Timely Plant Defenses Protect Against Caterpillar Herbivory

COMMENTARY

Timely plant defenses protect against caterpillar herbivory

Georg Jander1 Boyce Thompson Institute for Plant Research, Ithaca, NY 14853-1801

s sessile, photosynthetic organ- isms, plants benefit greatly from A a circadian clock that adjusts their overall metabolism in an- ticipation of the highly predictable arrival of sunrise and sunset. Thus, it is not sur- prising that about one-third of all plant genes show evidence of circadian regulation in their expression patterns (1, 2). However, closer examination of this diurnally regulated transcription shows that it comprises not only the predictable genes involved in photosynthesis, carbon me- Fig. 1. (A) Trichoplusia ni (cabbage looper) caterpillar feeding on Arabidopsis.(B) Under normal growth tabolism, and water uptake but numerous conditions, when the circadian clocks of the caterpillars and the plants are synchronized, both caterpillar genes with known functions in plant de- feeding activity (red line) and jasmonate-mediated plant defenses (green line) peak during the day. (C)If fense. Recent studies show that the success the internal clock of cabbage loopers is shifted by 12 h, maximum feeding (red line) occurs at a time of of pathogen infections is influenced by reduced Arabidopsis defenses (green line) and the caterpillars grow more rapidly. the plant circadian clock (3–5). Accumu- lation of salicylic acid, a key signal for the growth was not observed in similar ex- has been focused almost exclusively on the induction of antimicrobial defenses, peaks periments with Arabidopsis mutants that glucosinolates, a crucifer-specific class of at night and may lead to elevated patho- are compromised in circadian regulation secondary metabolites. Tissue damage gen resistance in the early morning. Cy- or the induction of jasmonate-mediated caused by herbivory brings together glu- clical accumulation of herbivore-induced defense responses, showing that both of cosinolates and activating enzymes called plant metabolites (6), as well as reciprocal these plant functions are required for the myrosinases, resulting in the formation of effects of plant secondary metabolism on periodicity of herbivore defenses. toxic and deterrent breakdown products. the circadian clock (7), suggests that re- The hypothesized interactions between Although DNA microarray experiments sistance to insect herbivory also should circadian plant defense regulation and clearly show diurnal regulation of gluco- show diurnal regulation. This hypothesis cabbage looper herbivory can be con- sinolate-related genes (1, 7), there are as is confirmed by a study in PNAS (8), firmed by conducting experiments with yet no conclusive studies that demonstrate which provides a previously undescribed insects that have different diurnal feeding corresponding diurnal variation in the avenue for studying plant-herbivore inter- patterns. For instance, caterpillars of abundance of glucosinolates or their actions by demonstrating that plants can some species of noctuid moths, commonly breakdown products. Moreover, clock- benefit from synchrony in the pattern of called cutworms, feed almost exclusively shifted cabbage loopers exhibit a threefold diurnally regulated defenses and insect at night and hide during the day, a behav- increase in weight relative to synchronized feeding behavior. ior that may reduce predation by day- controls (8), an effect that is greater The report by Goodspeed et al. (8) is active parasitoid wasps. However, if di- than the growth changes observed with focused on laboratory studies of inter- urnal peaks in antiherbivore defenses, cabbage loopers feeding from Arabidopsis actions between the generalist lepidop- which have been observed in both Arabi- mutants with altered glucosinolate break- teran herbivore Trichoplusia ni (cabbage dopsis and Nicotiana attenuata (6, 8), are down (10), reduced myrosinase activity looper) and the small cruciferous plant a more general phenomenon in plants, (11), or even a complete absence of glu- Arabidopsis thaliana (Arabidopsis) (Fig. nocturnal feeding may also be an adapta- cosinolates (12). Thus, although glucosi- 1A). Cabbage looper herbivory and accu- tion to reduced nighttime plant defenses. nolates undoubtedly have important mulation of jasmonic acid, a plant hor- An interesting future comparison will be functions in protection against herbivory mone that triggers herbivore defenses in to conduct experiments similar to those (10–12), it is likely that additional de- many plant species, follow circadian cycles of Goodspeed et al. (8) but with night- fensive metabolites, or perhaps circadian that peak during the day, suggesting that feeding cutworms. In this case, one would cycles in the Arabidopsis nutritional con- Arabidopsis plants are allocating their re- expect that caterpillars that are clock- tent, also influence the observed changes sources to maximize defense when cater- shifted relative to their host plants will in caterpillar weight gain. pillars are feeding. To test this hypothesis, perform less well than nonshifted control An intriguing possibility is that diurnal the authors conducted experiments in caterpillars. Other Lepidoptera, for in- variation in plant metabolism, in addition ’ which cabbage loopers were entrained stance, Manduca sexta (tobacco horn- to the insects own internal clock, can separately from the host plants, using worm), are reported to show no circadian have a direct effect on cabbage looper a light cycle that shifted their circadian regulation of their feeding behavior (9). feeding patterns. For instance, behavior of Mythimna separata clocks by 12 h. Under subsequent con- Thus, even though N. attenuata, a natural (Oriental armyworm) stant-darkness conditions, caterpillars that host for tobacco hornworms, shows diurnal caterpillars, which feed at night and hide were feeding asynchronously with the variation in herbivore defense responses plant defense cycle consumed more leaf (6), one would predict few changes in cat- material and, at the end of the experiment, erpillar performance if it were clock-shifted Author contributions: G.J. wrote the paper. were threefold as heavy as synchronously relative to its host plants. The author declares no conflict of interest. feeding control caterpillars (Fig. 1 B and Research on the proximal causes of See companion article 10.1073/pnas.1116368109. C). Moreover, this effect on caterpillar Arabidopsis resistance to insect herbivory 1E-mail: [email protected].

