of Environmental Quality, 38, 2315-2321.
48. Grace, J.B. & Tilman, D. (1990) Perspectives on Plant Competition. Academic Press, New York, NY.
49. Grime, J.P. (1979) Plant Strategies and Vegetation Processes. Academic Press, London.
50. Hartmann, A., Rothballer, M. & Schmid, M. (2008) Lorenz hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant and Soil, 312, 7-14.
51. Hautier, Y., Niklaus, P.A. & Hector, A. (2009) Competition for light causes plant biodiversity loss after eutrophication RID G-5786-2010 RID H-4199-2011. Science, 324, 636-638.
52. Herms, D.A. & Mattson, W.J. (1992) The dilemma of plants: to grow or defend. The Quarterly Review of Biology, 67, 283-335.
53. Hisamatsu, T., King, R.W., Helliwell, C.A. & Koshioka, M. (2005) The involvement of gibberellin 20-oxidase genes in phytochrome-regulated petiole elongation of arabidopsis. Plant Physiology, 138, 1106-1116.
54. Ho, C. & Tsay, Y. (2010) Nitrate, ammonium, and potassium sensing and signaling. Current Opinion in Plant Biology, 13, 604-610.
55. Ho, C., Lin, S., Hu, H. & Tsay, Y. (2009) CHL1 functions as a nitrate sensor in plants. Cell, 138, 1184-1194.
56. Hodge, A. (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist, 162, 9-24.
57. Hodge, A., Robinson, D., Griffiths, B.S. & Fitter, A.H. (1999) Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant, Cell and Environment, 22, 811-820.
58. Hoffland, E. (1992) Quantitative-evaluation of the role of organic-acid exudation in the mobilization of rock phosphate by rape. Plant and Soil, 140, 279-289.
59. Holland, J.J., Roberts, D. & Liscum, E. (2009) Understanding phototropism: from darwin to today. Journal of Experimental Botany, 60, 1969-1978.
60. Holopainen, J.K. & Gershenzon, J. (2010) Multiple stress factors and the emission of plant VOCs. Trends in Plant Science, 15, 176-184.
61. Hornitschek, P., Lorrain, S., Zoete, V., Michielin, O. & Fankhauser, C. (2009) Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. Embo Journal, 28, 3893-3902.
62. Inderjit, Wardle, D.A., Karban, R. & Callaway, R.M. (2011) The ecosystem and evolutionary contexts of allelopathy. Trends in Ecology & Evolution, 26, 655-662.
63. Izaguirre, M.M., Mazza, C.A., Biondini, M., Baldwin, I.T. & Ballare, C.L. (2006) Remote sensing of future competitors: impacts on plant defenses. Proceedings of the National Academy of Sciences of the United States of America, 103, 7170-7174.
64. Karban, R., Baldwin, I.T., Baxter, K.J., Laue, G. & Felton, G.W. (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia, 125, 66-71.
65. Karban, R., Maron, J., Felton, G.W., Ervin, G. & Eichenseer, H. (2003) Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants. Oikos, 100, 325-332.
66. Kaur, H., Kaur, R., Kaur, S., Baldwin, I.T. & Inderjit (2009) Taking ecological function seriously: soil microbial communities can obviate allelopathic effects of released metabolites. PLoS One, 4, e4700.
67. Keddy, P.A. (1989) Competition. Chapman and Hall, London.
68. Kegge, W. & Pierik, R. (2010) Biogenic volatile organic compounds and plant competition. Trends in Plant Science, 15, 126-132.
69. Keller, M.M., Jaillais, Y., Pedmale, U.V., Moreno, J.E., Chory, J. & Ballare, C.L. (2011) Cryptochrome 1 and phytochrome B control shade-avoidance responses in arabidopsis via partially independent hormonal cascades. Plant Journal, 67, 195-207.
70. Kembel, S.W. & Cahill, J.F. (2005) Plant phenotypic plasticity belowground: a phylogenetic perspective on root foraging trade-offs. American Naturalist, 166, 216-230.
