A role for UV-B -induced DNA damage in photomorphogenic responses in etiolated Arabidopsis seedlings

Abstract

Ultraviolet (UV) radiation is a constituent of sunlight that influences plant morphology and growth. It induces photomorphogenic responses but also causes damage to DNA. Plant responses to DNA damage caused by UV-B light are often categorized as general mechanisms that get activated by other environmental stresses. Photodimers are formed through the direct absorption of UV-B light by DNA and are removed, in part, by nucleotide excision repair (NER). UV-B irradiation resulted in the accumulation of the two most common photodimers, cyclobutane pyrimidine dimers (CPDs) and pyrimidine-(6,4)-pyrimidinone dimers (6,4PPs), in etiolated wild type (wt) <italic>Arabidopsis</italic> seedlings. <italic>Arabidopsis</italic> mutants of the endonucleases that function in NER, <italic>xpf-3</italic> and <italic>uvr1-1</italic>, show hypersensitivity to UV-B (280-320 nm) in terms of hypocotyl growth inhibition. I hypothesized that the accumulation of UV-B-induced photodimers was responsible for the hypocotyl growth phenotype of these NER mutants after UV-B irradiation. It was also predicted that the accumulation of photodimers could ultimately trigger signaling pathways that result in cell-cycle arrest through stalled replication sites or double-strand breaks. This was tested using the <italic><underline>s</underline>uppressor <underline>o</underline>f <underline>g</underline>amma 1</italic> (<italic>sog1-1</italic>) mutant, which lacks a transcription factor responsible for gene induction and cell-cycle arrest after gamma irradiation, and a Col-0 line containing a CYCB1;1-GUS reporter construct. <italic>CYCB1;1</italic> encodes a cyclin that accumulates in response to cell-cycle arrest at the G2/M transition. The main conclusion from this work is that hypocotyl growth inhibition induced by UV-B light in etiolated <italic>Arabidopsis</italic> seedlings, which is a classic photomorphogenic response, is influenced by signals originating from UV-B light absorption by DNA that lead to cell-cycle arrest. Furthermore, this process is shown to occur independently of <italic>UVR8</italic> and its signaling pathway responsible for <italic>CHS</italic> induction. This work also demonstrates that UV-B-induced DNA damage can be responsible for specific photomorphogenic responses, at least in etiolated <italic>Arabidopsis</italic> seedlings, and does not simply induce general stress responses.