UV RESISTANCE LOCUS Research Articles

Chromosome-level baobab genome illuminates its evolutionary trajectory and environmental adaptation

Baobab (Adansonia digitata) is a long-lived tree endemic to Africa with economic, ecological, and cultural importance, yet its genomic features are underexplored. Here, we report a chromosome-level reference genome anchored to 42 chromosomes for A. digitata, alongside draft assemblies for a sibling tree, two trees from distinct locations in Africa, and A. za from Madagascar. The baobab genome is uniquely rich in DNA transposons, which make up 33%, while LTR retrotransposons account for 10%. A. digitata experienced whole genome multiplication (WGM) around 30 million years ago (MYA), followed by a second WGM event 3–11 MYA, likely linked to autotetraploidy. Resequencing of 25 trees identify three subpopulations, with gene flow across West Africa distinct from East Africa. Gene enrichment and fixation index (Fst) analyses show baobab retained multiple circadian, flowering, and light-responsive genes, which likely support longevity through the UV RESISTANCE LOCUS 8 (UVR8) pathway. In sum, we provide genomic resources and insights for baobab breeding and conservation.

Nuclear accumulation of rice UV-B photoreceptors is UV-B- and OsCOP1-independent for UV-B responses

In plants, the conserved plant-specific photoreceptor UV RESISTANCE LOCUS 8 (UVR8) perceives ultraviolet-B (UV-B) light and mediates UV-B-induced photomorphogenesis and stress acclimation. In this study, we reveal that UV-B light treatment shortens seedlings, increases stem thickness, and enhances UV-B stress tolerance in rice (Oryza sativa) via its two UV-B photoreceptors OsUVR8a and OsUVR8b. Although the rice and Arabidopsis (Arabidopsis thaliana) UVR8 (AtUVR8) photoreceptors all form monomers in response to UV-B light, OsUVR8a, and OsUVR8b function is only partially conserved with respect to AtUVR8 in UV-B-induced photomorphogenesis and stress acclimation. UV-B light and CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) promote the nuclear accumulation of AtUVR8; by contrast, OsUVR8a and OsUVR8b constitutively localize to the nucleus via their own nuclear localization signals, independently of UV-B light and the RING-finger mutation of OsCOP1. We show that OsCOP1 negatively regulates UV-B responses, and shows weak interaction with OsUVR8s, which is ascribed to the N terminus of OsCOP1, which is conserved in several monocots. Furthermore, transcriptome analysis demonstrates that UV-B-responsive gene expression differs globally between Arabidopsis and rice, illuminating the evolutionary divergence of UV-B light signaling pathways between monocot and dicot plants.

OsUVR8b, rather than OsUVR8a, plays a predominant role in rice UVR8-mediated UV-B response.

UV RESISTANCE LOCUS 8 (UVR8) has been identified in Arabidopsis thaliana as the receptor mediating responses to UV-B radiation. However, UVR8-mediated UV-B signaling pathways in rice, which possesses two proteins (UVR8a and UVR8b) with high identities to AtUVR8, remain largely unknown. Here, UVR8a/b were found to be predominantly expressed in rice leaves and leaf sheaths, while the levels of UVR8b transcript and UVR8b protein were both higher than those of UVR8a. Compared to wild-type (WT) plants, uvr8b and uvr8a uvr8b rice mutants exposed to UV-B showed reduced UV-B-induced growth inhibition and upregulation of CHS and HY5 transcripts alongside UV-B acclimation. However, uvr8a mutant was similar to WT plants and exhibited changes comparable with WT. Overexpressing OsUVR8a/b enhanced UV-B-induced growth inhibition and acclimation to UV-B. UV-B was able to enhance the interaction between E3 ubiquitin ligase OsCOP1 and OsUVR8a/b, whereas the interaction of the homologous protein of Arabidopsis REPRESSOR OF UV-B PHOTOMORPHOGENESIS2 (AtRUP2) in rice with OsUVR8a/b was independent of UV-B. Additionally, OsUVR8a/b proteins were also found in the nucleus and cytoplasm even in the absence of UV-B. The abundance of OsUVR8 monomer showed an invisible change in the leaves of rice seedlings transferred from white light to that supplemented with UV-B, even though UV-B was able to weaken the interactions between OsUVR8a and OsUVR8b homo and heterodimers. Therefore, both OsUVR8a and OsUVR8b, which have different localization and response patterns compared with AtUVR8, function in the response of rice to UV-B radiation, whereas OsUVR8b plays a predominant role in this process.