71. Keuskamp, D.H., Pollmann, S., Voesenek, L.A.C.J., Peeters, A.J.M. & Pierik, R. (2010) Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proceedings of the National Academy of Sciences of the United States of America, 107, 22740-22744.
72. Keuskamp, D.H., Sasidharan, R., Vos, I., Peeters, A.J.M., Voesenek, L.A.C.J. & Pierik, R. (2011) Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in arabidopsis seedlings. Plant Journal, 67, 208-217.
73. Kozuka, T., Kobayashi, J., Horiguchi, G., Demura, T., Sakakibara, H., Tsukaya, H. & Nagatani, A. (2010) Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiology, 153, 1608-1618.
74. De Kroon, H., Visser, E.J.W., Huber, H., Mommer, L. & Hutchings, M.J. (2009) A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant Cell and Environment, 32, 704-712.
75. de Kroon, H., Mommer, L., Nishiwaki, A., de Kroon, H. & Visser, E.J.W. (2003) Root competition: towards a mechanistic understanding. Root Ecology, pp. 215-234. Berlin, Springer-Verlag.
76. Krouk, G., Lacombe, B., Bielach, A., Perrine-Walker, F., Malinska, K., Mounier, E., Hoyerova, K., Tillard, P., Leon, S., Ljung, K., Zazimalova, E., Benkova, E., Nacry, P. & Gojon, A. (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell, 18, 927-937.
77. Kurepin, L.V., Qaderi, M.M., Back, T.G., Reid, D.M. & Pharis, R.P. (2008) A rapid effect of applied brassinolide on abscisic acid concentrations in brassica napus leaf tissue subjected to short-term heat stress. Plant Growth Regulation, 55, 165-167.
78. Leivar, P. & Quail, P.H. (2011) PIFs: pivotal components in a cellular signaling hub. Trends in Plant Science, 16, 19-28.
79. Li, L., Li, S., Sun, J., Zhou, L., Bao, X., Zhang, H. & Zhang, F. (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proceedings of the National Academy of Sciences of the United States of America, 104, 11192-11196.
80. Li, L., Ljung, K., Breton, G., Schmitz, R.J., Pruneda-Paz, J., Cowing-Zitron, C., Cole, B.J., Ivans, L.J., Pedmale, U.V., Jung, H.-S., Ecker, J.R., Kay, S.A. & Chory, J. (2012) Linking photoreceptor excitation to changes in plant architecture. Genes & Development, 26, 785-790.
81. Linkohr, B.I., Williamson, L.C., Fitter, A.H. & Leyser, H.M.O. (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of arabidopsis. Plant Journal, 29, 751-760.
82. Lorrain, S., Allen, T., Duek, P.D., Whitelam, G.C. & Fankhauser, C. (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant Journal, 53, 312-323.
83. de Lucas, M., Daviere, J.M., Rodriguez-Falcon, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blazquez, M.A., Titarenko, E. & Prat, S. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature, 451, 480-484.
84. Lynch, J. (1995) Root architecture and plant productivity. Plant Physiology, 109, 7-13.
85. Mahall, B.E. & Callaway, R.M. (1991) Root communication among desert shrubs. Proceedings of the National Academy of Science USA, 88, 874-876.
86. Mas, P., Devlin, P.F., Panda, S. & Kay, S.A. (2000) Functional interaction of phytochrome B and cryptochrome 2. Nature, 408, 207-211.
87. Micallef, S.A., Shiaris, M.P. & Colon-Carmona, A. (2009) Influence of arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. Journal of Experimental Botany, 60, 1729-1742.
88. Mommer, L., van Ruijven, J., de Caluwe, H., Smit-Tiekstra, A.E., Wagemaker, C.A.M., Ouborg, N.J., Bogemann, G.M., van der Weerden, G.M., Berendse, F. & de Kroon, H. (2010) Unveiling below-ground species abundance in a biodiversity experiment: a test of vertical niche differentiation among grassland species. Journal of Ecology, 98, 1117-1127.
