Plant plant signalling, the shade-avoidance response and competition

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1 Journal of Experimental Botany, Vol. 50, No. 340, pp , November 1999 Plant plant signalling, the shade-avoidance response and competition Pedro J. Aphalo1,3, Carlos L. Ballaré2 and Ana L. Scopel2 1 Joensuu Research Station, Finnish Forest Research Institute, FIN Joensuu, Finland 2 IFEVA (Agricultural Plant Physiology and Ecology Research Institute), University of Buenos Aires and CONICET, 1417 Buenos Aires, Argentina Received 1 September 1998; Accepted 30 June 1999 Abstract Key words: Competition, informational signals, photomorphogenesis, phytochrome, shade avoidance. Plastic responses Plasticity is essential for plant survival, and indeed for the survival of any organism (see Table 1 for a definition of terms). Plastic responses are expressed over a variety of time scales, from the rapid movements of antenna proteins and pigments between PSII and PSI during short-term acclimation to fluctuations in light intensity, to the changes in crown shape or root architecture that may take years to develop. Plastic responses, which essentially depend on changes in gene expression and protein function, are continuously implemented in the plant and serve a number of functions, including the maintenance of metabolic homeostasis, foraging for resources, and defence. In most cases plastic responses involve metabolic as well as morphological and developmental components. Table 1. Definitions Plant plant signalling Plasticity Shade avoidance Competition Plants generate and perceive informational signals. An interaction (between plants) is considered to be informational when it involves the exchange of an insignificant amount of matter or energy, in quantitat- ive terms, but in spite of this has a profound effect on plants by modulating their developmental programme. This article discusses how plants use light signals to detect neighbouring plants and outlines the implica- tions of shade-avoidance responses for the development of size and fitness hierarchies in canopies. The role of shade avoidance as a stabilizing force in mono- specific canopies is noted. This is the flow of information between individuals. An interaction is considered to be informational when it involves the exchange of an insignificant amount of matter or energy, in quantitative terms, but in spite of this has a profound effect on plants by modulating their developmental programme. Phenotypic plasticity is the expression of variability among individuals of identical genotype. Throughout the life of an individual plant, plastic responses are triggered by a variety of input signals and are constrained by the possible combinations of protein synthesis and action specified in the plant s genotype. This is the response of plants to shade by increasing the elongation of vertical stems and petioles which results in leaf blades located higher in the canopy profile. This is the negative effects which one organism has upon another by consuming, or controlling access to a resource that is limited in availability (Keddy, 1989). Although it is not uncommon in ecology textbooks to describe plant responses to environmental stresses as inevitable consequences of limitations or imbalances in the resources available to the plant, it is seldom pointed out that these responses (1) are based on finely-tuned and co-ordinated information transduction cascades, (2) do not necessarily represent the only possible solution to the resource conflicts presented by the environment, and (3) sometimes they even anticipate changes in resource availability (see Aphalo and Ballaré. 1995; Ballaré, 1999, and references therein). Plastic responses are triggered by a variety of signals, including things that are frequently 3 To whom correspondence should be addressed: Faculty of Forestry, University of Joensuu, PO Box 111, FIN-80110, Joensuu, Finland. Fax: pedro.aphalo@joensuu.fi Oxford University Press 1999

