Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence

In many ecological scenarios, the success of an individual plant is defined by the behavioural decisions that it makes when confronted with the risks of competition with other plants, and biomass losses to insect herbivores. These decisions involve expression of shade avoidance responses and induced chemical defences. Because these responses are costly, they frequently engender resource allocation dilemmas. In this review, I discuss the mechanisms that trigger adaptive responses to competitors and herbivores, highlighting the role of phytochromes as central organizers of the overall resource allocation strategy of plants. Phytochromes sense the reduction in the red to far-red (R : FR) ratio of sunlight caused by the proximity of other plants. Shade-intolerant plants respond to low R : FR ratios with shade avoidance behaviours and reduced investment in defence. Pfr depletion leads to increased stability of growth-promoting phytochrome-interacting factors (PIFs), and results in the production of auxins and gibberellins, degradation of DELLA proteins, which are repressors of PIFs, and reduced sensitivity to jasmonates. Thus, phytochrome appears to fulfil its organizational role by regulating the relative strength of the signalling circuits controlled by growth-related and defence-related hormones. I point out cases of signalling redundancy and discuss the significance of recent work on hormone signalling for our understanding of the mechanisms that control adaptive plant behaviour.     

Differential genetic variation in adaptive strategies to a common environmental signal in Arabidopsis accessions: phytochrome-mediated shade avoidance

Shade avoidance is a syndrome of plastic responses to light signals encountered in crowded plant communities and is a crucial component of competitive strategy in higher plants. The responses are mediated via signal perception by specific members of the phytochrome family of photoreceptors, which detect the relative proportions of red (R) and far‐red (FR) radiation within dense communities. We analysed two aspects of shade avoidance, the acceleration of flowering and the enhancement of elongation growth, displayed by more than 100 accessions of Arabidopsis thaliana (Heyn.) in response to FR‐proximity signals. Both traits showed wide variation between accessions, which was unrelated to the latitude of the location of original collection. Flowering acceleration is a major feature of shade avoidance in rosette plants such as Arabidopsis, and most accessions showed dramatic responses, but several were identified as being recalcitrant to the proximity signal. These accessions are likely to be informative in the analysis of quantitative variation in shade avoidance. Hypocotyl elongation, treated here as an indicator of elongation growth responses, also varied widely amongst accessions. The variations in flowering acceleration and elongation were not correlated, indicating that microevolution in the downstream pathways from signal perception has occurred separately.     

Contrasting shade avoidance responses in two perennial grasses: a field investigation in simulated sparse and dense canopies

We designed an experiment with potted plants grown outdoors to investigate the expression of shade avoidance in simulated sparse and dense canopies by two perennial grasses known to express contrasting responses to low red:far-red ratios (R:FR). Plants were grown in canopy microenvironments designed to lower the R:FR by reflection of horizontally propagated FR from neighbors and by direct attenuation of R by filters located above plants. Two specific hypotheses were tested: (1) Paspalum dilatatum will express greater shade avoidance than Schizachyrium scoparium to low R:FR in both sparse and dense canopies, and (2) low R:FR will produce greater expressions of shade avoidance in sparse than in dense canopies in both species. P. dilatatum was more responsive to low R:FR than S. scoparium in both the sparse and dense canopies and lower ramet number plant^–1 was the only common shade avoidance response between species in sparse canopies. P. dilatatum also showed significant reductions in juvenile ramet initiation, juvenile ramet mass, total shoot mass, and shoot:root ratios in sparse canopies, but only juvenile ramet initiation was reduced in dense canopies. The suppression of juvenile ramet initiation in the dense canopy was at least partially modulated by the vertically propagated R:FR because a similar reduction in PFD and horizontally propagated R:FR showed 42% greater juvenile ramet initiation in the respective control. S. scoparium only showed a significant reduction in ramet number plant^–1 and a significant increase in blade length in sparse canopies, but no significant responses occurred in dense canopies. Consequently, neither hypothesis was rejected. Variable shade avoidance responses between species and canopy densities indicate that both interspecific variation and various proportions of vertically and horizontally propagated low R:FR can influence the expression of shade avoidance responses of perennial grasses in field settings.     

