Growth Control by Ethylene: Adjusting Phenotypes to the Environment

Journal of Plant Growth Regulation - Tập 26 - Trang 188-200 - 2007
Ronald Pierik1, Rashmi Sasidharan1,2, Laurentius A. C. J. Voesenek1
1Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, Utrecht, The Netherlands
2Department of Biological Sciences, University of Calgary, Calgary, Canada

Tóm tắt

Plants phenotypically adjust to environmental challenges, and the gaseous plant hormone ethylene modulates many of these growth adjustments. Ethylene can be involved in environmentally induced growth inhibition as well as growth stimulation. Still, ethylene has long been considered a growth inhibitory hormone. There is, however, accumulating evidence indicating that growth promotion is a common feature in ethylene responses. This is evident in environmental challenges, such as flooding and competition, where the resulting avoidance responses can help plants avoid adversity. To show how ethylene-mediated growth enhancement can facilitate plant performance under adverse conditions, we explored a number of these examples. To escape adversity, plants can optimize growth and thereby tolerate abiotic stresses such as drought, and this response can also involve ethylene. In this article we indicate how opposing effects of ethylene on plant growth can be brought about, by discussing a unifying, biphasic ethylene response model. To understand the mechanistic basis for this multitude of ethylene-mediated growth responses, the involvement of ethylene in processes that control cell expansion is also reviewed.

Tài liệu tham khảo

Abeles FB, Morgan PW, Saltveit ME .1992. Ethylene in Plant Biology. San Diego, CA, USA, Academic Press, pp 1–398 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. Am Nat 166:650–660 Anten NPR, Casado-Garcia R, Pierik R, Pons TL. 2006. Ethylene sensitivity affects changes in growth patterns, but not stem properties, in response to mechanical stress in tobacco. Physiol Plant 128:274–282 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 Ballaré CL. 1999. Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. Trends Plant Sci 4:97–102 Bartels D, Sunkar R. 2005. Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58 Baskin TI. 2001. On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215:150–171 Belfield EJ, Ruperti B, Roberts JA, Queen-Mason S. 2005. Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission in Sambucus nigra. J Exp Bot 56:817–823 Beltrano J, Ronco MG, Montaldi ER. 1999. Drought stress syndrome in wheat is provoked by ethylene evolution imbalance and reversed by rewatering, aminoethoxyvinylglycine, or sodium benzoate. J Plant Growth Regul 18:59–64 Benschop JJ, Bou J, Peeters AJM, Wagemaker N, Guhl K, et al. 2006. Long-term submergence-induced elongation in Rumex palustris requires abscisic acid-dependent biosynthesis of gibberellin. Plant Physiol 141:1644–1652 Benschop JJ, Jackson MB, Guhl K, Vreeburg RAM, Croker SJ, et al. 2005. Contrasting interactions between ethylene and abscisic acid in Rumex species differing in submergence tolerance. Plant J 44:756–768 Binder BM, O’Malley OC, Wang W, Moore JM, Parks BM, et al. 2004. Arabidopsis seedling growth response and recovery to ethylene. A kinetic analysis. Plant Physiol 136:2913–2920 Blom CWPM. 1999. Adaptations to flooding stress: from plant community to molecule. Plant Biol 1:261–273 Boller T, Kende H. 1980. Regulation of wound ethylene synthesis in plants. Nature 286:259–260 Borch K, Bouma TJ, Lynch JP, Brown KM. 1999. Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ 22:425–431 Braam J. 2005. In touch: plant responses to mechanical stimuli. New Phytol 165:373–389 Bray EA. 1997. Plant responses to water deficit. Trends Plant Sci 2:48–54 Brummell DA, Bird CR, Schuch W, Bennett AB. 1997. An endo-1,4-beta-glucanase expressed at high levels in rapidly expanding tissues. Plant Mol Biol 33:87–95 Calabrese EJ. 2004. Hormesis: from marginalization to mainstream: a case for hormesis as the default dose–response model in risk assessment. Toxicol Appl Pharmacol 197:125–136 Cao XF, Linstead P, Berger F, Kieber J, Dolan L. 1999. Differential ethylene sensitivity of epidermal cells is involved in the establishment of cell pattern in the Arabidopsis root. Physiol Plant 106:311–317 Cho HT, Kende H. 1997. Expression of expansin genes is correlated with growth in deepwater rice. Plant Cell 9:1661–1671 Cho SK, Kim JE, Park JA, Eom TJ, Kim WT. 2006. Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants. FEBS Lett 580:3136–3144 Clark DG, Gubrium EK, Barrett JE, Nell TA, Klee HJ. 1999. Root formation in ethylene-insensitive plants. Plant Physiol 121:53–59 Colmer TD. 2003. Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17–36 Cosgrove DJ. 2005. Growth of the plant cell wall. Nature Cell Biol 6:850–861 Cosgrove DJ, Li LC, Cho HT, Hoffmann-Benning S, Moore RC, et al. 2002. The growing world of expansins. Plant Cell Physiol 43:1436–1444 Cox MCH, Benschop JJ, Vreeburg RAM, Wagemaker CAM, Moritz T, et al. 2004. The roles of ethylene, auxin, abscisic acid, and gibberellin in the hyponastic growth of submerged Rumex palustris petioles. Plant Physiol 136:2948–2960 Darley CP, Forrester AM, Queen-Mason SJ. 2001. The molecular basis of plant cell wall extension. Plant Mol Biol 47:179–195 de Kroon H, Mommer L. 2006. Root foraging theory put to the test. Trends Ecol Evol 21:113–116 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 Fischer K, Schopfer P. 1997. Interaction of auxin, light, and mechanical stress in orienting microtubules in relation to tropic curvature in the epidermis of maize coleoptiles. Protoplasma 196:108–116 Foo E, Ross JJ, Davies NW, Reid JB, Weller JL. 2006. A role for ethylene in the phytochrome-mediated control of vegetative development. Plant J 46:911–921 Franklin KA, Whitelam GC. 2005. Phytochromes and shade-avoidance responses in plants. Ann Bot 96:169–175 Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M. 2000. Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404 Fukao T, Xu KN, Ronald PC, Bailey-Serres J. 2006. A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034 Grbic V, Bleecker AB. 1995. Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J 8:595–602 Guzmán P, Ecker JR. 1990. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523 He C-J, Morgan PW, Drew MC. 1992. Enhanced sensitivity to ethylene in nitrogen- or phosphate-starved roots of Zea mays L. during aerenchyma formation. Plant Physiol 98:137–142 Himmelspach R, Williamson RE, Wasteneys GO. 2003. Cellulose microfibril alignment recovers from DCB-induced disruption despite microtubule disorganization. Plant J 36:565–575 Hiwasa K, Rose JKC, Nakano R, Inaba A, Kubo Y. 2003. Differential expression of seven α-expansin genes during growth and ripening of pear fruit. Physiol Plant 117:564–572 Hodge A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24 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 Hua J, Chang C, Sun Q, Meyerowitz EM. 1995. Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269:1712–1714 Hua J, Meyerowitz EM. 1998. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271 Izaguirre MM, Mazza CA, Biondini M, Baldwin IT, Ballare CL. 2006. Remote sensing of future competitors: impacts on plant defenses. Proc Natl Acad Sci USA 103:7170–7174 Jackson RB, Caldwell MM. 1993. Geostatistical patterns of soil heterogeneity around individual perennial plants. J Ecol 81:683–692 Jaffe MJ, Forbes S. 1993. Thigmomorphogenesis—the effect of mechanical perturbation on plants. Plant Growth Regul 12:313–324 Johnson KA, Sistrunk ML, Polisenky DH, Braam J. 1998. Arabidopsis thaliana responses to mechanical stimulation do not require ETR1 or EIN2. Plant Physiol 116:643–649 Kende H, Van der Knaap E, Cho H-T. 1998. Deepwater rice: a model plant to study stem elongation. Plant Physiol 118:1105–1110 Kim JH, Cho H-T, Kende H. 2000. A-expansins in the