Structural and functional components of chloroplast are encoded by genes localized both to nuclear and plastid genomes of plant cell. Development from etioplasts to chloroplasts is triggered by light receptors that activate the expression of photosynthesis-associated nuclear genes (PhaNGs). In addition to photoreceptor-mediated pathways, retrograde signals from the chloroplast to the nucleus activate or repress the expression of nuclear genes involved in acclimatory or stress responses in plant leaves. A plant mesophyll cell contains up to 100 chloroplasts that function autonomously, raising intriguing questions about homogeneity and coordination of retrograde signals transmitted from chloroplast to nucleus. We have previously demonstrated that the knockout of the chloroplast regulatory protein, chloroplast NADPH-dependent thioredoxin reductase (NTRC) leads to a heterogeneous population of chloroplasts with a range of different functional states. The heterogeneous chloroplast population activates both redox-dependent and undifferentiated plastid-generated retrograde signaling pathways in the mutant leaves. Transcriptome data from the ntrc knockout lines suggest that the induction of the redox-dependent signaling pathway depends on light conditions and leads to activation of stress-responsive gene expression. Analysis of mutants in different developmental stages allows to dissect signals from normal and anomalous chloroplasts. Thus, the signals derived from anomalous chloroplasts repress expression of PhaNGs as well as genes associated with light receptor signaling and differentiation of stomata, implying interaction between retrograde pathways and plant development. Analysis of the nuclear gene expression in mutants of retrograde signaling pathways in ntrc background would reveal the components that mediate signals generated from heterogeneous plastids to nucleus.

Plants synchronize their cellular and physiological functions according to the photoperiod (the length of the light period) in the cycle of 24 h. Photoperiod adjusts several traits in the plant life cycle, including flowering and senescence in annuals and seasonal growth cessation in perennials. Photoperiodic development is controlled by the coordinated action of photoreceptors and the circadian clock. During the past 10 years, remarkable progress has been made in understanding the molecular mechanism of the circadian clock, especially with regard to the transition of Arabidopsis from the vegetative growth to the reproductive phase. Besides flowering photoperiod also modifies plant photosynthetic structures and traits. Light signals controlling biogenesis of chloroplasts and development of leaf photosynthetic structures are perceived both by photoreceptors and in chloroplasts. In this review, we provide evidence suggesting that the photoperiodic development of Arabidopsis leaves mimics the acclimation of plant to various light intensities. Furthermore, the chloroplast-to-nucleus retrograde signals that adjust acclimation to light intensity are proposed to contribute also to the signaling pathways that control photoperiodic acclimation of leaves.

The biogenesis and function of chloroplast are controlled both by anterograde mechanisms involving nuclear-encoded proteins targeted to chloroplast and by retrograde signals from plastid to nucleus contributing to regulation of nuclear gene expression. A number of experimental evidences support the implication of chlorophyll biosynthesis intermediates on the retrograde signaling, albeit an earlier-postulated direct link between accumulation of chlorophyll intermediates and changes in nuclear gene expression has recently been challenged. By characterization of Arabidopsis mutants lacking the chloroplast localized NADPH-thioredoxin reductase (NTRC) we have recently proposed that imbalanced activity of chlorophyll biosynthesis in developing cells modifies the chloroplast signals leading to alterations in nuclear gene expression. These signals appear to initiate from temporal perturbations in the flux through the pathway from protoporphyrin to protochlorophyllide rather than from the accumulation of a single intermediate of the tetrapyr-role pathway.