Retrograde Signals: Integrators of Interorganellar Communication and Orchestrators of Plant Development

Souza, Amancio de; Wang, Jinzheng; Dehesh, Katayoon

doi:10.1146/annurev-arplant-042916-041007

Cited by 187 publications

(171 citation statements)

References 140 publications

(159 reference statements)

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“…Currently, increasing evidence is accumulating for communication networks between organelles that are regulated in part by retrograde (= organelle to nucleus) signals (Chan et al, 2016;Kmiecik et al, 2016;de Souza et al, 2017). In contrast, anterograde (= nucleus to organelle) signals mainly regulate biogenesis of the organelles as well as maintenance, for example, in repair processes during stress situations.…”

Section: Anterograde Signals To Organelles Via Phosphorylation Of Tramentioning

confidence: 99%

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

et al. 2018

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The evolutionarily conserved SNF1-related protein kinase 1 (SnRK1) kinase complex is a key regulator in adjusting cellular metabolism during starvation, stress conditions, and growth-promoting conditions. Over the last two decades, extensive genetic evidence for a widespread SnRK1 signaling network has accumulated. It is now well established that SnRK1 is a central integrator of energy signaling. However, little is known about the connections between the cytoplasmic and nuclear-localized SnRK1 and plastids and mitochondria as the main energy-producing compartments in the cell. Here, we review recent findings indicating how SnRK1 affects metabolic adaptation, including plastidial and mitochondrial functions. Special emphasis is put on identified direct targets of SnRK1, which would eventually enable cross talk with organelles. In this context, a number of transcription factors (TFs) are emerging as mediators of SnRK1 signaling, potentially linking SnRK1 activity to organellar functions. Furthermore, many SnRK1 targets act in various hormonal signaling pathways, which are at least partly localized in plastids. With this review, we summarize the current knowledge on SnRK1 organelle interaction and provide ideas on the potential molecular mechanisms governing these interactions. METABOLIC REPROGRAMMING BY SNRK1 KINASE ACTIVITY UNDER DIFFERENT GROWTH AND STRESS CONDITIONSAlready under optimal growth conditions, plants need to continuously adjust their metabolic balance between autotrophic growth based on photosynthesis during the day and respiration during the night. At daytime, sugars and other metabolites are produced by photosynthesis in chloroplasts and further distributed to be used in other metabolic pathways at different cellular compartments or transported to nonphotosynthetic sink tissues. During the night, starch and sugars supply carbon equivalents for respiration, providing the necessary energy for further growth and metabolic activities. Additionally, metabolic reprogramming is required for plants to adjust their metabolism to diverse biotic and abiotic environmental stimuli. This often leads to a stop of plant growth involving a reduction in ribosomal protein synthesis, and in parallel, accumulation of protective metabolites or defense compounds. This switching of cellular energy metabolism is mediated by the activity of the evolutionarily conserved AMPK/ SNF1/SnRK1 kinase complex (Box 1; Crozet et al.,

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Section: Anterograde Signals To Organelles Via Phosphorylation Of Tramentioning

confidence: 99%

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

et al. 2018

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“…Extensive studies have uncovered the basic photosynthetic and metabolic processes of chloroplast development (Kangasjärvi et al, 2014; Kaur, 2014; de Souza et al, 2016). …”

Section: Introductionmentioning

confidence: 99%

WHITE STRIPE LEAF4 Encodes a Novel P-Type PPR Protein Required for Chloroplast Biogenesis during Early Leaf Development

et al. 2017

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Pentatricopeptide repeat (PPR) proteins comprise a large family in higher plants and perform diverse functions in organellar RNA metabolism. Despite the rice genome encodes 477 PRR proteins, the regulatory effects of PRR proteins on chloroplast development remains unknown. In this study, we report the functional characterization of the rice white stripe leaf4 (wsl4) mutant. The wsl4 mutant develops white-striped leaves during early leaf development, characterized by decreased chlorophyll content and malformed chloroplasts. Positional cloning of the WSL4 gene, together with complementation and RNA-interference tests, reveal that it encodes a novel P-family PPR protein with 12 PPR motifs, and is localized to chloroplast nucleoids. Quantitative RT-PCR analyses demonstrate that WSL4 is a low temperature response gene abundantly expressed in young leaves. Further expression analyses show that many nuclear- and plastid-encoded genes in the wsl4 mutant are significantly affected at the RNA and protein levels. Notably, the wsl4 mutant causes defects in the splicing of atpF, ndhA, rpl2, and rps12. Our findings identify WSL4 as a novel P-family PPR protein essential for chloroplast RNA group II intron splicing during early leaf development in rice.

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“…This coordination is achieved by a mutual information Exchange between nucleus and plastids that is called "anterograde" (from nucleus toward plastids) and "retrograde" (from plastids toward nucleus) signaling. This mutual signaling has been studied extensively, but is still far from being understood (Chi et al, 2013;Chan et al, 2016;de Souza et al, 2016;Kleine and Leister, 2016). The retrograde plastidial signals that are identified so far are numerous and of very diverse nature (see below).…”

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confidence: 99%

Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1

et al. 2017

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Plants possessing dysfunctional plastids due to defects in pigment biosynthesis or translation are known to repress photosynthesisassociated nuclear genes via retrograde signals from the disturbed organelles toward the nucleus. These signals are thought to be essential for proper biogenesis and function of the plastid. Mutants lacking plastid-encoded RNA polymerase-associated proteins (PAPs) display a genetic arrest in eoplast-chloroplast transition leading to an albino phenotype in the light. Retrograde signaling in these mutants, therefore, could be expected to be similar as under conditions inducing plastid dysfunction. To answer this question, we performed plastome-and genomewide array analyses in the pap7-1 mutant of Arabidopsis (Arabidopsis thaliana). In parallel, we determined the potential overlap with light-regulated expression networks. To this end, we performed a comparative expression profiling approach using light-and dark-grown wild-type plants as relative control for the expression profiles obtained from lightgrown pap7-1 mutants. Our data indicate a specific impact of retrograde signals on metabolism-related genes in pap7-1 mutants reflecting the starvation situation of the albino seedlings. In contrast, light regulation of PhANGs and other nuclear gene groups appears to be fully functional in this mutant, indicating that a block in chloroplast biogenesis per se does not repress expression of them as suggested by earlier studies. Only genes for light harvesting complex proteins displayed a significant repression indicating an exclusive retrograde impact on this gene family. Our results indicate that chloroplasts and arrested plastids each emit specific signals that control different target gene modules both in positive and negative manner.

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Retrograde Signals: Integrators of Interorganellar Communication and Orchestrators of Plant Development

Cited by 187 publications

References 140 publications

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

WHITE STRIPE LEAF4 Encodes a Novel P-Type PPR Protein Required for Chloroplast Biogenesis during Early Leaf Development

Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1

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