semiaquatic ferns Marsilea quadrifolia and Regnellidium diphyllum: evolutionary aspects and physiological role in rachis elongation. Planta 212:85–92 Kurepin LV, Walton LJ, Reid DM, Pharis RP, Chinnappa CC. 2006. Growth and ethylene evolution by shade and sun ecotypes of Stellaria longipes in response to varied light quality and irradiance. Plant Cell Environ 29:647–652 Lang JM, Eisinger WR, Green PB. 1982. Effects of ethylene on the orientation of microtubules and cellulose microfibrils of pea epicotyl cells with polylamellata cell walls. Protoplasma 110:5–14 Le J, Vandenbussche F, De Cnodder T, Van der Straeten D, Verbelen JP. 2005. Cell elongation and microtubule behavior in the Arabidopsis hypocotyl: responses to ethylene and auxin. J Plant Growth Regul 24:166–178 Lynch J, Brown KM. 1997. Ethylene and plant responses to nutritional stress. Physiol Plant 100:613–619 Ma Z, Baskin TI, Brown KM, Lynch J. 2003. Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131:1381–1390 Ma Z, Walk TC, Marcus A, Lynch JP. 2001. Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach. Plant Soil 236:221–235 Manavella PA, Arce AL, Dezar CA, Bitton F, Renou J-P, et al. 2006. Cross-talk between ethylene and drought signalling pathways is mediated by the sunflower Hahb-4 transcription factor. Plant J 48:125–137 Millenaar FF, Cox MCH, van Berkel YEM, Welschen RAM, Pierik R, et al. 2005. Ethylene-induced differential growth of petioles in Arabidopsis. Analyzing natural variation, response kinetics, and regulation. Plant Physiol 137:998–1008 Mittler R. 2006. Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19 Mommer L, Lenssen JPM, Huber H, Visser EJW, de Kroon H. 2006. Ecophysiological determinants of plant performance under flooding: a comparative study of seven plant families. J Ecol 94:1117–1129 Mommer L, Pedersen O, Visser EJW. 2004. Acclimation of a terrestrial plant to submergence facilitates gas exchange under water. Plant Cell Environ 27:1281–1287 Munné-Bosch S, Penuelas J, Ansenio D, Llusia J. 2004. Airborne ethylene may alter antioxidant protection and reduce tolerance of Holm oak to heat and drought stress. Plant Physiol 136:2937–2947 Paredez AR, Somerville CR, Ehrhardt DW. 2006. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495 Pierik R, Cuppens MLC, Voesenek LACJ, Visser EJW. 2004a. Interactions between ethylene and gibberellins in phytochrome-mediated shade avoidance responses in tobacco. Plant Physiol 136:2928–2936 Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ. 2006. The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci 11:176–183 Pierik R, Visser EJW, de Kroon H, Voesenek LACJ. 2003. Ethylene is required in tobacco to successfully compete with proximate neighbours. Plant Cell Environ 26:1229–1234 Pierik R, Voesenek LACJ, de Kroon H, Visser EJW. 2004b. Density-induced plant size reduction and size inequalities in ethylene-sensing and ethylene-insensitive tobacco. Plant Biol 6:201–205 Pierik R, Whitelam GC, Voesenek LACJ, de Kroon H, Visser EJW. 2004c. Canopy studies on ethylene-insensitive tobacco identify ethylene as a novel element in blue light and plant–plant signalling. Plant J 38:310–319 Rijnders JHGM, Yang YY, Kamiya Y, Takahashi N, Barendse GWM, et al. 1997. Ethylene enhances gibberellin levels and petiole sensitivity in flooding-tolerant Rumex palustris but not in flooding-intolerant R. acetosa. Planta 203:20–25 Roberts IN, Lloyd CW, Roberts K. 1985. Ethylene-induced microtubule reoreintations: mediation by helical arrays. Planta 164:439–447 Rose JKC, Braam J, Fry SC, Nishitani K. 2002. The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435 Rose JKC, Lee HH, Bennett AB. 1997. Expression of a divergent expansin gene is fruit-specific and ripening-regulated. Proc Natl Acad Sci USA 94:5955–5960 Saab IN, Sachs MM. 1996. A flooding-induced xyloglucan endo-transglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma. Plant Physiol 112:385–391 Schmidt W, Schikora A. 2001. Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiol 125:2078–2084 Sharp RE. 2002. Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ 25:211–222 Shi YH, Zhu SW, Mao XZ, Feng JX, Qin YM, et al. 2006. Transcriptome profiling, molecular biological, and physiological studies reveal a major role for ethylene in cotton fiber cell elongation. Plant Cell 18:651–664 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 KA, Robertson PD. 1971. Effect of ethylene on root extension of cereals. Nature 234:148–149 Spollen WG, LeNoble ME, Samuels TD, Bernstein N, Sharp RE. 2000. Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. Plant Physiol 122:967–976 Steffens B, Wang JX, Sauter M. 2006. Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223:604–612 Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM. 2005. A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17:2230–2242 Sugimoto K, Himmelspach R, Williamson RE, Wasteneys GO. 2003. Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15:1414–1429 Tanimoto M, Roberts K, Dolan L. 1995. Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J 8:943–948 Tholen DJH, Voesenek LACJ, Poorter H. 2004. Ethylene insensitivity does not increase leaf area or relative growth rate in Arabidopsis, Nicotiana tabacum, and Petunia x hybrida. Plant Physiol 134:1803–1812 Van Eck WHJM, Lenssen JPM, Van de Steeg HM, Blom CWPM, de Kroon H. 2006. Seasonal dependent effects of flooding on plant species survival and zonation: a comparative study of 10 terrestrial grassland species. Hydrobiologia 565:59–69 Visser EJW, Bogemann GM. 2006. Aerenchyma formation in the wetland plant Juncus effusus is independent of ethylene. New Phytol 171:305–314 Visser EJW, Nabben RHM, Blom CWPM, Voesenek LACJ. 1997. Elongation by primary lateral roots and adventitious roots during conditions of hypoxia and high ethylene concentrations. Plant Cell Environ 20:647–653 Visser EJW, Pierik R. 2007. Inhibition of root elongation by ethylene in wetland and non-wetland plant species and the impact of longitudinal ventilation. Plant Cell Environ 30:31–38 Voesenek LACJ, Benschop JJ, Bou J, Cox MCH, Groeneveld HW, et al. 2003. Interactions between plant hormones regulate submergence-induced shoot elongation in the flooding-tolerant dicot Rumex palustris. Ann Bot 91:205–211 Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM. 2006. How plants cope with complete submergence. New Phytol 170:213–226 Voesenek LACJ, Rijnders JHGM, Peeters AJM, Van de Steeg HM, de Kroon H. 2004. Plant hormones regulate fast shoot elongation under water: from genes to community. Ecology 85:16–27 Vreeburg RAM, Benschop JJ, Peeters AJM, Colmer TD, Ammerlaan A, et al. 2005. Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris. Plant J 43:597–610 Winz RA, Baldwin IT. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts. Plant Physiol 125:2189–2202 Wu YJ, Spollen WG, Sharp RE, Hetherington PR, Fry SC. 1994. Root-growth maintenance at low water potentials—increased activity of xyloglucan endotransglycosylase and its possible regulation by abscisic-acid. Plant Physiol 106:607–615 Wu YJ, Thorne ET, Sharp RE, Cosgrove DJ. 2001. Modification of expansin transcript levels in the maize primary root at low water potentials. Plant Physiol 126:1471–1479 Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, et al. 2006. Sub1A is an ethylene-response-factor–like gene that confers submergence tolerance to rice. Nature 442:705–708 Xu KN, Mackill DJ. 1996. A major locus for submergence tolerance mapped on rice chromosome 9. Mol Breed 2:219–224 Young TE, Meeley RB, Gallie DR. 2004. ACC synthase expression regulates leaf performance and drought tolerance in maize. Plant J 40:813–825 Zhang XL, Zhang ZJ, Chen J, Chen Q, Wang XC, et al. 2005. Expressing TERF1 in tobacco enhances drought tolerance and abcisic acid sensitivity during seedling development. Planta 222:494–501 Zhu JK. 2002. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273