A synchronized, large-scale field experiment using Arabidopsis thaliana reveals the significance of the UV-B photoreceptor UVR8 under natural conditions.

This study determines the functional role of the plant ultraviolet-B radiation (UV-B) photoreceptor, UV RESISTANCE LOCUS 8 (UVR8) under natural conditions using a large-scale 'synchronized-genetic-perturbation-field-experiment'. Laboratory experiments have demonstrated a role for UVR8 in UV-B responses but do not reflect the complexity of outdoor conditions where 'genotype × environment' interactions can mask laboratory-observed responses. Arabidopsis thaliana knockout mutant, uvr8-7, and the corresponding Wassilewskija wild type, were sown outdoors on the same date at 21 locations across Europe, ranging from 39°N to 67°N latitude. Growth and climatic data were monitored until bolting. At the onset of bolting, rosette size, dry weight, and phenolics and glucosinolates were quantified. The uvr8-7 mutant developed a larger rosette and contained less kaempferol glycosides, quercetin glycosides and hydroxycinnamic acid derivatives than the wild type across all locations, demonstrating a role for UVR8 under field conditions. UV effects on rosette size and kaempferol glycoside content were UVR8 dependent, but independent of latitude. In contrast, differences between wild type and uvr8-7 in total quercetin glycosides, and the quercetin-to-kaempferol ratio decreased with increasing latitude, that is, a more variable UV response. Thus, the large-scale synchronized approach applied demonstrates a location-dependent functional role of UVR8 under natural conditions.

UVR8-TCP4-LOX2 module regulates UV-B tolerance in Arabidopsis.

The phytohormone jasmonate (JA) coordinates stress and growth responses to increase plant survival in unfavorable environments. Although JA can enhance plant UV-B stress tolerance, the mechanisms underlying the interaction of UV-B and JA in this response remain unknown. In this study, we demonstrate that the UV RESISTANCE LOCUS 8 - TEOSINTE BRANCHED1, Cycloidea and PCF 4 - LIPOXYGENASE2 (UVR8-TCP4-LOX2) module regulates UV-B tolerance dependent on JA signaling pathway in Arabidopsis thaliana. We show that the nucleus-localized UVR8 physically interacts with TCP4 to increase the DNA-binding activity of TCP4 and upregulate the JA biosynthesis gene LOX2. Furthermore, UVR8 activates the expression of LOX2 in a TCP4-dependent manner. Our genetic analysis also provides evidence that TCP4 acts downstream of UVR8 and upstream of LOX2 to mediate plant responses to UV-B stress. Our results illustrate that the UV-B-dependent interaction of UVR8 and TCP4 serves as an important UVR8-TCP4-LOX2 module, which integrates UV-B radiation and JA signaling and represents a new UVR8 signaling mechanism in plants.

Phosphorylation of Arabidopsis UVR8 photoreceptor modulates protein interactions and responses to UV-B radiation

Exposure of plants to ultraviolet-B (UV-B) radiation initiates transcriptional responses that modify metabolism, physiology and development to enhance viability in sunlight. Many of these regulatory responses to UV-B radiation are mediated by the photoreceptor UV RESISTANCE LOCUS 8 (UVR8). Following photoreception, UVR8 interacts directly with multiple proteins to regulate gene expression, but the mechanisms that control differential protein binding to initiate distinct responses are unknown. Here we show that UVR8 is phosphorylated at several sites and that UV-B stimulates phosphorylation at Serine 402. Site-directed mutagenesis to mimic Serine 402 phosphorylation promotes binding of UVR8 to REPRESSOR OF UV-B PHOTOMORPHOGENESIS (RUP) proteins, which negatively regulate UVR8 action. Complementation of the uvr8 mutant with phosphonull or phosphomimetic variants suggests that phosphorylation of Serine 402 modifies UVR8 activity and promotes flavonoid biosynthesis, a key UV-B-stimulated response that enhances plant protection and crop nutritional quality. This research provides a basis to understand how UVR8 interacts differentially with effector proteins to regulate plant responses to UV-B radiation.