89. Mommer, L., Visser, E.J.W., van Ruijven, J., de Caluwe, H., Pierik, R. & de Kroon, H. (2011) Contrasting root behaviour in two grass species: a test of functionality in dynamic heterogeneous conditions. Plant and Soil, 344, 347-360.
90. Morelli, G. & Ruberti, I. (2000) Shade avoidance responses. Driving auxin along lateral routes. Plant Physiology, 122, 621-626.
91. Moreno, J.E., Tao, Y., Chory, J. & Ballare, C.L. (2009) Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proceedings of the National Academy of Sciences of the United States of America, 106, 4935-4940.
92. Morgan, D.C. & Smith, H. (1976) Linear relationship between phytochrome photoequilibrium and growth in plants under simulated natural irradiation. Nature, 262, 210-212.
93. Mullen, J.L., Weinig, C. & Hangarter, R.P. (2006) Shade avoidance and the regulation of leaf inclination in arabidopsis. Plant Cell and Environment, 29, 1099-1106.
94. Muller, C.H., Haines, B.L. & Muller, W.H. (1964) Volatile growth inhibitors produced by aromatic shrubs. Science, 143, 471.
95. Ninkovic, V. (2003) Volatile communication between barley plants affects biomass allocation. Journal of Experimental Botany, 54, 1931-1939.
96. Nishida, N., Tamotsu, S., Nagata, N., Saito, C. & Sakai, A. (2005) Allelopathic effects of volatile monoterpenoids produced by salvia leucophylla: inhibition of cell proliferation and DNA synthesis in the root apical meristem of brassica campestris seedlings. Journal of Chemical Ecology, 31, 1187-1203.
97. Novoplansky, A. (2009) Picking battles wisely: plant behaviour under competition. Plant Cell and Environment, 32, 726-741.
98. Ormeno, E., Fernandez, C. & Mevy, J. (2007) Plant coexistence alters terpene emission and content of mediterranean species. Phytochemistry, 68, 840-852.
99. Ormeno, E., Bousquet-Melou, A., Mevy, J., Greff, S., Robles, C., Bonin, G. & Fernandez, C. (2007) Effect of intraspecific competition and substrate type on terpene emissions from some mediterranean plant species. Journal of Chemical Ecology, 33, 277-286.
100. Pedmale, U.V., Celaya, R.B. & Liscum, E. (2010) Phototropism: mechanism and outcomes. The Arabidopsis Book/American Society of Plant Biologists, 8, e0125.
101. Peret, B., De Rybel, B., Casimiro, I., Benkova, E., Swarup, R., Laplaze, L., Beeckman, T. & Bennett, M.J. (2009) Arabidopsis lateral root development: an emerging story. Trends in Plant Science, 14, 399-408.
102. Pierik, R., de Wit, M. & Voesenek, L.A.C.J. (2011) Growth-mediated stress escape: convergence of signal transduction pathways activated upon exposure to two different environmental stresses. New Phytologist, 189, 122-134.
103. Pierik, R., Visser, E.J.W., de Kroon, H. & Voesenek, L.A.C.J. (2003) Ethylene is required in tobacco to successfully compete with proximate neighbours. Plant, Cell and Environment, 26, 1229-1234.
104. Pierik, R., Voesenek, L.A.C.J., de Kroon, H. & Visser, E.J.W. (2004a) Density-induced plant size reduction and size inequalities in ethylene-sensing and ethylene-insensitive tobacco. Plant Biology, 6, 201-205.
105. Pierik, R., Cuppens, M.L.C., Voesenek, L.A.C.J. & Visser, E.J.W. (2004b) Interactions between ethylene and gibberellins in phytochrome-mediated shade avoidance responses in tobacco. Plant Physiology, 136, 2928-2936.
106. Pierik, R., Whitelam, G.C., Voesenek, L.A.C.J., de Kroon, H. & Visser, E.J.W. (2004c) Canopy studies on ethylene-insensitive tobacco identify ethylene as a novel element in blue light and plant-plant signalling. The Plant Journal, 38, 310-319.
107. Pierik, R., Millenaar, F.F., Peeters, A.J.M. & Voesenek, L.A.C.J. (2005) New perspectives in flooding research: the use of shade avoidance and arabidopsis thaliana. Annals of Botany, 96, 533-540.
