Interactions between Ethylene and Gibberellins in Phytochrome-Mediated Shade Avoidance Responses in Tobacco

Oxford University Press (OUP) - Tập 136 Số 2 - Trang 2928-2936 - 2004
Ronald Pierik1,2, Mieke L.C. Cuppens1,2, Laurentius A. C. J. Voesenek1,2, Eric J. W. Visser1,2
1Department of Experimental Plant Ecology, Radboud University Nijmegen, Toernooiveld, 6525 ED Nijmegen, The Netherlands (R.P., M.L.C.C., E.J.W.V.); and Department of Plant Ecophysiology, Utrecht University, 3584 CA Utrecht, The Netherlands (R.P., L.A.C.J.V.)
2Department of Plant Ecophysiology, Utrecht University, 3584 CA Utrecht, The Netherlands (R.P., L.A.C.J.V.)

Tóm tắt

Abstract Plants respond to proximate neighbors with a suite of responses that comprise the shade avoidance syndrome. These phytochrome-mediated responses include hyponasty (i.e. a more vertical orientation of leaves) and enhanced stem and petiole elongation. We showed recently that ethylene-insensitive tobacco (Nicotiana tabacum) plants (Tetr) have reduced responses to neighbors, showing an important role for this gaseous plant hormone in shade avoidance. Here, we investigate interactions between phytochrome signaling and ethylene action in shade avoidance responses. Furthermore, we investigate if ethylene acts in these responses through an interaction with the GA class of hormones. Low red to far-red light ratios (R:FR) enhanced ethylene production in wild-type tobacco, resulting in shade avoidance responses, whereas ethylene-insensitive plants showed reduced shade avoidance responses. Plants with inhibited GA production showed hardly any shade avoidance responses at all to either a low R:FR or increased ethylene concentrations. Furthermore, low R:FR enhanced the responsiveness of hyponasty and stem elongation in both wild-type and Tetr plants to applied GA3, with the stem elongation process being more responsive to GA3 in the wild type than in Tetr. We conclude that phytochrome-mediated shade avoidance responses involve ethylene action, at least partly by modulating GA action.

Từ khóa


Tài liệu tham khảo

Achard P, Vriezen WH, Van der Straeten D, Harberd N (2003) Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell  15  :  2816–2825

Aphalo PJ, Ballaré CL, Scopel AL (1999) Plant-plant signalling, the shade avoidance response and competition. J Exp Bot  50  :  1629–1634

Ballaré CL (1999) Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. Trends Plant Sci  4  :  97–102

Beall FD, Yeung EC, Pharis RP (1996) Far-red light stimulates internode elongation, cell division, cell elongation, and gibberellin levels in bean. Can J Bot  74  :  743–752

Chory J, Li J (1997) Gibberellins, brassinosteroids and light-regulated development. Plant Cell Environ  20  :  801–806

Emery RJN, Pearce DW, Pharis RP, Reid DM, Chinnappa CC (2001) Stem elongation and gibberellins in alpine and prairie ecotypes of Stellaria longipes.  Plant Growth Regul  35  :  17–29

Emery RJN, Reid DM, Chinnappa CC (1994) Phenotypic plasticity of stem elongation in two ecotypes of Stellaria longipes: the role of ethylene and response to wind. Plant Cell Environ  17  :  691–700

Finlayson SA, Jung I-J, Mullet JE, Morgan PW (1999) The mechanism of rhythmic ethylene production in Sorghum: the role of phytochrome B and simulated shading. Plant Physiol  119  :  1083–1089

Finlayson SA, Lee I-J, Morgan PW (1998) Phytochrome B and the regulation of circadian ethylene production in sorghum. Plant Physiol  116  :  17–25

Fiorani F, Bogemann GM, Visser EJW, Lambers H, Voesenek LACJ (2002) Ethylene emission and responsiveness to applied ethylene vary among Poa species that inherently differ in leaf elongation rates. Plant Physiol  129  :  1382–1390

