The Shade Avoidance Syndrome: Multiple Responses Mediated by Multiple Phytochromes

Plant, Cell and Environment (1997) 20, 840Ð844

TECHNICAL REPORT (white this line if not required) The shade avoidance syndrome: multiple responses mediated by multiple phytochromes

H. SMITH & G. C. WHITELAM

Department of Botany, University of Leicester, Leicester LE1 7RH, UK

ABSTRACT somewhat difficult. In the first half of this century, there was a great deal of research on the responses of plants to In recent years, the concept of shade avoidance has pro- artificial shade, using neutral density screens to simulate vided a functional meaning to the role of the phytochrome the reduction in irradiance that occurs in natural plant photoreceptor family in mature plants in their natural canopies. That research must now be regarded as essen- environment, and the question of which of these phy- tially irrelevant, as the reduction in irradiance under shade tochromes is responsible for shade avoidance reactions is now known not to be a reliable signal. The earliest has inevitably been raised. Unfortunately, a misconception reported observations linking phytochromes to shade has arisen that phytochrome B is solely responsible for avoidance responses are probably those of Cumming detecting the environmental signal that initiates the shade (1963), who demonstrated that the germination of avoidance syndrome. This view is too simplistic, and is Chenopodium rubrum seeds was sensitive to R:FR over a based upon a selective interpretation of the available evi- wide range, and speculated that this behaviour may be dence. In this short Commentary, we review the concept of important in optimizing germination in relation to the pres- the shade avoidance syndrome, show how the misconcep- ence of vegetation shade. At about the same time, the pio- tion arose, and emphasize the plurality of perception and neers of modern photomorphogenesis, Hendricks & response that is crucial to successful competition for light. Borthwick (1963), remarked, almost in passing, that over- Key-words: mutants; phytochromes; shade avoidance. hanging foliage might modify vegetative development through effects on stem and leaf growth. Kasperbauer and THE SHADE AVOIDANCE SYNDROME colleagues, in a number of publications, noted the importance of FR light filtered through or reflected by vegetation Whenever plants grow in close proximity, in forests, in in crop plants, particularly in relation to the orientation of herbaceous communities, in grassland swards or in planting rows (e.g. Kasperbauer 1971). hedgerows, there is competition for light. The resource of The demonstration that shade avoidance reactions are radiant energy in dense plant stands is unreliable and phytochrome-mediated via the perception of the relative patchy, and evolution has provided plants with two princi- amounts of R and FR radiation came as a result of quantita- pal approaches to provide for survival under such environ- tive measurements and simulation experiments carried out mental conditions. Essentially, plants may avoid shade, or in the 1970s. First, natural radiation spectra were analysed they may tolerate shade. The angiosperms in particular and summarized in terms of R:FR ratio (Holmes & Smith have evolved impressive capacity to avoid shade, and this 1975, 1977). These natural variations were then related to may be one of the factors that have contributed to their suc- estimated Pfr/P, the phytochrome photoequilibrium, the cess. Shade avoidance represents one of the most impor- relationship being a rectangular hyperbola (Smith & tant competitive strategies that plants possess, and its Holmes 1977). By simulating shade avoidance extension effectiveness is undoubtedly a consequence of the multi- growth responses using artificial light sources which pro- plicity of responses that are available to the shaded plant. vided uniform photosynthetically active radiation (PAR) Responses to shade are many and varied, and it is now but which varied in R:FR, the role of phytochrome-per- fully accepted that shade avoidance reactions are all initi- ceived variations in light quality was then firmly estab- ated by a single environmental signal, the reduction in the lished (Morgan & Smith 1976, 1978, 1981). The range of ratio of red (R) to far-red (FR) radiation (i.e. R:FR) that responses to reduced R:FR ratio correlated identically with occurs within crowded plant communities. We use the the observed growth responses of plants to shade in the nat- term ‘syndrome’ to describe the multiple responses to low ural environment, and indeed plants naturally adapted to R:FR, in analogy to medical conditions in which multiple shade conditions showed weaker responses to R:FR than symptoms are caused by a single underlying problem. did those adapted to open conditions (Morgan & Smith The concept of shade avoidance has been with us for at 1979). least 20 years, although tracing the origin of the term is Ecologists have long been used to the idea that plants avoid shade, and Grime (1979), in his book on vegetation Correspondence: Harry Smith, Department of Botany, University strategies, used the term ‘shade avoidance’ as an index of Leicester, Leicester LE1 7RH, UK. term, although it is difficult to find the term in the text! In

