Shade avoidance: Phytochrome signalling and other aboveground neighbour detection cues

Journal of Experimental Botany

Volumn 65, Issue 11, 2014, Pages 2815-2824

  Pierik, Ronald ^a   De Wit, Mieke ^b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Arabidopsis; canopy; competition; cryptochrome; mechanostimulation; phytochrome, shade avoidance.

Indexed keywords

PHYTOCHROME; VOLATILE ORGANIC COMPOUND;

ADAPTATION; LIGHT; METABOLISM; PLANT; RADIATION RESPONSE; SIGNAL TRANSDUCTION; TIME;

ADAPTATION, PHYSIOLOGICAL; LIGHT; PHYTOCHROME; PLANT COMPONENTS, AERIAL; SIGNAL TRANSDUCTION; TIME FACTORS; VOLATILE ORGANIC COMPOUNDS;

EID: 84902478009     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert389     Document Type: Review

References (105)

1. Ahmad M, Lin CT, Cashmore AR. 1995. Mutations throughout an Arabidopsis blue-light photoreceptor impair blue-light-responsive anthocyanin accumulation and inhibition of hypocotyl elongation. The Plant Journal 8, 653-658.
2. Anten NPR, Casado-Garcia R, Nagashima H. 2005. Effects of mechanical stress and plant density on mechanical characteristics, growth, and lifetime reproduction of tobacco plants. American Naturalist 166, 650-660.
3. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA. 2006. Volatile signaling in plant-plant interactions: Talking trees in the genomics era. Science 311, 812-815.
4. Ballaré CL, Sánchez RA, Scopel AL, Casal JJ, Ghersa CM. 1987. Early detection of neighbour plants by phytochrome perception of spectral changes in reflected sunlight. Plant, Cell and Environment 10, 551-557.
5. Ballaré CL, Scopel AL, Radosevich SR, Kendrick RE. 1992. Phytochrome-mediated phototropism in de-etiolated seedlings. Occurrence and ecological significance. Plant Physiology 100, 170-177.
6. Ballaré CL, Scopel AL, Sánchez RA. 1990. Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies. Science 247, 329-331.
7. Ballaré CL, Scopel AL, Sánchez RA. 1991. Photocontrol of stem elongation in plant neighbourhoods: effects of photon fluence rate under natural conditions of radiation. Plant, Cell and Environment 14, 57-65.
8. Banerjee R, Schleicher E, Meier S, Viana RM, Pokorny R, Ahmad M, Bittl R, Batschauer A. 2007. The signaling state of Arabidopsis cryptochrome 2 contains flavin semiquinone. Journal of Biological Chemistry 282, 14916-14922.
9. Bouly J, Schleicher E, Dionisio-Sese M, et al. 2007. Cryptochrome blue light photoreceptors are activated through interconversion of flavin redox states. Journal of Biological Chemistry 282, 9383-9391.
10. Braam J. 2005. In touch: plant responses to mechanical stimuli. New Phytologist 165, 373-389.
11. Braam J, Davis RW. 1990. Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60, 357-364.
12. Carabelli M, Possenti M, Sessa G, Ciolfi A, Sassi M, Morelli G, Ruberti I. 2007. Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes and Development 21, 1863-1868.
13. Casal JJ. 2012. Shade avoidance. The Arabidopsis Book 10, e0157-e0157.
14. Casal JJ, Smith H. 1988. The loci of perception for phytochrome control of internode growth in lightgrown mustard: promotion by low phytochrome photequilibria in the internode is enhanced by blue light perceived by the leaves. Planta 176, 277-282.
15. Chaves I, Pokorny R, Byrdin M, et al. 2011. The cryptochromes: blue light photoreceptors in plants and animals. Annual Review of Plant Biology 62, 335-364.
16. Chehab EW, Yao C, Henderson Z, Kim S, Braam J. 2012. Arabidopsis touch-induced morphogenesis is jasmonate mediated and protects against pests. Current Biology 22, 701-706.
17. Christie JM. 2007. Phototropin blue-light receptors. Annual Review of Plant Biology 58, 21-45.
