► The conserved TOR and SnRK1 protein kinases are central hubs coordinating cellular adaptations to changes in nutrient and energy status. ► Many conserved elements of the TOR and SnRK1 signaling ...pathways exist in plants and play roles which have been probably more or less adapted to the plants’ specific needs. ► In yeast and animals, the TOR and Snf1/AMPK protein kinases have antagonistic roles in adjusting several cellular processes like autophagy. ► It will be important to determine how the TOR signaling pathway interacts in plants with that of SnRK1.
The perception of nutrient and energy levels inside and outside the cell is crucial to adjust growth and metabolism to available resources. The signaling pathways centered on the conserved TOR and SnRK1/Snf1/AMPK kinases have crucial and numerous roles in nutrient and energy sensing and in translating this information into metabolic and developmental adaptations. In plants evidence is mounting that, like in other eukaryotes, these signaling pathways have pivotal and antagonistic roles in connecting external or intracellular cues to many biological processes, including ribosome biogenesis, regulation of translation, cell division, accumulation of reserves and autophagy. Data on the plant TOR pathway have been hitherto rather scarce but recent findings have shed new light on its roles in plants. Moreover, the distinctive energy metabolism of photosynthetic organisms may reveal new features of these ancestral eukaryotic signaling elements.
TOR Signaling and Nutrient Sensing Dobrenel, Thomas; Caldana, Camila; Hanson, Johannes ...
Annual review of plant biology,
04/2016, Letnik:
67, Številka:
1
Journal Article
Recenzirano
All living organisms rely on nutrients to sustain cell metabolism and energy production, which in turn need to be adjusted based on available resources. The evolutionarily conserved target of ...rapamycin (TOR) protein kinase is a central regulatory hub that connects environmental information about the quantity and quality of nutrients to developmental and metabolic processes in order to maintain cellular homeostasis. TOR is activated by both nitrogen and carbon metabolites and promotes energy-consuming processes such as cell division, mRNA translation, and anabolism in times of abundance while repressing nutrient remobilization through autophagy. In animals and yeasts, TOR acts antagonistically to the starvation-induced AMP-activated kinase (AMPK) sucrose nonfermenting 1 (Snf1) kinase, called Snf1-related kinase 1 (SnRK1) in plants. This review summarizes the immense knowledge on the relationship between TOR signaling and nutrients in nonphotosynthetic organisms and presents recent findings in plants that illuminate the crucial role of this pathway in conveying nutrient-derived signals and regulating many aspects of metabolism and growth.
Summary
In many crop species, natural variation in eIF4E proteins confers resistance to potyviruses. Gene editing offers new opportunities to transfer genetic resistance to crops that seem to lack ...natural eIF4E alleles. However, because eIF4E are physiologically important proteins, any introduced modification for virus resistance must not bring adverse phenotype effects. In this study, we assessed the role of amino acid substitutions encoded by a Pisum sativum eIF4E virus‐resistance allele (W69L, T80D S81D, S84A, G114R and N176K) by introducing them independently into the Arabidopsis thaliana eIF4E1 gene, a susceptibility factor to the Clover yellow vein virus (ClYVV). Results show that most mutations were sufficient to prevent ClYVV accumulation in plants without affecting plant growth. In addition, two of these engineered resistance alleles can be combined with a loss‐of‐function eIFiso4E to expand the resistance spectrum to other potyviruses. Finally, we use CRISPR‐nCas9‐cytidine deaminase technology to convert the Arabidopsis eIF4E1 susceptibility allele into a resistance allele by introducing the N176K mutation with a single‐point mutation through C‐to‐G base editing to generate resistant plants. This study shows how combining knowledge on pathogen susceptibility factors with precise genome‐editing technologies offers a feasible solution for engineering transgene‐free genetic resistance in plants, even across species barriers.
