Sunlight Brightens Learning and Memory.

Sunlight can alter mood, behavior, and cognition, but the cellular basis of this phenomenon remains to be fully elucidated. In this issue of Cell, Zhu et al. shed light on a UV-dependent metabolic pathway that leads to increased synaptic release of glutamate and enhanced motor learning and memory in mice.

Amazon forest biogeography predicts resilience and vulnerability to drought.

Amazonia contains the most extensive tropical forests on Earth, but Amazon carbon sinks of atmospheric CO2 are declining, as deforestation and climate-change-associated droughts1-4 threaten to push these forests past a tipping point towards collapse5-8. Forests exhibit complex drought responses, indicating both resilience (photosynthetic greening) and vulnerability (browning and tree mortality), that are difficult to explain by climate variation alone9-17. Here we combine remotely sensed photosynthetic indices with ground-measured tree demography to identify mechanisms underlying drought resilience/vulnerability in different intact forest ecotopes18,19 (defined by water-table depth, soil fertility and texture, and vegetation characteristics). In higher-fertility southern Amazonia, drought response was structured by water-table depth, with resilient greening in shallow-water-table forests (where greater water availability heightened response to excess sunlight), contrasting with vulnerability (browning and excess tree mortality) over deeper water tables. Notably, the resilience of shallow-water-table forest weakened as drought lengthened. By contrast, lower-fertility northern Amazonia, with slower-growing but hardier trees (or, alternatively, tall forests, with deep-rooted water access), supported more-drought-resilient forests independent of water-table depth. This functional biogeography of drought response provides a framework for conservation decisions and improved predictions of heterogeneous forest responses to future climate changes, warning that Amazonia's most productive forests are also at greatest risk, and that longer/more frequent droughts are undermining multiple ecohydrological strategies and capacities for Amazon forest resilience.

Hotspot shelters stimulate frog resistance to chytridiomycosis.

Many threats to biodiversity cannot be eliminated; for example, invasive pathogens may be ubiquitous. Chytridiomycosis is a fungal disease that has spread worldwide, driving at least 90 amphibian species to extinction, and severely affecting hundreds of others1-4. Once the disease spreads to a new environment, it is likely to become a permanent part of that ecosystem. To enable coexistence with chytridiomycosis in the field, we devised an intervention that exploits host defences and pathogen vulnerabilities. Here we show that sunlight-heated artificial refugia attract endangered frogs and enable body temperatures high enough to clear infections, and that having recovered in this way, frogs are subsequently resistant to chytridiomycosis even under cool conditions that are optimal for fungal growth. Our results provide a simple, inexpensive and widely applicable strategy to buffer frogs against chytridiomycosis in nature. The refugia are immediately useful for the endangered species we tested and will have broader utility for amphibian species with similar ecologies. Furthermore, our concept could be applied to other wildlife diseases in which differences in host and pathogen physiologies can be exploited. The refugia are made from cheap and readily available materials and therefore could be rapidly adopted by wildlife managers and the public. In summary, habitat protection alone cannot protect species that are affected by invasive diseases, but simple manipulations to microhabitat structure could spell the difference between the extinction and the persistence of endangered amphibians.

Autonomous self-burying seed carriers for aerial seeding.

Aerial seeding can quickly cover large and physically inaccessible areas1 to improve soil quality and scavenge residual nitrogen in agriculture2, and for postfire reforestation3-5 and wildland restoration6,7. However, it suffers from low germination rates, due to the direct exposure of unburied seeds to harsh sunlight, wind and granivorous birds, as well as undesirable air humidity and temperature1,8,9. Here, inspired by Erodium seeds10-14, we design and fabricate self-drilling seed carriers, turning wood veneer into highly stiff (about 4.9 GPa when dry, and about 1.3 GPa when wet) and hygromorphic bending or coiling actuators with an extremely large bending curvature (1,854 m-1), 45 times larger than the values in the literature15-18. Our three-tailed carrier has an 80% drilling success rate on flat land after two triggering cycles, due to the beneficial resting angle (25°-30°) of its tail anchoring, whereas the natural Erodium seed's success rate is 0%. Our carriers can carry payloads of various sizes and contents including biofertilizers and plant seeds as large as those of whitebark pine, which are about 11 mm in length and about 72 mg. We compare data from experiments and numerical simulation to elucidate the curvature transformation and actuation mechanisms to guide the design and optimization of the seed carriers. Our system will improve the effectiveness of aerial seeding to relieve agricultural and environmental stresses, and has potential applications in energy harvesting, soft robotics and sustainable buildings.

