Wheat inositol pyrophosphate kinase TaVIH2-3B modulates cell-wall composition for drought tolerance in Arabidopsis

Inositol pyrophosphates (PP-InsPs) are high-energy cellular molecules involved in different signalling and regulatory responses. Two distinct classes of inositol phosphate kinases responsible for the synthesis of PP-InsPs have been identified in Arabidopsis i.e. ITPKinase (inositol 1,3,4 trisphosphate 5/6 kinase) and PP-IP5Kinase (diphosphoinositol pentakisphosphate kinases). Plant PP-IP5Ks are capable of synthesizing InsP8 and were shown to control pathogenic defence and phosphate response signals. However, other roles offered by plant PP-IP5Ks, especially towards abiotic stress, remain poorly understood. Here, we characterized two Triticum aestivum L. (hexaploid wheat) PPIP5K homologs, TaVIH1 and TaVIH2, for their physiological functions. We demonstrated that wheat VIH proteins could utilize InsP7 as the substrate to produce InsP8, a process that requires the functional VIH-kinase domains. At the transcriptional level, both TaVIH1 and TaVIH2 are expressed in different wheat tissues, including developing grains, but show selective response to abiotic stresses during drought-mimic experiments. Overexpression of TaVIH2-3B homolog in Arabidopsis conferred tolerance to drought stress and rescued the sensitivity of Atvih2 mutants. RNAseq analysis of TaVIH2-3B transgenic lines of Arabidopsis showed a genome-wide reprogramming with remarkable effects on cell-wall biosynthesis genes with enhanced the accumulation of polysaccharides (arabinogalactan, cellulose and arabinoxylan). Overall, this work identifies a novel function of VIH proteins, implying their roles in modulating cell-wall homeostasis genes and providing water-deficit stress tolerance.