Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival.
The maintenance of functional chloroplasts in photosynthetic eukaryotes requires real-time coordination of the nuclear and plastid genomes. Tetrapyrroles play a significant role in plastid-to-nucleus retrograde signaling in plants to ensure that nuclear gene expression is attuned to the needs of the chloroplast. Well-known sites of synthesis of chlorophyll for photosynthesis, plant chloroplasts also export heme and heme-derived linear tetrapyrroles (bilins), two critical metabolites respectively required for essential cellular activities and for light sensing by phytochromes. Here we establish that Chlamydomonas reinhardtii, one of many chlorophyte species that lack phytochromes, can synthesize bilins in both plastid and cytosol compartments. Genetic analyses show that both pathways contribute to iron acquisition from extracellular heme, whereas the plastid-localized pathway is essential for light-dependent greening and phototrophic growth. Our discovery of a bilin-dependent nuclear gene network implicates a widespread use of bilins as retrograde signals in oxygenic photosynthetic species. Our studies also suggest that bilins trigger critical metabolic pathways to detoxify molecular oxygen produced by photosynthesis, thereby permitting survival and phototrophic growth during the light period.
Department of Molecular and Cellular Biology, University of California, Davis, CA 95616, USA.
Deqiang
D
Duanmu
David
D
Casero
Rachel M
RM
Dent
Sean
S
Gallaher
Wenqiang
W
Yang
Nathan C
NC
Rockwell
Shelley S
SS
Martin
Matteo
M
Pellegrini
Krishna K
KK
Niyogi
Sabeeha S
SS
Merchant
Arthur R
AR
Grossman
J Clark
JC
Lagarias
D001654:Bile Pigments / Q000378:metabolism*; D001664:Biliverdine / Q000494:pharmacology; D055162:Biocatalysis / Q000187:drug effects / Q000528:radiation effects; D016825:Chlamydomonas reinhardtii / Q000166:cytology / Q000201:enzymology / Q000235:genetics / Q000502:physiology*; D002734:Chlorophyll / Q000378:metabolism; D002736:Chloroplasts / Q000187:drug effects / Q000201:enzymology / Q000528:radiation effects; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant / Q000187:drug effects / Q000528:radiation effects; D053263:Gene Regulatory Networks / Q000187:drug effects / Q000528:radiation effects; D017343:Genes, Plant / Q000235:genetics; D006418:Heme / Q000378:metabolism; D006419:Heme Oxygenase (Decyclizing) / Q000235:genetics / Q000378:metabolism; D007501:Iron / Q000494:pharmacology; D008027:Light; D009154:Mutation / Q000235:genetics; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism; D010641:Phenotype; D052817:Phototrophic Processes / Q000187:drug effects / Q000235:genetics; D052980:Phycobilins / Q000096:biosynthesis; D010798:Phycocyanin / Q000096:biosynthesis; D010858:Pigmentation / Q000187:drug effects / Q000235:genetics / Q000528:radiation effects; D030821:Plants, Genetically Modified; D015398:Signal Transduction / Q000187:drug effects / Q000235:genetics / Q000528:radiation effects; D013347:Subcellular Fractions / Q000187:drug effects / Q000378:metabolism / Q000528:radiation effects
D001654:Bile Pigments; D052980:Phycobilins; D010798:Phycocyanin; D002734:Chlorophyll; C011069:phycocyanobilin; D006418:Heme; D007501:Iron; D010088:Oxidoreductases; D006419:Heme Oxygenase (Decyclizing); D001664:Biliverdine