Spider Mites Cause More Damage to Tomato in the Dark When Induced Defenses Are Lower

Abstract

Plants have evolved robust mechanisms to cope with incidental variation (e.g. herbivory) and periodical variation (e.g. light/ darkness during the day-night cycle) in their environment. It has been shown that a plant's susceptibility to pathogens can vary during its day-night cycle. We demonstrated earlier that the spider mite Tetranychus urticae induces jasmonate-and salicylatemediated defenses in tomato plants while the spider mite T. evansi suppresses these defenses probably by secreting salivary effector proteins. Here we compared induction/suppression of plant defenses; the expression of mite-effector genes and the amount of damage due to mite feeding during the day and during the night. T. urticae feeding upregulated the expression of jasmonate and salicylate marker-genes albeit significantly higher under light than under darkness. Some of these marker-genes were also upregulated by T. evansi-feeding albeit to much lower levels than by T. urticae-feeding. The expression of effector 28 was not affected by light or darkness in either mite species. However, the expression of effector 84 was considerably higher under light, especially for T. evansi. Finally, while T. evansi produced overall more feeding damage than T. urticae both mites produced consistently more damage during the dark phase than under light. Our results suggest that induced defenses are subject to diurnal variation possibly causing tomatoes to incur more damage due to mite-feeding during the dark phase. We speculate that mites, but especially T. evansi, may relax effector production during the dark phase because under these conditions the plant's ability to upregulate defenses is reduced.

Intraspecific variation for host immune activation by the spider mite Tetranychus evansi

“…For T. evansi this seems to be the case, as the effector 84 was found to be highly plastic in certain conditions (e.g. the presence of heterospecific competitors [ 37 ]; light–dark cycles [ 42 ]; developmental stages [ 81 ]).…”

“…There is evidence that plant defence interference (e.g. spider mites [ 37 ]; aphids [ 38 ]) and effector production by herbivores (spider mites [ 39 , 40 ]; Lepidoptera [ 41 ]) are plastic traits that can be influenced by environmental cues such as competition [ 37 ], light–dark cycles [ 42 ] or temperature [ 41 ]. This plasticity may serve to limit physiological or ecological costs associated with immune interference.…”

Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco

“…In nature, plants must cope with environments characterized by periodic changes that accompany day/night cycles that include fluctuations in many factors in addition to light: temperature, humidity, and innumerable biotic interactions. For instance, plants need to adopt to rhythms of attacks by pathogens and herbivores, or activity patterns of beneficial species, such as pollinators and natural enemies of herbivores [ 4 , 6 , 57 , 58 ]. To cope with this environmental rhythmicity, plants have evolved both endogenous rhythms and the ability to coordinate responses to changes in specific environmental factors.…”

Diurnal rhythmicity in metabolism and salivary effector expression shapes host colonization by aphids

“…For example, the cabbage looper ( Trichoplusia ni ), a generalist herbivore, shows rhythms in feeding, with peak feeding occurring during the latter part of the day (8). Conversely, cell-content feeders like spider mites ( Tetranychus urticae ) exploit a nighttime “lull” in jasmonate-induced defenses, causing more damage during the night (9). Given that aphids rely entirely on acquiring phloem sap from plants for their reproduction and survival, they likely need to anticipate, respond to, and counteract the challenges posed by daily rhythms in their hosts.…”