Abstract
The assembly of photosynthetically competent chloroplasts occurs in angiosperm seedlings when first exposed to light, and is due to the control by light of photosynthesis-associated nuclear genes (PhANGs), also dependent upon plastid-to-nucleus “biogenic” communication signals. The relationship between light- and plastid signal-regulation of PhANGs is close but poorly understood. In contrast, many conifers green in the dark and the promoter of a pine PhANG, Lhcb, is active in the dark in tobacco. Here, we show that the activity of this promoter in tobacco is sensitive to plastid photobleaching, or to the inhibition of plastid translation in the light or the dark, and the same interventions reduce expression of the native gene in pine seedlings, demonstrating classic plastid biogenic signaling in gymnosperms. Furthermore, Arabidopsis mutations causing defective plastid biogenesis suppress the effect in darkness of mutations in COP1 and DET1, repressors of photomorphogenesis, for the expression of several PhANGs but not a photosynthesis-unrelated, light-regulated gene. GLK transcriptional regulators mediate the response of LHCB but not of other tested PhANGs. We propose the ability to suppress PhANG response to positive plastid biogenic signals in the dark may have contributed to the evolution of light-controlled chloroplast biogenesis.
Highlights
The development of flowering plant chloroplasts occurs in the light, and involves the expression of 1000s of genes encoded in the nucleus, the import of their products into developing plastids, as well as the expression of ca. 120 protein and RNA-encoding genes by the genome of the chloroplast itself (Waters and Langdale, 2009; Jarvis and López-Juez, 2013)
The study by Kojima et al (1994) described a small degree of light responsiveness of the pine Lhcb promoter in tobacco seedlings, which could be attributed to developmental effects as it could be observed in control lines with a constitutive reporter driven by the 35S promoter
We examined the response of the pine promoter to plastid signals, both those revealed by photooxidative damage that follows carotenoid synthesis inhibition by norflurazon, and those dependent on plastid translation which is blocked by the antibiotic lincomycin (Figure 2, with blot quantitation in Supplementary Figure S1)
Summary
The development of flowering plant chloroplasts occurs in the light, and involves the expression of 1000s of genes encoded in the nucleus, the import of their products into developing plastids, as well as the expression of ca. 120 protein and RNA-encoding genes by the genome of the chloroplast itself (Waters and Langdale, 2009; Jarvis and López-Juez, 2013). If ongoing plastid biogenesis is impaired, by failure to safely complete chlorophyll biosynthesis (because of photooxidative damage to membrane complexes, caused by carotenoid synthesis mutations or chemical inhibitors like norflurazon), or to express the chloroplast genome (because of organelle translation mutations or inhibitors), or to import nuclear-encoded proteins, PhANG expression is downregulated (Inaba et al, 2011; Chi et al, 2013). This reveals the existence of plastid-to-nucleus communication, called plastid retrograde signaling, plastid biogenic signaling. Biogenic signals resulting at least from defects in tetrapyrrole (primarily chlorophyll) biosynthesis and from deficiencies of organellar gene expression can themselves be, to a degree, genetically separated (Vinti et al, 2000; Mochizuki et al, 2001; Gray et al, 2003; Chi et al, 2013)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