Photomorphogenesis and canopy dynamics. Phytochrome-mediated proximity perception accounts for the growth dynamics of canopies of Populus trichocarpa × deltoides'Beaupré'

The phytochrome family of signal-transducing photoreceptors provides plants with the capacity to perceive variations in the relative fluxes of red (R) and far-red (FR) radiation. This capacity has been proposed to be of ecological value in the perception of the proximity of neighbouring plants and the consequent induction of shade avoidance responses. The work reported here has evaluated this potential by determining quantitatively the effect of neighbour proximity on the growth of canopies of Populus trichocarpa×deltoides‘Beaupré’ trees, and relating the measured variables to the long-term vectoral radiation quality inside each canopy. The spectral distribution of radiation inside four canopies of Populus trichocarpa×deltoides‘Beaupre’ of different densities was monitored throughout the growing season. Spectral distributions inside the canopies were measured in 10° wedges at different heights and angles. The results are presented as PFD over 400–700 nm (PFD400–700) and PFD over 400–800 nm (PFD400–700). Results are also presented for the calculated phytochrome photoequilibrium (Pfr/P) and red:far-red ratio (R:FR). Data are presented as in-canopy angular and height profiles, and as diurnal and seasonal variations. PFD_400–700 and Pfr/P were found to be reduced inside each canopy, the reduction being greatest in the most dense canopy, and least in the most open canopy. At any height within each canopy, calculated Pfr/P decreased linearly with time throughout the growing season, until leaf senescence began. The reduction was greater in the denser canopies and was found to be similar for three consecutive field seasons. Linear relationships were found between plant stem growth rate, plant spacing and Pfr/P calculated from radiation propagated approximately horizontally within the canopies. The findings support the role of phytochrome in proximity perception in the natural environment and provide a quantitative basis for investigating the competitive interactions between plants growing in dense stands. The hypothesis is proposed that the dynamics of developing or regenerating canopies can be accounted for on the basis of phytochrome-mediated perception of the proximity of neighbouring plants.     

The function, action and adaptive significance of phytochrome in light-grown plants

Abstract. It has previously been proposed that the fundamental function of phytochrome in the natural environment is the perception of the relative proportions of red and far-red light, i.e. the red: far-red ratio. This paper re-evaluates this hypothesis, for vegetative green plants, in the light of recent findings. Essentially, three issues are considered: (a) the modulation of the response to red: far-red by fluence rate: (b) the anticipation of competition for light by perception of changes in red: far-red that precede actual shading: and (c) characteristics of phytochrome that may be important in the mechanism of photoperception (i.e. the accumulation of photoconversion intermediates, and the stability of Pfr). We conclude: (a) the red: far-red ratio provides a reliable signal of plant density, even before shading by neighbours occurs: (b) plants are able to perceive and respond to these signals, and that possible ambiguities due to low red: far-red at low solar angles may be avoided by modulation of the perception process by fluence-rate dependent mechanisms; (c) although direct experimental evidence does not yet exist, circumstantial evidence suggests that the perception of red: far-red may confer positive adaptive advantage; and (d) plants of certain species perceive and respond to fluence rate changes, mediated perhaps by a blue-light absorbing photoreceptor or by phytochrome, but that these responses do not necessarily lead to shade avoidance reactions and their ecological relevance is not fully understood.     

Ethylene is required in tobacco to successfully compete with proximate neighbours

Plants sense neighbours even before these cause a decrease in photosynthetic light availability. Light reflected by proximate neighbours signals a plant to adjust growth and development, in order to avoid suppression by neighbour plants. These phenotypic changes are known as the shade‐avoidance syndrome and include enhanced shoot elongation and more upright‐positioned leaves. In the present study it was shown that these shade‐avoidance traits in tobacco (Nicotiana tabacum) are also induced by low concentrations of ethylene. Furthermore, it was shown that transgenic plants, insensitive to ethylene, have a delayed appearance of shade‐avoidance traits. The increase in both leaf angles and stem elongation in response to neighbours are delayed in ethylene‐insensitive plants. These data show that ethylene is an important component in the regulation of neighbour‐induced, shade‐avoidance responses. Consequently, ethylene‐insensitive plants lose competition with wild‐type neighbours, demonstrating that sensing of ethylene is required for a plant to successfully compete for light.     

