The Potassium-Dependent Transcriptome of Arabidopsis Reveals a Prominent Role of Jasmonic Acid in Nutrient Signaling  

Abstract

Full genome microarrays were used to assess transcriptional responses of Arabidopsis seedlings to changing external supply of the essential macronutrient potassium (K+). Rank product statistics and iterative group analysis were employed to identify differentially regulated genes and statistically significant coregulated sets of functionally related genes. The most prominent response was found for genes linked to the phytohormone jasmonic acid (JA). Transcript levels for the JA biosynthetic enzymes lipoxygenase, allene oxide synthase, and allene oxide cyclase were strongly increased during K+ starvation and quickly decreased after K+ resupply. A large number of well-known JA responsive genes showed the same expression profile, including genes involved in storage of amino acids (VSP), glucosinolate production (CYP79), polyamine biosynthesis (ADC2), and defense (PDF1.2). Our findings highlight a novel role of JA in nutrient signaling and stress management through a variety of physiological processes such as nutrient storage, recycling, and reallocation. Other highly significant K+-responsive genes discovered in our study encoded cell wall proteins (e.g. extensins and arabinogalactans) and ion transporters (e.g. the high-affinity K+ transporter HAK5 and the nitrate transporter NRT2.1) as well as proteins with a putative role in Ca2+ signaling (e.g. calmodulins). On the basis of our results, we propose candidate genes involved in K+ perception and signaling as well as a network of molecular processes underlying plant adaptation to K+ deficiency.

Natural Variation of Arabidopsis Root Architecture Reveals Complementing Adaptive Strategies to Potassium Starvation

“…In a classic study, Drew (1975) showed an increase in overall lateral root (LR) growth of barley seedlings, even when K was supplied only to parts of the root system. Conversely, a typical response of Arabidopsis (Arabidopsis thaliana) Columbia (Col-0) seedlings to low K is the drastic reduction of LR elongation (Armengaud et al, 2004;Shin and Schachtman, 2004). Conflicting data have been published on the effect of low K on main root (MR) growth in the same species, ranging from no effect (Shin and Schachtman, 2004) to impaired MR elongation (Jung et al, 2009;Kim et al, 2010).…”

“…Conflicting data have been published on the effect of low K on main root (MR) growth in the same species, ranging from no effect (Shin and Schachtman, 2004) to impaired MR elongation (Jung et al, 2009;Kim et al, 2010). Some components involved in K starvation responses have been identified, such as jasmonates (Armengaud et al, 2004(Armengaud et al, , 2010, reactive oxygen species (Shin and Schachtman, 2004), and ethylene (Jung et al, 2009). However, the molecular identity of a root K sensor acting at the base of the signaling cascade is so far unknown.…”

“…Even in fertilized fields, rapid K uptake by plants can lead to K shortage in the root environment, especially early in the growth season. Root adaptations to K deficiency (low K) take place at the physiological (Armengaud et al, 2004;Shin and Schachtman, 2004;Alemán et al, 2011), metabolic (Armengaud et al, 2009a), and morphological levels. In a classic study, Drew (1975) showed an increase in overall lateral root (LR) growth of barley seedlings, even when K was supplied only to parts of the root system.…”

Polyamines: potent modulators of plant responses to stress

“…They further noted that the increase in ADC activity, induced by K ' deficiency, did not appear to involve changes in mRNA or protein abundance, suggesting the post-translational regulation mechanism for ADC activation. Recently, full genome microarrays were used to assess transcriptional responses of Arabidopsis seedlings to changing external supply of K ' (Armengaud et al 2004). The physiological rationale for Put increase is unclear.…”

The role of calcium sensor-interacting protein kinases in plant adaptation to potassium-deficiency: new answers to old questions

“…Although cellular and tissue K + -homeostasis can protect metabolically active cells from serious K + -deficiency for a limited period of time, it is clear that a plant that experiences long-term K + -deficiency will have to re-prioritise its growth, development and metabolism to achieve maximal seed production with limited resources. Research in our lab has identified jasmonic acid (JA) as a potential central integrator of the adaptation process [9]. Microarray analysis showed that a large percentage of the K + -responsive transcriptome is related to JA, and a rise of JA during K + -deficiency, as well as the specificity of this response for K + -deficiency, have since been confirmed [A Amtmann, P Armengaud, unpublished data].…”