18. Cifuentes-Esquivel N, Bou-Torrent J, Galstyan A, Gallemí M, Sessa G, Salla Martret M, Roig-Villanova I, Ruberti I, Martinez-Garcia JF. 2013. The bHLH proteins BEE and BIM positively modulate the shade avoidance syndrome in Arabidopsis seedlings. The Plant Journal 75, 989-1002.
19. Clack T, Mathews S, Sharrock R. 1994. The phytochrome apoprotein family in Arabidopsis is encoded by 5 genes-the sequences and expression of PHYD and PHYE. Plant Molecular Biology 25, 413-427.
20. de Kroon H, Hendriks M, van Ruijven J, Ravenek J, Padilla FM, Jongejans E, Visser EJW, Mommer L. 2012. Root responses to nutrients and soil biota: drivers of species coexistence and ecosystem productivity. Journal of Ecology 100, 6-15.
21. de Wit M, Kegge W, Evers JB, Vergeer-van Eijk MH, Gankema P, Voesenek LACJ, Pierik R. 2012. Plant neighbor detection through touching leaf tips precedes phytochrome signals. Proceedings of the National Academy of Sciences, USA 109, 14705-14710.
22. Demarsy E, Fankhauser C. 2009. Higher plants use LOV to perceive blue light. Current Opinion in Plant Biology 12, 69-74.
23. Dicke M. 2009. Behavioural and community ecology of plants that cry for help. The Plant Cell and Environment 32, 654-665.
24. Dicke M, Baldwin IT. 2010. The evolutionary context for herbivoreinduced plant volatiles: beyond the cry for help. Trends in Plant Science 15, 167-175.
25. Djakovic-Petrovic T, de Wit M, Voesenek LACJ, Pierik R. 2007. DELLA protein regulation in growth responses to canopy signals. The Plant Journal 51, 117-126.
26. Fankhauser C, Ulm R. 2011. Light-regulated interactions with SPA proteins underlie cryptochrome-mediated gene expression. Genes and Development 25, 1004-1009.
27. Favory J, Stec A, Gruber H, et al. 2009. Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO Journal 28, 591-601.
28. Finlayson SA, Jung IJ, Mullet JE, Morgan PW. 1999. The mechanism of rhythmic ethylene production in Sorghum. The role of phytochrome B and simulated shading. Plant Physiology 119, 1083-1089.
29. Folta KM. 2004. Green light stimulates early stem elongation, antagonizing light-mediated growth inhibition. Plant Physiology 135, 1407-1416.
30. Foo E, Ross JJ, Davies NW, Reid JB, Weller JL. 2006. A role for ethylene in the phytochrome-mediated control of vegetative development. The Plant Journal 46, 911-921.
31. Franklin KA. 2008. Shade avoidance. New Phytologist 179, 930-944.
32. Franklin KA, Davis SJ, Stoddart WM, Vierstra RD, Whitelam GC. 2003. Mutant analyses define multiple roles for phytochrome C in Arabidopsis thaliana photomorphogenesis. The Plant Cell 15, 1981-1989.
33. Frost CJ, Appel M, Carlson JE, De Moraes CM, Mescher MC, Schultz JC. 2007. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecology Letters 10, 490-498.
34. Grime JP and Jeffrey DW. 1965. Seedling establishment in vertical gradients of sunlight. Journal of Ecology 53, 621-642.
35. Gommers CMM, Visser EJW, St Onge KR, Voesenek LACJ, Pierik R. 2013. Shade tolerance: when growing tall is not an option. Trends in Plant Science 18, 65-71.
36. Hamant O, Heisler MG, Jonsson H, et al. 2008. Developmental patterning by mechanical signals in Arabidopsis. Science 322, 1650-1655.
37. Hamant O, Traas J. 2010. The mechanics behind plant development. New Phytologist 185, 369-385.
38. Haswell ES, Peyronnet R, Barbier-Brygoo H, Meyerowitz EM, Frachisse J. 2008. Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Current Biology 18, 730-734.
39. Heil M, Silva Bueno JC. 2007. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proceedings of the National Academy of Sciences, USA 104, 5467-5472.
40. Henry H, Thomas S. 2002. Interactive effects of lateral shade and wind on stem allometry, biomass allocation, and mechanical stability in Abutilon theophrasti (Malvaceae). American Journal of Botany 89, 1609-1615.