www.pnas.org/cgi/doi/10.1073/pnas.1201443109 PNAS Early Edition | 1of2 Downloaded by guest on October 1, 2021 during the day to avoid predators, is dic- crucifers, there are few reports of cabba- studied Columbia-0 accession. However, tated primarily by diurnal variation in geloopers on Arabidopsis in the ﬁeld. there is considerable natural variation in volatile emissions from the host plants Thus, if the daytime peak in Arabidopsis the Arabidopsis circadian clock (14), pro- rather than caterpillar perception of the jasmonate production has indeed evolved duction of defensive metabolites (15), and day-night cycle (13). If there are similar herbivore pressures that this species faces interactions between Arabidopsis and cab- Clock-shifted cabbage across a geographical range that extends bage loopers, the clock-shift experiments from the equator to the Arctic Circle. conducted by Goodspeed et al. (8) could loopers exhibit a Therefore, experiments with additional result in caterpillars that spend a greater Arabidopsis accessions will likely show dif- part of the day feeding. Observations of threefold increase in ferent circadian interactions with insect circadian cycles in cabbage looper feeding ﬁ herbivores. These ideas, and likely many have only been conducted with an arti cial weight relative to future studies in the area of plant–insect diet. Therefore, it is not yet possible to interactions, follow directly from a new determine whether increased Arabidopsis synchronized controls. awareness of the complex interplay between tissue consumption by clock-shifted cab- the circadian rhythms of plants and insect bage loopers is attributable to more rapid feeding during the time that is dictated by in response to herbivory, this selective herbivores that has been provided by the their circadian clocks or attributable to pressure probably includes not only cab- research of Goodspeed et al. (8). a shift in the herbivory pattern to include bage loopers but numerous other day- Arabidopsis ACKNOWLEDGMENTS. I thank Ping Wang for additional feeding times. active species. Like most re- Trichoplusia ni caterpillars, and Meena Haribal for Although cabbage loopers are gener- search, the experiments conducted by photography. This work was supported by Na- alist herbivores that commonly feed on Goodspeed et al. (8) involved only the well- tional Science Foundation Award IOS-1139329.

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