108. Pierik, R., Tholen, D., Poorter, H., Visser, E.J.W. & Voesenek, L.A.C.J. (2006) The janus face of ethylene: growth inhibition and stimulation. Trends in Plant Science, 11, 176-183.
109. Pierik, M., van Ruijven, J., Bezemer, T.M., Geerts, R.H.E.M. & Berendse, F. (2011) Recovery of plant species richness during long-term fertilization of a species-rich grassland. Ecology, 92, 1393-1398.
110. Poorter, H., Niklas, K.J., Reich, P.B., Oleksyn, J., Poot, P. & Mommer, L. (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist, 193, 30-50.
111. Rasmann, S., Kollner, T.G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J. & Turlings, T.C.J. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature, 434, 732-737.
112. Remans, T., Nacry, P., Pervent, M., Filleur, S., Diatloff, E., Mounier, E., Tillard, P., Forde, B.G. & Gojon, A. (2006) The arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proceedings of the National Academy of Sciences of the United States of America, 103, 19206-19211.
113. Richardson, A.E., Lynch, J.P., Ryan, P.R., Delhaize, E., Smith, F.A., Smith, S.E., Harvey, P.R., Ryan, M.H., Veneklaas, E.J., Lambers, H., Oberson, A., Culvenor, R.A. & Simpson, R.J. (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant and Soil, 349, 121-156.
114. Robinson, D. (1996) Variation, co-ordination and compensation in root systems in relation to soil variability. Plant and Soil, 187, 57-66.
115. Robinson, D., Hodge, A., Griffiths, B.S. & Fitter, A.H. (1999) Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proceedings of the Royal Society of London, 266, 431-435.
116. Roig-Villanova, I., Bou-Torrent, J., Galstyan, A., Carretero-Paulet, L., Portoles, S., Rodriguez-Conception, M. & Garcia, J.F.M. (2007) Interaction of shade avoidance and auxin responses: a role for two novel atypical bHLH proteins. Embo Journal, 26, 4756-4767.
117. Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K.D. & Coruzzi, G.M. (2011) Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proceedings of the National Academy of Sciences of the United States of America, 108, 18524-18529.
118. Runyon, J.B., Mescher, M.C. & De Moraes, C.M. (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science, 313, 1964-1967.
119. Sasidharan, R., Voesenek, L.A.C.J. & Pierik, R. (2011) Cell wall modifying proteins mediate plant acclimatization to biotic and abiotic stresses. Critical Reviews in Plant Sciences, 30, 548-562.
120. Sasidharan, R., Chinnappa, C.C., Voesenek, L. & Pierik, R. (2008) The regulation of cell wall extensibility during shade avoidance: a study using two contrasting ecotypes of stellaria longipes. Plant Physiology, 148, 1557-1569.
121. Sasidharan, R., Chinnappa, C.C., Staal, M., Elzenga, J.T.M., Yokoyama, R., Nishitani, K., Voesenek, L.A.C.J. & Pierik, R. (2010) Light quality-mediated petiole elongation in arabidopsis during shade avoidance involves cell wall modification by xyloglucan Endotransglucosylase/Hydrolases. Plant Physiology, 154, 978-990.
122. Savaldi-Goldstein, S., Peto, C. & Chory, J. (2007) The epidermis both drives and restricts plant shoot growth. Nature, 446, 199-202.
123. Schenk, H.J. (2006) Root competition: beyond resource depletion. Journal of Ecology, 94, 725-739.
124. Schmitt, J., McCormac, A.C. & Smith, H. (1995) A test of the adaptive plasticity hypothesis using transgenic and mutant plants disabled in phytochrome-mediated elongation responses to neighbors. The American Naturalist, 146, 937-953.
125. Sellaro, R., Hoecker, U., Yanovsky, M., Chory, J. & Casal, J.J. (2009) Synergism of red and blue light in the control of arabidopsis gene expression and development. Current Biology, 19, 1216-1220.