2 1630 Aphalo et al. considered only in terms of their energetic value or deleterious effects. Thus, signals that engage specific response programmes include: (1) specific external clues (such as changes in the red:far-red ratio, biotic elicitors, etc), (2) variations in the amount of resources available to the plant (e.g. incident PPFD, hexose level in a particular tissue, etc.), and ( 3) products of cellular damage (e.g. DNA lesions, free radicals, etc). Any molecular mechanism that is capable of extracting information from 1, 2, and 3, and transforming that information into a potentially useful plastic response is bound to be under continuous selective pressure. Frequently, the functional details of the mechanisms that allow plants to sense and react plastically to changes in their environment tend to be ignored or overlooked in descriptions of plant responses to competition or to abiotic stresses. There are limitations associated with the use of very simple models of plant function. For example, it is clear that competition models that are simply based on resource consumption cannot account for plastic, active morphological responses of the plants, which in many environments are critical for the outcome of competition. In the next section the role of informational signals in shaping competitive interactions among plants is discussed. Detection of neighbouring plants At low densities the height of the stem increased with density, but above 500 seedlings per square metre density had little effect on height ( Fig. 1). The spread of height values differed very little among densities. Density had Incident light is partly reflected, partly absorbed and partly transmitted by plant leaves (Campbell and Norman, 1998). The proportion of light reflected, absorbed and transmitted depends on the wavelength and, particularly important for this discussion, is the high absorptance of red light and the high reflectance and transmittance of far-red light. This property of leaves makes them behave both as coloured mirrors and coloured filters. Phytochromes are photoreceptors that mediate many responses to shading by vegetation by sensing changes in the red to far-red photon ratio (R5FR) (Smith, 1994, 1995; Smith and Whitelam, 1997, and references Fig. 1. Effect of canopy density on growth. (a) Height, (b) dry mass therein). Phytochromes can also elicit responses to shadarranged in a Nelder design. For each density a box plot indicates: 5%, (shoot+roots) of silver birch seedlings grown in equal volume containers ing by detecting changes in total irradiance (Balleré et al., 25%, 50% (median), 75%, and 95% quantiles, and outliers (*, #). Each 1991; Casal et al., 1997). box plot was calculated from measurements on 28 individual seedlings. Experimental design: seeds of Central Finland origin were sown in Responses to growth density trays and the seedlings transplanted, when they had one or two true leaves visible, into Ray-Leach containers (165 cm3, SC-10 super cell, The association between light quality in the canopy and Stuewe & Sons, Corvallis, Oregon) filled with fertilized peat. The pots were immediately (4 June) placed in custom-built trays with holes for plasticity of plant height and mass can be illustrated the pots following a Nelder pattern with 11 rays 6 39 apart, and 12 by reference to a recent experiment. Nelder cartwheel arcs at distances from the centre of the wheel from 39.3 cm to plots (Nelder, 1962) have been used frequently to study cm. Each tray was an approximately 73 wide section of a circle. Four replicate trays were used. Data from the two outermost border responses of plants to population density. They are usu- rows of seedlings on all sides were discarded because of edge-effects. ally laid out in the field or forest, with plants interacting The seedlings were located in a non-heated and well ventilated both above- and below-ground. However, in this Nelder greenhouse at Suonenjoki, Finland (62 39 N, E). The seedlings experiment with Betula pendula, pots were used to restrict density effects to those occurring above-ground. grew undisturbed for one growing season, and were harvested in the autumn after leaves had dropped (PJ Aphalo and R Rikala, unpublished data).

3 Shade avoidance and competition 1631 little effect on seedling total dry mass (shoot plus roots). The spread of dry mass values was notably larger for the highest density. At low densities, root mass ratio, that is the proportion of the total plant dry mass located in the roots, decreased from 0.51 to 0.33 as a function of increasing density. Above 500 seedlings per square metre density had little effect on allocation, with no further decrease in root mass ratio (data not shown). To show better how variability amongst individuals was affected by density, the coefficient of variability (standard deviation divided by the mean) is used. The variability in the dry mass of the seedlings greatly increased with density, while variability in height slightly decreased ( Fig. 2). This shows that there is a stabilizing force that greatly reduces the impact on height of the differences in seedling size measured as biomass. As a consequence of this stabilizing force, even at high density very few individuals were suppressed by competition. Photon irradiance of red and far-red light was measured with a cylindrical light collector which sees only light propagating horizontally. These data were measured early in the growing season. At low densities the main effect was an increase in far-red irradiance caused by reflection, while at higher densities the predominant effect was the decrease in red irradiance caused by absorption ( Fig. 3). The R5FR calculated from these data decreased steadily with density, even at very low densities, with an almost linear slope on the logarithm of density. Fig. 3. Effect of canopy density on red and far-red horizontal irradiance. Similar changes in R5FR with density have been shown (a) Photon irradiance of red and far-red light, (b) red to far-red photon ratio. Photon irradiance was measured near noon, under a clear sky, in canopies of Datura ferox and Sinapis alba seedlings with a red5far-red sensor (SKR-110, Skye Instruments Ltd., Llandrindod Wells, UK) with a cylindrical light collector (Ballaré et al., 1987) located at 2/3 of stem height. One plant was temporarily removed from a canopy of young silver birch seedlings grown in equal volume containers arranged in a Nelder design, and replaced with the sensor. Each point is the mean of four measurements, on rays located 90 apart, one in each of four trays. Measurement was done when the seedlings were approximately mm tall, depending on the density, and had a leaf area of approximately 15 cm2 each, giving a leaf area index (LAI) of 1.3 at the highest canopy density (PJ Aphalo and R Rikala, unpublished results). See legend to Fig. 1 for experimental details. (Ballaré et al., 1991). It has also been shown that the R5FR of the radiation propagating horizontally changes with depth in an artificial canopy of poplar saplings (Gilbert et al., 1995). Ritchie obtained further evidence of changes in horizontal R5FR with density, and its correlation with apparent effects of density on growth and morphology of trees ( Ritchie, 1997). Fig. 2. Effect of canopy density on size inequalities. Coefficient of variation (a) height, (b) dry mass (shoot+roots) of silver birch seedlings grown in equal volume containers arranged in a Nelder design. Seedlings were measured at the end of their first growing season, after leaves had dropped. Points are means of four independent estimates of coefficient of variability (CV ) calculated from seven seedlings from each of four replicate Nelder plots (PJ Aphalo and R Rikala, unpublished results). See legend to Fig. 1 for experimental details. Theroleofphytochromesassensorsofdensity In the previous section, data were presented showing that R5FR is correlated with plant density and depth in the canopy. It has been shown that plants can sense reflected far-red light received at their growing internodes (Ballaré et al., 1987, 1990). However, the questions remained as