Franklin KA, Praekelt U, Stoddart WM, Billingham OE, Halliday KJ, Whitelam GC (2003) Phytochromes B, D and E act redundantly to control multiple physiological responses in Arabidopsis. Plant Physiol  131  :  1340–1346

García-Martínez JL, Keith B, Bonner BA, Stafford AE, Rappaport L (1987) Phytochrome regulation of the response to exogenous gibberellins by epicotyls of Vigna sinensis.  Plant Physiol  85  :  212–216

Harberd NP (2003) Relieving DELLA restraint. Science  299  :  1853–1854

Hoffmann-Benning S, Kende H (1992) On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiol  99  :  1156–1161

Imaseki H, Pjon C-H, Furya M (1971) Phytochrome action in Oryza sativa L. Plant Physiol  48  :  241–244

Kende H, Van der Knaap E, Cho H-T (1998) Deepwater rice: a model plant to study stem elongation. Plant Physiol  118  :  1105–1110

Knoester M, Van Loon LC, Van den Heuvel J, Hennig J, Bol JF, Linthorst HJM (1998) Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proc Natl Acad Sci USA  95  :  1933–1937

Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene is required for differential cell elongation in the Arabidopsis hypocotyl. Cell  85  :  183–194

López-Juez E, Kobayashi M, Sakurai A, Kamiya Y, Kendrick RE (1995) Phytochrome, gibberellins, and hypocotyl growth. Plant Physiol  107  :  131–140

Morelli G, Ruberti I (2000) Shade avoidance responses: driving auxin along lateral routes. Plant Physiol  122  :  621–626

Pierik R, Visser EJW, de Kroon H, Voesenek LACJ (2003) Ethylene is required in tobacco to succesfully compete with proximate neighbours. Plant Cell Environ  26  :  1229–1234

Pierik R, Whitelam GC, Voesenek LACJ, de Kroon H, Visser EJW (2004) Canopy studies on ethylene-insensitive tobacco identify ethylene as a novel element in blue light and plant-plant signalling. Plant J  38  :  310–319

Reid JB, Hasan O, Ross JJ (1990) Internode length in Pisum: gibberellins and the response to far-red-rich light. J Plant Physiol  137  :  46–52

Rijnders JHGM, Yang YY, Kamiya Y, Takahashi N, Barendse GWM, Blom CWPM, Voesenek LACJ (1997) Ethylene enhances gibberellin levels and petiole sensitivity in flooding-tolerant Rumex palustris but not in flooding-intolerant R. acetosa.  Planta  203  :  20–25

Samimy C (1978) Effect of light on ethylene production and hypocotyl growth of soybean seedlings. Plant Physiol  61  :  772–774

Smalle J, Haegman M, Kurepa J, Van Montagu M, Van der Straeten D (1997) Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proc Natl Acad Sci USA  94  :  2756–2761

Smith H (2000) Phytochromes and light signal perception by plants: an emerging synthesis. Nature  407  :  585–591

Smith H, Whitelam GC (1997) The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ  20  :  840–844

Vangronsveld J, Clijsters H, Van Poucke M (1988) Phytochrome-controlled ethylene biosynthesis of intact etiolated bean seedlings. Planta  174  :  19–24

Voesenek LACJ, Benschop JJ, Bou J, Cox MCH, Groeneveld HW, Millenaar FF, Vreeburg RAM, Peeters AJM (2003) Interactions between plant hormones regulate submergence-induced shoot elongation in the flooding-tolerant dicot Rumex palustris.  Ann Bot (Lond)  91  :  205–211

Voesenek LACJ, Harren FJM, Bogemann GM, Blom CWPM, Reuss J (1990) Ethylene production and petiole growth in Rumex plants induced by soil waterlogging: the application of a continuous flow system and a laser driven intracavity photoacoustic detection system. Plant Physiol  94  :  1071–1077

Weller JL, Ross JJ, Reid JB (1994) Gibberellins and phytochrome regulation of stem elongation in pea. Planta  192  :  489–496

Whitelam GC, Devlin PF (1997) Roles of different phytochromes in Arabidopsis photomorphogenesis. Plant Cell Environ  20  :  752–758