Abstract
Thiamine (vitamin B1) is ubiquitous and essential for cell energy supply in all organisms as a vital metabolic cofactor, known for over a century. In plants, it is established that biosynthesis de novo is taking place predominantly in green tissues and is furthermore limited to plastids. Therefore, transport mechanisms are required to mediate the movement of this polar metabolite from source to sink tissue to activate key enzymes in cellular energy generating pathways but are currently unknown. Similar to thiamine, polyamines are an essential set of charged molecules required for diverse aspects of growth and development, the homeostasis of which necessitates long-distance transport processes that have remained elusive. Here, a yeast-based screen allowed us to identify Arabidopsis (Arabidopsis thaliana) PUT3 as a thiamine transporter. A combination of biochemical, physiological, and genetic approaches permitted us to show that PUT3 mediates phloem transport of both thiamine and polyamines. Loss of function of PUT3 demonstrated that the tissue distribution of these metabolites is altered with growth and developmental consequences. The pivotal role of PUT3 mediated thiamine and polyamine homeostasis in plants, and its importance for plant fitness is revealed through these findings.
Highlights
Thiamine is essential for all organisms being well recognized in its diphosphorylated form, thiamine diphosphate (TDP; Supplemental Fig. S1), as a necessary cofactor for key metabolic enzymes involved in glycolysis and the citric acid cycle (Fitzpatrick and Thore, 2014)
This study was initiated by performing a complementation screen employing a cDNA library from Arabidopsis (Minet et al, 1992) with the yeast mutant CVY4, deficient in both the biosynthesis and the transport of thiamine (Vogl et al, 2008)
A single Arabidopsis locus (At5g05630) encoding a protein belonging to the amino acid permease family was found to restore growth in the presence of low levels of thiamine (1.2 mM), complementing the impairment in thiamine transport in this yeast strain (Fig. 1A)
Summary
Thiamine (vitamin B1) is essential for all organisms being well recognized in its diphosphorylated form, thiamine diphosphate (TDP; Supplemental Fig. S1), as a necessary cofactor for key metabolic enzymes involved in glycolysis and the citric acid cycle (Fitzpatrick and Thore, 2014). In plants, it is necessary for the Calvin cycle, the biochemical route of carbon fixation (Khozaei et al, 2015). A series of micrografting and biochemical experiments demonstrated that PUT3 is important for long-distance transport of both thiamine and polyamines and thereby revealed its importance for homeostasis of these essential molecules and maintenance of plant fitness
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