4 1632 Aphalo et al. to which phytochromes are responsible for sensing the functional phytochrome A ( phya), and a blue light R5FR changes in horizontally propagated radiation and phororeceptor mutant (cry1) were used (Ballaré and how important are these phytochrome-mediated Scopel, 1997). In this experiment canopy biomass per responses in driving the plastic adjustments of plants in unit ground area was fairly independent of density for all growing canopies. More recent experiments with trans- genotypes except phyb. For this mutant, which does not genic tobacco and photomorphogenic mutants of respond in a normal way to far-red light, canopy biomass Arabidopsis not only shed some light on these questions, decreased with increasing density, even though the constitutive but also reveal the importance of photomorphogenic phenotype of this mutant was similar to that of plasticity per se on stand performance. shade acclimated plants of the wild type. The results for In an experiment with Nicotiana tabacum plants grown the production of fruits per unit ground area were very at different densities, a homozygous line of transgenic similar to those for canopy biomass: production of fruits tobacco was used that over-expresses an oat PHYA cdna decreased with increasing density in phyb, while it and a wild-type isogenic line (Ballaré et al., 1994). The remained constant in the other genotypes. Figure 5 shows height of the wild type increased with density and in the dependency on density of the coefficient of variation response to far-red light whereas that of the transgenic for the number of fruits per plant. Again, only phyb was line did not. The relationship between size inequality significantly different from the wild type: as density among individuals and density, was also altered in the increased variability increased more steeply in the mutant. PHYA over-expressor. At high densities, inequality measured as the coefficient of variability of shoot dry mass (Fig. 4) was clearly much smaller in the wild type than Population-level implications of shade avoidance in the transgenic line. Furthermore, at the highest density, The results from these two experiments using mutant and the mean dry mass ratio between the largest and smallest transgenic plants are puzzling at first sight: neither popula- plant in each experimental unit was 5 for the wild type tions deficient in phytochrome (plants always similar to and 27 for the PHYA over-expressing transgenic line: the individuals growing at very high density), nor those over- stabilizing process that moderates size structuring was expressing phytochrome (plants always similar to individuals not active in the transgenic line, which does not respond growing at low density) perform well at high in a normal way to far-red light. density. What is it that is common to these two contrasting In another experiment recently with Arabidopsis thaliana, genotypes: they both have reduced plasticity, in neither a wild-type line ( WT), a mutant which lacks func- of them height growth responds in a normal way to the tional phytochrome B ( phyb), a mutant which lacks Fig. 5. Effect of increasing canopy density on variability ofreproductive Fig. 4. Effect of increasing canopy density on size inequalities among output among neighbours in monocultures of Arabidopsis plants. The neighbours in monocultures of tobacco plants. Average coefficient of solid line is the coefficient of variability (CV ) versus density relationship variability (CV ) of above-ground dry mass per plant for each density for the wild type. The dashed lines show the same relationship for the treatment. Density expressed through leaf area index (LAI). Bars mutants. Means of three replicate trays, each with an area of 3.36 indicate 1 SE, means of five replicates (redrawn from Ballaré et al., 1994) m2 (redrawn from Ballaré and Scopel, 1997).

