Plant Stress Signaling
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We are ultimately interested in signaling processes that operate ubiquitously in Nature, such as those related to the nutrient and energy status, and in how they have been modified to the needs of autotrophic and multi-cellular plants. In contrast to animals, plant growth is largely conditioned by environmental inputs. Such plasticity allows the plant to optimise its growth and development according to the prevailing conditions, ensuring the best possible chance to complete its life cycle and contributing to the striking phenotypic variation of the plant kingdom. Stress can have a great impact on growth, on developmental transitions, as well as on the characteristics of newly formed organs. Often associated with stress is a reduction in photosynthesis and/or respiration, which in turn results in an energy deficit in the cell. Dealing with such imbalances in the energy status is of uttermost importance, since even short periods of starvation can cause growth arrest and result, for example, in seed abortion characteristic of episodes of drought and heat.
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Massachusetts General Hospital, Harvard Medical School, Boston, USA
Jen Sheen
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Browsing Plant Stress Signaling by Author "Baena-González, Elena"
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- Dissection of miRNA Pathways Using Arabidopsis Mesophyll ProtoplastsPublication . Martinho, Cláudia; Confraria, Ana; Elias, Carlos Alexandre; Crozet, Pierre; Rubio-Somoza, Ignacio; Weigel, Detlef; Baena-González, ElenaMicroRNAs (miRNAs) control gene expression mostly post-transcriptionally by guiding transcript cleavage and/or translational repression of complementary mRNA targets, thereby regulating developmental processes and stress responses. Despite the remarkable expansion of the field, the mechanisms underlying miRNA activity are not fully understood. In this article, we describe a transient expression system in Arabidopsis mesophyll protoplasts, which is highly amenable for the dissection of miRNA pathways. We show that by transiently overexpressing primary miRNAs and target mimics, we can manipulate miRNA levels and consequently impact on their targets. Furthermore, we developed a set of luciferase-based sensors for quantifying miRNA activity that respond specifically to both endogenous and overexpressed miRNAs and target mimics. We demonstrate that these miRNA sensors can be used to test the impact of putative components of the miRNA pathway on miRNA activity, as well as the impact of specific mutations, by either overexpression or the use of protoplasts from the corresponding mutants. We further show that our miRNA sensors can be used for investigating the effect of chemicals on miRNA activity. Our cell-based transient expression system is fast and easy to set up, and generates quantitative results, being a powerful tool for assaying miRNA activity in vivo.
- Energy Signaling in the Regulation of Gene Expression during StressPublication . Baena-González, Elena;Maintenance of homeostasis is pivotal to all forms of life. In the case of plants, homeostasis is constantly threatened by the inability to escape environmental fluctuations, and therefore sensitive mechanisms must have evolved to allow rapid perception of environmental cues and concomitant modification of growth and developmental patterns for adaptation and survival. Re-establishment of homeostasis in response to environmental perturbations requires reprogramming of metabolism and gene expression to shunt energy sources from growth-related biosynthetic processes to defense, acclimation, and, ultimately, adaptation. Failure to mount an initial 'emergency' response may result in nutrient deprivation and irreversible senescence and cell death. Early signaling events largely determine the capacity of plants to orchestrate a successful adaptive response. Early events, on the other hand, are likely to be shared by different conditions through the generation of similar signals and before more specific responses are elaborated. Recent studies lend credence to this hypothesis, underpinning the importance of a shared energy signal in the transcriptional response to various types of stress. Energy deficiency is associated with most environmental perturbations due to their direct or indirect deleterious impact on photosynthesis and/or respiration. Several systems are known to have evolved for monitoring the available resources and triggering metabolic, growth, and developmental decisions accordingly. In doing so, energy-sensing systems regulate gene expression at multiple levels to allow flexibility in the diversity and the kinetics of the stress response.
- Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinasesPublication . Crozet, Pierre; Margalha, Leonor; Confraria, Ana; Rodrigues, Américo; Martinho, Cláudia; Adamo, Mattia; Elias, Carlos A.; Baena-González, ElenaThe SNF1 (sucrose non-fermenting 1)-related protein kinases 1 (SnRKs1) are the plant orthologs of the budding yeast SNF1 and mammalian AMPK (AMP-activated protein kinase). These evolutionarily conserved kinases are metabolic sensors that undergo activation in response to declining energy levels. Upon activation, SNF1/AMPK/SnRK1 kinases trigger a vast transcriptional and metabolic reprograming that restores energy homeostasis and promotes tolerance to adverse conditions, partly through an induction of catabolic processes and a general repression of anabolism. These kinases typically function as a heterotrimeric complex composed of two regulatory subunits, β and γ, and an α-catalytic subunit, which requires phosphorylation of a conserved activation loop residue for activity. Additionally, SNF1/AMPK/SnRK1 kinases are controlled by multiple mechanisms that have an impact on kinase activity, stability, and/or subcellular localization. Here we will review current knowledge on the regulation of SNF1/AMPK/SnRK1 by upstream components, post-translational modifications, various metabolites, hormones, and others, in an attempt to highlight both the commonalities of these essential eukaryotic kinases and the divergences that have evolved to cope with the particularities of each one of these systems.
