A light-dependent molecular link between competition cues and defence responses in plants.

Growth responses to competition1 and defence responses to the attack of consumer organisms2 are two classic examples of adaptive phenotypic plasticity in plants. However, the mechanistic and functional links between these responses are not well understood. Jasmonates, a family of lipid-derived signals, are potent growth inhibitors and central regulators of plant immunity to herbivores and pathogens3,4, with both roles being evolutionarily conserved from bryophytes5 to angiosperms6. When shade-intolerant plants perceive the proximity of competitors using the photoreceptor phytochrome B, they activate the shade-avoidance syndrome and downregulate jasmonate responses7. Despite the central implications of this light-mediated change in the growth/defence balance for plant adaptation and crop yield8,9, the mechanisms by which photoreceptors relay light cues to the jasmonate signalling pathway remain poorly understood10. Here, we identify a sulfotransferase (ST2a) that is strongly upregulated by plant proximity perceived by phytochrome B via the phytochrome B-phytochrome interacting factor signalling module. By catalysing the formation of a sulfated jasmonate derivative, ST2a acts to reduce the pool of precursors of active forms of jasmonates and represents a direct molecular link between photoreceptors and hormone signalling in plants. The metabolic step defined by this enzyme provides a molecular mechanism for prioritizing shade avoidance over defence under intense plant competition.

Soybean resistance to stink bugs (Nezara viridula and Piezodorus guildinii) increases with exposure to solar UV-B radiation and correlates with isoflavonoid content in pods under field conditions.

Solar UV-B radiation (280-315 nm) has a significant influence on trophic relationships in natural and managed ecosystems, affecting plant-insect interactions. We explored the effects of ambient UV-B radiation on the levels of herbivory by stink bugs (Nezara viridula and Piezodorus guildinii) in field-grown soybean crops. The experiments included two levels of UV-B radiation (ambient and attenuated UV-B) and four soybean cultivars known to differ in their content of soluble leaf phenolics. Ambient UV-B radiation increased the accumulation of the isoflavonoids daidzin and genistin in the pods of all cultivars. Soybean crops grown under attenuated UV-B had higher numbers of unfilled pods and damaged seeds than crops grown under ambient UV-B radiation. Binary choice experiments with soybean branches demonstrated that stink bugs preferred branches of the attenuated UV-B treatment. We found a positive correlation between percentage of undamaged seeds and the contents of daidzin and genistin in pods. Our results suggest that constitutive and UV-B-induced isoflavonoids increase plant resistance to stink bugs under field conditions.

No time for candy: passionfruit (Passiflora edulis) plants down-regulate damage-induced extra floral nectar production in response to light signals of competition.

Plant fitness is often defined by the combined effects of herbivory and competition, and plants must strike a delicate balance between their ability to capture limiting resources and defend against herbivore attack. Many plants use indirect defenses, such as volatile compounds and extra floral nectaries (EFN), to attract canopy arthropods that are natural enemies of herbivorous organisms. While recent evidence suggests that upon perception of low red to far-red (R:FR) ratios, which signal the proximity of competitors, plants down-regulate resource allocation to direct chemical defenses, it is unknown if a similar phytochrome-mediated response occurs for indirect defenses. We evaluated the interactive effects of R:FR ratio and simulated herbivory on nectar production by EFNs of passion fruit (Passiflora edulis f. flavicarpa). The activity of petiolar EFNs dramatically increased in response to simulated herbivory and hormonal treatment with methyl jasmonate (MeJA). Low R:FR ratios, which induced a classic "shade-avoidance" repertoire of increased stem elongation in P. edulis, strongly suppressed the EFN response triggered by simulated herbivory or MeJA application. Strikingly, the EFN response to wounding and light quality was localized to the branches that received the treatments. In vines like P. edulis, a local response would allow the plants to precisely adjust their light harvesting and defense phenotypes to the local conditions encountered by individual branches when foraging for resources in patchy canopies. Consistent with the emerging paradigm that phytochrome regulation of jasmonate signaling is a central modulator of adaptive phenotypic plasticity, our results demonstrate that light quality is a strong regulator of indirect defenses.

Beneficial effects of solar UV-B radiation on soybean yield mediated by reduced insect herbivory under field conditions.

Ultraviolet-B radiation (UV-B: 280-315 nm) has damaging effects on cellular components and macromolecules. In plants, natural levels of UV-B can reduce leaf area expansion and growth, which can lead to reduced productivity and yield. UV-B can also have important effects on herbivorous insects. Owing to the successful implementation of the Montreal Protocol, current models predict that clear-sky levels of UV-B radiation will decline during this century in response to ozone recovery. However, because of climate change and changes in land use practices, future trends in UV doses are difficult to predict. In the experiments reported here, we used an exclusion approach to study the effects of solar UV-B radiation on soybean crops, which are extensively grown in many areas of the world that may be affected by future variations in UV-B radiation. In a first experiment, performed under normal management practices (which included chemical pest control), we found that natural levels of UV-B radiation reduced soybean yield. In a second experiment, where no pesticides were applied, we found that solar UV-B significantly reduced insect herbivory and, surprisingly, caused a concomitant increase in crop yield. Our data support the idea that UV-B effects on agroecosystems are the result of complex interactions involving multiple trophic levels. A better understanding of the mechanisms that mediate the anti-herbivore effect of UV-B radiation may be used to design crop varieties with improved adaptation to the cropping systems that are likely to prevail in the coming decades in response to agricultural intensification.