41. Holm M, Ma L, Qu L, Deng X. 2002. Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes and Development 16, 1247-1259.
42. Holmes MG, Smith H. 1975. The function of phytochrome in plants growing in the natural environment. Nature 254, 512-514.
43. Hornitschek P, Kohnen MV, Lorrain S, et al. 2012. Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. The Plant Journal 71, 699-711.
44. Jaillais Y, Chory J. 2010. Unraveling the paradoxes of plant hormone signaling integration. Nature Structural and Molecular Biology 17, 642-645.
45. Karban R, Maron J, Felton GW, Ervin G, Eichenseer H. 2003. Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants. Oikos 100, 325-332.
46. Kegge W, Pierik R. 2010. Biogenic volatile organic compounds and plant competition. Trends in Plant Science 15, 126-132.
47. Kegge W, Weldegergis BT, Soler R, Eijk MV, Dicke M, Voesenek LACJ, Pierik R. 2013. Canopy light cues affect emission of constitutive and methyl jasmonate-induced volatile organic compounds in Arabidopsis thaliana. New Phytologist 200, 861-874.
48. Keller MM, Jaillais Y, Pedmale UV, Moreno JE, Chory J, Ballaré CL. 2011. Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades. The Plant Journal 67, 195-207.
49. Keuskamp DH, Pollmann S, Voesenek LACJ, Peeters AJM, Pierik R. 2010a. Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proceedings of the National Academy of Sciences, USA 107, 22740-22744.
50. Keuskamp DH, Sasidharan R, Pierik R. 2010b. Physiological regulation and functional significance of shade avoidance responses to neighbors. Plant Signaling and Behavior 5, 655-662.
51. Keuskamp DH, Sasidharan R, Vos I, Peeters AJM, Voesenek LACJ, Pierik R. 2011. Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. The Plant Journal 67, 208-217
52. Kiba T, Henriques R, Sakakibara H, Chua N. 2007.Targeted degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL complex regulates clock function and photomorphogenesis in Arabidopsis thaliana. The Plant Cell 19, 2516-2530.
53. 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.
54. Kung C. 2005. A possible unifying principle for mechanosensation. Nature 436, 647-654.
55. Kurepin LV, Shah S, Reid DM. 2007. Light quality regulation of endogenous levels of auxin, abscisic acid and ethylene production in petioles and leaves of wild type and ACC deaminase transgenic Brassica napus seedlings. Plant Growth Regulation 52, 53-60.
56. Lau OS, Deng XW. 2012. The photomorphogenic repressors COP1 and DET1: 20 years later. Trends in Plant Science 17, 584-593.
57. Leivar P, Tepperman JT, Cohn MM, Monte E, Al-Sady B, Erickson E, Quail PH. 2012. Dynamic antagonism between phytochromes and PIF family basis helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. The Plant Cell 24, 1398-1419.
58. Li L, Ljung K, Breton G, et al. 2012. Linking photoreceptor excitation to changes in plant architecture. Genes and Development 26, 785-790.
59. Lian H, He S, Zhang Y, Zhu D, Zhang J, Jia K, Sun S, Li L, Yang H. 2011. Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism. Genes and Development 25, 1023-1028.
60. Lin C, Yang H, Guo H, Mockler T, Chen J, Cashmore AR. 1998. Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proceedings of the National Academy of Sciences, USA 95, 2686-2690.
61. Liu B, Zuo Z, Liu H, Liu X, Lin C. 2011. Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Genes and Development 25, 1029-1034.
62. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C. 2008. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. The Plant Journal 53, 312-323.
63. Mas P, Devlin PF, Panda S, Kay SA. 2000. Functional interaction of phytochrome B and cryptochrome 2. Nature 408, 207-211.
