Enhancing inositol pyrophosphate accumulation in plants alters growth, phosphate homeostasis, and insect herbivory

Phosphate (Pi) is a critical nutrient for plants and is often a limiting factor in food production, as many agricultural soils are limited in available Pi. Inositol pyrophosphates (PP-InsPs) are signaling molecules involved in Pi sensing and jasmonic acid (JA)-regulated plant defense. Here, we report that overexpression of 1,3,4-trisphosphate 5/6-kinase 1 (ITPK1) and the kinase domain of the dual-domain diphosphoinositol pentakisphosphate kinase 2 (VIP2KD) in Arabidopsis thaliana results in unique elevations in PP-InsPs, accompanied by altered leaf growth and senescence patterns, as well as delayed time to flowering. While plants overexpressing ITPK1 and VIP2KD (ITPK1 OX and VIP2KD OX) accumulated significantly lower levels of Pi, transcriptomic and qRT-PCR analysis revealed that these plants showed elevated expression of Pi starvation response genes. Our transcriptomic analysis also revealed ITPK1 OX and VIP2KD OX showed a significant enrichment in differentially expressed genes relating to plant defense and hypoxia. Of the two transgenic types, VIP2KD OX had significantly higher expression of more diverse plant defense-related differentially expressed genes and showed greater resistance to Trichoplusia ni compared to WT and ITPK1 OX plants. ITPK1 OX, although also having elevated PP-InsPs, was fed upon by insect larvae comparably to WT plants. Taken together, our data indicate the elevation of certain PP-InsPs may be a useful strategy for developing new traits in crop plants.