Long-day photoperiod enhances jasmonic acid-related plant defense

Agricultural crops are exposed to a range of daylengths, which act as important environmental cues for the control of developmental processes such as flowering. To explore the additional effects of daylength on plant function, we investigated the transcriptome of Arabidopsis (Arabidopsis thaliana) plants grown under short days (SD) and transferred to long days (LD). Compared with that under SD, the LD transcriptome was enriched in genes involved in jasmonic acid-dependent systemic resistance. Many of these genes exhibited impaired expression induction under LD in the phytochrome A (phyA), cryptochrome 1 (cry1), and cry2 triple photoreceptor mutant. Compared with that under SD, LD enhanced plant resistance to the necrotrophic fungus Botrytis cinerea. This response was reduced in the phyA cry1 cry2 triple mutant, in the constitutive photomorphogenic1 (cop1) mutant, in the myc2 mutant, and in mutants impaired in DELLA function. Plants grown under SD had an increased nuclear abundance of COP1 and decreased DELLA abundance, the latter of which was dependent on COP1. We conclude that growth under LD enhances plant defense by reducing COP1 activity and enhancing DELLA abundance and MYC2 expression. A given crop species can typically be exposed to a range of different photoperiods, the nature of which depend on sowing date, duration of the cycle, and latitude. Daylength profoundly affects the timing of key developmental transitions, including flowering in many species, tuberization in potato (Solanum tuberosum), and bud set and growth cessation in trees (Jackson, 2009). The ability to respond specifically to current daylength helps to reduce the risk of plants being exposed to severe stressful conditions (Casal et al., 2004). Response to daylength also can enhance the tolerance to seasonal abiotic stress. Short days (SD) anticipate the cold temperatures of winter and increase freezing tolerance (Alonso-Blanco et al., 2005; Lee and Thomashow, 2012). Long days (LD) can induce antioxidative capacities in plants (Becker et al., 2006) and mimic plant acclimation to high light intensities (Lepistö and Rintamäki, 2012) that is typical of summer. In Arabidopsis (Arabidopsis thaliana), growth under LD maintains the activity of phytochrome A (phyA), cryptochrome 1 (cry1), and cry2 photoreceptors, which promote flowering (Andrés and Coupland, 2012). These photoreceptors stabilize CONSTANS (CO; Valverde et al., 2004) by reducing the activity of the CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1)-SUPRESSOR OF PHYA-105 1 (SPA1)-SPA3-SPA4 complex (Liu et al., 2008). Growth under LD also enhances the expression of CO (Sawa et al., 2007) and the stability of CO protein (Song et al., 2012) via the action of the FLAVIN-BINDING, KELCH REPEAT, F-BOX photoreceptor (Lee et al., 2017). In turn, CO enhances the expression of FLOWERING LOCUS T (FT), which promotes flowering (Andrés and Coupland, 2012). The phyB photoreceptor, PHYTOCHROME INTERACTING FACTOR4 (PIF4), and PIF7 play important roles in repressing the C-repeat-binding factor pathway and freezing tolerance under LD (Lee and Thomashow, 2012). These examples illustrate that different photoreceptors and downstream pathways mediate diverse outputs of photoperiodic signals. The aim of this work was to explore the occurrence of additional responses to photoperiod mediated by phyA, cry1, and cry2 and to elucidate their key signaling components. To identify and prioritize these responses, we analyzed the transcriptome of plants grown under either SD or LD and tested biological responses guided by overrepresented Gene Ontology (GO) terms. Our results show that growth under LD compared with growth under SD enhances the expression of defense-related genes and plant resistance to the necrotrophic pathogen Botrytis cinerea. Growth under LD does not increase jasmonic acid (JA) levels; however, plants grown in LD had enhanced JA-induced defense by increasing the expression of MYC2 and reducing COP1 nuclear activity, which, in turn, allowed for the increased stability of DELLA proteins (Lorenzo et al., 2004; Wild et al., 2012; Chico et al., 2014).