64. Millenaar FF, Cox MCH, de Jong van Berkel YEM, Welschen RAM, Pierik R, Voesenek LACJ, Peeters AJM. 2005. Ethyleneinduced differential growth in petioles of Arabidopsis thaliana: analyzing natural variation, response kinetics and regulation. Plant Physiology 137, 998-1008.
65. Millenaar FF, van Zanten M, Cox MCH, Pierik R, Voesenek L, Peeters AJM. 2009. Differential petiole growth in Arabidopsis thaliana: photocontrol and hormonal regulation. New Phytologist 184, 141-152.
66. Morelli G, Ruberti I. 2000. Shade avoidance responses. Driving auxin along lateral routes. Plant Physiology 122, 621-626.
67. Moreno JE, Tao Y, Chory J, Ballaré CL. 2009. Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proceedings of the National Academy of Sciences, USA 106, 4935-4940.
68. Morgan D, Smith H. 1978. Function of phytochrome in naturalenvironment. 7. Relationship between phytochrome photoequilibrium and development in light grown Chenopodium-album L. Planta 142, 187-193.
69. Morgan D, Smith H. 1979. Function of phytochrome in the naturalenvironment. 8. Systematic relationship between phytochromecontrolled development and species habitat, for plants grown in simulated natural radiation. Planta 145, 253-258.
70. Mullen JL, Weinig C, Hangarter RP. 2006. Shade avoidance and the regulation of leaf inclination in Arabidopsis. The Plant Cell and Environment 29, 1099-1106.
71. Nagashima H, Hikosaka K. 2012. Not only light quality but also mechanical stimuli are involved in height convergence in crowded Chenopodium album stands. New Phytologist 195, 803-811.
72. Ninkovic V. 2003. Volatile communication between barley plants affects biomass allocation. Journal of Experimental Botany 54, 1931-1939.
73. Pierik R, Cuppens MLC, Voesenek LACJ, Visser EJW. 2004a. Interactions between ethylene and gibberellins in phytochromemediated shade avoidance responses in tobacco. Plant Physiology 136, 2928-2936.
74. Pierik R, Djakovic-Petrovic T, Keuskamp DH, de Wit M, Voesenek L. 2009. Auxin and ethylene regulate elongation responses to neighbor proximity signals independent of gibberellin and DELLA proteins in Arabidopsis. Plant Physiology 149, 1701-1712.
75. Pierik R, Whitelam GC, Voesenek LACJ, de Kroon H, Visser EJW. 2004b. 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.
76. Pierik R, Mommer L, Voesenek LA. 2013. Molecular mechanisms of plant competition: neighbour detection and response strategies. Functional Ecology 27, 841-853.
77. Polko JK, van Zanten M, van Rooij JA, Maree AFM, Voesenek LACJ, Peeters AJM, Pierik R. 2012. Ethylene-induced differential petiole growth in Arabidopsis thaliana involves local microtubule reorientation and cell expansion. New Phytologist 193, 339-348.
78. Rizzini L, Favory J, Cloix C, et al. 2011. Perception of UV-B by the Arabidopsis UVR8 protein. Science 332, 103-106.
79. Roig-Villanova I, Bou-Torrent J, Galstyan A, Carretero-Paulet L, Portoles S, Rodriguez-Conception M, Garcia JFM. 2007. Interaction of shade avoidance and auxin responses: a role for two novel atypical bHLH proteins. EMBO Journal 26, 4756-4767.
80. Rolauffs S, Fackendahl P, Sahm J, Fiene G, Hoecker U. 2012. Arabidopsis COP1 and SPA genes are essential for plant elongation but not for acceleration of flowering time in response to a low red light to far-red light ratio. Plant Physiology 160, 2015-2027.
81. Runyon JB, Mescher MC, De Moraes CM. 2006. Volatile chemical cues guide host location and host selection by parasitic plants. Science 313, 1964-1967.
82. Salisbury FJ, Hall A, Grierson GS, Halliday KJ. 2007. Phytochrome coordinates Arabidopsis shoot and root development. The Plant Journal 50, 429-438.
