Convergent energy and stress signaling

Abstract

Plants are constantly confronted by multiple types of stress. Despite their distinct origin and mode of perception, nutrient deprivation and most stresses have an impact on the overall energy status of the plant, leading to convergent downstream responses that include largely overlapping transcriptional patterns. The emerging view is that this transcriptome reprogramming in energy and stress signaling is partly regulated by the evolutionarily conserved energy sensor protein kinases, SNF1 (sucrose non-fermenting 1) in yeast, AMPK (AMP-activated protein kinase) in mammals and SnRK1 (SNF1-related kinase 1) in plants. Upon sensing the energy deficit associated with stress, nutrient deprivation and darkness, SnRK1 triggers extensive transcriptional changes that contribute to restoring homeostasis, promoting cell survival and elaborating longer-term responses for adaptation, growth and development.

Figure 1

Transcriptome response to energy deprivation mediated by SnRK1 activation. Extensive transcriptional reprogramming is an important part of the convergent responses to stress, nutrient starvation and darkness [2,8,10,11,24,25]. Energy deficiency is sensed by the SnRK1 PKs that trigger the induction (280 genes) and repression (320 genes) of genes involved in a wide variety of cellular processes [2]. (a) The SnRK1 target gene list was generated by filtering overlapped genes controlled by transient KIN10 activation in Arabidopsis mesophyll protoplasts and by various starvation conditions in cultured cells, seedlings and leaves. The microarray datasets were independently generated and are publicly accessible [2]. These 600 SnRK1 target genes are regulated in an opposite manner by sugar availability because glucose and sucrose inactivate SnRK1. (b) The functional categories for the SnRK1 target genes in the pie chart were assigned based on the classification in the MapMan program [8] and sorted in Excel.

Figure 2

Decoding diverse stress as convergent energy signaling. Besides triggering different stress-specific responses, multiple types of stress ultimately converge and generate energy-deficiency signals that result in the activation of the SnRK1 energy sensors [2,8,10,24,25]. Conversely, sugars have a repressive effect [2,18,20,21]. Phosphorylation at a conserved threonine residue (e.g. T175 in Arabidopsis KIN10, T210 in yeast SNF1 and T172 in human AMPKα) is required for SnRK1 activity, but the ultimate metabolic signal responsible for SnRK1 activation remains enigmatic. Upstream protein kinases (PKs), protein phosphatases (PPs), and additional regulatory subunits might contribute to the fine-tuning of the system and possibly confer tissue and cell-type specificity [33]. Activated SnRK1 initiates an energy-saving program at several levels, including massive transcriptional reprogramming that targets a wide range of cellular processes. The S-group bZIP (basic leucine zipper) transcription factors (TFs) mediate some SnRK1 activated genes [2]. In addition to contributing to the maintenance of cellular energy homeostasis and tolerance to stress, SnRK1 has profound effects at the whole-organism level, influencing growth, viability, reproduction and senescence, and is thus proposed to be central in the integration of metabolic, stress and developmental signals [2]. SnRK1 also phosphorylates and regulates enzymes mostly involved in carbon (C) and nitrogen (N) metabolism [,,,–42]. Abbreviations: AGPase, ADP-glucose pyrophosphorylase; HMGCoAR, 3-hydroxy-3-methylglutaryl-coenzyme A reductase; NR, nitrate reductase; SPS, sucrose phosphate synthase; TCA, tricarboxylic acid cycle; TPS5, trehalose-6-phosphate synthase 5.

Figure 3

A model depicting interactions of putative nutrient and energy signaling components. The blue components are part of a network that, upon sensing nutrient and/or energy deficiency, restricts growth and promotes nutrient remobilization, survival and tolerance to stress. The pink components form a hypothetical antagonistic network that couples nutrient and/or energy availability with growth. In response to energy deprivation, SnRK1 orchestrates an energy-saving program through direct enzyme regulation and through extensive transcriptional reprogramming that involves at least the S-group bZIP (basic leucine zipper) transcription factors (TFs) [2]. SnRK1 response is blocked by sugars, partly through the product of hexokinase (HXK) activity, glucose-6-phosphate (G6P) [63]. In addition to its catalytic role, HXK1 has a distinct signaling function in the nucleus, where it regulates the expression of photosynthetic genes, among others [71,72]. HXK might act in a cooperative manner with the TOR (target of rapamycin) PK (protein kinase) in the growth-promoting network. As in mammals [75], nutritional information might be conveyed to plant TOR through the PI3K/VPS34 protein [78]. In nutrient-rich conditions, mTOR (mammalian TOR) promotes growth partly through regulation of the translational machinery [79] and blocks the translation-inhibitory pathway mediated by the amino-acid-deficiency-sensing GCN2 PK. Similar functions seem to apply to the plant TOR [76,77] and to some extent to GCN2 [81,82]. Plants could have evolved unique modes of interplay between the SnRK1 and TOR pathways. A scenario is proposed where various growth-promoting and growth-limiting pathways interact to regulate metabolism, stress tolerance and development in response to the environment and nutrient availability. Solid lines denote proven connections in plants, whereas broken lines represent connections described for other organisms that might or might not exist in plants.