Shifting Nicotiana attenuata's diurnal rhythm does not alter its resistance to the specialist herbivore Manduca sexta

Abstract

Arabidopsis thaliana plants are less resistant to attack by the generalist lepidopteran Trichoplusia ni when plants and herbivores are entrained to opposite, versus identical diurnal cycles and tested under constant conditions. This effect is associated with circadian fluctuations in levels of jasmonic acid, the transcription factor MYC2, and glucosinolate contents in leaves. We tested whether a similar effect could be observed in a different plant-herbivore system: the native tobacco Nicotiana attenuata and its co-evolved specialist herbivore, Manduca sexta. We measured larval growth on plants under both constant and diurnal conditions following identical or opposite entrainment, profiled the metabolome of attacked leaf tissue, quantified specific metabolites known to reduce M. sexta growth, and monitored M. sexta feeding activity under all experimental conditions. Entrainment did not consistently affect M. sexta growth or plant defense induction. However, both were reduced under constant dark conditions, as was M. sexta feeding activity. Our data indicate that the response induced by M. sexta in N. attenuata is robust to diurnal cues and independent of plant or herbivore entrainment. We propose that while the patterns of constitutive or general damage-induced defense may undergo circadian fluctuation, the orchestration of specific induced responses is more complex.

Herbivore‐induced volatile blends with both “fast” and “slow” components provide robust indirect defence in nature

“…Feeding activity of 1st‐instar M. sexta larvae also peaked at midday, although less sharply, with feeding bouts at other times of day; and also displayed a diurnal rhythm (Figure e, first day ANOVA: F 5,29 = 15.674, p < .001; second day ANOVA: F 5,29 = 24.824, p < .001). M. sexta feeding activity generally increases as larvae grow (Herden et al., ), but on the third day feeding activities were lower than on the second day because larvae began to moult (Figure e). Feeding activity of M. sexta larvae was strongly temperature‐dependent (Figure S1a,c, Spearman's rho = 0.543, p < .001).…”

“…M. sexta feeding activity generally increases as larvae grow (Herden et al, 2016), but on the third day feeding activities were lower than on the second day because larvae began to moult (Figure 1e). Feeding activity of M. sexta larvae was strongly temperature-dependent ( Figure S1a,c, Spearman's rho = 0.543, p < .001).…”

Fitness consequences of altering floral circadian oscillations forNicotiana attenuata

“…It is thought that the circadian clock helps plants to anticipate abiotic factors, such as preparing the photosynthetic machinery at dawn to anticipate the rising of the sun (Green et al ) or to increase its pollination service (Vandenbrink et al ). The clock has been argued to help plants anticipate attack from herbivores (Bhardwaj et al ; Wang et al ; Goodspeed et al ; Zhang et al ), an inference which has not found support in the N. attenuata system (Herden et al ). Based on evolutionary considerations, beneficial biotic interactions, rather than antagonistic interactions, are more likely to be usefully anticipated by a circadian clock, because antagonists can readily counter a plant's clock‐mediated anticipation by changing the timing of their attack.…”

CIRCADIAN CLOCK-ASSOCIATED1 Controls Resistance to Aphids by Altering Indole Glucosinolate Production

“…S4). Herden et al (2016) presented a counterexample, in which they failed to observe any difference in larval growth of the specialist herbivore M. sexta reared on synchronous versus asynchronous wild tobacco. Thus, whether anticipatory defense benefits plants by increasing their defensive capacity can be an herbivorespecific response.…”

“…However, such anticipatory defense is not observed in wild tobacco (Nicotiana attenuata) interacting with its herbivore specialist tobacco hornworm (Manduca sexta). Instead, induced defense upon insect attack appears to be a more prominent response (Herden et al, 2016). How circadian oscillation influences aphid-plant interaction remains poorly understood.…”