Recessive resistance genes against plant viruses have been recognized for a long time but their molecular nature has only recently been linked to components of the eukaryotic translation initiation ...complex. Translation initiation factors, and particularly the eIF4E and eIF4G protein families, were found to be essential determinants in the outcome of RNA virus infections. Viruses affected by these genes belong mainly to potyviruses; natural viral resistance mechanisms as well as mutagenesis analysis in
Arabidopsis all converged to identify the same set of translation initiation factors. Their role in plant resistance against RNA viruses remains to be elucidated. Although the interaction with the protein synthesis machinery is probably a key element for successful RNA virus infection, other possible mechanisms will also be discussed.
cis-natural antisense transcripts (cis-NATs) are widespread in plants and are often associated with downregulation of their associated sense genes. We found that a cis-NAT positively regulates the ...level of a protein critical for phosphate homeostasis in rice (Oryza sativa). PHOSPHATE1;2 (PHO1;2), a gene involved in phosphate loading into the xylem in rice, and its associated cis-NAT PHO1;2 are both controlled by promoters active in the vascular cylinder of roots and leaves. While the PHO1;2 promoter is unresponsive to the plant phosphate status, the cis-NAT PHO1;2 promoter is strongly upregulated under phosphate deficiency. Expression of both cis-NAT PHO1;2 and the PHO1;2 protein increased in phosphate-deficient plants, while the PHO1;2 mRNA level remained stable. Downregulation of cis-NAT PHO1;2 expression by RNA interference resulted in a decrease in PHO1;2 protein, impaired the transfer of phosphate from root to shoot, and decreased seed yield. Constitutive overexpression of NAT PHO1;2 in trans led to a strong increase of PHO1;2, even under phosphate-sufficient conditions. Under all conditions, no changes occurred in the level of expression, sequence, or nuclear export of PHO1;2 mRNA. However, expression of cis-NATPHO1;2 was associated with a shift of both PHO1;2 and cis-NAT PHO1;2 toward the polysomes. These findings reveal an unexpected role for cis-NAT PHO1;2 in promoting PHO1;2 translation and affecting phosphate homeostasis and plant fitness.
TARGET OF RAPAMYCIN (TOR) is a conserved eukaryotic phosphatidylinositol-3-kinase-related kinase that plays a major role in regulating growth and metabolism in response to environment in plants. We ...performed a genetic screen for
ethylmethane sulfonate mutants resistant to the ATP-competitive TOR inhibitor AZD-8055 to identify new components of the plant TOR pathway. We found that loss-of-function mutants of the DYRK (dual specificity tyrosine phosphorylation regulated kinase)/YAK1 kinase are resistant to AZD-8055 and, reciprocally, that YAK1 overexpressors are hypersensitive to AZD-8055. Significantly, these phenotypes were conditional on TOR inhibition, positioning YAK1 activity downstream of TOR. We further show that the ATP-competitive DYRK1A inhibitor pINDY phenocopies
loss of function. Microscopy analysis revealed that YAK1 functions to repress meristem size and induce differentiation. We show that YAK1 represses cyclin expression in the different zones of the root meristem and that YAK1 is essential for TOR-dependent transcriptional regulation of the plant-specific SIAMESE-RELATED (SMR) cyclin-dependent kinase inhibitors in both meristematic and differentiating root cells. Thus, YAK1 is a major regulator of meristem activity and cell differentiation downstream of TOR.
The chloroplast originated from the endosymbiosis of an ancient photosynthetic bacterium by a eukaryotic cell. Remarkably, the chloroplast has retained elements of a bacterial stress response pathway ...that is mediated by the signaling nucleotides guanosine penta- and tetraphosphate (ppGpp). However, an understanding of the mechanism and outcomes of ppGpp signaling in the photosynthetic eukaryotes has remained elusive. Using the model plant Arabidopsis thaliana, we show that ppGpp is a potent regulator of chloroplast gene expression in vivo that directly reduces the quantity of chloroplast transcripts and chloroplast-encoded proteins. We then go on to demonstrate that the antagonistic functions of different plant RelA SpoT homologs together modulate ppGpp levels to regulate chloroplast function and show that they are required for optimal plant growth, chloroplast volume, and chloroplast breakdown during dark-induced and developmental senescence. Therefore, our results show that ppGpp signaling is not only linked to stress responses in plants but is also an important mediator of cooperation between the chloroplast and the nucleocytoplasmic compartment during plant growth and development.
