Trading direct for indirect defense? Phytochrome B inactivation in tomato attenuates direct anti‐herbivore defenses whilst enhancing volatile‐mediated attraction of predators

Abstract

Under conditions of competition for light, which lead to the inactivation of the photoreceptor phytochrome B (phyB), the growth of shade-intolerant plants is promoted and the accumulation of direct anti-herbivore defenses is down-regulated. Little is known about the effects of phyB on emissions of volatile organic compounds (VOCs), which play a major role as informational cues in indirect defense. We investigated the effects of phyB on direct and indirect defenses in tomato (Solanum lycopersicum) using two complementary approaches to inactivate phyB: illumination with a low red to far-red ratio, simulating competition, and mutation of the two PHYB genes present in the tomato genome. Inactivation of phyB resulted in low levels of constitutive defenses and down-regulation of direct defenses induced by methyl jasmonate (MeJA). Interestingly, phyB inactivation also had large effects on the blends of VOCs induced by MeJA. Moreover, in two-choice bioassays using MeJA-induced plants, the predatory mirid bug Macrolophus pygmaeus preferred VOCs from plants in which phyB was inactivated over VOCs from control plants. These results suggest that, in addition to repressing direct defense, phyB inactivation has consequences for VOC-mediated tritrophic interactions in canopies, presumably attracting predators to less defended plants, where they are likely to find more abundant prey.

The shade‐avoidance syndrome: multiple signals and ecological consequences

“…A recent study suggested that shifts in the blend of VOCs induced by phyB inactivation could play an important role in the attraction of predatory insects. Working with tomato, Cortés et al () found that when phyB was inactivated (by mutation or supplemental FR), leaf defenses were down‐regulated, as expected; however, at the same time, phyB inactivation led the plants to produce a blend of JA‐induced monoterpenes that increased their attractiveness to the predatory mirid bug Macrolopus pigmaeus (Cortés et al ). This predator can provide indirect protection to tomato plants by feeding on their insect herbivores (Lins et al ).…”

Optimizing aphid biocontrol with the predator Aphidoletes aphidimyza, based on biology and ecology

“…Similarly, no information currently exists on the effects of LED lights on the biology of A. aphidimyza . LED lights are now being widely adopted in the greenhouse industry and are known to affect lifetable characteristics and interactions between plants other natural enemy species …”

“…LED lights are now being widely adopted in the greenhouse industry and are known to affect lifetable characteristics and interactions between plants other natural enemy species. 101 Conditions inducing diapause (Section 2.3.4), namely photoperiod, have been mentioned as a cause of reduced efficacy of A. aphidimyza in the crop. 59,71 The occurrence of diapause at short daylengths in this biocontrol agent is a significant barrier to its year-round use for aphid control by growers.…”

Molecular Profiles of Contrasting Shade Response Strategies in Wild Plants: Differential Control of Immunity and Shoot Elongation

“…Many OMCL groups with possible functions in the JA-mediated defense against herbivores or necrotrophic pathogens appeared to be downregulated after 11.5 h of low R:FR treatment in G. pyrenaicum, but not, or to a lesser extent, in G. robertianum ( Figure 4B; Supplemental Figure 5A). Downregulation of defense pathways by low R:FR has also been described in Arabidopsis (Cargnel et al, 2014;Cerrudo et al, 2012;de Wit et al, 2013) and tomato (Cortés et al, 2016). Geranium orthologs of JA-inducible genes JASMONIC ACID RESPONSIVE3 (JR3), TRANSPARENT TESTA7 (TT7), and PRODUCTION OF ANTHOCYANIN PIGMENT1 (PAP1) were transcriptionally induced by a methyl-JA treatment, but this induction was suppressed by simultaneous exposure to low R:FR light in G. pyrenaicum ( Figure 4C (A) Heat map of the gene ontology clusters overrepresenting transcripts with a positive species*treatment interaction (log 2 fold changes are significantly higher in G. robertianum compared with G. pyrenaicum) at t = 11.5 h, and a role in plant defenses against pests.…”