126. Semchenko, M., John, E.A. & Hutchings, M.J. (2007) Effects of physical connection and genetic identity of neighbouring ramets on root-placement patterns in two clonal species. New Phytologist, 176, 644-654.
127. Sessa, G., Carabelli, M., Sassi, M., Ciolfi, A., Possenti, M., Mittempergher, F., Becker, J., Morelli, G. & Ruberti, I. (2005) A dynamic balance between gene activation and repression regulates the shade avoidance response in arabidopsis. Genes & Development, 19, 2811-2815.
128. Singh, H.P., Batish, D.R., Kaur, S., Arora, K. & Kohli, R.K. (2006) Alpha-pinene inhibits growth and induces oxidative stress in roots. Annals of Botany, 98, 1261-1269.
129. Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.Y., DoleZal, K., Schlereth, A., Jurgens, G. & Alonso, J.M. (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell, 133, 177-191.
130. Tao, Y., Ferrer, J.L., Ljung, K., Pojer, F., Hong, F.X., Long, J.A., Li, L., Moreno, J.E., Bowman, M.E., Ivans, L.J., Cheng, Y.F., Lim, J., Zhao, Y.D., Ballare, C.L., Sandberg, G., Noel, J.P. & Chory, J. (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell, 133, 164-176.
131. Thorpe, A.S. & Callaway, R.M. (2011) Biogeographic differences in the effects of centaurea stoebe on the soil nitrogen cycle: novel weapons and soil microbes. Biological Invasions, 13, 1435-1445.
132. Thorpe, A.S., Thelen, G.C., Diaconu, A. & Callaway, R.M. (2009) Root exudate is allelopathic in invaded community but not in native community: field evidence for the novel weapons hypothesis. Journal of Ecology, 97, 641-645.
133. Tilman, D. (1982) Resource Competition and Community Structure. Princeton University Press, Princeton, NJ.
134. Ton, J., D'Alessandro, M., Jourdie, V., Jakab, G., Karlen, D., Held, M., Mauch-Mani, B. & Turlings, T.C.J. (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant Journal, 49, 16-26.
135. Turlings, T.C.J. & Ton, J. (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Current Opinion in Plant Biology, 9, 421-427.
136. Vandenbussche, F., Pierik, R., Millenaar, F.F., Voesenek, L.A.C.J. & Van der Straeten, D. (2005) Reaching out of the shade. Current Opinion in Plant Biology, 8, 462-468.
137. Weijschede, J., Antonise, K., de Caluwe, H., de Kroon, H. & Huber, H. (2008) Effects of cell number and cell size on petiole length variation in a stoloniferous herb. American Journal of Botany, 95, 41-49.
138. Weiner, J. (1985) Size hierarchies in experimental populations of annual plants. Ecology, 66, 743-752.
139. Wenke, K., Kai, M. & Piechulla, B. (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta, 231, 499-506.
140. Whippo, C.W. & Hangarter, R.P. (2004) Phytochrome modulation of blue-light-induced phototropism. Plant, Cell and Environment, 27, 1223-1228.
141. Wilson, S.D. & Tilman, D. (1995) Competitive responses of 8 old-field plant-species in 4 environments. Ecology, 76, 1169-1180.
142. De Wit, M., Kegge, W., Evers, J.B., Vergeer-van Eijk, M.H., Voesenek, L.A.C.J. & Pierik, R. (2012) Plant neighbor detection through touching leaf tips precedes phytochrome signals. Proceedings of the National Academy of Sciences of the United States of America, 109, 14705-14710
143. Won, C., Shen, X., Mashiguchi, K., Zheng, Z., Dai, X., Cheng, Y., Kasahara, H., Kamiya, Y., Chory, Y. & Zhao, Y. (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 108, 18518-18523.
144. Zhang, H. & Forde, B.G. (1998) An arabidopsis MADS-box gene that controls nutrient-induced changes in root architecture. Science, 279, 407-409.
145. Zhang, H.M., Jennings, A., Barlow, P.W. & Forde, B.G. (1999) Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences of the United States of America, 96, 6529-6534.