Key Message
Arabidopsis single and double mutants for energy dissipation (
npq4
) and state transitions (
pph1
, blocked in State II) show enhanced growth and flowers + siliques production under ...controlled low-light conditions.
Non-photochemical quenching (NPQ) is a short-term regulation important to maintain efficient photosynthesis and to avoid photooxidative damages by dissipation of excess energy. Full activation of NPQ in plants requires the protonation of the PsbS protein, which is the sensor of the low lumenal pH triggering the thermal dissipation. State transitions are a second important photosynthetic regulation to respond to changes in light quality and unbalanced excitation of photosystems. State transitions allow energy redistribution between PSI and PSII through the reversible exchange of LHCII antenna complexes between photosystems thanks to the opposite action of the STN7 kinase and PPH1 phosphatase: phosphorylation of LHCII promotes its mobilization from PSII to PSI, while dephosphorylation has the opposite effect. In this work, we produced the
pph1
/
npq4
double mutant and characterized some photosynthetic, growth and reproduction properties in comparison with wild-type and single-mutant plants in high- and low-light conditions. Results indicate that in high light, the
pph1
mutant maintains good photoprotection ability, while
npq4
plants show more susceptibility to photodamages. The
pph1
/
npq4
double mutant showed a resistance to high-light stress similar to that of the single
npq4
mutant. In low-light condition, the single mutants showed a significant increase of growth and flowering compared to wild-type plants and this effect was further enhanced in the
pph1
/
npq4
double mutant. Results suggest that photosynthetic optimisation to improve crop growth and productivity might be possible, at least under controlled low-light conditions, by modifying NPQ and regulation of state transitions.
MicroRNAs (miRNAs) regulate gene expression posttranscriptionally through RNA silencing, a mechanism conserved in eukaryotes. Prevailing models entail most animal miRNAs affecting gene expression by ...blocking mRNA translation and most plant miRNAs, triggering mRNA cleavage. Here, using polysome fractionation in Arabidopsis thaliana, we found that a portion of mature miRNAs and ARGONAUTE1 (AGO1) is associated with polysomes, likely through their mRNA target. We observed enhanced accumulation of several distinct miRNA targets at both the mRNA and protein levels in an ago1 hypomorphic mutant. By contrast, translational repression, but not cleavage, persisted in transgenic plants expressing the slicing-inhibitor 2b protein from Cucumber mosaic virus. In agreement, we found that the polysome association of miR168 was lost in ago1 but maintained in 2b plants, indicating that translational repression is correlated with the presence of miRNAs and AGO1 in polysomes. This work provides direct biochemical evidence for a translational component in the plant miRNA pathway.
Plants, unlike animals, have plastic organ growth that is largely dependent on environmental information. However, so far, little is known about how this information is perceived and transduced into ...coherent growth and developmental decisions. Here, we report that the growth of Arabidopsis is positively correlated with the level of expression of the TARGET OF RAPAMYCIN (TOR) kinase. Diminished or augmented expression of the AtTOR gene results in a dose‐dependent decrease or increase, respectively, in organ and cell size, seed production and resistance to osmotic stress. Strong downregulation of AtTOR expression by inducible RNA interference also leads to a post‐germinative halt in growth and development, which phenocopies the action of the plant hormone abscisic acid, to an early senescence and to a reduction in the amount of translated messenger RNA. Thus, we propose that the AtTOR kinase is one of the contributors to the link between environmental cues and growth processes in plants.
PDF