- miRNAs mediate SnRK1-dependent energy signaling in ArabidopsisPublication . Confraria, Ana; Martinho, Cláudia; Elias, Alexandre; Rubio-Somoza, Ignacio; Baena-González, ElenaThe SnRK1 protein kinase, the plant ortholog of mammalian AMPK and yeast Snf1, is activated by the energy depletion caused by adverse environmental conditions. Upon activation, SnRK1 triggers extensive transcriptional changes to restore homeostasis and promote stress tolerance and survival partly through the inhibition of anabolism and the activation of catabolism. Despite the identification of a few bZIP transcription factors as downstream effectors, the mechanisms underlying gene regulation, and in particular gene repression by SnRK1, remain mostly unknown. microRNAs (miRNAs) are 20-24 nt RNAs that regulate gene expression post-transcriptionally by driving the cleavage and/or translation attenuation of complementary mRNA targets. In addition to their role in plant development, mounting evidence implicates miRNAs in the response to environmental stress. Given the involvement of miRNAs in stress responses and the fact that some of the SnRK1-regulated genes are miRNA targets, we postulated that miRNAs drive part of the transcriptional reprogramming triggered by SnRK1. By comparing the transcriptional response to energy deprivation between WT and dcl1-9, a mutant deficient in miRNA biogenesis, we identified 831 starvation genes misregulated in the dcl1-9 mutant, out of which 155 are validated or predicted miRNA targets. Functional clustering analysis revealed that the main cellular processes potentially co-regulated by SnRK1 and miRNAs are translation and organelle function and uncover TCP transcription factors as one of the most highly enriched functional clusters. TCP repression during energy deprivation was impaired in miR319 knockdown (MIM319) plants, demonstrating the involvement of miR319 in the stress-dependent regulation of TCPs. Altogether, our data indicates that miRNAs are components of the SnRK1 signaling cascade contributing to the regulation of specific mRNA targets and possibly tuning down particular cellular processes during the stress response.
- Shaping plant development through the SnRK1–TOR metabolic regulatorsPublication . Baena-González, Elena; Hanson, JohannesSnRK1 (Snf1-related protein kinase 1) and TOR (target ofrapamycin) are evolutionarily conserved protein kinases thatlie at the heart of energy sensing, playing central andantagonistic roles in the regulation of metabolism and geneexpression. Increasing evidence links these metabolicregulators to numerous aspects of plant development, fromgermination to flowering and senescence. This prompts thehypothesis that SnRK1 and TOR modify developmentalprograms according to the metabolic status to adjust plantgrowth to a specific environment. The aim of this review is toprovide support to this hypothesis and to incentivize furtherstudies on this topic by summarizing the work that establishesa genetic connection between SnRK1–TOR and plantdevelopment.
- SnRK1 and TOR: modulators of growth-defense trade-offs in plant stress responses.Publication . Margalha, Leonor; Confraria, Ana; Baena-González, ElenaThe evolutionarily conserved protein kinase complexes SnRK1 and TOR are central metabolic regulators essential for plant growth, development, and stress responses. They are activated by opposite signals, and the outcome of their activation is, in global terms, antagonistic. Similarly to their yeast and animal counterparts, SnRK1 is activated by the energy deficit often associated with stress to restore homeostasis, while TOR is activated in nutrient-rich conditions to promote growth. Recent evidence suggests that SnRK1 represses TOR in plants, revealing evolutionary conservation also in their crosstalk. Given their importance for integrating environmental information into growth and developmental programs, these signaling pathways hold great promise for reducing the growth penalties caused by stress. Here we review the literature connecting SnRK1 and TOR to plant stress responses. Although SnRK1 and TOR emerge mostly as positive regulators of defense and growth, respectively, the outcome of their activities in plant growth and performance is not always straightforward. Manipulation of both pathways under similar experimental setups, as well as further biochemical and genetic analyses of their molecular and functional interaction, is essential to fully understand the mechanisms through which these two metabolic pathways contribute to stress responses, growth, and development.