840 © 1997 Blackwell Science Ltd The shade avoidance syndrome 841 the natural environment, aggressive shade-avoiding allow for optimum germination appropriate to environ- species exhibit strong elongation responses in shade, sum- mental conditions. marized by Grime (1979) as follows: ‘in response to shade The most dramatic shade avoidance response, seen both plants produce less dry matter, retain photosynthate in the in natural shade and in low R:FR simulations, is the stimu- shoot at the expense of root growth, develop longer intern- lation of elongation growth. This response may not only be odes and petioles, and produce larger thinner leaves’. The quantitatively large, it can also be remarkably rapid, with adaptive significance of shade avoidance has recently been lag phases of a few minutes in some cases (Child & Smith demonstrated in relation to the adaptive plasticity concept 1987). In simulation experiments, extreme responses can be (Schmitt et al. 1995) and is discussed in detail by Schmitt obtained when the photosynthetically active radiation is (1997). The ecological significance of shade avoidance is maintained at reasonable levels, allowing the provision of reviewed by Ballaré et al. (1997). sufficient resources for shade avoidance to be maximized. When vegetation shade is simulated in growth cabinets In our laboratory, in a 3 week experiment, we have grown in which R:FR is low but PAR sufficient to allow for sus- sunflowers to 1 m tall under low R:FR radiation, when the tained growth, these phenological changes are exagger- controls grown in high R:FR reached only 25 cm! ated. Table 1 shows the main categories of response that Elongation responses to low R:FR are most easily observed are observed in plants growing under simulated shade in internodes, but petioles also show strong responses. In conditions. It can be seen that shade avoidance responses the monocots, elongation of leaves, and of leaf sheathes, is are important throughout the whole life cycle, from ger- stimulated by low R:FR. Tendrils and other organs capable mination to flowering and seed set. Germination under of polar longitudinal growth all show responses to low dense canopies would clearly be disadvantageous for R:FR. Concomitant with stem elongation (in dicots) is often seeds with small reserves; phytochrome-mediated shade a reduction in leaf development, although this can be vari- avoidance responses are evident at this stage with low able. In some species, but not all, leaf area growth is R:FR inhibiting germination and imposing secondary reduced under low R:FR. A more general response is a dormancy. In some cases, notably those of pioneer trees, reduction in leaf thickness, and in some cases a complete germination of seed held dormant in the soil bank breakdown of the characteristic palisade and spongy meso- requires a substantial daily period of high R:FR radia- phyll anatomy is observed (McLaren & Smith 1978). Other tion, such as only occurs in large canopy gaps (Vasquez- aspects of leaf development are also modified during shade Yanes & Smith 1982). Thus, shade avoidance responses avoidance including, commonly, a substantial reduction in chlorophyll production, readily observed by the naked eye. More variable are changes in the ratio of chlorophylls a:b, which is sometimes reduced and sometimes elevated under Table 1. The shade avoidance syndrome shade conditions. Essentially, however, shade avoidance responses result in increased shoot extension at the expense Response to shade of leaf development. This is manifested as a marked Physiological process (i.e. reduced R:FR ratio) strengthening of apical dominance and reduction in branching in dicots, or tillering in grasses (Casal et al. 1986). Germination Retarded Associated with increased apical dominance is a commonly Extension growth Accelerated seen phenomenon in which leaf angle is increased in Internode extension Rapidly increased response to low R:FR; in other words, leaves tend to re-ori- (lag c. 5 min) entate upwards under simulated shade conditions Petiole extension Rapidly increased Leaf extension Increased in cereals (Whitelam & Johnson 1982). A very important component of the shade avoidance Leaf development Retarded syndrome is an acceleration of flowering, seen clearly in Leaf area growth Marginally reduced Arabidopsis (Halliday et al. 1994), but readily observable Leaf thickness Reduced in all shade-avoiding plants. Although the adaptive signifi- Chloroplast development Retarded cance of this response to impending shade has not been Chlorophyll synthesis Reduced adequately investigated, it could reasonably be argued that Chlorophyll a:b ratio Balance changed accelerated flowering and seed production under shade Apical dominance Strengthened increase the probability of the survival of the organism, Branching Inhibited and therefore of the species. Accelerated flowering under Tillering Inhibited (in cereals and grasses) low R:FR is associated with reduced seed set, truncated fruit development and often a severe reduction in the ger- Flowering Accelerated minability of the seed produced. Overall, shade avoidance Rate of flowering Markedly increased involves a marked redirection of assimilates towards elon- Seed set Severe reduction Fruit development Truncated gation and away from structures dedicated to resource acquisition and storage. Assimilate distribution Marked change All of the responses collected together here under the Storage organ deposition Severe reduction shade avoidance syndrome are observable in natural, dense

