How Plants Take the Bad with the Good: Conserved UV-B Perception and Signaling in Chlamydomonas

The sun gives light, but it’s a package deal: Sunlight contains “good” wavelengths that plants can use for photosynthesis, but it also contains “bad” wavelengths that can damage cells. For example, the ozone layer absorbs most UV-B (wavelengths 280 to 315 nm) from sunlight; the remaining UV-B makes up less than 0.5% of the total light energy but can damage DNA and the photosynthetic apparatus. Not surprisingly, in addition to having mechanisms to sense longer, photosynthetically active wavelengths (phytochromes, cryptochromes, etc.), plants have also evolved mechanisms to sense shorter, potentially damaging wavelengths (reviewed in Heijde and Ulm, 2012). UV RESISTANCE LOCUS8 (UVR8) absorbs UV-B light via conserved tryptophan residues (rather than an exogenous chromophore as in other photoreceptors). Absorbing UV-B causes the UVR8 apparent homodimer to dissociate into monomers, which interact with CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1), an E3 ubiquitin ligase (Rizzini et al., 2011). This interaction initiates a transcriptional response that induces genes encoding protective factors such as enzymes in the phenylpropanoid biosynthesis pathway and damage-repair factors such as photolyases. The COP1-UVR8 interaction also induces the expression of negative regulators that interact directly with UVR8 to help it transition back into a homodimer, thus turning off the response and completing the cycle (see figure).

The UVR8 photocycle and UV acclimation in Chlamydomonas. Left: UV-B causes the UVR8 homodimer to dissociate into monomers, which can interact with COP1 to effect changes in gene expression. Right: Acclimation allows Chlamydomonas cells to survive damage by UV-B; acclimation fails in the COP1 mutant hit1. (Reprinted from Tilbrook et al. [2016]; Figures 2C and 7A.)

To examine the evolution of UV-B acclimation responses, Tilbrook et al. (2016) looked at whether the UVR8-COP1 pathway exists in Chlamydomonas reinhardtii. By querying the Chlamydomonas proteome with Arabidopsis thaliana UVR8, they identified a likely ortholog with 45% amino acid sequence identity, including the conserved tryptophan residues, and good predicted structural conservation. Moreover, Chlamydomonas UVR8 undergoes a similar UV-B-dependent monomerization that effects interaction with Chlamydomonas COP1 and even can complement an Arabidopsis uvr8 null mutant.

A conserved UVR8-COP1 UV-B pathway has functional consequences for Chlamydomonas cells. Chlamydomonas cultures grown under low-level UV-B show acclimation: They can survive UV-B stress better than nonacclimated cultures. Acclimated cells also showed less photoinhibition, measured by examining the chlorophyll fluorescence spectrum and the levels of the photosystem II core proteins D1 and D2. This acclimation response does not occur in Chlamydomonas cells of the high light tolerant1 (hit1) mutant line, which carry a mutation in Cr-COP1. The authors also used RNA-sequencing to show that acclimation to UV-B involves large changes to the Chlamydomonas transcriptome, which includes homologs of Arabidopsis genes involved in UV-B signaling and genes encoding stress-related light-harvesting complex proteins.

These observations show that plants have adapted to take the bad with the good, and that photosynthetic cells evolved mechanisms to acclimate to the UV-B radiation present in natural sunlight early in the green lineage. A further intriguing aspect of this work is the conserved role of COP1 in responding to light and possibly in integrating responses to different wavelengths. In addition to interacting with UVR8, in Arabidopsis COP1 also interacts with photoreceptors that respond to longer wavelengths. The evolution and function of the mechanisms producing specific outputs remains an intriguing topic for future research.