Functional divergence of Arabidopsis REPRESSOR OF UV-B PHOTOMORPHOGENESIS 1 and 2 in repression of flowering.

Photoperiodic plants coordinate the timing of flowering with seasonal light cues, thereby optimizing their sexual reproductive success. The WD40-repeat protein REPRESSOR OF UV-B PHOTOMORPHOGENESIS 2 (RUP2) functions as a potent repressor of UV RESISTANCE LOCUS 8 (UVR8) photoreceptor-mediated UV-B induction of flowering under noninductive, short-day conditions in Arabidopsis (Arabidopsis thaliana); however, in contrast, the closely related RUP1 seems to play no major role. Here, analysis of chimeric ProRUP1:RUP2 and ProRUP2:RUP1 expression lines suggested that the distinct functions of RUP1 and RUP2 in repressing flowering are due to differences in both their coding and regulatory DNA sequences. Artificial altered expression using tissue-specific promoters indicated that RUP2 functions in repressing flowering when expressed in mesophyll and phloem companion cells, whereas RUP1 functions only when expressed in phloem companion cells. Endogenous RUP1 expression in vascular tissue was quantified as lower than that of RUP2, likely underlying the functional difference between RUP1 and RUP2 in repressing flowering. Taken together, our findings highlight the importance of phloem vasculature expression of RUP2 in repressing flowering under short days and identify a basis for the functional divergence of Arabidopsis RUP1 and RUP2 in regulating flowering time.

Nitric oxide is a key part of the UV-B-induced photomorphogenesis in Arabidopsis

Ultraviolet- B (UV-B) radiation exerts a dual effect on plants. While high doses induce stress, lower doses act as a signal. The sensing of UV-B triggers a photomorphogenic response, causing changes like the hypocotyl shortening. This response is strongly regulated by the UV-B photoreceptor UV RESISTANCE LOCUS 8 (UVR8). Although nitric oxide (NO) was proven to inhibit hypocotyl elongation in Arabidopsis thaliana, its role in UV-B-induced photomorphogenesis remains unclear. By using the NO probe DAF-FM DA, we found that UV-B radiation induced the accumulation of NO in the hypocotyl. This event is dependent on the presence of UVR8. Moreover, the NO donor S-nitrosoglutathione (GSNO), restored the WT phenotype when the Arabidopsis line lacking UVR8 was grown in the presence of UV-B. Also, we found that DELLA proteins were necessary for GSNO sensing in UV-B-induced photomorphogenesis. We showed that, through DELLAs, GSNO negatively controlled the levels of gibberellin (GA) bioprocessing-related genes. Therefore, a downregulation of GA signaling by NO is proposed. On the other hand, GSNO supplementation before UV-B treatment inhibited the induction of genes of the UVR8 signaling pathway: HY5, CHS, and PHR1. This resulted in augmented DNA damage in short exposure to UV-B scenarios. Altogether, these results point to a complex regulation by NO of the UV-B-induced photomorphogenesis.

UV RESISTANCE LOCUS 8-Mediated UV-B Response Is Required Alongside CRYPTOCHROME 1 forPlant Survival in Sunlight under Field Conditions.

As sessile, photoautotrophic organisms, plants are subjected to fluctuating sunlight that includes potentially detrimental ultraviolet-B (UV-B) radiation. Experiments under controlled conditions have shown that the UV-B photoreceptor UV RESISTANCE LOCUS 8 (UVR8) controls acclimation and tolerance to UV-B in Arabidopsis thaliana; however, its long-term impact on plant fitness under naturally fluctuating environments remain poorly understood. Here, we quantified the survival and reproduction of different Arabidopsis mutant genotypes under diverse field and laboratory conditions. We found that uvr8 mutants produced more fruits than wild type when grown in growth chambers under artificial low-UV-B conditions but not under natural field conditions, indicating a fitness cost in the absence of UV-B stress. Importantly, independent double mutants of UVR8 and the blue light photoreceptor gene CRYPTOCHROME 1 (CRY1) in two genetic backgrounds showed a drastic reduction in fitness in the field. Experiments with UV-B attenuation in the field and with supplemental UV-B in growth chambers demonstrated that UV-B caused the cry1 uvr8 conditional lethal phenotype. Using RNA-seq data of field-grown single and double mutants, we explicitly identified genes showing significant statistical interaction of UVR8 and CRY1 mutations in the presence of UV-B in the field. They were enriched in Gene Ontology categories related to oxidative stress, photoprotection and DNA damage repair in addition to UV-B response. Our study demonstrates the functional importance of the UVR8-mediated response across life stages in natura, which is partially redundant with that of cry1. Moreover, these data provide an integral picture of gene expression associated with plant responses under field conditions.

