The upregulation of thiamine (vitamin B1) biosynthesis in Arabidopsis thaliana seedlings under salt and osmotic stress conditions is mediated by abscisic acid at the early stages of this stress response

Maria Rapala-Kozik,Agnieszka K Banas,Natalia Wolak,Marta Kujda

doi:10.1186/1471-2229-12-2

Abstract

BackgroundRecent reports suggest that vitamin B1 (thiamine) participates in the processes underlying plant adaptations to certain types of abiotic and biotic stress, mainly oxidative stress. Most of the genes coding for enzymes involved in thiamine biosynthesis in Arabidopsis thaliana have been identified. In our present study, we examined the expression of thiamine biosynthetic genes, of genes encoding thiamine diphosphate-dependent enzymes and the levels of thiamine compounds during the early (sensing) and late (adaptation) responses of Arabidopsis seedlings to oxidative, salinity and osmotic stress. The possible roles of plant hormones in the regulation of the thiamine contribution to stress responses were also explored.ResultsThe expression of Arabidopsis genes involved in the thiamine diphosphate biosynthesis pathway, including that of THI1, THIC, TH1 and TPK, was analyzed for 48 h in seedlings subjected to NaCl or sorbitol treatment. These genes were found to be predominantly up-regulated in the early phase (2-6 h) of the stress response. The changes in these gene transcript levels were further found to correlate with increases in thiamine and its diphosphate ester content in seedlings, as well as with the enhancement of gene expression for enzymes which require thiamine diphosphate as a cofactor, mainly α-ketoglutarate dehydrogenase, pyruvate dehydrogenase and transketolase. In the case of the phytohormones including the salicylic, jasmonic and abscisic acids which are known to be involved in plant stress responses, only abscisic acid was found to significantly influence the expression of thiamine biosynthetic genes, the thiamine diphosphate levels, as well as the expression of genes coding for main thiamine diphosphate-dependent enzymes. Using Arabidopsis mutant plants defective in abscisic acid production, we demonstrate that this phytohormone is important in the regulation of THI1 and THIC gene expression during salt stress but that the regulatory mechanisms underlying the osmotic stress response are more complex.ConclusionsOn the basis of the obtained results and earlier reported data, a general model is proposed for the involvement of the biosynthesis of thiamine compounds and thiamine diphosphate-dependent enzymes in abiotic stress sensing and adaptation processes in plants. A possible regulatory role of abscisic acid in the stress sensing phase is also suggested by these data.

Highlights

Recent reports suggest that vitamin B1 participates in the processes underlying plant adaptations to certain types of abiotic and biotic stress, mainly oxidative stress
Increased expression of thiamine biosynthesis genes during early response of Arabidopsis seedlings to oxidative, salt and osmotic stress The expression of the four main genes involved in thiamine biosynthesis in A. thaliana was analyzed during different phases of the responses to oxidative (0.25 μM paraquat; PQ), salt (200 mM NaCl) and osmotic (200 mM sorbitol; SOR) stress conditions
A fast sensing response by Arabidopsis seedlings to environmental changes (Figure 2) was observed through increases in the expression of two genes involved in early steps of thiamine biosynthesis, THI1 and THIC (2.9- and 2.2-fold increases, respectively) in the presence of high concentrations of salt or SOR, but not PQ

Summary

Introduction

Recent reports suggest that vitamin B1 (thiamine) participates in the processes underlying plant adaptations to certain types of abiotic and biotic stress, mainly oxidative stress. Plants can synthesize TDP de novo from simple precursors via biosynthetic pathways that bear the hallmarks of the systems utilized by both bacteria and yeast [2,3,4,5]. In this regard, the early stages of TDP biosynthesis include two parallel pathways. In the second of the parallel pathways, the thiazole moiety of thiamine (4-methyl-5-(2-hydroxyethyl)-thiazole phosphate, HET-P) is synthesized from glycine, NAD+ and a sulfur donor protein, in a similar manner to the system utilized in yeast [7]. The major enzyme involved in the HET-P formation is encoded by the THI1 gene, which has been characterized in both Arabidopsis and Zea mays [8,9]

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