Journal of Journal of Experimental Botany, Vol. 48, No. 307, pp. 201-210, February 1997 Experimental Botany REVIEW ARTICLE The role of ethylene in the development of plant form Liam Dolan1 John Innes Centre, Colney, Norwich NR4 7UH, UK Received 27 March 1996; Accepted 18 September 1996 Downloaded from https://academic.oup.com/jxb/article/48/2/201/652810 by guest on 02 October 2021 Abstract the number of parts determining their longevity and their ultimate fates. The fates of buds, for example, was largely Ethylene is a gaseous growth factor involved in a determined by their position on the tree. Buds formed diverse array of cellular, developmental and stress- within the last two years in the vicinity of the leader had related processes in plants. A number of examples of a greater chance of survival, of eventually developing as the role played by ethylene in the development of form long shoots or developing as inflorescences. Buds in more in plants are described; reaction wood formation, floral basal positions tended to be relatively dormant or more induction, sex determination, flooding-induced shoot likely to die (senesce or abscise) While many factors will elongation, and leaf abscission. Recent advances in be involved in the regulation of this pattern of develop- the understanding of the molecular mechanism under- ment it is clear that ethylene plays a key role in the pinning post-pollination perianth wilting in orchids is co-ordination of these processes and as such plays a reviewed. This study indicates that the process of central role in the development of form in plants. The post-pollination perianth wilting involves an early role played by ethylene in the development of form will increase in sensitivity to endogenous levels of ethylene be described using examples gleaned from many species which set in motion a chain of events in which ethylene of angiosperms and gymnosperms. While it is not intended autocatalytically induces its own synthesis in the pistil. to review the literature exhaustively, it will be shown how Ethylene also induces the expression of ACO in the ethylene acts in some of the processes that Maillette perianth which converts pistil-derived ACC into ethy- (1982) showed to be important in the establishment of lene which drives the wilting process. Concepts drawn plant (tree) form: secondary thickening and reaction from this system are then applied to the Arabidopsis wood formation, floral development, sex determination, root epidermis in which ethylene is a positive regulator floral senescence, leaf abscission, shoot elongation, and of root hair development in an effort to come to a cell differentiation. mechanistic understanding of the process of pattern formation in this system. Understanding the molecular basis of the role of ethylene in these model systems will provide useful paradigms for examining the part Ethylene biosynthesis and signal transduction played by ethylene in the diverse array of processes Ethylene is a gaseous growth factor that was identified in which this growth factor is involved. by Neljubov as the causative agent for laboratory air- induced horizontal growth of pea seedlings (Neljubov, Key words: Ethylene, development, plant form. 1901). In recent years there have been great advances in our understanding of ethylene biosynthesis and signal transduction (see Ecker, 1995; Zarembinski and Introduction Theologis, 1994, for reviews). Ethylene is derived from The development of plants involves the progressive birth the amino acid, methionine: methionine is converted and death of their iterated parts: shoots, roots, leaves, to 5-adenosyl methionine (SAM) by the action of flowers, and buds (Maillette, 1982). In her analysis of the methionine adenosyl transferase; SAM is converted to development of tree form in silver birch, Maillette (1982) 1-aminocyclopropane-l-carboxylic acid (ACC) by ACC examined the life history of the buds (meristems) and synthase (ACS): ACC is converted to ethylene by ACC showed that tree shape could be examined by counting oxidase (ACO) (see reviews by Yang and Hoffman, 1984; 1 Fax: +44 1603 501771. Oxford University Press 1997 202 Dolan Kende, 1993) (Fig. 1). ACS genes comprise a multi-gene the ethylene receptor (Chang et al, 1993). Its sequence family in most species examined to date (Liang et al, suggests that it is a histidine kinase similar to the bacterial 1992). Individual members of the gene family exhibit two component kinases and has recently been shown to tissue specific regulation or are transcriptionally activated bind ethylene. A similar gene, ERS which lacks the by a specific set of modulators such as auxin, flooding or receiver domain, may also act as an ethylene receptor mechanical stress (Abel et al, 1995; Olson et al, 1995; since not all ethylene responses are blocked in etrl Botella et al, 1995). ACO genes also comprise a gene mutants (Hua et al, 1995). Epsisatic interactions have family (Tang et al, 1993). Three members have