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- W2168989872 abstract "Light is a critical source of information for plants. Plants use the phytochromes (particularly phyB) to detect light signals associated with the proximity of competitors. A low ratio of red (R) to far-red (FR) radiation (R : FR) indicates increased competition intensity, and triggers morphological responses that allow the plant to escape shading from its neighbors (the shade avoidance syndrome, SAS) (reviewed in Ballaré, 2009; Kami et al., 2010; Martínez-García et al., 2010; Casal, 2012; Pierik & de Wit, 2014). Recent evidence from studies on light regulation of plant immunity has suggested that plants may also use ultraviolet-B (UV-B, 290–315 nm) radiation as an indicator of competition intensity and light availability (Demkura et al., 2010; Demkura & Ballaré, 2012). In addition, recent studies have shown that UV-B radiation can strongly repress SAS responses triggered by low R : FR ratios (Hayes et al., 2014). Ambient UV-B radiation causes damaging effects on plants, such as DNA damage (Mazza et al., 1999), and also induces adaptive photomorphogenic responses acting through a specific UV-B photoreceptor (UVR8) (Rizzini et al., 2011; Christie et al., 2012; Wu et al., 2012) (reviewed in Heijde & Ulm, 2012; Jenkins, 2014). Therefore, the possibility exists that plants integrate information perceived by phyB and UVR8 to make decisions about growth and defense when faced with a complex light environment, such as the one that characterizes vegetation canopies. In this Letter, we address this possibility and discuss how the interplay between UV-B and R : FR signaling fine tunes plant growth and defense to optimize resource utilization in patchy canopy environments. In Arabidopsis seedlings grown under artificial light, moderate levels of supplemental UV-B can strongly suppress hypocotyl elongation responses to low R : FR ratio (Hayes et al., 2014). However, under field conditions, phyB inactivation can trigger significant elongation responses even in plants growing under full sunlight. Perhaps the most dramatic example comes from studies with cucumber (Cucumis sativus), which showed that the phyB null mutant (lh) can grow hypocotyls as long as 30 cm even under summertime field conditions and high natural UV-B irradiance (Casal et al., 1994). To further explore the interactions between phyB inactivation and natural UV-B levels, we compared the growth of lh and wild type cucumbers under filters that either blocked (−UV-B) or transmitted UV-B radiation (+UV-B) (see Supporting Information Methods S1). We found a dramatic effect of phyB inactivation promoting hypocotyl elongation and a modest, but significant repression of elongation by solar UV-B radiation (Fig. 1a). Less spectacular responses to partial phyB inactivation have been reported in other field studies, under solar UV-B irradiances, using other plant species exposed to lateral FR radiation (reviewed in Ballaré, 1999). Since none of these field studies involved Arabidopsis plants, we characterized SAS responses to the proximity of competitors in wild-type and uvr8 Arabidopsis seedlings grown in the field under contrasting levels of UV-B radiation (Fig. 1b). Plants responded to the proximity of grass competitors with a rapid increase in leaf angles (hyponastic response). This hyponastic response was reduced by solar UV-B radiation, and the repressive effect of solar UV-B radiation was missing in a uvr8 mutant (Fig. 1c). Exploration of Arabidopsis transcriptome data in microarray databases (Tables S1–S3) further suggest the existence of antagonistic effects of low R : FR ratio and UV-B radiation on expression of growth (auxin)-related genes (Fig. 2a). For example YUCCA9, ATHB-2, IAA29 and SAUR23 were all strongly upregulated by low R : FR and downregulated by UV-B radiation (Table S3). Significant effects of UVR8 activation reducing the expression of selected auxin-related genes have been reported recently (Vandenbussche et al., 2014), particularly in plants exposed to low R : FR ratios (including YUCCA9 and IAA29; Hayes et al., 2014). In our meta-analysis of available microarray data, the effect of UV-B on the ‘Auxin’ gene ontology (GO) category appeared to be somewhat