Bilins are linear tetrapyrroles used as chromophores of phycobiliproteins and phytochromes for their light-harvesting and light-sensing properties, respectively. Enzymes for their biosynthesis first evolved in cyanobacteria and were subsequently transferred to photosynthetic eukaryotes during endosymbiosis. Although many present day eukaryotic algae lack both phycobiliproteins and phytochromes, as do some cyanobacteria, e.g. prochlorophytes, all oxygenic phototrophs retain a bilin biosynthetic pathway which consists of plastid-localized heme oxygenase (HO/HMOX1) and ferredoxin-dependent biliverdin reductase (FDBR) enzymes. We previously showed that bilins are retrograde signals released from plastids which mitigate oxidative stress during diurnal dark-to-light transitions, and are also required for maintenance of a functional photosynthetic apparatus in diurnal light-dark cycles in the green alga Chlamydomonas reinhardtii. We hypothesize that bilins are needed to sustain sufficient chlorophyll synthesis in light for repair of daily damage to the photosynthetic apparatus. The loss-of-function mutant of CrHMOX1, the enzyme responsible for the formation of biliverdin IXa (BV) from heme in C. reinhardtii, is phenotypically similar to non-lethal mutants in the chlorophyll biosynthesis pathway - all of which bleach under high light. One such mutant affects CrGUN4, which encodes a known positive regulator of Mg-chelatase activity. Our studies show that CrGUN4 can tightly binds bilins, and it can also interact with CrPCYA1 in a bilin-dependent manner. Localized to both thylakoid and stroma, CrPYCA and CrGUN4 are thus well positioned to function as bilin-dependent regulators of chlorophyll synthesis in the presence of both light and oxygen. Since C. reinhardtii lacks phytochromes, ongoing research seeks to identify cytosolic bilin binding proteins that might function as bilin (and/or light) sensors to regulate the diurnal oxidative stress pathway uncovered by our studies.
J. Clark Lagarias is a Distinguished Professor of Biochemistry at the University of California-Davis with degrees in Chemistry and Botany from the University of California-Berkeley. The recipient of the Paul K. and Ruth R. Stumpf Professorship in Plant Biochemistry in 1999, Dr. Lagarias was elected to the National Academy of Academy of Sciences in 2001, one of the highest honors accorded to a scientist or engineer in the United States. Internationally known for his work to understand the molecular basis of plant and cyanobacterial light perception, Lagarias' research interests hold significant potential for improving crop yield and for development of bilin-based fluorescent and optogenetic probes for live cell applications.