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.