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PDF Hosted at the Radboud Repository of the Radboud University Nijmegen PDF hosted at the Radboud Repository of the Radboud University Nijmegen This full text is a publisher's version. For additional information about this publication click this link. http://hdl.handle.net/2066/15894 Please be advised that this information was generated on 2014-11-12 and may be subject to change. j Plant Growth Regul (1992) 11:171-188 Jo u rn al of *Plant G fdw th l^gulation © 1992 Springer-Verlag New York Inc An Amalgamation Between Hormone Physiology and Plant Ecology: A Review on Flooding Resistance and Ethylene L. A. C. J. Voesenek,1 A. J. M. van der Sman,1 F. J. M. Harren,2 and C. W. P. M. Blom1 Departments of 'Ecology and 2Molecular and Laser Physics, University of Nijmegen, Nijmegen, The Netherlands Received 5 May, 1992; accepted 7 July, 1992 Abstract. Both distribution of terrestrial plants and between endogenous ethylene concentrations and species composition in flood plain communities are sensitivity towards this growth regulator (“ ethylene strongly influenced by flooding (waterlogging, par­ economy"). Much data has been gathered using a tial submergence, or submergence). The interaction recently developed laser-driven photoacoustic de­ between a plant’s flooding resistance and the sea­ tection technique capable of detecting six parts of sonal timing, duration, depth, or frequency of flood­ ethylene in 10 parts air flowing continuously over ing often determines plant distribution in flood the plant. plains. Flooding may be accompanied by marked physical changes in light, carbon availability, diffu­ sion rate of gases, and density of the environment. Various physiological processes may be affected by Flooding is common throughout the world (Koz- these flooding-induced physical changes, including lowski 1984). It can have a severe impact on terres­ aerobic respiration, photosynthesis, and processes trial plant life and also interfere with human activ­ in which light acts as a source of information (e.g., ities in these areas (Blom 1990A, Maltby 1991). phytochrome photoequilibrium). Certain plant spe­ Floods vary significantly in seasonal timing, dura­ cies acclimatize and adapt to these physical changes tion, depth, and frequency (Voesenek 1990). When to relieve the constraints imposed by the flooded this is combined with the wide variation in the ex­ environment. Underwater photosynthesis, en­ tent of flooding resistance among terrestrial plant hanced shoot elongation, adventitious roots, and species, one can expect a great influence on the aerenchyma formation are typical adaptive re­ occurrence and distribution of plant species (Blom sponses which are believed to improve the oxygen et al. 1990). Various aspects of flooding and plant status of submerged plants. Ethylene and other responses have been extensively reviewed in books plant hormones play a central role in the initiation (Crawford 1987, Etherington 1983, Hook and Craw­ and regulation of most of these adaptive responses, ford 1978, Hook et al. 1988, Jackson et al. 1991, which permit “ escape” from anaerobiosis. Mecha­ Kozlowski 1984), special journal issues (Blom nisms of direct tolerance of anaerobic conditions, 1990B), and separate papers (Armstrong 1979, 1982, such as a vigorous fermentative respiratory path­ Armstrong et al. 1991, Blom 1990C, Crawford 1982, way, are of particular importance when the plant is 1983, 1989, Davy et al. 1990, Drew 1983, 1990, very deeply submerged, or during the night and Drew and Lynch 1980, Ernst 1990, Jackson 1982, when the water is sufficiently turbid to exclude 1985A, 1985B, 1987, Laanbroek 1990, Osborne light. 1984, Ridge 1985). These articles provide clear ev­ Studies on the cosmopolitan genus Rumex, dis­ idence that the physical changes accompanying tributed in a flooding gradient on river flood plains, flooding have a strong impact on plant hormones have integrated plant hormone physiology with and that these in turn play a central role in the ini­ plant ecology. Rumex species showed a high degree tiation and regulation of many acclimatic and/or of interspecific variation in ethylene production adaptive responses of terrestrial plants upon flood­ rates, endogenous ethylene concentrations, ethyl­ ing (see also Reid and Bradford 1984). In this con­ ene sensitivity, and ethylene-mediated growth re­ text a key role is reserved for the gaseous plant sponses. The field distribution of Rumex species in hormone ethylene (Jackson 1985A, 1985B, 1987, flooding gradients is explained in terms of a balance 1990, Jackson and Pearce 1991, Ku et al. 1970, Mus- 172 L. A. C. J. Voesenek et al. grave et al. 1972, Osborne 1984, Ridge 1985, 1987). lated more to root porosity (aerenchyma) (Arm­ Only a few studies on ethylene and flooding, how­ strong 1979, Justin and Armstrong 