© 1997 Blackwell Science Ltd, Plant, Cell and Environment, 20, 840Ð844 842 H. Smith and G. C. Whitelam communities, and can be simulated by growing plants during the photoperiod, it is now apparent that many such under low R:FR ratio conditions. Furthermore, by simply responses are detectable in this class of mutants. For exposing plants to horizontal FR radiation with white light instance, the hypocotyls of light-grown cucumber lh from above, similar responses are induced, consistent with seedlings, although already elongated, show a significant the notion that plants anticipate impending shading by additional elongation response to supplementary FR detecting FR reflection signals from neighbouring vegeta- (Whitelam & Smith 1991; Smith et al. 1992). This tion (Morgan & Smith 1981; Child & Smith 1987; Ballaré response is a classical element of the shade avoidance syn- et al. 1987). The question therefore becomes: which phyto- drome. These findings could indicate that the lh mutation is chromes are responsible for sensing FR reflection signals leaky, and so produced some functional phyB, or they and for mediating the shade avoidance syndrome? could indicate that phytochromes other than the phyB-like species that are absent in lh are also able to mediate responses to the R:FR ratio. HOW DID THE ASSUMPTION THAT phyB IS Null alleles of the Arabidopsis phyB mutant also show SOLELY RESPONSIBLE FOR MEDIATING typical shade avoidance responses to supplementary FR SHADE AVOIDANCE RESPONSES ARISE? given during the photoperiod and to EOD FR treatments The long hypocotyl (lh) mutant of cucumber was one of the (e.g. Whitelam & Smith 1991; Goto et al. 1991; Robson et first mutants deficient in phytochrome B (phyB) to be al. 1993; Halliday et al. 1994; Devlin et al. 1996). Both characterized in any detail. Spectrophotometric and daytime reduction in R:FR ratio and EOD FR treatments immunochemical analyses of the phytochrome status of induce an early flowering response in wild-type etiolated and light-grown lh plants provided evidence that, Arabidopsis seedlings. This represents an obvious mani- whilst the mutant possessed wild-type levels of light-labile festation of the shade avoidance syndrome in many plants. phytochrome A (phyA), it showed a deficiency in the light- Although phyB-null mutants are early flowering under stable phytochrome pool; specifically, a polypeptide control conditions, they nevertheless display a clear early- species reactive with a monoclonal antibody raised against flowering response to simulated vegetational shade a recombinant fragment of tobacco PHYB was absent in (Whitelam & Smith 1991; Goto et al. 1991; Halliday et al. extracts of lh seedlings (Adamse et al. 1988; López-Juez 1994; Devlin et al. 1996). Arabidopsis mutants that are et al. 1992). Prior to the demonstration that lh lacks an null for phyB, although already elongated, also show immunochemically detectable PHYB-like protein, it was increased elongation growth responses to both reduced established that seedlings of the lh mutant had aberrant R:FR ratio and EOD FR (Devlin et al. 1996). These obser- responses to light (e.g. Adamse et al. 1987) and that light- vations provide a very clear indication that phyB is not the grown lh seedlings resemble wild-type seedlings showing sole mediator of the shade avoidance syndrome in the shade avoidance syndrome (e.g. López-Juez et al. Arabidopsis. 1990; Ballare et al. 1991). Moreover, it was reported that The phenotype of the Arabidopsis phyB mutant is rather already elongated lh seedlings show no further elongation variable and does not always phenocopy wild-type plant responses to end-of-day (EOD) FR light treatments or to responses to low R:FR ratio. Thus, whereas low R:FR ratio supplementary FR during the photoperiod (e.g. Adamse et always leads to a decrease in leaf area and a decrease in al. 1988; López-Juez et al. 1990; Ballare et al. 1991). From specific stem weight in wild-type seedlings, the phyB these observations it was concluded that lh seedlings were mutant can sometimes constitutively display increased leaf completely devoid of the photoresponses mediated by the area and increased specific stem weight (Robson et al. phytochrome(s) that was active in shade detection. Since lh 1993). Furthermore, since leaf area and specific stem seedlings were subsequently shown to lack a PHYB-like weight of the phyB mutant respond to low R:FR ratio in the polypeptide (López-Juez et al. 1992), it is inferred that same way as in wild type, these shade avoidance responses phyB (alone) mediates responses to vegetational shade in of the phyB mutant are sometimes exaggerated (Robson et cucumber. al. 1993). The analysis of phyB-deficient mutants in other species, Through the analysis of phyA mutants, and phyA phyB most notably the phyB-null mutants of Arabidopsis, con- double mutants, it is apparent that phyA is not necessary for firmed the striking similarity between the phenotypes of display of the shade avoidance syndrome in Arabidopsis such mutants and the phenotypes of wild-type plants dis- (Yanovsky et al. 1995; Devlin et al. 1996; Whitelam & playing the shade avoidance syndrome (e.g. Nagatani et al. Devlin 1997). In fact, at least during seedling establishment, 1991; Somers et al. 1991; Devlin et al. 1992; Reed et al. the action of phyA in plants exposed to low R:FR ratio 1993). This, too, lent support to the notion that phyB medi- antagonizes that of phyB in the control of elongation growth ates responses to vegetational shade. (Yanovsky et al. 1995; Smith et al. 1997). Consequently, phyA mutants display such exaggerated elongation responses to low R:FR ratio that many of them die. This sug- EVIDENCE FROM MUTANT PLANTS THAT gests that a possible role for phyA in de-etiolating seedlings OTHER PHYTOCHROMES ARE INVOLVED is to limit some of the shade avoidance responses. Despite initial suggestions that phyB-deficient mutants Recently, the retained shade avoidance responses of showed no responses to EOD FR or to supplementary FR Arabidopsis phyA phyB double mutants has been exploited

