Abstract
Engineering osmotolerant plants is a challenge for modern agriculture. An interaction between osmotic stress response and phosphate homeostasis has been reported in plants, but the identity of molecules involved in this interaction remains unknown. In this study we assessed the role of phytic acid (PA) in response to osmotic stress and/or phosphate deficiency in Arabidopsis thaliana. For this purpose, we used Arabidopsis lines (L7 and L9) expressing a bacterial beta-propeller phytase PHY-US417, and a mutant in inositol polyphosphate kinase 1 gene (ipk1-1), which were characterized by low PA content, 40% (L7 and L9) and 83% (ipk1-1) of the wild-type (WT) plants level. We show that the PHY-overexpressor lines have higher osmotolerance and lower sensitivity to abscisic acid than ipk1-1 and WT. Furthermore, PHY-overexpressors showed an increase by more than 50% in foliar ascorbic acid levels and antioxidant enzyme activities compared to ipk1-1 and WT plants. Finally, PHY-overexpressors are more tolerant to combined mannitol stresses and phosphate deficiency than WT plants. Overall, our results demonstrate that the modulation of PA improves plant growth under osmotic stress, likely via stimulation of enzymatic and non-enzymatic antioxidant systems, and that beside its regulatory role in phosphate homeostasis, PA may be also involved in fine tuning osmotic stress response in plants.
Highlights
Soil salinity adversely affects plant growth and development and constitutes de facto, one of the major environmental constraints limiting agricultural production worldwide[1]
In combination with our previous results[51] showing that the overexpression of PHY-US417 improves the growth of plants under Pi deficiency, we demonstrate here that the PHY-US417 over-expression increases antioxidant activities and osmotic stress tolerance, and improves the plant capacity to tolerate combined osmotic stress and Pi deficiency
By contrast to ipk[1], this salt hypersensitivity was not observed in PHY-overexpressors (L7 and L9), which rather exhibit higher seed germination rates under salt stress compared to WT (82–86% for L7 and L9 versus 67% for WT)
Summary
Soil salinity adversely affects plant growth and development and constitutes de facto, one of the major environmental constraints limiting agricultural production worldwide[1]. Two major PA biosynthesis pathways have been reported in higher plants, namely the lipid-dependent and the lipid-independent signaling pathways (for review see[19,20]) These two pathways differ essentially in their early intermediate steps leading from myo-inositol (Ins) to myo-inositol trisphosphates InsP319. In addition to its important cellular roles, PA is considered as anti-nutritional factor, preventing the uptake of essential minerals such as iron, zinc, magnesium and calcium since it acts as a strong chelator of cations[27,28] and proteins[29] To overcome these problems, the reduction of seed phytate content can serve as a sustainable solution[19] and several low phytic acid (lpa) mutants have been generated by classical mutations, or RNAi approaches (for review[17]). Mutation that perturbs the end of the PA pathway, in one of the genes coding for inositol kinases (e.g. IPK1) causes a significant reduction in PA as observed in Arabidopsis Atipk1.135, rice Osipk[136] and maize Zm ipk[137,38]
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