1987, Laan et al. ever, try to relate interspecific variation in physio­ 1989, Smirnoff and Crawford 1983) and to the ter­ logical mechanisms to the ecology of those plant minal products of anaerobic respiration (McMan- species. Ridge (1987) related two types of shoot mon and Crawford 1971, Roberts et al. 1984A) than elongation in response to submergence (large, rapid to the role of hormones. In the present paper, the growth vs. small, delayed growth) with flooding re­ ethylene economy of several Rumex species, de­ gimes (predominantly aquatic vs. emergents in shal­ fined as the balance between endogenous ethylene low waters, marshes, or in areas subjected to brief concentration and sensitivity towards this growth shallow floods). Ridge also presented a provoking regulator (see Voesenek 1990), will be related to the analysis of both costs and benefits of the two types flooding resistance of the species. It is an intriguing of ethylene-mediated shoot elongation. Mitchell possibility that plant distribution and flooding resis­ (1976) and Osborne (1984) also attempted to relate tance in dry-wet gradients correlate with differ­ the variation in shoot elongation under water of ences in hormone physiology. Firstly, the selection Polygonum species and Ranunculus species to their of the genus Rumex as a model for study will be field distribution. Dodds and coworkers (1982) ex­ discussed, followed by a survey of general environ­ amined the relation between waterlogging resis­ mental changes induced by flooding and the impact tance and ethylene metabolism in 21 different cul- on terrestrial plants. The ethylene economy will be tivars of Viciafaba. They suggested that the water­ introduced by a description of a recently developed logging resistance of the various cultivars was photoacoustic detection technique which can mon­ related to the ability to remove (metabolize) in­ itor ethylene levels as low as 6 ppt (6:1012), and then creased amounts of ethylene. Finally, Jackson and will be discussed in relation to waterlogging, com­ coworkers (1987) compared rice varieties of differ­ plete submergence, and field distribution of Rumex ent submergence tolerance, with respect to their species. ethylene responses. Accumulated ethylene was ca­ sually related to fast leaf extension and chlorosis in the submergence-intolerant forms of rice. Pearce and Jackson (1991) compared submergence re­ Rumex as a Model sponses of Barnyard grass (Echinochloa oryzoides) and rice in relation to gaseous changes in the plants. The present study concentrates on the correlative The same changes (i.e., oxygen shortage, elevated and possibly causal relationship between ethylene ethylene, and carbon dioxide) brought about oppo­ economy and flooding resistance and plant distribu­ site effects in the two species growing in the same tion. Three approaches were integrated, that is, habitat. Poorly aerated solutions enhanced shoot ecophysiology, comparative physiology, and a growth in rice and inhibited it in Echinochloa. study of the complete life cycle. Physiological ecol­ These two species probably have contrasting strat­ ogy may provide insights into physiological mech­ egies for survival. anisms underlying acclimatic responses and adap­ Overall, little is known about the hormonal regu­ tive traits of plants under stress. When comparing lation of ecologically significant processes in plant closely related plant species distributed along a development. In a different area of plant physiolog­ stress gradient, a species’ position within such a ical ecology, Dijkstra et al. (1990) showed a positive gradient can be linked directly to specific “ fitness- correlation between the relative growth rates of two increasing” physiological mechanisms (Blom 1987, inbred lines of Plantago major (the fast-growing P. Osmond et al. 1987). Since stress may have differ­ major spp. pleiosperma and the slow-growing P. ent effects on consecutive stages in the life cycle, major spp. major) and their endogenous gibberellin studying several stages in the life cycle is a prereq­ concentrations. A reversion of the growth rate of uisite to achieve complete understanding of plant both lines was realized by the application of exog­ distribution (Grime 1979). enous G A 3 and addition of specific gibberellin in­ The choice of the cosmopolitan genus Rumex as a hibitors (Dijkstra and Kuiper 1989). The ecological model to study the relation between ethylene econ­ significance of differences in growth rate is exten­ omy and flooding resistance is based on the follow­ sively discussed in Grime and Hunt (1975), Grime ing arguments: (1979), Chapin (1980), and Tilman (1988). Up to now, although one was aware of the im­ 1. Eight Rumex species occur in Dutch river flood portant role of hormones in adaptive responses of plains within
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