dependent on the experimental conditions (Fig. S1) and largely conserved in uvr8 (Fig. S2). Taken together, physiological (Fig. 1) and transcriptomic (Fig. 2a; Table S3) results are consistent with the idea that solar UV-B radiation moderates the growth responses to neighbor proximity triggered by low R : FR ratios. The magnitude of the effect of UV-B (and UVR8) is likely to vary with the relative levels of R : FR and UV-B radiation, which emphasizes the need for using experimental approaches that cover the natural range of variation of these light signals. Solar UV-B radiation promotes plant defense against herbivorous insects and some pathogens, and here again the effects of solar UV-B are opposite to those of low R : FR ratio (Ballaré et al., 2012). The positive effect of (natural) UV-B radiation on plant immunity has often been attributed to the accumulation of leaf phenolics, although enhanced signaling through the jasmonate (JA) defense pathway is also thought to play an important role (Ballaré, 2014). Accumulation of soluble phenolic compounds is one of the most ubiquitous responses to UV-B radiation (Searles et al., 2001), which is to be expected given the key role played by these compounds in UV-photoprotection (Braun & Tevini, 1993; Mazza et al., 2000). In Arabidopsis, the accumulation of both phenylpropanoids (sinapates) and flavonoids is boosted by UV-B radiation (Li et al., 1993; Landry et al., 1995), in a UVR8-dependent manner (Kliebenstein et al., 2002; Demkura & Ballaré, 2012). Some of these compounds (sinapates) have been shown to mediate the positive effect of UV-B radiation on plant immunity against fungal pathogens (Demkura & Ballaré, 2012). In contrast to the consistent effect of UV-B, the effects of R : FR ratio on levels of soluble leaf phenolics can be quite variable (Table 1), and often not significant. These observations at the metabolite level are totally consistent with our meta-analysis of transcriptome data in Arabidopsis: supplemental UV-B has a robust effect increasing the expression of phenylpropanoid- and flavonoid-related genes, whereas the effects of FR are generally very modest (Fig. 2b,c; Table S3). The effects of UV-B on phenylpropanoid- and flavonoid-related genes are mostly mediated by UVR8 (Fig. S2b,c). Reductions in UV-B radiation and R : FR ratio may have convergent effects repressing JA signaling. Genetic evidence in Arabidopsis and Nicotiana indicates that some of the anti-herbivore effects of solar UV-B are missing in plants impaired in the biosynthesis of bioactive JA (Caputo et al., 2006; Demkura et al., 2010). Solar UV-B can increase JA synthesis or expression of JA biosynthetic genes in Nicotiana spp. (Izaguirre et al., 2003; Ðinh et al., 2012), although this is not always the case (Demkura et al., 2010). In species of the Solanaceae, UV-B increases plant sensitivity to JA for activation of proteinase inhibitors (Stratmann et al., 2000; Demkura et al., 2010). However, this enhancing effect was not detected in Arabidopsis for other markers of the JA response (Demkura & Ballaré, 2012). Available microarray data indicate that UV-B radiation increases the expression of some JA-related genes (Fig. 2d; see also Table S3 and Fig. S1), but this effect appears to be highly dependent on the experimental conditions (Fig. S1xiii–xvi), and to some extent conserved in uvr8 mutants (Fig. S2d). The effects of low R : FR reducing JA sensitivity are very well documented (reviewed in Ballaré, 2014). Transcriptome data in Arabidopsis do not reveal major effects of R : FR ratio on JA-related genes in healthy (non-induced) plants (Fig. 2d), which is consistent with the idea that R : FR regulates JA signaling predominantly by reducing the response to the JA burst produced by the plant in response to herbivory or pathogen attack (Moreno et al., 2009; Cerrudo et al., 2012; De Wit et al., 2013). The effect of low R : FR ratios repressing the induction of JA-dependent genes correlates with the down-regulation of specific metabolites involved in direct (Cargnel et al., 2014) and indirect (Izaguirre et al., 2013; Kegge et al., 2013) defenses. From an ecological point of view, down-regulation of JA responses under conditions of low R : FR and UV-B irradiance is likely to