An apocarotenoid retrograde signal post-transcriptionally controls protein levels, plastid biogenesis and plant development during extended periods of darkness

Cazzonelli CI1, Hou X2, Alagoz Y1, Rivers J2, Dhami N1, Lee J3, Shashikanth M2 and Pogson B2

  1. Hawkesbury Institute for the Environment, University of Western Sydney, Hawkesbury Campus, Bourke Street, Richmond, NSW AUSTRALIA 2753.
  2. Australian Research Council Centre of Excellence in Plant Energy Biology, College of Medicine, Biology and Environment, Research School of Biology, The Australian National University, Canberra, ACT 26.
  3. Centre for Advanced Microscopy, The Australian National University, Canberra, ACT 2601, Australia.

Cleavage products of cis-carotenes are reported to regulate nuclear gene expression, carotenoid homeostasis and leaf development in plants. Environmental conditions that affect their biosynthesis, their physiological functions and regulatory targets remain unknown. Carotenoid isomerase (crtiso) mutants display various virescent phenotypes depending upon the environmental conditions. Here we demonstrate a physiological link between day length (extended darkness), the accumulation of a cis-carotenes and control over plastid biogenesis. Chemical inhibition of carotenoid cleavage dioxygenase activity restored prolamellar body (PLB) formation crtiso/ccr2 etioplasts during skotomorphogenesis providing evidence for a novel cis-carotene derived apocarotenoid signal (ACS) that controls plastid biogenesis A forward genetic screen identified an epistatic interaction between the ζ-carotene isomerase (ziso-155) and Arabidopsis ccr2 mutants that blocked the biosynthesis of specific cis-carotenes, restored PLB formation in ccr2 etioplasts during skotomorphogenesis, and prevented leaf virescence in plants grown under shorter photoperiod. Transcriptomic analysis of ccr2 ziso-155 mutant tissues revealed down-regulation of repressors of photomorphogenesis and up-regulation of photosynthesis associated nuclear gene (PhANG) expression that correlated with normal plastid development. We next identified a mutation in DEETIOLATED 1 (det1-154) that restored PLB formation in ccr2 and reduced specific cis-carotenes to levels below a threshold that promoted the efficient biogenesis of plastids in plants grown under extended periods of darkness. det1-154 reduced transcription of protochlorophyllide oxidoreductase (POR) and ACS post-transcriptionally maintained POR protein levels. We describe a model whereby a retrograde ACS acts via an alternative signaling pathway downstream of DET1 to post-transcriptionally regulate POR, ELONGATED HYPOCOTYL5 (HY5) and PHYTOCHROME-INTERACTING FACTOR3 (PIF3) thereby coordinating PhANG expression and plastid development during extended periods of darkness.