Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior

Abstract

Diverse life forms have evolved internal clocks enabling them to monitor time and thereby anticipate the daily environmental changes caused by Earth's rotation. The plant circadian clock regulates expression of about one-third of the Arabidopsis genome, yet the physiological relevance of this regulation is not fully understood. Here we show that the circadian clock, acting with hormone signals, provides selective advantage to plants through anticipation of and enhanced defense against herbivory. We found that cabbage loopers (Trichoplusia ni) display rhythmic feeding behavior that is sustained under constant conditions, and plants entrained in light/dark cycles coincident with the entrainment of the T. ni suffer only moderate tissue loss due to herbivory. In contrast, plants entrained out-of-phase relative to the insects are significantly more susceptible to attack. The in-phase entrainment advantage is lost in plants with arrhythmic clocks or deficient in jasmonate hormone; thus, both the circadian clock and jasmonates are required. Circadian jasmonate accumulation occurs in a phase pattern consistent with preparation for the onset of peak circadian insect feeding behavior, providing evidence for the underlying mechanism of clock-enhanced herbivory resistance. Furthermore, we find that salicylate, a hormone involved in biotrophic defense that often acts antagonistically to jasmonates, accumulates in opposite phase to jasmonates. Our results demonstrate that the plant circadian clock provides a strong physiological advantage by performing a critical role in Arabidopsis defense.circadian rhythm | diurnal rhythm | plant-herbivore interaction | jasmonic acid | salicylic acid I n the battle between plant host and herbivore, plants appear to be disadvantaged due to their relative immobility because once herbivorous insects attack, plants cannot escape by relocating. However, it is well-documented that plants can detect attack by insect herbivores and, in response, activate defense responses (1). These defense responses include accumulation of proteins and compounds that are toxic to and/or act to deter feeding of herbivores, thereby reducing herbivore performance and increasing plant resistance. Jasmonate hormones are critical for plant herbivore defense (1-3) and for the regulation of both herbivore and wound-responsive gene expression (4).Remarkably, many genes regulated in expression by wounding also have strong circadian regulation. Over 40% of genes whose expression is induced by wounding have peak circadian expression at subjective dusk, and over 80% of genes down-regulated by wounding have peak expression at subjective dawn (5). However, it remained to be determined whether this circadian regulation of wound-inducible genes enables plants to anticipate herbivore attack through a cyclical activation of defense response. Here we demonstrate that Arabidopsis plants that are entrained such that their subjective day is in-phase with Trichoplusia ni subjective day have increased resistance to herbivory. In contrast,...

Genome-wide identification of CCA1 targets uncovers an expanded clock network inArabidopsis

“…Consistent with the known role of CCA1 in regulating responses to abiotic and biotic stresses, we observe enrichment in genes with GO terms associated with response to both biotic and abiotic stresses, including response to low temperature and light ( Fig. S1E) (8,9,25,(33)(34)(35). Putative CCA1 targets also are enriched for genes involved in hormone response, including gibberellic acid and abscisic acid, as is consistent with the known role of the circadian clock in the regulation of daily cycles of hormone sensitivity (22,36).…”

“…Although considered a bona fide transcriptional repressor, CCA1 also can activate the expression of the clock genes PSEUDO-RESPONSE REGULATOR 9 (PRR9) and PRR7 by binding directly to their promoters (23). CCA1 is considered a master regulator of clock function, and its misexpression causes severe clock phenotypes that result in altered plant growth and stress responses in Arabidopsis (11,22,24,25).To gain a better understanding of the role that the circadian clock plays in the control of these multiple biological processes through CCA1, either directly or through indirect regulation of downstream factors, we performed ChIP sequencing (ChIP-Seq) analyses to …”

A bHLH-Type Transcription Factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, Acts as a Repressor to Negatively Regulate Jasmonate Signaling inArabidopsis

“…However, new insights have recently emerged on the regulatory mechanisms of JA signaling, including identification of JAZ binding partners, and the influence of circadian rhythms and hormonal crosstalk (Hou et al, 2010;Qi et al, 2011;Song et al, 2011;Goodspeed et al, 2012;Hong et al, 2012;Shin et al, 2012;Yang et al, 2012). These suggest that JA signaling encompasses multiple complicated regulatory mechanisms.…”

Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis

“…Cold treatment caused a greater increase in gene expression at ZT15 than ZT0 ( Supplementary Fig. 8, a versus b and c versus d) because of gating of induction by the circadian clock and diurnal regulation of stress responses 19,21,22 . Interestingly, higher than MPV induction of stress-responsive genes in the hybrids occurred only at some specific time points (for example, COR15A at ZT3 and ZT9 and COR78 at ZT9).…”

“…In Arabidopsis thaliana, the RNA-directed DNA methylation pathway mediates a parent-of-origin effect on circadian rhythms, leading to biomass heterosis in reciprocal F1 hybrids 18 . In A. thaliana diploids, the circadian clock regulates abiotic 19,20 and biotic [21][22][23] stress responses. However, there is a tradeoff between stress responses and fitness; constitutive expression of stressresponsive genes reduces fitness and growth 24,25 , while repressing disease resistance genes promotes growth 26 .…”