Mirusviruses link herpesviruses to giant viruses.

DNA viruses have a major influence on the ecology and evolution of cellular organisms1-4, but their overall diversity and evolutionary trajectories remain elusive5. Here we carried out a phylogeny-guided genome-resolved metagenomic survey of the sunlit oceans and discovered plankton-infecting relatives of herpesviruses that form a putative new phylum dubbed Mirusviricota. The virion morphogenesis module of this large monophyletic clade is typical of viruses from the realm Duplodnaviria6, with multiple components strongly indicating a common ancestry with animal-infecting Herpesvirales. Yet, a substantial fraction of mirusvirus genes, including hallmark transcription machinery genes missing in herpesviruses, are closely related homologues of giant eukaryotic DNA viruses from another viral realm, Varidnaviria. These remarkable chimaeric attributes connecting Mirusviricota to herpesviruses and giant eukaryotic viruses are supported by more than 100 environmental mirusvirus genomes, including a near-complete contiguous genome of 432 kilobases. Moreover, mirusviruses are among the most abundant and active eukaryotic viruses characterized in the sunlit oceans, encoding a diverse array of functions used during the infection of microbial eukaryotes from pole to pole. The prevalence, functional activity, diversification and atypical chimaeric attributes of mirusviruses point to a lasting role of Mirusviricota in the ecology of marine ecosystems and in the evolution of eukaryotic DNA viruses.

Structures of a phycobilisome in light-harvesting and photoprotected states.

Phycobilisome (PBS) structures are elaborate antennae in cyanobacteria and red algae1,2. These large protein complexes capture incident sunlight and transfer the energy through a network of embedded pigment molecules called bilins to the photosynthetic reaction centres. However, light harvesting must also be balanced against the risks of photodamage. A known mode of photoprotection is mediated by orange carotenoid protein (OCP), which binds to PBS when light intensities are high to mediate photoprotective, non-photochemical quenching3-6. Here we use cryogenic electron microscopy to solve four structures of the 6.2 MDa PBS, with and without OCP bound, from the model cyanobacterium Synechocystis sp. PCC 6803. The structures contain a previously undescribed linker protein that binds to the membrane-facing side of PBS. For the unquenched PBS, the structures also reveal three different conformational states of the antenna, two previously unknown. The conformational states result from positional switching of two of the rods and may constitute a new mode of regulation of light harvesting. Only one of the three PBS conformations can bind to OCP, which suggests that not every PBS is equally susceptible to non-photochemical quenching. In the OCP-PBS complex, quenching is achieved through the binding of four 34 kDa OCPs organized as two dimers. The complex reveals the structure of the active form of OCP, in which an approximately 60 Å displacement of its regulatory carboxy terminal domain occurs. Finally, by combining our structure with spectroscopic properties7, we elucidate energy transfer pathways within PBS in both the quenched and light-harvesting states. Collectively, our results provide detailed insights into the biophysical underpinnings of the control of cyanobacterial light harvesting. The data also have implications for bioengineering PBS regulation in natural and artificial light-harvesting systems.

Multiple light signaling pathways control solar tracking in sunflowers.

Sunflowers are famous for their ability to track the sun throughout the day and then reorient at night to face east the following morning. This occurs by differential growth patterns, with the east sides of stems growing more during the day and the west sides of stems growing more at night. This process, termed heliotropism, is generally believed to be a specialized form of phototropism; however, the underlying mechanism is unknown. To better understand heliotropism, we compared gene expression patterns in plants undergoing phototropism in a controlled environment and in plants initiating and maintaining heliotropic growth in the field. We found the expected transcriptome signatures of phototropin-mediated phototropism in sunflower stems bending towards monochromatic blue light. Surprisingly, the expression patterns of these phototropism-regulated genes are quite different in heliotropic plants. Most genes rapidly induced during phototropism display only minor differences in expression across solar tracking stems. However, some genes that are both rapidly induced during phototropism and are implicated in growth responses to foliar shade are rapidly induced on the west sides of stems at the onset of heliotropism, suggesting a possible role for red light photoreceptors in solar tracking. To test the involvement of different photoreceptor signaling pathways in heliotropism, we modulated the light environment of plants initiating solar tracking. We found that depletion of either red and far-red light or blue light did not hinder the initiation or maintenance of heliotropism in the field. Together, our results suggest that the transcriptional regulation of heliotropism is distinct from phototropin-mediated phototropism and likely involves inputs from multiple light signaling pathways.

