Plant, Cell atid Environment (1997) 20, 840-844

The shade avoidance syndrome: multiple responses mediatedby multiple phytochromes

H. SMITH & G. C. WHITELAM

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

ABSTRACT

In recent years, the concept of shade avoidance has pro-vided a functional meaning to the role of the phytochromephotoreceptor family in mature plants in their naturalenvironment, and the question of which of these phy-tochromes is responsihie for shade avoidance reactionshas inevitably been raised. Unfortunately, a misconceptionhas arisen that phytochrome B is solely responsible fordetecting the environmental signal that initiates the shadeavoidance syndrome. This view is too simplistic, and isbased upon a selective interpretation of the available evi-dence. In this short Commentary, we review the concept ofthe shade avoidance syndrome, show how the misconcep-tion arose, and emphasize the plurality of perception andresponse that is crucial to successful competition for light.Key-words: mutants; phytochromes; shade avoidance.

THE SHADE AVOIDANCE SYNDROME

Whenever plants grow in close proximity, in forests, inherbaceous communities, in grassland swards or inhedgerows, there is competition for light. The resource ofradiant energy in dense plant stands is unrehable andpatchy, and evolution has provided plants with two princi-pal approaches to provide for survival under such environ-mental conditions. Essentially, plants may avoid shade, orthey may tolerate shade. The angiospenns in particularhave evolved impressive capacity to avoid shade, and thismay be one of the factors that have contributed to their suc-cess. Shade avoidance represents one of the most impor-tant competitive strategies that plants possess, and itseffectiveness is undoubtedly a consequence of the multi-plicity of responses that are available to the shaded plant.Responses to shade are many and varied, and it is nowfully accepted that shade avoidance reactions are all initi-ated by a single environmental signal, the reduction in theratio of red (R) to far-red (ER) radiation (i.e. R:ER) thatoccurs within crowded plant communities. We use theterm 'syndrome' to describe the multiple responses to lowR:ER, in analogy to medical conditions in which multiplesymptoms are caused by a single underlying problem.

The concept of shade avoidance has been with us for atleast 20 years, although tracing the origin of the term is

Correspondence: Harry Smith. Department of Botany, Universityof Leicester. Leicester LEI 7RH, UK.

somewhat difficult. In the first half of this century, therewas a great deal of research on the responses of plants toartificial shade, using neutral density screens to simulatethe reduction in irradiance that occurs in natural plantcanopies. That research must now be regarded as essen-tially irrelevant, as the reduction in irradiance under shadeis now known not to be a reliable signal. The earliestreported observations linking phytochromes to shadeavoidance responses are probably those of Cumming(1963), who demonstrated that the germination ofChenopodium ruhrutu seeds was sensitive to R:ER over awide range, and speculated that this behaviour may beimportant in optimizing germination in relation to the pres-ence of vegetation shade. At about the same time, the pio-neers of modern photomorphogenesis, Hendricks &Borthwick (1963), remarked, almost in passing, that over-hanging foliage might modify vegetative developmentthrough effects on stem and leaf growth. Kasperbauer andcolleagues, in a number of publications, noted the impor-tance of ER light filtered through or reflected by vegetationin crop plants, particularly in relation to the orientation ofplanting rows (e.g. Kasperbauer 1971).

The demonstration that shade avoidance reactions arephytochrome-mediated via the perception of the relativeamounts of R and ER radiation came as a result of quantita-tive measurements and simulation experiments carried outin the 1970s. Eirst, natural radiation spectra were analysedand summarized in terms of R:ER ratio (Holmes & Smith1975, \911). These natural variations were then related toestimated Pfr/P, the phytochrome photoequilibrium, therelationship being a rectangular hyperbola (Smith &Holmes 1977). By simulating shade avoidance extensiongrowth responses using artificial light sources which pro-vided uniform photosynthetically active radiation (PAR)but which varied in R:ER, the role of phytochrome-per-ceived variations in light quality was then firmly estab-lished (Morgan & Smith 1976, 1978, 1981). The range ofresponses to reduced R:ER ratio correlated identically withthe observed growth responses of plants to shade in the nat-ural environment, and indeed plants naturally adapted toshade conditions showed weaker responses to R:ER thandid those adapted to open conditions (Morgan & Smith1979).