© 1997 Blackwell Science Ltd, Plant, Cell and Environment, 20, 840Ð844 The shade avoidance syndrome 843 in screens to identify new photoreceptor mutants. light: photosensory ecology and agricultural implications. Plant, Significantly, some mutants that show no detectable addi- Cell and Environment 20, 820Ð825. tional responses (flowering time and/or elongation Ballaré C.L., Sánchez R.A., Scopel A.L., Casal J.J. & Ghersa C.M. (1987) Early detection of neighbour plants by phytochrome per- growth) to either supplementary FR during the photope- ception of spectral changes in reflected sunlight. Plant, Cell and riod or to EOD FR have been isolated (P. F. Devlin and Environment 10, 551Ð557. G. C. Whitelam, unpublished results). The analysis of Ballaré C.L., Casal J.J. & Kendrick R.E. (1991) Responses of light- these mutants may provide information about the grown wild-type and long-hypocotyl mutant cucumber seedlings involvement of photoreceptors in the shade avoidance to natural and simulated shade light. Photochemistry and syndrome. Photobiology 54, 819Ð826. Analysis of the tri mutant of tomato (see Kendrick et Casal J.J., Sánchez R.A. & Deregibus V.A. (1986) The effect of al. 1997) provides compelling evidence that phyB is not plant density on tillering: The involvement of R/FR ratio and the proportion of radiation intercepted per plant. Environmental and the sole mediator of the shade avoidance syndrome in all Experimental Botany 26, 365Ð371. plants. This mutant has been shown to be deficient in a Child R. & Smith H. (1987) Phytochrome action in light-grown homologue of phyB (van Tuinen et al. 1995; Kerckhoffs mustard: Kinetics, fluence-rate compensation and ecological sig- et al. 1996). However, unlike many other phyB-deficient nificance. Planta 172, 219Ð229. mutants, light-grown tri seedlings do not obviously Child R., Morgan D.C. & Smith H. (1981) Control of development resemble the shade avoidance syndrome of wild-type in Chenopodium album by shadelight: The effect of light quality plants. Furthermore, tri seedlings show more or less nor- (Red: Far-red ratio) on morphogenesis. New Phytologist 89, 545Ð555. mal responses to both supplementary FR during the pho- Cumming B.G. (1963) The dependence of germination on photope- toperiod and EOD FR (e.g. Kerckhoffs et al. 1992). The riod, light quality, and temperature in Chenopodium spp. observation that phyB is not necessary for the shade Canadian Journal of Botany 41, 1211Ð1233. avoidance syndrome in tomato is consistent with the Devlin P.F., Halliday K.J., Harberd N.P. & Whitelam G.C. (1996) notion that phyB does not play a significant role in these The rosette habit of Arabidopsis thaliana is dependent upon phy- responses. A similar situation exists in Nicotiana tochrome action: novel phytochromes control internode elonga- plumbaginifolia in which two mutants have been isolated tion and flowering time. Plant Journal 10, 1127Ð1134. Devlin P.F., Rood S.B., Somers D.E., Quail P.H. & Whitelam G.C. and characterized that have lesions in a PHYB ortho- (1992) Photophysiology of the elongated internode (ein) mutant logue, and are null for the phyB photoreceptor (M. of Brassica rapa: ein mutant lacks a detectable phytochrome B- Hudson, P. R. H. Robson, Y. Kraepiel, M. Caboche and like polypeptide. Plant Physiology 100, 1442Ð1447. H. Smith, unpublished results). These mutants have nor- Devlin P.F., Somers D.E., Quail P.H. & Whitelam G.C. (1997) The mal responses to low R:FR ratio. However, the possibility ELONGATED INTERNODE (EIN) gene of Brassica rapa that there is redundancy among the phytochromes of encodes phytochrome B. 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