Chloroplasts in plant cells show active glassy behavior under low-light conditions.

Plants have developed intricate mechanisms to adapt to changing light conditions. Besides phototropism and heliotropism (differential growth toward light and diurnal motion with respect to sunlight, respectively), chloroplast motion acts as a fast mechanism to change the intracellular structure of leaf cells. While chloroplasts move toward the sides of the plant cell to avoid strong light, they accumulate and spread out into a layer on the bottom of the cell at low light to increase the light absorption efficiency. Although the motion of chloroplasts has been studied for over a century, the collective organelle motion leading to light-adapting self-organized structures remains elusive. Here, we study the active motion of chloroplasts under dim-light conditions, leading to an accumulation in a densely packed quasi-2D layer. We observe burst-like rearrangements and show that these dynamics resemble systems close to the glass transition by tracking individual chloroplasts. Furthermore, we provide a minimal mathematical model to uncover relevant system parameters controlling the stability of the dense configuration of chloroplasts. Our study suggests that the meta-stable caging close to the glass transition in the chloroplast monolayer serves a physiological relevance: Chloroplasts remain in a spread-out configuration to increase the light uptake but can easily fluidize when the activity is increased to efficiently rearrange the structure toward an avoidance state. Our research opens questions about the role that dynamical phase transitions could play in self-organized intracellular responses of plant cells toward environmental cues.

Unexpected metabolic rewiring of CO2 fixation in H2-mediated materials-biology hybrids.

A hybrid approach combining water-splitting electrochemistry and H2-oxidizing, CO2-fixing microorganisms offers a viable solution for producing value-added chemicals from sunlight, water, and air. The classic wisdom without thorough examination to date assumes that the electrochemistry in such a H2-mediated process is innocent of altering microbial behavior. Here, we report unexpected metabolic rewiring induced by water-splitting electrochemistry in H2-oxidizing acetogenic bacterium Sporomusa ovata that challenges such a classic view. We found that the planktonic S. ovata is more efficient in utilizing reducing equivalent for ATP generation in the materials-biology hybrids than cells grown with H2 supply, supported by our metabolomic and proteomic studies. The efficiency of utilizing reducing equivalents and fixing CO2 into acetate has increased from less than 80% of chemoautotrophy to more than 95% under electroautotrophic conditions. These observations unravel previously underappreciated materials' impact on microbial metabolism in seemingly simply H2-mediated charge transfer between biotic and abiotic components. Such a deeper understanding of the materials-biology interface will foster advanced design of hybrid systems for sustainable chemical transformation.

A thermal receptor for nonvisual sunlight detection in myriapods.

Organisms from cyanobacteria to humans have evolved a wide array of photoreceptive strategies to detect light. Sunlight avoidance behavior is common in animals without vision or known photosensory genes. While indirect light perception via photothermal conversion is a possible scenario, there is no experimental evidence for this hypothesis. Here, we show a nonvisual and extraocular sunlight detection mechanism by identifying the broad-range thermal receptor 1 (BRTNaC1, temperature range = 33 to 48 °C) in centipede antennae. BRTNaC1, a heat-activated cation-permeable ion channel, is structurally related to members of the epithelial sodium channel family. At the molecular level, heat activation of BRTNaC1 exhibits strong pH dependence controlled by two protonatable sites. Physiologically, temperature-dependent activation of BRTNaC1 upon sunlight exposure comes from a striking photothermal effect on the antennae, where a slightly acidic environment (pH 6.1) of the body fluid leads to the protonation of BRTNaC1 and switches on its high thermal sensitivity. Furthermore, testosterone potently inhibits heat activation of BRTNaC1 and the sunlight avoidance behavior of centipedes. Taken together, our study suggests a sophisticated strategy for nonvisual sunlight detection in myriapods.

Kinetic modeling identifies targets for engineering improved photosynthetic efficiency in potato (Solanum tuberosum cv. Solara).