Ecologists have long been used to the idea that plantsavoid shade, and Grime (1979), in his book on vegetationstrategies, used the term 'shade avoidance' as an indexterm, although it is difficult to find the term in the text! In

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The shade avoidatice syndrotrie 841

the natural environment, aggressive shade-avoidingspecies exhibit strong elongation responses in shade, sum-marized by Grime (1979) as follows: 'in response to shadeplants produce less dry matter, retain photosynthate in theshoot at the expense of root growth, develop longer intern-odes and petioles, and produce larger thinner leaves'. Theadaptive significance of shade avoidance has recently beendemonstrated in relation to the adaptive plasticity concept(Schmitt et ciL 1995) and is discussed in detail by Schmitt(1997). The ecological significance of shade avoidance isreviewed by Ballare et al. (1997).

When vegetation shade is simulated in growth cabinetsin which R:ER is low but PAR sufficient to allow for sus-tained growth, these phenological changes are exagger-ated. Table 1 shows the main categories of response thatare observed in plants growing under simulated shadeconditions. It can be seen that shade avoidance responsesare important throughout the whole liie cycle, from ger-mination to flowering and seed set. Germination underdense canopies would clearly be disadvantageous ibrseeds with small reserves; phytochrome-mediated shadeavoidance responses are evident at this stage with lowR:ER inhibiting germination and imposing secondarydormancy. In some cases, notably those of pioneer trees,germination of seed held dormant in the soil bankrequires a substantial daily period of high R:ER radia-tion, such as only occurs in large canopy gaps (Vasquez-Yanes & Smith 1982). Thus, shade avoidance responses

Table 1. The sliadc avoidance syndi\)nie

Physiological processResponse to shade(i.e. reduced R:FR ralio)

Gerinination

Extension growthIntemode exleiision

Pcliolc exicnsionLeaf extension

Leal" developmentLeaf area growthLeaf thickness

Chloroplast developmentChlorophyll synthesisChlorophyll cr.h ratio

Apical dominanceBranchingTillering

(in cereals and grasses)

FloweringRate of (loweringSeed setFruit development

Assimilate distributionStorage organ deposilion

Retarded

AcceleratedRapidly increased(lag c. 5 min)

Rapidly increasedIncreased in cereals

RetardedMarginally reducedReduced

RetardedReducedBalance changed

StrengthenedInhibitedInhibited

AcceleratedMarkedly increasedSevere reductionTruncaled

Marked changeSevere reduction

allow for optimum germination appropriate to environ-mental conditions.

The most dramatic shade avoidance response, seen bothin natural shade and in low R:ER simulations, is the stimu-lation of elongation growth. This response may not only bequantitatively large, it can also be remaikably rapid, withlag phases of a few minutes in some cases (Child & Smith1987). In simulation experiments, extreme responses can beobtained when the photosynthetically active radiation ismaintained at reasonable levels, allowing the provision ofsufficient resources for shade avoidance to be maximized.In ouv laboratory, in a 3 week experiment, we have grownsunflowers to 1 m tall under low R:ER radiation, when thecontrols grown in high R:ER reached only 25 cm!Elongation responses to low R:ER are most easily observedin internodes, but petioles also show strong responses. Inthe monocots, elongation of leaves, and of leaf sheathes, isstimulated by low R:ER. Tendrils and other organs capableof polar longitudinal growth all show responses to lowR:ER. Concomitant with stem elongation (in dicots) is oftena reduction in leaf development, although this can be vari-able. In some species, but not all, leaf area growth isreduced under low R:ER. A more general response is areduction in leaf thickness, and in some cases a completebreakdown of the characteristic palisade and spongy meso-phyll anatomy is observed (McLaren & Smith 1978). Otheraspects of leaf development are also modified during shadeavoidance including, commonly, a substantial reduction inchlorophyll production, readily observed by the naked eye.More \ariahlc are changes in the ratio of chlorophylls ci:b,which is sometimes teduced and sotnetimes elevated undershade conditions. Essentially, however, shade avoidanceresponses result in increased shoot extension at the expenseof leaf development. This is maniiested as a markedstrengthening of apical dominance and reduction in branch-ing in dicots, or tillering in grasses (Casal ct al. 1986).Associated with increased apical dominance is a commonlyseen phenomenon in which leaf angle is increased inrespotise to low R:ER; in other words, leaves tend to re-ori-entate upwards under simulated shade conditions(Whitelam & Johnson 1982).

