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1.
Sci Adv ; 10(25): eadj3268, 2024 Jun 21.
Article in English | MEDLINE | ID: mdl-38896607

ABSTRACT

Chloroplasts are the powerhouse of the plant cell, and their activity must be matched to plant growth to avoid photooxidative damage. We have identified a posttranslational mechanism linking the eukaryotic target of rapamycin (TOR) kinase that promotes growth and the guanosine tetraphosphate (ppGpp) signaling pathway of prokaryotic origins that regulates chloroplast activity and photosynthesis in particular. We find that RelA SpoT homolog 3 (RSH3), a nuclear-encoded enzyme responsible for ppGpp biosynthesis, interacts directly with the TOR complex via a plant-specific amino-terminal region which is phosphorylated in a TOR-dependent manner. Down-regulating TOR activity causes a rapid increase in ppGpp synthesis in RSH3 overexpressors and reduces photosynthetic capacity in an RSH-dependent manner in wild-type plants. The TOR-RSH3 signaling axis therefore regulates the equilibrium between chloroplast activity and plant growth, setting a precedent for the regulation of organellar function by TOR.


Subject(s)
Arabidopsis Proteins , Arabidopsis , Chloroplasts , Photosynthesis , Signal Transduction , Chloroplasts/metabolism , Arabidopsis Proteins/metabolism , Arabidopsis Proteins/genetics , Arabidopsis/metabolism , Arabidopsis/genetics , Phosphorylation , Protein Processing, Post-Translational , Gene Expression Regulation, Plant , Guanosine Tetraphosphate/metabolism , TOR Serine-Threonine Kinases/metabolism , Phosphatidylinositol 3-Kinases
2.
New Phytol ; 243(2): 506-508, 2024 Jul.
Article in English | MEDLINE | ID: mdl-38794831

Subject(s)
Photosynthesis , Ions
3.
New Phytol ; 237(4): 1086-1099, 2023 02.
Article in English | MEDLINE | ID: mdl-36349398

ABSTRACT

The nucleotides guanosine tetraphosphate and guanosine pentaphosphate (together (p)ppGpp) are found in a wide range of prokaryotic and eukaryotic organisms where they are associated with stress signalling. In this review, we will discuss recent research highlighting the role of (p)ppGpp signalling as a conserved regulator of photosynthetic activity in the chloroplasts of plants and algae, and the latest discoveries that open up new perspectives on the emerging roles of (p)ppGpp in acclimation to environmental stress. We explore how rapid advances in the study of (p)ppGpp signalling in prokaryotes are now revealing large gaps in our understanding of the molecular mechanisms of signalling by (p)ppGpp and related nucleotides in plants and algae. Filling in these gaps is likely to lead to the discovery of conserved as well as new plant- and algal-specific (p)ppGpp signalling mechanisms that will offer new insights into the taming of the chloroplast and the regulation of stress tolerance.


Subject(s)
Guanosine Pentaphosphate , Guanosine Tetraphosphate , Guanosine Tetraphosphate/metabolism , Guanosine Pentaphosphate/metabolism , Photosynthesis , Plants/metabolism , Chloroplasts/metabolism
4.
New Phytol ; 236(1): 86-98, 2022 10.
Article in English | MEDLINE | ID: mdl-35715975

ABSTRACT

The nucleotides guanosine tetraphosphate and pentaphosphate (or (p)ppGpp) are implicated in the regulation of chloroplast function in plants. (p)ppGpp signalling is best understood in the model vascular plant Arabidopsis thaliana in which it acts to regulate plastid gene expression to influence photosynthesis, plant development and immunity. However, little information is known about the conservation or diversity of (p)ppGpp signalling in other land plants. We studied the function of ppGpp in the moss Physcomitrium (previously Physcomitrella) patens using an inducible system for triggering ppGpp accumulation. We used this approach to investigate the effects of ppGpp on chloroplast function, photosynthesis and growth. We demonstrate that ppGpp accumulation causes a dramatic drop in photosynthetic capacity by inhibiting chloroplast gene expression. This was accompanied by the unexpected reorganisation of the thylakoid system into super grana. Surprisingly, these changes did not affect gametophore growth, suggesting that bryophytes and vascular plants may have different tolerances to defects in photosynthesis. Our findings point to the existence of both highly conserved and more specific targets of (p)ppGpp signalling in the land plants that may reflect different growth strategies.


Subject(s)
Arabidopsis , Bryopsida , Arabidopsis/metabolism , Bryopsida/metabolism , Chloroplasts/metabolism , Genes, Chloroplast , Guanosine Pentaphosphate/metabolism , Guanosine Tetraphosphate/metabolism , Thylakoids/metabolism
5.
Elife ; 112022 02 14.
Article in English | MEDLINE | ID: mdl-35156611

ABSTRACT

Guanosine pentaphosphate and tetraphosphate (together referred to as ppGpp) are hyperphosphorylated nucleotides found in bacteria and the chloroplasts of plants and algae. In plants and algae artificial ppGpp accumulation can inhibit chloroplast gene expression, and influence photosynthesis, nutrient remobilization, growth, and immunity. However, it is so far unknown whether ppGpp is required for abiotic stress acclimation in plants. Here, we demonstrate that ppGpp biosynthesis is necessary for acclimation to nitrogen starvation in Arabidopsis. We show that ppGpp is required for remodeling the photosynthetic electron transport chain to downregulate photosynthetic activity and for protection against oxidative stress. Furthermore, we demonstrate that ppGpp is required for coupling chloroplastic and nuclear gene expression during nitrogen starvation. Altogether, our work indicates that ppGpp is a pivotal regulator of chloroplast activity for stress acclimation in plants.


Subject(s)
Arabidopsis/metabolism , Guanosine Pentaphosphate/metabolism , Guanosine Tetraphosphate/metabolism , Nitrogen/metabolism , Photosynthesis , Acclimatization , Arabidopsis/genetics , Chloroplasts/physiology , Cyanobacteria/cytology , Gene Expression Regulation, Plant , Plant Cells , Stress, Physiological
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