Potato (Solanum tuberosum) is a significant non-grain food crop in terms of global production. However, its yield potential might be raised by identifying means to release bottlenecks within photosynthetic metabolism, from the capture of solar energy to the synthesis of carbohydrates. Recently, engineered increases in photosynthetic rates in other crops have been directly related to increased yield - how might such increases be achieved in potato? To answer this question, we derived the photosynthetic parameters Vcmax and Jmax to calibrate a kinetic model of leaf metabolism (e-Photosynthesis) for potato. This model was then used to simulate the impact of manipulating the expression of genes and their protein products on carbon assimilation rates in silico through optimizing resource investment among 23 photosynthetic enzymes, predicting increases in photosynthetic CO2 uptake of up to 67%. However, this number of manipulations would not be practical with current technologies. Given a limited practical number of manipulations, the optimization indicated that an increase in amounts of three enzymes - Rubisco, FBP aldolase, and SBPase - would increase net assimilation. Increasing these alone to the levels predicted necessary for optimization increased photosynthetic rate by 28% in potato.

Metal-Organic Frameworks as Photocatalysts for Solar-Driven Overall Water Splitting.

Metal-organic frameworks (MOFs) have been frequently used as photocatalysts for the hydrogen evolution reaction (HER) using sacrificial agents with UV-vis or visible light irradiation. The aim of the present review is to summarize the use of MOFs as solar-driven photocatalysts targeting to overcome the current efficiency limitations in overall water splitting (OWS). Initially, the fundamentals of the photocatalytic OWS under solar irradiation are presented. Then, the different strategies that can be implemented on MOFs to adapt them for solar photocatalysis for OWS are discussed in detail. Later, the most active MOFs reported until now for the solar-driven HER and/or oxygen evolution reaction (OER) are critically commented. These studies are taken as precedents for the discussion of the existing studies on the use of MOFs as photocatalysts for the OWS under visible or sunlight irradiation. The requirements to be met to use MOFs at large scale for the solar-driven OWS are also discussed. The last section of this review provides a summary of the current state of the field and comments on future prospects that could bring MOFs closer to commercial application.

Ancient inhabitants of the Basin of Mexico kept an accurate agricultural calendar using sunrise observatories and mountain alignments.

In the hot dry spring of monsoon-driven environments, keeping an accurate calendar to regulate the annual planting of crops is of critical importance. Before the Spanish conquest, the Basin of Mexico had a highly productive farming system able to feed its very large population. However, how they managed to keep their farming dates in synchrony with the solar year is not known. In this paper, we show that the observation of sunrise against the Basin's eastern horizon could have provided an accurate solar calendar and that some important sunrise landmarks coincide well with the themes of seasonal festivities described in early codices. We also show that a long stone causeway in the summit of Mount Tlaloc aligns perfectly with the rising sun on February 23 to 24, in coincidence with the Basin's new year in the Mexica calendar. Third, we demonstrate that, when viewed from the sacred Mount Tepeyac in the bottom of the Basin, sunrise aligns with Mount Tlaloc also on February 24. The importance of Mount Tlaloc as a calendric landmark seems to be corroborated by illustrations and texts in ancient Mexica codices. Our findings demonstrate that by using carefully developed alignments with the rugged eastern horizon, the inhabitants of the Basin of Mexico were able to adjust their calendar to keep in synchrony with the solar year and successfully plan their corn harvests.

Sunlight can convert atmospheric aerosols into a glassy solid state and modify their environmental impacts.

Secondary organic aerosol (SOA) plays a critical, yet uncertain, role in air quality and climate. Once formed, SOA is transported throughout the atmosphere and is exposed to solar UV light. Information on the viscosity of SOA, and how it may change with solar UV exposure, is needed to accurately predict air quality and climate. However, the effect of solar UV radiation on the viscosity of SOA and the associated implications for air quality and climate predictions is largely unknown. Here, we report the viscosity of SOA after exposure to UV radiation, equivalent to a UV exposure of 6 to 14 d at midlatitudes in summer. Surprisingly, UV-aging led to as much as five orders of magnitude increase in viscosity compared to unirradiated SOA. This increase in viscosity can be rationalized in part by an increase in molecular mass and oxidation of organic molecules constituting the SOA material, as determined by high-resolution mass spectrometry. We demonstrate that UV-aging can lead to an increased abundance of aerosols in the atmosphere in a glassy solid state. Therefore, UV-aging could represent an unrecognized source of nuclei for ice clouds in the atmosphere, with important implications for Earth's energy budget. We also show that UV-aging increases the mixing times within SOA particles by up to five orders of magnitude throughout the troposphere with important implications for predicting the growth, evaporation, and size distribution of SOA, and hence, air pollution and climate.

