Chemodiverse cell system responses to UV in an algal sister of land plants.

Abstract

Plant terrestrialization necessitated overcoming a barrage of stressors.¹ Embryophytes (land plants) use an integrated response network to adjust their molecular physiology in response to terrestrial stressors²-one of the important stressors is UV irradiance. The zygnematophytes are the closest streptophyte algal relatives of embryophytes,^3,4,5,6 renowned for their UV resilience^7,8,9 and key for inferring the UV response toolkit of the earliest embryophytes.^10,11 Throughout evolution, specialized metabolism radiated, yielding chemodiverse responses to environmental challenges^12,13,14,15 ranging from UV-shielding flavonoids and coumarins to the polymer lignin of tracheophytes¹⁶; homologs of the underpinning core pathway occur in streptophyte algae.¹⁷ Here, we exposed the zygnematophyte Mesotaenium to UV-B irradiation and profiled its physiological, morphological, transcriptomic, and metabolomic features. After UV-B exposure, the cells showed rapid photophysiological responses and progressively growing terminal vacuoles. Our transcriptome data capture dynamic changes in gene expression in (1) core downstream homologs of phenol metabolic enzymes, photophysiological homeostats, and DNA repair factors and (2) upstream components featuring key homologs of kinase-mediated signaling cascades, as well as light quality and abscisic acid-mediated signaling components. To scrutinize the acclimatory chassis, we created a metabolite feature database specifically for the Mesotaenium metabolome. The metabolome displayed pronounced temporal shifts, with several phenolic features that accumulate along the UV-stress-acclimation kinetics. Overall, we capture chemodiverse responses, including various phenolics such as methoxypsoralen-like derivatives and coumarins. We establish an integrated model for UV responses in the closest algal relatives of embryophytes, illuminating the toolkit that allowed the progenitors of embryophytes to move out of a protective water column.