83. Sasidharan R, Chinnappa CC, Staal M, Elzenga JTM, Yokoyama R, Nishitani K, Voesenek LACJ, 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.
84. Sasidharan R, Chinnappa CC, 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.
85. Schmitt J. 1997. Is photomorphogenic shade avoidance adaptive? Perspectives from population biology. Plant, Cell and Environment 20, 826-830.
86. Schmitt J, McCormac AC, Smith H. 1995. A test of the adaptive plasticity hypothesis using transgenic and mutant plants disabled in phytochrome-mediated elongation responses to neighbors. American Naturalist 146, 937-953.
87. Sellaro R, Crepy M, Ariel Trupkin S, Karayekov E, Sabrina Buchovsky A, Rossi C, Casal JJ. 2010. Cryptochrome as a sensor of the blue/green ratio of natural radiation in Arabidopsis. Plant Physiology 154, 401-409.
88. Sellaro R, Hoecker U, Yanovsky M, Chory J, Casal JJ. 2009. Synergism of red and blue light in the control of Arabidopsis gene expression and development. Current Biology 19, 1216-1220.
89. 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 and Development 19, 2811-2815.
90. Smalle J, Haegman M, Kurepa J, Van Montagu M, Van der Straeten D. 1997. Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proceedings of the National Academy of Sciences, USA 94, 2756-2761.
91. Smith H. 1982. Light quality, photoperception, and plant strategy. Annual Review of Plant Physiology and Plant Molecular Biology 33, 481-518.
92. Smith H. 2000. Phytochromes and light signal perception by plants-an emerging synthesis. Nature 407, 585-591.
93. Smith H, Holmes MG. 1977. Function of phytochrome in naturalenvironment. 3. Measurement and calculation of phytochrome photoequilibria. Photochemistry and photobiology 25, 547-550.
94. Sorin C, Salla-Martret M, Bou-Torrent J, Roig-Villanova I, Martinez-Garcia JF. 2009. ATHB4, a regulator of shade avoidance, modulates hormone response in Arabidopsis seedlings. The Plant Journal 59, 266-277.
95. Stamm P, Kumar PP. 2010. The phytohormone signal network regulating elongation growth during shade avoidance. Journal of Experimental Botany 61, 2889-2903.
96. Steindler C, Matteucci A, Sessa G, Weimar T, Ohgishi M, Aoyama T, Morelli G, Ruberti I. 1999. Shade avoidance responses are mediated by the ATHB-2 HD-Zip protein, a negative regulator of gene expression. Development 126, 4235-4245.
97. Tanaka SI, Nakamura S, Mochizuki N, Nagatani A. 2002. Phytochrome in cotyledons regulates the expression of genes in the hypocotyl through auxin-dependent and -independent pathways. Plant and Cell Physiology 43, 1171-1181.
98. Tao Y, Ferrer JL, Ljung K, et al. 2008. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133, 164-176.
99. Valladares F, Niinemets U. 2008. Shade tolerance, a key plant feature of complex nature and consequences RID A-3816-2008. Annual Review of Ecology Evolution and Systematics 39, 237-257.
100. Vermeulen PJ, Anten NPR, Schieving F, Werger MJA, During HJ. 2008. Height convergence in response to neighbour growth: genotypic differences in the stoloniferous plant Potentilla reptans. New Phytologist 177, 688-697.
101. 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.
102. Yamaguchi R, Nakamura M, Mochizuki N, Kay SA, Nagatani A. 1999. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. Journal of Cell Biology 145, 437-445.
103. Zhang T, Maruhnich SA, Folta KM. 2011. Green light induces shade avoidance symptoms. Plant Physiology 157, 1528-1536.
104. Zheng X, Wu S, Zhai H, et al. 2013. Arabidopsis phytochrome B promotes SPA1 nuclear accumulation to repress photomorphogenesis under far-red light. The Plant Cell 25, 115-133.
105. Zuo Z, Liu H, Liu B, Liu X, Lin C. 2011. Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Current Biology 21, 841-847.