Flash drought early warning based on the trajectory of solar-induced chlorophyll fluorescence.

Flash drought often leads to devastating effects in multiple sectors and presents a unique challenge for drought early warning due to its sudden onset and rapid intensification. Existing drought monitoring and early warning systems are based on various hydrometeorological variables reaching thresholds of unusually low water content. Here, we propose a flash drought early warning approach based on spaceborne measurements of solar-induced chlorophyll fluorescence (SIF), a proxy of photosynthesis that captures plant response to multiple environmental stressors. Instead of negative SIF anomalies, we focus on the subseasonal trajectory of SIF and consider slower-than-usual increase or faster-than-usual decrease of SIF as an early warning for flash drought onset. To quantify the deviation of SIF trajectory from the climatological norm, we adopt existing formulas for a rapid change index (RCI) and apply the RCI analysis to spatially downscaled 8-d SIF data from GOME-2 during 2007-2018. Using two well-known flash drought events identified by the operational US Drought Monitor (in 2012 and 2017), we show that SIF RCI can produce strong predictive signals of flash drought onset with a lead time of 2 wk to 2 mo and can also predict drought recovery with several weeks of lead time. While SIF RCI shows great early warning potential, its magnitude diminishes after drought onset and therefore cannot reflect the current drought intensity. With its long lead time and direct relevance for agriculture, SIF RCI can support a global early warning system for flash drought and is especially useful over regions with sparse hydrometeorological data.

Evolution of plasticity prevents postinvasion extinction of a native forb.

Exotic plant invaders pose a serious threat to native plants. However, despite showing inferior competitive ability and decreased performance, native species often subsist in invaded communities. The decline of native populations is hypothesized to be halted and eventually reversed if adaptive evolutionary changes can keep up with the environmental stress induced by invaders, that is, when population extinction is prevented by evolutionary rescue (ER). Nevertheless, evidence for the role of ER in postinvasion persistence of native flora remains scarce. Here, I explored the population density of a native forb, Veronica chamaedrys, and evaluated the changes in the shade-responsive traits of its populations distributed along the invasion chronosequence of an exotic transformer, Heracleum mantegazzianum, which was replicated in five areas. I found a U-shaped population trajectory that paralleled the evolution of plasticity to shade. Whereas V. chamaedrys genotypes from intact, more open sites exhibited a shade-tolerance strategy (pronounced leaf area/mass ratio), reduced light availability at the invaded sites selected for a shade-avoidance strategy (greater internode elongation). Field experiments subsequently confirmed that the shifts in shade-response strategies were adaptive and secured postinvasion population persistence, as indicated by further modeling. Alternative ecological mechanisms (habitat improvement or arrival of immigrants) were less likely explanations than ER for the observed population rebound, although the contribution of maternal effects cannot be dismissed. These results suggest that V. chamaedrys survived because of adaptive evolutionary changes operating on the same timescale as the invasion-induced stress, but the generality of ER for postinvasion persistence of native plants remains unknown.

Two light sensors decode moonlight versus sunlight to adjust a plastic circadian/circalunidian clock to moon phase.

Many species synchronize their physiology and behavior to specific hours. It is commonly assumed that sunlight acts as the main entrainment signal for ∼24-h clocks. However, the moon provides similarly regular time information. Consistently, a growing number of studies have reported correlations between diel behavior and lunidian cycles. Yet, mechanistic insight into the possible influences of the moon on ∼24-h timers remains scarce. We have explored the marine bristleworm Platynereis dumerilii to investigate the role of moonlight in the timing of daily behavior. We uncover that moonlight, besides its role in monthly timing, also schedules the exact hour of nocturnal swarming onset to the nights' darkest times. Our work reveals that extended moonlight impacts on a plastic clock that exhibits <24 h (moonlit) or >24 h (no moon) periodicity. Abundance, light sensitivity, and genetic requirement indicate that the Platynereis light receptor molecule r-Opsin1 serves as a receptor that senses moonrise, whereas the cryptochrome protein L-Cry is required to discriminate the proper valence of nocturnal light as either moonlight or sunlight. Comparative experiments in Drosophila suggest that cryptochrome's principle requirement for light valence interpretation is conserved. Its exact biochemical properties differ, however, between species with dissimilar timing ecology. Our work advances the molecular understanding of lunar impact on fundamental rhythmic processes, including those of marine mass spawners endangered by anthropogenic change.