An acylcyclohexadione retardant inhibits gibberellin A1 metabolism, thereby nullifying phytochrome-modulation of cowpea epicotyl explants

The regulation by phytochrome of stem elongation in light-grown plants depends on gibberellins (GAs). To investigate whether this is mediated by a change in GA metabolism, the effect of the GA biosynthesis inhibitor LAB 198 999 (an acylcyclohexadione derivative) on the end-of-day far-red (FR) response in cowpea ( Vigna sinensis L.) epicotyl explants has been investigated. Growth of epicotyl explants of light-grown seedlings was enhanced when treated with far-red light before incubation in the dark (end-of-day FR effect). Low doses of LAB 198 999 (0.05 and 0.5 μg explant⁻¹) reduced the effect of FR, whereas 5 to 50 μg explant⁻¹ stimulated elongation of both red light (R)- and FR-treated epicotyl explants while nullifying the differences between R and FR treatments. In paclobutrazol-treated epicotyl explants, FR enhanced the response to applied GA₁ and GA₂₀, whereas LAB 198 999 increased the activity of GA₁ and decreased that of GA₂₀, [³H]Gibberellin A₁, injected into the basal part of the epicotyl, was transported and metabolized mainly to [³H]GA₈ in the apical 20 mm of the epicotyl. The conversion of [³H]GA₁ to [³H]GA₈ was dramatically reduced by both end-of-day FR treatments and LAB 198 999 applications. In addition, both treatments enhanced epicotyl elongation. It is proposed that the regulation of cowpea epicotyl growth by phytocrome is mediated, at least partially, by modifying GA₁ degradation.     

Simulating the effects of localized red:far-red ratio on tillering in spring wheat (Triticum aestivum) using a three-dimensional virtual plant model

The outgrowth of tiller buds in Poaceae is influenced by the ratio of red to far-red light irradiance (R:FR). At each point in the plant canopy, R:FR is affected by light scattered by surrounding plant tissues. This paper presents a three-dimensional virtual plant modelling approach to simulate local effects of R:FR on tillering in spring wheat (Triticum aestivum). R:FR dependence of bud outgrowth was implemented in a wheat model, using three hypothetical responses of bud extension to R:FR (unit step, curvilinear and linear response). Bud break occurred when a threshold bud length was reached. Simulations were performed for three plant population densities. In accordance with experimental observations, fewer tillers per plant were simulated for higher plant population densities. The linear and curvilinear responses caused a delay in the increase in tiller number compared with experimental data. The unit step response approached experimental results best. It is suggested that a model based on relatively simple relations can be used to simulate degree of tillering. This study has shown that the virtual plant approach is a promising tool with which to address crop morphological and ecological research questions where the determining factors act at the level of the individual plant organ.     

Impaired phytochrome-mediated shade-avoidance responses in the aurea mutant of tomato

Internode extension-growth responses to neighbouring plants and to red to far-red ratios (R:FR) were investigated in wild-type (WT) and aurea (au)-mutant seedlings of tomato grown under natural radiation. The genomic location of the au mutant is not known, but one of its consequences is the reduced phytochrome level. In WT seedlings, internode growth was promoted by the presence of non-shading neighbours reflecting far-red light (FR), the shade of a tall canopy, FR provided as a supplement during the photoperiod, and FR pulses either provided at the end of the day or delayed into the dark period. Supplementary FR during the photoperiod also promoted growth in herbicide-treated partially bleached WT seedlings. The au mutant showed higher background extension-growth rates, but only responded to the most severe treatments: deep shade light and very low R:FR at the end of the day, i.e. au-mutant seedlings were less sensitive than WT seedlings to R:FR signals. Wild-type seedlings were transferred from the glasshouse to a growth room and exposed to white light with two levels of phytochrome-absorbable radiation but similar phytochrome photoequilibria and radiation for photosynthesis. The plants exposed to the lowest level showed a transient increase of internode extension growth rate and a simultaneous reduction of response to FR pulses, i.e. reproduced some of the features of au-mutant seedlings. Phytochrome itself could set the degree of response to Pfr during neighbour detection.     

Additional cause for reduced JA-Ile in the root of a Lotus japonicus phyB mutant

Light is critical for supplying carbon for use in the energetically expensive process of nitrogen-fixing symbiosis between legumes and rhizobia. We recently showed that root nodule formation in phyB mutants [which have a constitutive shade avoidance syndrome (SAS) phenotype] was suppressed in white light, and that nodulation in wild-type is controlled by sensing the R/FR ratio through jasmonic acid (JA) signaling. We concluded that the cause of reduced root nodule formation in phyB mutants was the inhibition of JA-Ile production in root. Here we show that the shoot JA-Ile level of phyB mutants is higher than that of the wild-type strain MG20, suggesting that translocation of JA-Ile from shoot to root is impeded in the mutant. These results indicate that root nodule formation in phyB mutants is suppressed both by decreased JA-Ile production, caused by reduced JAR1 activity in root, and by reduced JA-Ile translocation from shoot to root.