been shown that the CTR1 gene, a negative regulator of the identified in the orchid Phalaeopsis (Nadeau et al, 1993). ethylene response, acts downstream of the receptor Both ACS and ACO are positively regulated by ethylene (Kieber et al, 1993). CTR1 encodes a serine-threonine in a number of systems (O'Neill et al, 1993). kinase similar to members of the Raf kinase family ACC is water soluble and has been shown to move (Kieber et al, 1993). It is possible that the role of this through the apoplast over great distances (from roots to gene is to modulate flux through the signalling pathway. shoots) in tomato plants and has been shown to move A number of other genes have been identified which act Downloaded from https://academic.oup.com/jxb/article/48/2/201/652810 by guest on 02 October 2021 from stigmatic surfaces to petals in a number of species downstream of CTR1 which are involved in specific (Bradford and Yang, 1980; Reid et al, 1984; Woltering, aspects of ethylene responses such as root elongation, 1990). Ethylene is 14 times as soluble in lipid as in water hypocotyl hook opening etc. (Roman et al, 1995). and other solutes present in the aqueous phase (as in the cytoplasm) will decrease its solubililty (see Abeles et al, 1992, for a description of the physical characteristics of Development of form: processes in which ethylene ethylene). Consequently, ethylene might be expected to plays a key role act locally in the absence of air spaces. Tree shape The genetic dissection of the ethylene signal transduc- tion pathway has provided powerful insights into the Upon germination the shoot meristem laid down in the molecular mechanism that underpin the ethylene response developing embryo produces a shoot system composed and has provided developmental biologists with a wealth of iterated units, leaf, node, internode, and axillary bud. of tools to examine specific aspects of plant development The pattern in which these units of construction are put (Ecker, 1995; Roman et al, 1995). Screening mutant together is highly invariant within a species, e.g. phyllo- populations for plants exhibiting abnormal ethylene taxy is generally invariant within a species although it responses has led to the identification of a number of may change with ontogeny. Nevertheless, the number and genes that are involved in ethylene signal transduction stature of the units that survive in long-lived plants (such (Bleecker et al, 1988; Guzman and Ecker, 1990; Kieber as trees) is largely determined by environmental factors etal, 1993; Roman et al, 1995; Huae/ al, 1995) (Fig. 1). such as light, water availability, physical stress, etc. That The ETHYLENE RESISTANT1 (ETR1) gene encodes physical stress is an important feature in the determination of plant form has been well documented. A striking example of the effect of mechanical stress not only on plant stature but the stature of an entire vegetation type, Biosynthesis Signal transduction is the elfin montane forests of central America. Methionine Ethylene Didymopanax pittieri is a tree that grows on and below + exposed hill crests in montane rain forests. Lawton (1982) 1 1 A9 clearly showed that plant stature is determined by proxim- SAM ETR1IEIN4 ity to the crest and, consequently, wind-induced mechan- 1 1 AM3 ical stress. Plants at the crest, have relatively thicker 1 trunks and finer twigs while those growing in less exposed ACC CTR1 areas are relatively taller with thicker twigs. He rules out a genetic basis for the morphological differentiation and, 1 1 therefore, highlights the importance of thigmmorphogen- Ethylene EIN2 esis, the morphological changes in response to physical stimuli, in the development of plant form. A\ In a classic set of experiments on the development of Various ethylene compression wood in Pinus strobus, Sinnott (1952) high- responses lighted the regulative role of reaction wood in response to physical stimulation. Reaction wood is a specialized Fig. 1. Simplified schematic diagram of the pathways of ethylene wood type that is formed in trees in response to physical biosynthesis and ethylene signal transduction. Adapted from figures in Zarembinski and Theologis (1994) and Roman et al. (1995). stress (Scurfield, 1973). Reaction wood in gymnosperms, Ethylene and plant form 203 such as P. strobus forms on the underside of stressed Leaf abscission branches, thereby serving to support or reorientate the Mailette's (1982) study showed that while the formation limb. In angiosperms, reaction wood forms on the upper of long and short shoots was a major factor in the side of the branch and serves to 'pull' the limb into development of birch tree form so also was the regulated position. Sinnott (1952) tied vertical shoot axes and loss (abscission) of these structures. The abscission of lateral branches in various abnormal positions, let them leaves in response to ethylene is one of the earliest develop for a further 2 years and examined the develop- documented effects of ethylene.