A very important component of the shade avoidancesyndrome is an acceleration of flowering, seen clearly inArabidopsis (Halliday et al. 1994), but readily obscr\ablein all shade-avoiding plants. Although the adaptive signifi-cance of this response to impending shade has not beenadequately investigated, it could reasonably be argued thataccelerated flowering and seed production under shadeincrease the probability of the survival of the organism,and therefore of the species. Accelerated flowering underlow R:ER is associated with reduced seed set, truncatedfruit development and otten a sevete teductit>n in the ger-minability of the seed produced. Overall, shade axoidanceinvolves a marked redirection of assimilates towards CUMI-galion and away from structtircs dedicated to resourceacquisition and storage.

All of the responses collected together here tinder theshade avoidance syndrome are observable in natural, dense

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842 H. Stvith and G. C. Whitelam

communities, and can be simulated by growing plantsunder low R:ER ratio conditions. Eurthermore, by simplyexposing plants to horizontal ER radiation with white lightfrom above, similar responses are induced, consistent withthe notion that plants anticipate impending shading bydetecting ER reflection signals from neighbouring vegeta-tion (Morgan & Smith 1981; Child & Smith 1987; Ballareetal. 1987). The question therefore becomes: which phyto-chromes are responsible for sensing ER reflection signalsand for mediating the shade avoidance syndrome?

HOW DID THE ASSUMPTION THAT phyB ISSOLELY RESPONSIBLE FOR MEDIATINGSHADE AVOIDANCE RESPONSES ARISE?

The long hypocotyl {IK) mutant of cucumber was one of thefirst mutants deficient in phytochrome B (phyB) to becharacterized in any detail. Spectrophotometric andimmunochemical analyses of the phytochrome status ofetiolated and light-grown Ih plants provided evidence that,whilst the mutant possessed wild-type levels of light-labilephytochrome A (phy A), it showed a deficiency in the light-stable phytochrome pool; specifically, a polypeptidespecies reactive with a monoclonal antibody raised againsta recombinant fragment of tobacco PHYB was absent inextracts of Ih seedlings (Adamse et al. 1988; Lopez-Juezet al. 1992). Prior to the demonstration that Ih laeks animmunochemically detectable PHYB-like protein, it wasestablished that seedlings of the Ih mutant had aberrantresponses to light (e.g. Adamse et al. 1987) and that light-grown Ih seedlings resemble wild-type seedlings showingthe shade avoidance syndrome (e.g. Lopez-Juez et al.1990; Ballare et al. 1991). Moreover, it was reported thatalready elongated Ih seedlings show no further elongationresponses to end-of-day (EOD) ER light treatments or tosupplementary FR during the photoperiod (e.g. Adamse etal. 1988; Lopez-Juez e/fl/. 1990; Ballare e/a/. 1991). Eromthese observations it was concluded that Ih seedlings werecompletely devoid of the photoresponses mediated by thephytochrome(s) that was active in shade detection. Since Ihseedlings were subsequently shown to lack a PHYB-likepolypeptide (Lopez-Juez et al. 1992), it is inferred thatphyB (alone) mediates responses to vegetational shade incucumber.

The analysis of phyB-deficient mutants in other species,most notably the phyB-null mutants of Arabidopsis, con-firmed the striking similarity between the phenotypes ofsuch mutants and the phenotypes of wild-type plants dis-playing the shade avoidance syndrome (e.g. Nagatani etal.1991; Somers et al. 1991; Devlin et al. 1992; Reed et al.1993). This, too, lent support to the notion that phyB medi-ates responses to vegetational shade.

EVIDENCE FROM MUTANT PLANTS THATOTHER PHYTOCHROMES ARE INVOLVED

Despite initial suggestions that phyB-deficient mutantsshowed no responses to EOD ER or to supplementary ER

during the photoperiod, it is now apparent that many suchresponses are detectable in this class of mutants. Eorinstance, the hypocotyls of light-grown cucumber Ihseedlings, although already elongated, show a significantadditional elongation response to supplementary ER(Whitelarn & Smith 1991; Smith et al. 1992). Thisresponse is a classical element of the shade avoidance syn-drome. These flndings could indicate that the Ih tnutation isleaky, and so produced some functional phyB, or theycould indicate that phytochromes other than the phyB-likespecies that are absent in Ih are also able to mediateresponses to the R:ER ratio.