Overexpression of Brassica napus COMT1 in Arabidopsis heightens UV-B-mediated resistance to Plutella xylostella herbivory.

UV-B radiation regulates numerous morphogenic, biochemical and physiological responses in plants, and can stimulate some responses typically associated with other abiotic and biotic stimuli, including invertebrate herbivory. Removal of UV-B from the growing environment of various plant species has been found to increase their susceptibility to consumption by invertebrate pests, however, to date, little research has been conducted to investigate the effects of UV-B on crop susceptibility to field pests. Here, we report findings from a multi-omic and genetic-based study investigating the mechanisms of UV-B-stimulated resistance of the crop, Brassica napus (oilseed rape), to herbivory from an economically important lepidopteran specialist of the Brassicaceae, Plutella xylostella (diamondback moth). The UV-B photoreceptor, UV RESISTANCE LOCUS 8 (UVR8), was not found to mediate resistance to this pest. RNA-Seq and untargeted metabolomics identified components of the sinapate/lignin biosynthetic pathway that were similarly regulated by UV-B and herbivory. Arabidopsis mutants in genes encoding two enzymes in the sinapate/lignin biosynthetic pathway, CAFFEATE O-METHYLTRANSFERASE 1 (COMT1) and ELICITOR-ACTIVATED GENE 3-2 (ELI3-2), retained UV-B-mediated resistance to P. xylostella herbivory. However, the overexpression of B. napus COMT1 in Arabidopsis further reduced plant susceptibility to P. xylostella herbivory in a UV-B-dependent manner. These findings demonstrate that overexpression of a component of the sinapate/lignin biosynthetic pathway in a member of the Brassicaceae can enhance UV-B-stimulated resistance to herbivory from P. xylostella.

ELONGATED HYPOCOTYL5 (HY5) and HY5 HOMOLOGUE (HYH) maintain shade avoidance suppression in UV-B.

Reductions in red to far-red ratio (R:FR) provide plants with an unambiguous signal of vegetational shade and are monitored by phytochrome photoreceptors. Plants integrate this information with other environmental cues to determine the proximity and density of encroaching vegetation. Shade-sensitive species respond to reductions in R:FR by initiating a suite of developmental adaptations termed shade avoidance. These include the elongation of stems to facilitate light foraging. Hypocotyl elongation is driven by increased auxin biosynthesis promoted by PHYTOCHROME INTERACTING FACTORs (PIF) 4, 5 and 7. UV-B perceived by the UV RESISTANCE LOCUS 8 (UVR8) photoreceptor rapidly inhibits shade avoidance, in part by suppressing PIF4/5 transcript accumulation and destabilising PIF4/5 protein. Here, we show that longer-term inhibition of shade avoidance is sustained by ELONGATED HYPOCOTYL 5 (HY5) and HY5 HOMOLOGUE (HYH), which regulate transcriptional reprogramming of genes involved in hormone signalling and cell wall modification. HY5 and HYH are elevated in UV-B and suppress the expression of XYLOGLUCAN ENDOTRANSGLUCOSYLASE/HYDROLASE (XTH) genes involved in cell wall loosening. They additionally increase expression GA2-OXIDASE1 (GA2ox1) and GA2ox2, encoding gibberellin catabolism enzymes that act redundantly to stabilise the PIF-inhibiting DELLA proteins. UVR8 therefore regulates temporally distinct signalling pathways to first rapidly inhibit and subsequently maintain suppression of shade avoidance following UV-B exposure.

UV-B-induced modulation of constitutive heterochromatin content in Arabidopsis thaliana.

