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 Ca(2+) 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.

Figure 1.

Biological system and experimental design. A, Phenotype of Arabidopsis seedlings grown vertically on petri dishes for 2 weeks after germination. Left, Complete medium (2 mm K⁺). Right, K⁺-free medium (−K). For composition of media see “Materials and Methods.” B, Resupply experiments; 2-week-old K-starved seedlings were provided with 5 mL of sterile −K medium supplemented with 10 mm KCl. Control plants received fresh −K medium with or without additional 10 mm NaCl. C, Overview of microarray experiments. Each column represents one array. Control samples are shown in green, treated samples in red. All eight comparisons were carried out for three independent biological replicates (24 arrays in total).

Figure 2.

Seedling ion content after K⁺ starvation and resupply. Potassium, sodium, and calcium levels were measured with ICP-OES in shoots (A) and roots (B) of 2-week-old seedlings grown either on complete medium (black boxes) or on −K⁺ medium (white boxes). Ion content was also analyzed at 6 and 24 h after resupplying 10 mm KCl (gray boxes), 10 mm NaCl (bold dashed boxes), or a fresh K⁺-free-solution (light dashed boxes) to K⁺-starved plants. Fifty seedlings were pooled for each sample. Averages and ses of three independent experiments are shown.

Figure 3.

Expression profiles of highly significant K⁺-responsive genes related to JA-related genes were extracted from RP lists for K⁺ resupply experiments with FDR below 0.001%. On the left side AGI number, common name (if available) and a short description based on MIPS, TAIR, or TIGR are given for each gene. Genes identified by iGA are shown in italics. Functional super-categories extracted from iGA (Tables II–V) are given as vertical labels. On the right side expression profiles over all experimental conditions (compare Fig. 1C) are shown. Tissues and treatments are given on the top. Colors indicate change of transcript level in the treated samples with respect to the control samples (red for up-regulation, green for down-regulation, see color bar at the bottom of Fig. 4). For resupply treatments (+K⁺) respective controls are given in brackets (Na for supply of Na⁺ instead of K⁺, 0 for supply of K⁺-free medium). K⁺-starved plants were compared to plants grown on K⁺-sufficient medium. For each comparison data from three replicate experiments are shown.

Figure 4.

Expression profiles of highly significant K⁺-responsive genes related to cell walls, transport, or calcium signaling. For explanation see Figure 3.

Figure 5.

Model of molecular processes underlying plant adaptation to K⁺ deficiency. Putative components of K⁺ deficiency and adaptive responses are shown in boxes. Connecting lines are based on K⁺-responsive genes identified in this study (shown in italics) and published information (see text). Black arrows indicate stimulation, dashed lines inhibition. Known K⁺ deficiency symptoms are shown in white boxes. Putative components of signaling events are indicated in dark gray. Lighter gray shading marks different JA-dependent processes potentially leading to adaptive nutrient management and defense responses. For further discussion see text.