A look into the invisible: ultraviolet-B sensitivity in an insect (Caliothrips phaseoli) revealed through a behavioural action spectrum.

Caliothrips phaseoli, a phytophagous insect, detects and responds to solar ultraviolet-B radiation (UV-B; lambda or= 400 nm) failed to elicit any response. All but six ommatidia of the thrips compound eye were highly fluorescent when exposed to UV-A of wavelengths longer than 330 nm. We hypothesized that the fluorescent compound acts as an internal filter, preventing radiation with lambda > 330 nm from reaching the photoreceptor cells. Calculations based on the putative filter transmittance and a visual pigment template of lambda(max) = 360 nm produced a sensitivity spectrum that was strikingly similar to the action spectrum of UV-induced behavioural response. These results suggest that specific UV-B vision in thrips is achieved by a standard UV-A photoreceptor and a sharp cut-off internal filter that blocks longer UV wavelengths in the majority of the ommatidia.

Solar ultraviolet-B radiation and insect herbivory trigger partially overlapping phenolic responses in Nicotiana attenuata and Nicotiana longiflora.

BACKGROUND AND AIMS: Plants exposed to solar ultraviolet-B radiation (UV-B, 280-315 nm) frequently suffer less insect herbivory than do plants that receive attenuated levels of UV-B. This anti-herbivore effect of solar UV-B exposure, which has been documented in several ecosystems, is in part mediated by changes in plant tissue quality. Exposure to UV-B can modify the abundance of a number of secondary metabolites, including phenolic compounds with potential impacts on insect herbivores. The aim of this study is to assess the potential anti-herbivore role of UV-B-induced phenolic compounds by comparing the phenolic profiles induced by UV-B and simulated insect herbivory in two wild species of the genus Nicotiana. METHODS: Plants grown under field and glasshouse conditions were exposed to contrasting levels of UV-B. Half of the plants of the attenuated UV-B treatment were given a simulated herbivory treatment, where leaves were mechanically damaged and immediately treated with oral secretions of Manduca sexta caterpillars. This treatment is known to mimic the impact of real herbivory on the expression of plant defences in Nicotiana. Phenolic profiles induced by UV-B and simulated herbivory were characterized using high-performance liquid chromatography-mass spectrometry (HPLC-MS). KEY RESULTS: UV-B induced the accumulation of several UV-absorbing phenolic compounds that are known to play a significant role in UV-B screening. Interestingly, there was a significant convergence in the phenolic profiles induced by UV-B and simulated herbivory: chlorogenic acid and dicaffeoylspermidine isomers, in particular, displayed a similar pattern of response to these stimuli. In contrast, rutin, the only flavonoid that accumulated in significant quantities in the experiments, was only induced by UV-B. CONCLUSIONS: The results suggest that the anti-herbivory effect induced by UV-B may be mediated at least in part by the accumulation of phenylpropanoid derivatives that are similar to those induced by the plant in response to insect herbivory.

Remote sensing of future competitors: impacts on plant defenses.

Far-red radiation (FR) reflected by green tissues is a key signal that plants use to detect the proximity of future competitors. Perception of increased levels of FR elicits a suite of responses collectively known as the shade-avoidance syndrome, which includes increased stem elongation, production of erect leaves, and reduced lateral branching. These responses improve the access to light for plants that occur in crowded populations. Responses to the proximity of competitors are known to affect the susceptibility to disease and predation in several organisms, including social animals. However, the impacts of warning signals of competition on the expression of defenses have not been explicitly investigated in plants. In the experiments reported here, we show that reflected FR induced a dramatic down-regulation of chemical defenses in wild tobacco (Nicotiana longiflora). FR altered the expression of several defense-related genes, inhibited the accumulation of herbivore-induced phenolic compounds, and augmented the performance of the specialist herbivore Manduca sexta. Complementary studies with tomato suggested that the effects of FR on defenses are mediated by the photoreceptor phytochrome B. The central implication of these results is that shade-intolerant species such as wild tobacco and tomato activate functional changes that affect their ability to cope with herbivore attack in response to phytochrome signals of future competition, even in the absence of real competition for resources. These findings suggest that competition overshadowed herbivory during the evolution of this group of species and add a new axis to the definition of the shade-avoidance syndrome.