Sunlight regulates transcriptional programs and triggers the shaping of the genome throughout plant development. Among the different sunlight wavelengths that reach the surface of the Earth, UV-B (280-315nm) controls the expression of hundreds of genes for the photomorphogenic responses and also induces the formation of photodamage that interfere with genome integrity and transcriptional programs. The combination of cytogenetics and deep-learning-based analyses allowed determining the location of UV-B-induced photoproducts and quantifying the effects of UV-B irradiation on constitutive heterochromatin content in different Arabidopsis natural variants acclimated to various UV-B regimes. We identified that UV-B-induced photolesions are enriched within chromocenters. Furthermore, we uncovered that UV-B irradiation promotes constitutive heterochromatin dynamics that differs among the Arabidopsis ecotypes having divergent heterochromatin contents. Finally, we identified that the proper restoration of the chromocenter shape, upon DNA repair, relies on the UV-B photoreceptor, UV RESISTANCE LOCUS 8 (UVR8). These findings shed the light on the effect of UV-B exposure and perception in the modulation of constitutive heterochromatin content in Arabidopsis thaliana.

Interaction between UV-B and plant anthocyanins.

UV-B is an important light condition for inducing anthocyanin synthesis in plants. Plants have corresponding photoreceptors such as UV RESISTANCE LOCUS8 (UVR8) and transduce light signals to the nucleus, which regulate the expression of structural and regulatory genes for anthocyanin synthesis through members such as ELONGATED HYPOCOTYL 5 (HY5), thereby increasing or decreasing anthocyanin accumulation. At the same time, excessive UV-B irradiation (artificial light experiments or extreme environmental conditions) is a light stress for plants, which can damage plants and cause DNA damage or even cell death and other adverse effects. In addition, the effect of UV-B on anthocyanin accumulation in plants is usually combined with other abiotic factors, including other wavelengths of light, water deficit conditions, high or low temperatures, and heavy metal ions, all of which cause plants to change their anthocyanin accumulation in time to adapt to variable survival conditions. The review aims to bring together our understanding of the interactions between UV-B and anthocyanins, which can help further the development of the anthocyanin industry.

Mechanisms of UV-B light-induced photoreceptor UVR8 nuclear localization dynamics.

Light regulates the subcellular localization of plant photoreceptors, a key step in light signaling. Ultraviolet-B radiation (UV-B) induces the plant photoreceptor UV RESISTANCE LOCUS 8 (UVR8) nuclear accumulation, where it regulates photomorphogenesis. However, the molecular mechanism for the UV-B-regulated UVR8 nuclear localization dynamics is unknown. With fluorescence recovery after photobleaching (FRAP), cell fractionation followed by immunoblotting and co-immunoprecipitation (Co-IP) assays we tested the function of UVR8-interacting proteins including CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1), REPRESSOR OF UV-B PHOTOMORPHOGENESIS 1 (RUP1) and RUP2 in the regulation of UVR8 nuclear dynamics in Arabidopsis thaliana. We showed that UV-B-induced rapid UVR8 nuclear translocation is independent of COP1, which previously was shown to be required for UV-B-induced UVR8 nuclear accumulation. Instead, we provide evidence that the UV-B-induced UVR8 homodimer-to-monomer photo-switch and the concurrent size reduction of UVR8 enables its monomer nuclear translocation, most likely via free diffusion. Nuclear COP1 interacts with UV-B-activated UVR8 monomer, thereby promoting UVR8 nuclear retention. Conversely, RUP1and RUP2, whose expressions are induced by UV-B, inhibit UVR8 nuclear retention via attenuating the UVR8-COP1 interaction, allowing UVR8 to exit the nucleus. Collectively, our data suggest that UV-B-induced monomerization of UVR8 promotes its nuclear translocation via free diffusion. In the nucleus, COP1 binding promotes UVR8 monomer nuclear retention, which is counterbalanced by the major negative regulators RUP1 and RUP2.