Solar urticaria involves rapid mast cell STAT3 activation and neutrophil recruitment, with FcεRI as an upstream regulator.

BACKGROUND: Solar urticaria is a rare photodermatosis characterized by rapid-onset sunlight-induced urticaria, but its pathophysiology is not well understood. OBJECTIVE: We sought to define cutaneous cellular and molecular events in the evolution of solar urticaria following its initiation by solar-simulated UV radiation (SSR) and compare with healthy controls (HC). METHODS: Cutaneous biopsy specimens were taken from unexposed skin and skin exposed to a single low (physiologic) dose of SSR at 30 minutes, 3 hours, and 24 hours after exposure in 6 patients with solar urticaria and 6 HC. Biopsy specimens were assessed by immunohistochemistry and bulk RNA-sequencing analysis. RESULTS: In solar urticaria specimens, there was enrichment of several innate immune pathways, with striking early involvement of neutrophils, which was not observed in HC. Multiple proinflammatory cytokine and chemokine genes were upregulated (including IL20, IL6, and CXCL8) or identified as upstream regulators (including TNF, IL-1ß, and IFN-γ). IgE and FcεRI were identified as upstream regulators, and phosphorylated signal transducer and activator of transcription 3 expression in mast cells was increased in solar urticaria at 30 minutes and 3 hours after SSR exposure, suggesting a mechanism of mast cell activation. Clinical resolution of solar urticaria by 24 hours mirrored resolution of inflammatory gene signature profiles. Comparison with available datasets of chronic spontaneous urticaria showed transcriptomic similarities relating to immune activation, but several transcripts were identified solely in solar urticaria, including CXCL8 and CSF2/3. CONCLUSIONS: Solar urticaria is characterized by rapid signal transducer and activator of transcription 3 activation in mast cells and involvement of multiple chemotactic and innate inflammatory pathways, with FcεRI engagement indicated as an early event.

Solar ultraviolet radiation exposure, and incidence of childhood acute lymphocytic leukaemia and non-Hodgkin lymphoma in a US population-based dataset.

BACKGROUND: Acute lymphocytic leukaemia (ALL) and non-Hodgkin lymphoma (NHL) are among the commonest types of childhood cancer. Some previous studies suggested that elevated ultraviolet radiation (UVR) exposures increase ALL risk; many more indicate NHL risk is reduced. METHODS: We assessed age<20 ALL/NHL incidence in Surveillance, Epidemiology and End Results data using AVGLO-derived UVR irradiance/cumulative radiant exposure measures, using quasi-likelihood models accounting for underdispersion, adjusted for age, sex, racial/ethnic group and other county-level socioeconomic variables. RESULTS: There were 30,349 cases of ALL and 8062 of NHL, with significant increasing trends of ALL with UVR irradiance (relative risk (RR) = 1.200/mW/cm2 (95% CI 1.060, 1.359, p = 0.0040)), but significant decreasing trends for NHL (RR = 0.646/mW/cm2 (95% CI 0.512, 0.816, p = 0.0002)). There was a borderline-significant increasing trend of ALL with UVR cumulative radiant exposure (RR = 1.444/MJ/cm2 (95% CI 0.949, 2.197, p = 0.0865)), and significant decreasing trends for NHL (RR = 0.284/MJ/cm2 (95% CI 0.166, 0.485, p < 0.0001)). ALL and NHL trend RR is substantially increased among those aged 0-3. All-age trend RRs are most extreme (increasing for ALL, decreasing for NHL) for Hispanics for both UVR measures. CONCLUSIONS: Our more novel finding, of excess UVR-related ALL risk, is consistent with some previous studies, but is not clear-cut, and in need of replication.

UV RESISTANCE LOCUS 8-Mediated UV-B Response Is Required Alongside CRYPTOCHROME 1 for Plant 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.