Remote sensing of future competitors: impacts on plant defenses

Abstract

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.

Fig. 1.

Effects of exposing N. longiflora plants to FR supplementation on insect performance. (A) Schematic diagram of the irradiation system used to provide supplementary FR, simulating the proximity of nonshading neighbors (ambient = control with natural R:FR). (B) Results of the growth bioassay with M. sexta caterpillars. Thin bars indicate 1 SE (n = 6). The results shown are from a single representative experiment. The whole experiment was repeated six times, with independent cohorts of plants and insects. On average, caterpillars of the FR treatment had 48% more mass at the end of the bioassays than those reared on plants from the ambient treatment (P = 0.0006).

Fig. 2.

Effects of FR and simulated M. sexta herbivory on the abundance of defense-related transcripts. (A) Schematic comparison of the effects of FR and herbivory on the abundance of photosynthesis-related transcripts (n = 25 transcripts). (B) Comparison of the effects of FR and herbivory on the abundance of transcripts involved in secondary metabolism and stress signaling (n = 120 transcripts). (C) Comparison of the effects of FR and herbivory on the expression of genes encoding enzymes of the biosynthetic pathways that lead to the formation of phenolic compounds (n = 7 transcripts for the C6–C3 group and 4 for the C15 group). The height of the box is proportional to the number of transcripts that displayed the pattern of response specified by each color combination (green, down-regulated; red, up-regulated; black, not affected). For a full list of genes, see Table 1. (D) Biosynthetic chart showing the metabolic roles of the products of genes that were significantly regulated by herbivory.

Fig. 3.

Effects of FR on induced phenolic compounds. Plants of the FR and ambient treatment (Fig. 1A) were either exposed to simulated herbivory 72 h before sampling for analysis of leaf phenolics or left undisturbed. (A) Total soluble phenolics. (B) CHA. (C) Impact of FR on the magnitude of the response induced by herbivory. The induction ratio is the concentration of a given group of compounds in plants of the herbivory treatment relative to its concentration in plants of the control treatment. The C6–C3 group includes several CHA isomers, whereas rutin and two kaempherol derivatives are included in the C15 class. In A–C, thin bars indicate 1 SE (n = 4), and the interaction term of the ANOVA is significant at P = 0.05.

Fig. 4.

Effects of phyB mutations in tomato on insect performance and herbivory. (A) Phenotype of plants of the phyB1-phyB2 double mutant of tomato (phyB1-phyB2) grown under natural daylight in a glasshouse; the wild-type variety Money Maker (MM) is shown for comparison. (B) Effects of the phyB1-phyB2 double mutation on the growth of S. eridania caterpillars (thin bars indicate 1 SE; n = 15). (C) Effects of the phyB1-phyB2 double mutation on thrips preference when plants were exposed for 1 week to attack by colonies of C. phaseoli in a glasshouse. Average numbers of thrips per plant (±SE; n = 25) were: phyB1-phyB2 = 4.1 (0.7) and MM = 0.7 (0.2). (D) Intensity of natural herbivory by chewing insects on phyB1-phyB2 plants and wild-type plants under field conditions (thin bars indicate 1 SE; n = 13).