- SnRK1 and trehalose 6-phosphate – two ancient pathways converge to regulate plant metabolism and growthPublication . Baena-González, Elena; Lunn, JohnSUCROSE-NON-FERMENTING1-RELATED KINASE1 (SnRK1) belongs to a family of protein kinases that originated in the earliest eukaryotes and plays a central role in energy and metabolic homeostasis. Trehalose 6-phosphate (Tre6P) is the intermediate of trehalose biosynthesis, and has even more ancient roots, being found in all three domains of life – Archaea, Bacteria and Eukarya. In plants, the function of SnRK1 has diverged from its orthologues in fungi and animals, evolving new roles in signalling of nutrient status and abiotic stress. Tre6P has also acquired a novel function in plants as a signal and homeostatic regulator of sucrose, the dominant sugar in plant metabolism. These two ancient pathways have converged in a unique way in plants, enabling them to coordinate their metabolism, growth and development with their environment, which is essential for their autotrophic and sessile lifestyle
- SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plantsPublication . Pedrotti, Lorenzo; Wurzinger, Bernhard; Anrather, Dorothea; Simeunovic, Andrea; Weiste, Christoph; Valerio, Concetta; Dietrich, Katrin; Kirchler, Tobias; Nägele, Thomas; Vicente Carbajosa, Jesús; Hanson, Johannes; Baena-González, Elena; Chaban, Christina; Weckwerth, Wolfram; Dröge-Laser, Wolfgang; Teige, MarkusMetabolic adjustment to changing environmental conditions, particularly balancing of growth and defense responses, is crucial for all organisms to survive. The evolutionary conserved AMPK/Snf1/SnRK1 kinases are well-known metabolic master regulators in the low-energy response in animals, yeast and plants. They act at two different levels: by modulating the activity of key metabolic enzymes, and by massive transcriptional reprogramming. While the first part is well established, the latter function is only partially understood in animals and not at all in plants. Here we identified the Arabidopsis transcription factor bZIP63 as key regulator of the starvation response and direct target of the SnRK1 kinase. Phosphorylation of bZIP63 by SnRK1 changed its dimerization preference, thereby affecting target gene expression and ultimately primary metabolism. A bzip63 knock-out mutant exhibited starvation-related phenotypes, which could be functionally complemented by wild type bZIP63, but not by a version harboring point mutations in the identified SnRK1 target sites.
- SUMOylation represses SnRK1 signaling in ArabidopsisPublication . Crozet, Pierre; Margalha, Leonor; Butowt, Rafal; Fernandes, Noémia; Elias, Carlos A.; Orosa, Beatriz; Tomanov, Konstantin; Teige, Markus; Bachmair, Andreas; Sadanandom, Ari; Baena-González, ElenaThe SnRK1 protein kinase balances cellular energy levels in accordance with extracellular conditions and is thereby key for plant stress tolerance. In addition, SnRK1 has been implicated in numerous growth and developmental processes from seed filling and maturation to flowering and senescence. Despite its importance, the mechanisms that regulate SnRK1 activity are poorly understood. Here, we demonstrate that the SnRK1 complex is SUMOylated on multiple subunits and identify SIZ1 as the E3 Small Ubiquitin-like Modifier (SUMO) ligase responsible for this modification. We further show that SnRK1 is ubiquitinated in a SIZ1-dependent manner, causing its degradation through the proteasome. In consequence, SnRK1 degradation is deficient in siz1-2 mutants, leading to its accumulation and hyperactivation of SnRK1 signaling. Finally, SnRK1 degradation is strictly dependent on its activity, as inactive SnRK1 variants are aberrantly stable but recover normal degradation when expressed as SUMO mimetics. Altogether, our data suggest that active SnRK1 triggers its own SUMOylation and degradation, establishing a negative feedback loop that attenuates SnRK1 signaling and prevents detrimental hyperactivation of stress responses.
- The Arabidopsis SR45 Splicing Factor, a Negative Regulator of Sugar Signaling, Modulates SNF1-Related Protein Kinase 1 StabilityPublication . Carvalho, Raquel F.; Szakonyi, Dóra; Simpson, Craig G.; Barbosa, Inês C.R.; Brown, John W.S.; Baena-González, Elena; Duque, PaulaThe ability to sense and respond to sugar signals allows plants to cope with environmental and metabolic changes by adjusting growth and development accordingly. We previously reported that the SR45 splicing factor negatively regulates glucose signaling during early seedling development in Arabidopsis thaliana Here, we show that under glucose-fed conditions, the Arabidopsis sr45-1 loss-of-function mutant contains higher amounts of the energy-sensing SNF1-Related Protein Kinase 1 (SnRK1) despite unaffected SnRK1 transcript levels. In agreement, marker genes for SnRK1 activity are upregulated in sr45-1 plants, and the glucose hypersensitivity of sr45-1 is attenuated by disruption of the SnRK1 gene. Using a high-resolution RT-PCR panel, we found that the sr45-1 mutation broadly targets alternative splicing in vivo, including that of the SR45 pre-mRNA itself. Importantly, the enhanced SnRK1 levels in sr45-1 are suppressed by a proteasome inhibitor, indicating that SR45 promotes targeting of the SnRK1 protein for proteasomal destruction. Finally, we demonstrate that SR45 regulates alternative splicing of the Arabidopsis 5PTase13 gene, which encodes an inositol polyphosphate 5-phosphatase previously shown to interact with and regulate the stability of SnRK1 in vitro, thus providing a mechanistic link between SR45 function and the modulation of degradation of the SnRK1 energy sensor in response to sugars.