5 Shade avoidance and competition 1633 proximity of neighbours. Because of this, canopies of information obtained both from signals internal and either of these constitutive or non-plastic genotypes external to the individual plants. These decisions underlie have a reduced ability to stabilize size inequalities. many plant responses to environmental signals, of biotic If the shorter individuals grow taller (proportionally to and abiotic origin, including shade avoidance. their dry mass) when shaded, their share of the light When moving the viewpoint from the individual plant (energy) resource improves and, consequently, the intensity to the mono-specific stand, new emergent properties of of asymmetrical competition for light decreases. By the system appear, and the apparent ecological function reducing differences in height among individuals, shadeavoidance of shade avoidance as traditionally described (Casal and indirectly reduces the variation in growth rate Smith, 1989; Schmitt, 1997) needs to be expanded: in and size (measured as dry mass) and reproductive output. addition to its important role in the competition for light Reducing size inequalities can improve canopy per- between individuals, shade-avoidance responses may play formance because individuals which die before reproduction, a less frequently recognized, but nevertheless central role or produce a meagre yield of propagules, have in shaping the structure and evolution of plant captured resources (mineral nutrients, water and light) populations. early in the season making them unavailable to the successful individuals which later out-competed them. In this way with large size inequalities among individuals Acknowledgements the pool of resources available for reproduction and We wish to thank Dr Geoff R Squire, Dr Bruce Marshall and growth would be partly wasted decreasing the efficiency Dr LD Incoll for organizing the session at the Society of of their use by the canopy as a whole, as apparently was Experimental Biology 1998 Annual Meeting and inviting PJA the case for phyb in the experiment with Arabidopsis to participate. mutants described in the previous section. In summary, therefore: References (1) Higher canopy-level productivity is associated with Aphalo PJ, Ballaré CL On the importance of informationreduced size inequality among neighbours. acquiring systems in plant plant interactions. Functional Ecology 9, (2) Apparently, for high population-level reproductive Ballaré CL Keeping up with the neighbours: phytochrome output at high densities (yield in cultivated stands) it is sensing and other signalling mechanisms. Trends in Plant not as important that the population is composed of Science 4, individuals with the right phenotype for shade conditions Ballaré CL, Sánchez RA, Scopel AL, Casal JJ, Ghersa CM. as it is that the population is composed of individuals Early detection of neighbour plants by phytochrome perception of spectral changes in reflected sunlight. Plant, able dynamically to adjust their phenotype as the canopy Cell and Environment 10, develops. Ballaré CL, Scopel AL Phytochrome signalling in plant canopies testing its population-level implications with (3) Shade avoidance by shorter individuals decreases photoreceptor mutants of Arabidopsis. Functional Ecology the relative competitive advantage of the taller ones. 11, Ballaré CL, Scopel AL, Sánchez RA Far-red radiation (4) Shade avoidance by shorter individuals tends to reflected from adjacent leaves: an early signal of competition stabilize the size structure of a canopy (i.e. decreases in plant canopies. Science 247, variation in height, dry mass and reproductive output Ballaré CL, Scopel AL, Sánchez RA Photocontrol of among individuals). stem elongation in plant neighbourhoods: effects of photon fluence rate under natural conditions of radiation. Plant, Cell (5) Phytochrome plays a very important role, but other and Environment 14, factors such as light other than red and far-red, wind, Ballaré CL, Scopel AL, Jordan ET, Vierstra RD Signalling among neighboring plants and the development of size temperature, and transpiration demand may be also inequalities in plant populations. Proceedings of the National important in stabilizing plant size inequalities in the field. Academy of Sciences, USA 91, Campbell GS, Norman JM An introduction to environmental Conclusions biophysics, 2nd edn. New York: Springer. Casal JJ, Sánchez RA, Yanovsky MJ The function of Plants of course do not make decisions in the way humans phytochrome A. Plant, Cell and Environment 20, Casal JJ, Smith H The function, action, and adaptive do, as they do not have neural information-processing significance of phytochrome in light-grown plants. Plant, Cell systems. Yet, they are certainly capable of actively chan- and Environment 12, ging their metabolic rates and developmental programmes Gilbert IR, Seavers GP, Jarvis PG, Smith H Photomorphogenesis and canopy dynamics phytochromein response to a variety of input signals and, therefore, mediated proximity perception accounts for the growth they are able to make decisions, at the very least in the dynamics of canopies of Populus trichocarpa deltoides way computers do. These decisions are made based on Beaupre. Plant, Cell and Environment 18,

6 1634 Aphalo et al. Keddy PA Competition. London: Chapman and Hall. the phytochrome family. In: Kendrick RE, Kronenberg Nelder JA New kinds of systematic designs for spacing GHM, eds. Photomorphogenesis in plants, 2nd edn. Dordrecht: experiments. Biometrics 18, Kluwer Academic Publishers, Ritchie GA Evidence for red:far-red signaling and Smith H Physiological and ecological function within the photomorphogenic growth response in Douglas-fir (Pseudo- phytochrome family. Annual Review of Plant Physiology and tsuga menziesii) seedlings. Tree Physiology 17, Plant Molecular Biology 46, Schmitt J Is photomorphogenic shade avoidance adapt- Smith H, Whitelam GC The shade avoidance syndrome ive perspectives from population biology. Plant, Cell and multiple responses mediated by multiple phytochromes. Plant, Environment 20, Cell and Environment 20, Smith H Sensing the light environment: the functions of

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