An Ancient Bacterial Signaling Pathway Regulates Chloroplast Function to Influence Growth and Development in Arabidopsis

Sugliani, Matteo; Abdelkefi, Hela; Ke, Hang; Bouveret, Emmanuelle; Robaglia, Christophe; Caffarri, Stefano; Field, Ben

doi:10.1105/tpc.16.00045

Cited by 88 publications

(274 citation statements)

References 69 publications

(115 reference statements)

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“…In Arabidopsis thaliana, all of these proteins localize to the chloroplast (19,56), and ppGpp levels rise in plants in response to darkness and other stresses, including wounding (57). Two recent studies have also shown that ppGpp levels affect photosynthetic capacity and chloroplast development in Arabidopsis (19,58). Thus, it is likely that aspects of the stringent response pathway are conserved between cyanobacteria and chloroplasts.…”

Section: Conservation and Adaptation Of Stringent Response Mechanisms Inmentioning

confidence: 99%

The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus

Hood

Higgins

Flamholz

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

106

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The cyanobacterium Synechococcus elongatus relies upon photosynthesis to drive metabolism and growth. During darkness, Synechococcus stops growing, derives energy from its glycogen stores, and greatly decreases rates of macromolecular synthesis via unknown mechanisms. Here, we show that the stringent response, a stress response pathway whose genes are conserved across bacteria and plant plastids, contributes to this dark adaptation. Levels of the stringent response alarmone guanosine 3′-diphosphate 5′-diphosphate (ppGpp) rise after a shift from light to dark, indicating that darkness triggers the same response in cyanobacteria as starvation in heterotrophic bacteria. High levels of ppGpp are sufficient to stop growth and dramatically alter many aspects of cellular physiology, including levels of photosynthetic pigments and polyphosphate, DNA content, and the rate of translation. Cells unable to synthesize ppGpp display pronounced growth defects after exposure to darkness. The stringent response regulates expression of a number of genes in Synechococcus, including ribosomal hibernation promoting factor (hpf), which causes ribosomes to dimerize in the dark and may contribute to decreased translation. Although the metabolism of Synechococcus differentiates it from other model bacterial systems, the logic of the stringent response remains remarkably conserved, while at the same time having adapted to the unique stresses of the photosynthetic lifestyle.

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Section: Conservation and Adaptation Of Stringent Response Mechanisms Inmentioning

confidence: 99%

The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus

Hood

Higgins

Flamholz

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

106

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“…Surprisingly, despite decreased transcript levels, AccD protein level increases in line accumulating alarmones (Maekawa et al 2015; Sugliani et al 2016). …”

Section: Role Of Rsh Proteins and Alarmones In Chloroplastsmentioning

confidence: 99%

“…Thus, despite the very high level of homology between bacteria and plants in the RSH domain structure and function as well as molecular targets of alarmones, (p)ppGpp-mediated responses in plants become different, according to Sugliani et al (2016) likely due to the evolutionary gene transfer of vast amount of endosymbiont/plastid DNA into the host genome. Since chloroplasts do not proliferate as frequently as bacteria, it is also understandable that their DNA replication would be rather differently regulated.…”

Section: Role Of Rsh Proteins and Alarmones In Chloroplastsmentioning

confidence: 99%

“…This implies that (p)ppGpp during senescence promote not only nutrient reallocation but also remobilization by stimulating chlorophyll and Rubisco degradation (Sugliani et al 2016). Therefore, the plant stringent response is not only linked to stress responses in plants but also required for optimal plant growth and development.…”

Section: Role Of Rsh and Alarmones In Plantsmentioning

confidence: 99%

“…However, lines retaining residual AtCRSH expression do not show that phenotype (Sugliani et al 2016). …”

Section: Role Of Rsh and Alarmones In Plantsmentioning

confidence: 99%

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Within and beyond the stringent response-RSH and (p)ppGpp in plants