RUP2 facilitates UVR8 redimerization via two interfaces

The plant UV-B photoreceptor UV RESISTANCE LOCUS 8 (UVR8) exists as a homodimer in its inactive ground state. Upon UV-B exposure, UVR8 monomerizes and interacts with a downstream key regulator, the CONSTITUTIVE PHOTOMORPHOGENIC 1/SUPPRESSOR OF PHYA (COP1/SPA) E3 ubiquitin ligase complex, to initiate UV-B signaling. Two WD40 proteins, REPRESSOR OF UV-B PHOTOMORPHOGENESIS 1 (RUP1) and RUP2 directly interact with monomeric UVR8 and facilitate UVR8 ground state reversion, completing the UVR8 photocycle. Here, we reconstituted the RUP-mediated UVR8 redimerization process in vitro and reported the structure of the RUP2-UVR8W285A complex (2.0 Å). RUP2 and UVR8W285A formed a heterodimer via two distinct interfaces, designated Interface 1 and 2. The previously characterized Interface 1 is found between the RUP2 WD40 domain and the UVR8 C27 subregion. The newly identified Interface 2 is formed through interactions between the RUP2 WD40 domain and the UVR8 core domain. Disruption of Interface 2 impaired UV-B induced photomorphogenic development in Arabidopsis thaliana. Further biochemical analysis indicated that both interfaces are important for RUP2-UVR8 interactions and RUP2-mediated facilitation of UVR8 redimerization. Our findings suggest that the two-interface-interaction mode is adopted by both RUP2 and COP1 when they interact with UVR8, marking a step forward in understanding the molecular basis that underpins the interactions between UVR8 and its photocycle regulators.

Phylogenomics-Based Reconstruction and Molecular Evolutionary Histories of Brassica Photoreceptor Gene Families.

Photosensory proteins known as photoreceptors (PHRs) are crucial for delineating light environments in synchronization with other environmental cues and regulating their physiological variables in plants. However, this has not been well studied in the Brassica genus, which includes several important agricultural and horticultural crops. Herein, we identified five major PHR gene families—phytochrome (PHY), cryptochrome (CRY), phototropin (PHOT), F-box containing flavin binding proteins (ZTL/FKF1/LKP2), and UV RESISTANCE LOCUS 8 (UVR8)—genomic scales and classified them into subfamilies based on their phylogenetic clustering with Arabidopsis homologues. The molecular evolution characteristics of Brassica PHR members indicated indirect expansion and lost one to six gene copies at subfamily levels. The segmental duplication was possibly the driving force of the evolution and amplification of Brassica PHRs. Gene replication retention and gene loss events of CRY, PHY, and PHOT members found in diploid progenitors were highly conserved in their tetraploid hybrids. However, hybridization events were attributed to quantitative changes in UVR8 and ZTL/FKF1/LKP2 members. All PHR members underwent purifying selection. In addition, the transcript expression profiles of PHR genes in different tissue and in response to exogenous ABA, and abiotic stress conditions suggested their multiple biological significance. This study is helpful in understanding the molecular evolution characteristics of Brassica PHRs and lays the foundation for their functional characterization.

Cysteines have a role in conformation of the UVR8 photoreceptor.

SUMMARYThe UV RESISTANCE LOCUS 8 (UVR8) photoreceptor mediates plant responses to Ultraviolet‐B (UV‐B) wavelengths. The UVR8 dimer dissociates into monomers following UV‐B photoreception, a process accompanied by conformational changes that facilitate interaction of UVR8 with proteins that initiate responses. However, the importance of particular amino acids in maintaining UVR8 conformation and modulating protein interactions is poorly understood. Here we examine the roles of cysteine amino acids C231 and C335 in UVR8 structure and function. UVR8C231S,C335S mutant protein forms dimers and monomerizes similarly to wild‐type UVR8. UVR8C231S,C335S interacts with CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) in plants to initiate photomorphogenic responses to UV‐B, although the interaction is weaker when examined in yeast two‐hybrid assays. Similarly, the interaction of UVR8C231S,C335S with REPRESSOR OF UV‐B PHOTOMORPHOGENESIS (RUP) proteins is weaker in both plants and yeast compared with wild‐type UVR8. Re‐dimerization of UVR8 in plants, which is mediated by RUP proteins, occurs with reduced efficiency in UVR8C231S,C335S. Fluorescence resonance energy transfer analysis indicates that UVR8C231S,C335S has an altered conformation in plants, in that the N‐ and C‐termini appear closer together, which may explain the altered protein interactions.

Arabidopsis B-box transcription factors BBX20-22 promote UVR8 photoreceptor-mediated UV-B responses.