Null alleles of the Arabidopsis phyB mutant also showtypical shade avoidance responses to supplementary ERgiven during the photoperiod and to EOD ER treatments(e.g. Whitelam & Smith 1991; Goto et al. 1991; Robson etal. 1993; Halliday et al. 1994; Devlin et al. 1996). Bothdaytime reduction in R:ER ratio and EOD ER treatmentsinduce an early flowering response in wild-typeArabidopsis seedlings. This represents an obvious mani-festation of the shade avoidance syndrome in many plants.Although phyB-null mutants are early flowering undercontrol conditions, they nevertheless display a clear early-flowering response to simulated vegetational shade(Whitelam & Smith 1991; Goto era/. 1991; Halliday era/.1994; Devlin et al 1996). Arabidopsis mutants that arenull for phyB, although already elongated, also showincreased elongation growth responses to both reducedR:ER ratio and EOD ER (Devlin et al. 1996). These obser-vations provide a very clear indication that phyB is not thesole mediator of the shade avoidance syndrome inArabidopsis.

The phenotype of the Arabidopsis phyB mutant is rathervariable and does not always phenocopy wild-type plantresponses to low R:ER ratio. Thus, whereas low R:ER ratioalways leads to a decrease in leaf area and a decrease inspecific stem weight in wild-type seedlings, the phyBmutant can sometimes constitutively display increased leafarea and increased specific stem weight (Robson et al.1993). Eurthermore, since leaf area and specific stemweight of the phyB mutant respond to low R:ER ratio in thesame way as in wild type, these shade avoidance responsesof the phyB mutant are sometimes exaggerated (Robson etal. 1993).

Through the analysis of phyA mutants, and phyA phyBdouble mutants, it is apparent that phyA is not necessary fordisplay of the shade avoidance syndrome in Arabidopsis(Yanovsky et al. 1995; Devlin et al. 1996; Whitelam &Devlin 1997). In fact, at least during seedling establishment,the action of phyA in plants exposed to low R:ER ratioantagonizes that of phyB in the control of elongation growth(Yanovsky et al. 1995; Smith et al. 1997). Consequently,phyA mutants display such exaggerated elongationresponses to low R.ER ratio that many of them die. This sug-gests that a possible role for phyA in de-etiolating seedlingsis to limit some of the shade avoidance responses.

Recently, the retained shade avoidance responses ofArabidopsis/?/z>;A phyB double mutants has been exploited

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The shade avoidance syndrome 843

in screens to identify new photoreceptor mutants.Significantly, some mutants that show no detectable addi-tional responses (flowering time and/or elongationgrowth) to either supplementary ER during the photope-riod or to EOD ER have been isolated (P. E. Devlin andG. C. Whitelam, unpublished results). The analysis ofthese mutants may provide information about theinvolvement of photoreceptors in the shade avoidancesyndrome.

Analysis of the t/i mutant of tomato (see Kendrick etal. 1997) provides compelling evidence that phyB is notthe sole mediator of the shade avoidance syndrome in allplants. This mutant has been shown to be deficient in ahomologue of phyB (van Tuinen et al. 1995; Kerckhoffset al. 1996). However, unlike many other phyB-deficientmutants, light-grown tri seedlings do not obviouslyresemble the shade avoidance syndrome of wild-typeplants. Eurthermore, tri seedlings show more or less nor-mal responses to both supplementary ER during the pho-toperiod and EOD ER (e.g. Kerckhoffs et al. 1992). Theobservation that phyB is not necessary for the shadeavoidance syndrotne in tomato is consistent with thenotion that phyB does not play a signiflcant role in theseresponses. A similar situation exists in Nicotianaplumbaginifolia in which two mutants have been isolatedand characterized that have lesions in a PHYB ortho-logue, and are null for the phyB photoreceptor (M.Hudson, P. R. H. Robson, Y. Kraepiel, M. Caboche andH. Smith, unpublished results). These mutants have nor-mal responses to low R:ER ratio. However, the possibilitythat there is redundancy among the phytochromes oftomato and N. plumhaginifolia with respect to the shadeavoidance syndrome cannot be dismissed.

CONCLUSIONS

Despite initial attempts to ascribe the shade avoidance syn-drome to the action of a single member of the phytochromefamily, it is now clear that multiple phytochromes areinvolved. This is perhaps not suiprising given the com-plexity and importance of these responses. Eurthermore, itseems likely that the contributions of different members ofthe phytochrome family to the shade avoidance syndrome,and the degree of redundancy among the phytochromes,will be different in different plant species. Thus, conclu-sions drawn from the analysis of one plant species cannotbe universally applied.

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© 1997 Blackwell Science Ltd, Plant, Cell and Environtnent, 20, 840-844