Boniecka

Prusińska

Dąbrowska

et al. 2017

Planta

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Main conclusionPlant RSH proteins are able to synthetize and/or hydrolyze unusual nucleotides called (p)ppGpp or alarmones. These molecules regulate nuclear and chloroplast transcription, chloroplast translation and plant development and stress response.Homologs of bacterial RelA/SpoT proteins, designated RSH, and products of their activity, (p)ppGpp—guanosine tetra—and pentaphosphates, have been found in algae and higher plants. (p)ppGpp were first identified in bacteria as the effectors of the stringent response, a mechanism that orchestrates pleiotropic adaptations to nutritional deprivation and various stress conditions. (p)ppGpp accumulation in bacteria decreases transcription—with exception to genes that help to withstand or overcome current stressful situations, which are upregulated—and translation as well as DNA replication and eventually reduces metabolism and growth but promotes adaptive responses. In plants, RSH are nuclei-encoded and function in chloroplasts, where alarmones are produced and decrease transcription, translation, hormone, lipid and metabolites accumulation and affect photosynthetic efficiency and eventually plant growth and development. During senescence, alarmones coordinate nutrient remobilization and relocation from vegetative tissues into seeds. Despite the high conservancy of RSH protein domains among bacteria and plants as well as the bacterial origin of plant chloroplasts, in plants, unlike in bacteria, (p)ppGpp promote chloroplast DNA replication and division. Next, (p)ppGpp may also perform their functions in cytoplasm, where they would promote plant growth inhibition. Furthermore, (p)ppGpp accumulation also affects nuclear gene expression, i.a., decreases the level of Arabidopsis defense gene transcripts, and promotes plants susceptibility towards Turnip mosaic virus. In this review, we summarize recent findings that show the importance of RSH and (p)ppGpp in plant growth and development, and open an area of research aiming to understand the function of plant RSH in response to stress.

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Chloroplast Genome

Howe

2016

Encyclopedia of Life Sciences

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Chloroplasts contain a genome that is a relic of the endosymbiont that gave rise to the organelle. These genomes typically contain 100–200 genes and encode proteins important for photosynthesis and other chloroplast functions, although dinoflagellate algae have a greatly reduced and fragmented chloroplast genome. Many, but not all, nonphotosynthetic taxa retain a remnant chloroplast genome. In some organisms the chloroplast genome may be retained to allow redox‐mediated control of gene expression, whereas in others it may continue to exist because transfer of essential genes to the nucleus is no longer possible. Multiple ribonucleic acid (RNA) polymerases are involved in chloroplast transcription in land plants, and post‐transcriptional processing involving nuclear‐encoded RNA‐binding proteins also plays an important part in the expression of the chloroplast genome. Gene expression may be regulated at a number of levels, and redox poise in the organelle may be particularly important for this. Key Concepts Chloroplasts originated in the ancestor of plants and red and green algae by endosymbiotic acquisition of a cyanobacterium, and then spread to many other eukaryotic lineages. There are other examples of stable acquisition of a cyanobacterium by a nonphotosynthetic host. Chloroplast genomes are typically 100–200 kbp in size, and include a set of genes for proteins essential to photosynthesis. Other genes present in the ancestral symbiont have been lost or relocated to the nucleus. Many nonphotosynthetic organisms retain remnant chloroplasts, with genomes, reflecting the fact that photosynthesis is not the only biochemical process that takes place in the chloroplast. In many organisms, gene transfer from chloroplast to nucleus can still take place, at an unexpectedly high frequency. Establishment of the chloroplast has resulted in the development of nuclear‐encoded RNA‐binding protein families and, in land plants, additional RNA polymerases that play a central role in chloroplast gene expression. Post‐transcriptional RNA processing plays an important role in chloroplast gene expression. In photosynthetic organisms, chloroplast gene expression is closely linked to the organelle's redox poise. The chloroplast can also influence the expression of nuclear genes.

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An Ancient Bacterial Signaling Pathway Regulates Chloroplast Function to Influence Growth and Development in Arabidopsis

Cited by 88 publications

References 69 publications

The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus

The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus

Within and beyond the stringent response-RSH and (p)ppGpp in plants

Chloroplast Genome

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