UV RESISTANCE LOCUS 8–Mediated UV-B Response Is Required Alongside CRYPTOCHROME 1 for Plant Survival in Sunlight under Field Conditions

Abstract

As sessile, photoautotrophic organisms, plants are subjected to fluctuating sunlight that includes potentially detrimental ultraviolet-B radiation (UV-B). 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 impacts on plant fitness remain poorly understood in naturally fluctuating environments. Here we quantified the survival and reproduction of different Arabidopsis mutant genotypes in 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 in natural field conditions, indicating a fitness cost in 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 experiments in field and with supplemental UV-B in growth chambers demonstrated that UV-B caused the conditional cry1 uvr8 lethality phenotype. Using RNA-seq data of field-grown single and double mutants, we explicitly identified genes showing 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.

Photoreceptor–induced sinapate synthesis contributes to photoprotection in Arabidopsis

“…Phytochrome and cryptochrome signalling contribute to UV tolerance (Rai et al, 2019; Tissot and Ulm, 2020; Stockenhuber et al, 2024). In agreement, under prolonged UV exposure, uvr8 mutants are more UV sensitive than wild type, but uvr8 cry1 and uvr8 phyB are even more UV sensitive than uvr8 mutants (Figure 5A) (Tissot and Ulm, 2020).…”

“…UVR8 and cryptochromes act together to ensure plant survival when grown in the field in the presence of UV (Rai et al, 2019; Stockenhuber et al, 2024). However, the extent to which other photoprotective mechanisms activated upon light perception contribute to UV tolerance is not well understood.…”

“…Evidence in Arabidopsis and Chlamydomonas reinhardtii suggests that UVR8 controls an acclimatory response that maintains optimal photosynthetic efficiency under elevated UV-B (Davey et al, 2012; Tilbrook et al, 2016). Recent studies indicate that UVR8 acts in concert with other photoreceptors, mainly cry1, to ensure survival under UV containing sunlight (Morales et al, 2013; Rai et al, 2019; Rai et al, 2020; Tissot and Ulm, 2020; Stockenhuber et al, 2024), but the underlying mechanism has remained enigmatic.…”