5.3. Shade and biotic stress responses
Under shade conditions, plant defense against pathogens and insects is weakened (Ballaré, 2014; Fernandez-Milmanda et al., 2020). For instance,phyB Arabidopsis mutants are more susceptible to the fungal pathogen Fusarium oxysporum than wild-type plants (Kazan & Manners, 2011). Similarly, tomato plants mutated in phyB are less resistant to Spodoptera eridania caterpillars or the thripsCaliothrips phaseoli (Izaguirre, Mazza, Biondini, Baldwin, & Ballare, 2006). Also, Arabidopsis resistance to Botrytis cinerea and Pseudomonas syringae decreased after exposure to low R:FR ratios mimicking shade conditions (Cerrudo et al., 2012; de Wit et al., 2013).
Low ratios of R:FR (< 1) are characteristic for shade and environments with densely standing plants resulting in a partial inactivation of PfrB. In plants, low R:FR ratios are usually associated with the shade avoidance syndrome (SAS). Common phenotypical changes related to SAS are leaf hyponasty, an increase in hypocotyl and internode elongation and extended petioles to gain as much light as possible (Sessa, Carabelli, Possenti, Morelli, & Ruberti, 2018; Yang & Li, 2017).
Under low R:FR, SA- and JA-mediated pathogen defense responses are compromised. The decreased SA-induced resistance in low R:FR is associated with an inhibition of SA-responsive kinases. Especially NPR1, representing an important transcriptional regulator positively affecting SA-induced defense genes, is not phosphorylated during low R:FR, thereby inhibiting transcription of target genes (de Wit et al., 2013). Recently, it was shown that FR light affects JA content directly by diminishing the level of JA-Ile derivates in A. thalianasubjected to Spodoptera littoralis caterpillars (Fernandez-Milmanda et al., 2020). The authors identified a sulfotransferase (ST2a), whose activity is strongly upregulated by FR in a phyB/PIF-dependent manner, to be responsible for the reduction of the active JA pool and thus causing an attenuation of JA response upon FR illumination. FR light negatively affects the JA-controlled extra floral nectar secretion in lima bean (Phaseolus lunatus ; Radhika, Kost, Mithofer, and Boland, 2010). In shade-grown common milkweed (Asclepias syriaca ), the JA burst following herbivore attack ofDanaus plexippus caterpillars was halved compared to plants grown in sun and the latex content decreased (Agrawal, Kearney, Hastings, & Ramsey, 2012). Shade conditions also lower plant sensitivity to JA (Moreno, Tao, Chory, & Ballare, 2009), resembling the repressive effect of SA on JA responses on the expression of defense genes such asERF1 and PDF1.2 (Kazan & Manners, 2012; Pieterse, Leon-Reyes, Van der Ent, & Van Wees, 2009; Verhage, van Wees, & Pieterse, 2010). JA-regulated defense genes are induced by transcription factors like MYC2 which are repressed by JASMONATE ZIM DOMAIN10 (JAZ10). Under low R:FR ratios, or in phyB mutants, the stability of JAZ10 is enhanced resulting in weakened defense responses (Ballaré, 2014; Leone, Keller, Cerrudo, & Ballare, 2014). In addition, Cerrudo et al. (2012) revealed that functional JAZ10 is necessary for a reduced defense of Arabidopsis plants against B. cinerea infection under shade conditions. In low R:FR ratio, not only JAZ stability is improved, but also gibberellin (GA) activity is enhanced resulting in a reduction of DELLA functionality. As a consequence, JAZ proteins can interact with MYCs thereby preventing the transcription of target genes – a process which is normally prevented by DELLAs (Ballaré, 2014; Hou, Lee, Xia, Yan, & Yu, 2010; Navarro et al., 2008). This indicates that not only JA and SA, but also GA responds to shade and impacts defense responses in plants.
Together, the quest for light through shade-avoidance responses is prioritized over plant immune responses, as reviewed by Ballaré (2014).
CONCLUSIONS
In this review, we have described that light acts itself as a stressor and in addition regulates the outcome of numerous other abiotic and biotic stress responses. Plants have evolved complex crosstalk between light signaling and the different stress response pathways to survive and be prepared for future stress events. For instance, shortening of the days during autumn releases the phyB-dependent inhibitory effect onCBF gene induction upon cold thereby preparing plants for the coming winter (Figure 2). Light pretreatment may result in improved tolerance to different stresses. For example, thermotolerance is improved after pretreatment with light (Figure 3). Fluctuating light, as plants experience under sunfleck conditions, prepares them for following excessive light exposures (Figure 1). Not only light intensity, but also light quality affects stress responses of plants and different wavelengths might have different functions. Light of most wavelengths improves stress tolerance, but shade conditions have different effects on different stresses. A decreased R:FR ratio improves stress defense especially under drought stress (Figure 4) and cold stress (Figure 2), but under heat stress and during pathogen attack, plants prioritize growth instead of defense (Figure 5). In these cases plants often invest more in offspring than in defense mechanisms (Fernandez-Milmanda et al., 2020).
It is quite clear from the topics described above, that plants evolved mechanisms implementing light information into stress signaling pathways to improve their tolerance to stress. The increasing number of experimental work addressing this crosstalk suggests that this is a growing area of research which will lead in the future to many more insights in the role of light during plant responses to abiotic and biotic stresses.