help the plant to redirect resources from defense to rapid elongation, thereby increasing its ability to compete for light. Recent work on the effects of R : FR and UV-B on growth- and defense-related hormonal pathways (Hayes et al., 2014; Leone et al., 2014) can provide important clues to understand the mechanisms by which R : FR and UV-B signals are used by the plant to optimize resource allocation in patchy canopies (Fig. 3). Reduced JA signaling under low R : FR ratios has been attributed to increased stability of JAZ10 (Leone et al., 2014) (and presumably other JAZ proteins – Chico et al., 2014), and increased turnover of DELLA proteins (Leone et al., 2014). JAZs are key repressors of JA signaling (Browse, 2009; Fonseca et al., 2009; Kazan & Manners, 2012), and DELLA proteins, which are key repressors of gibberellin (GA) signaling (Harberd et al., 2009), are known to recruit JAZs into inactive protein complexes (Hou et al., 2010; Yang et al., 2012). Hayes et al. (2014) reported that UV-B supplementation can stabilize DELLAs. Therefore, it is conceivable that changes in DELLA turnover are functionally important not only to define the balance between UV-B and low R : FR in the modulation of growth responses, but also in the regulation of JA signaling and plant immunity in canopies (Fig. 3). UVR8 and phyB cooperatively modulate the balance between growth and defense through both convergent and parallel signaling pathways (Fig. 3). The use of common signaling elements (such as DELLA proteins), provides a simple mechanism to reinforce the response when both photoreceptors sense contingent information (e.g. under deep canopy shade or in the open), or to balance out their effects when they perceive conflicting canopy signals (e.g. during proximity perception). In the latter case, FR reflected by neighboring plants provides the plant with a key warning signal of oncoming competition when light levels are still high (Ballaré et al., 1990). However, because excessive responses to low R : FR may entail fitness costs (Casal et al., 1994; Dorn et al., 2000; McGuire & Agrawal, 2005), moderation of these responses by UVR8 in canopy gaps (Fig. 1) may be ecologically advantageous. In addition, the use of independent signaling pathways may allow for one photoreceptor to dominate the pattern of response. This appears to be the case for accumulation of phenolic sunscreens, where UVR8 has a distinctly dominant role (Table 1; Fig. 2). Since UV-B can penetrate more in leaf canopies than longer wavelengths (Flint & Caldwell, 1998), an overriding role of the UVR8 pathway may induce adaptive UV-B photoprotection even under conditions of low R : FR. The emerging map of interactions between UVR8 and phyB signaling (Fig. 3) is revealing exciting new insights into the mechanisms used by plants to optimize growth and defense plasticity in variable light environments. This research was financially supported by grants from CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas), ANPCyT (Agencia Nacional de Promoción Científica y Tecnológica) and UBACyT (Universidad de Buenos Aires Ciencia y Técnica). The authors thank Amy Austin for helpful discussions and comments on the manuscript and Pablo Rosano for his assistance in the field experiments. Please note: Wiley Blackwell are not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. Fig. S1 Effect of experimental conditions on the response to UV-B radiation for the GO categories discussed in this study. Fig. S2 Effects of UVR8 in the responses to UV-B reported in Fig. 2. Table S1 GO categories (http://geneontology.org/) used in this study Table S2 Microarray experiments used in this study Methods S1 Additional methods on the physiological experiments and microarray meta-analysis. Table S3 Effects of supplemental FR and UV-B on the Arabidopsis transcriptome Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article." @default.
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- W2168989872 date "2015-02-06" @default.
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- W2168989872 title "Photoreceptors <scp>UVR</scp> 8 and phytochrome B cooperate to optimize plant growth and defense in patchy canopies" @default.
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