SUMMARYPlants undergo photomorphogenic development in the presence of light. Photomorphogenesis is repressed by the E3 ubiquitin ligase CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1), which binds to substrates through their valine–proline (VP) motifs. The UV RESISTANCE LOCUS 8 (UVR8) photoreceptor senses UV‐B and inhibits COP1 through the cooperative binding of its own VP motif and photosensing core to COP1, thereby preventing COP1 binding to substrates, including the basic leucine zipper (bZIP) transcriptional regulator ELONGATED HYPOCOTYL 5 (HY5). As a key promoter of visible light and UV‐B photomorphogenesis, HY5 requires coregulators for its function. The B‐box family transcription factors BBX20–BBX22 were recently described as HY5 rate‐limiting coactivators under red light, but their role in UVR8 signaling was unknown. Here we describe a hypermorphic bbx21‐3D mutant with enhanced photomorphogenesis, carrying a proline‐to‐leucine mutation at position 314 in the VP motif that impairs the interaction with and regulation by COP1. We show that BBX21 and BBX22 are UVR8‐dependently stabilized after UV‐B exposure, which is counteracted by a repressor induced by HY5/BBX activity. bbx20 bbx21 bbx22 mutants under UV‐B are impaired in hypocotyl growth inhibition, photoprotective pigment accumulation and the expression of several HY5‐dependent genes under continuous UV‐B, but the immediate induction of marker genes after exposure to UV‐B remains surprisingly rather unaffected. We conclude that BBX20–BBX22 contribute to HY5 activity in a subset of UV‐B responses, but that additional, presently unknown, coactivators for HY5 are functional in early UVR8 signaling.

Transcription factors BBX11 and HY5 interdependently regulate the molecular and metabolic responses to UV-B.

UV-B radiation acts as a developmental cue and a stress factor for plants, depending on dose. Activation of the transcription factor ELONGATED HYPOCOTYL 5 (HY5) in a UV RESISTANCE LOCUS 8 (UVR8)-dependent manner leads to the induction of a broad set of genes under UV-B. However, the underlying molecular mechanisms regulating this process are less understood. Here, we use molecular, biochemical, genetic, and metabolomic tools to identify the B-BOX transcription factor B-BOX PROTEIN 11 (BBX11) as a component of the molecular response to UV-B in Arabidopsis (Arabidopsis thaliana). BBX11 expression is induced by UV-B in a dose-dependent manner. Under low UV-B, BBX11 regulates hypocotyl growth suppression, whereas it protects plants exposed to high UV-B radiation by promoting the accumulation of photo-protective phenolics and antioxidants, and inducing DNA repair genes. Our genetic studies indicate that BBX11 regulates hypocotyl elongation under UV-B partially dependent on HY5. Overexpression of BBX11 can partially rescue the high UV-B sensitivity of hy5, suggesting that HY5-mediated UV-B stress tolerance is partially dependent on BBX11. HY5 regulates the UV-B-mediated induction of BBX11 by directly binding to its promoter. BBX11 reciprocally regulates the mRNA and protein levels of HY5. We report here the role of a BBX11-HY5 feedback loop in regulating photomorphogenesis and stress tolerance under UV-B.

Transcriptome and metabolome analyses revealed that narrowband 280 and 310\xa0nm UV-B induce distinctive responses in Arabidopsis

In plants, the UV-B photoreceptor UV RESISTANCE LOCUS8 (UVR8) perceives UV-B and induces UV-B responses. UVR8 absorbs a range of UV-B (260–335 nm). However, the responsiveness of plants to each UV-B wavelength has not been intensively studied so far. Here, we performed transcriptome and metabolome analyses of Arabidopsis using UV light emitting diodes (LEDs) with peak wavelengths of 280 and 310 nm to investigate the differences in the wavelength-specific UV-B responses. Irradiation with both UV-LEDs induced gene expression of the transcription factor ELONGATED HYPOCOTYL 5 (HY5), which has a central role in the UVR8 signaling pathway. However, the overall transcriptomic and metabolic responses to 280 and 310 nm UV-LED irradiation were different. Most of the known UV-B-responsive genes, such as defense-related genes, responded only to 280 nm UV-LED irradiation. Lipids, polyamines and organic acids were the metabolites most affected by 280 nm UV-LED irradiation, whereas the effect of 310 nm UV-LED irradiation on the metabolome was considerably less. Enzymatic genes involved in the phenylpropanoid pathway upstream in anthocyanin biosynthesis were up-regulated only by 280 nm UV-LED irradiation. These results revealed that the responsivenesses of Arabidopsis to 280 and 310 nm UV-B were significantly different, suggesting that UV-B signaling is mediated by more complex pathways than the current model.