Regulation of plant biotic interactions and abiotic stress responses by inositol polyphosphates

Abstract

Inositol pyrophosphates (PP-InsPs), derivatives of inositol hexakisphosphate (phytic acid, InsP₆) or lower inositol polyphosphates, are energy-rich signaling molecules that have critical regulatory functions in eukaryotes. In plants, the biosynthesis and the cellular targets of these messengers are not fully understood. This is because, in part, plants do not possess canonical InsP₆ kinases and are able to synthesize PP-InsP isomers that appear to be absent in yeast or mammalian cells. This review will shed light on recent discoveries in the biosynthesis of these enigmatic messengers and on how they regulate important physiological processes in response to abiotic and biotic stresses in plants.

Keywords: auxin response; inositol pyrophosphate; jasmonic acid signaling pathway; phosphate homeostasis; plant biotic and abiotic stress responses; salicylic acid signaling pathway.

FIGURE 1

Inositol pyrophosphate biosynthesis pathway in plants and protein architecture of kinases. (A) ITPK1/2 and VIH1/2 phosphorylate InsP6 to generate 5-InsP7 and 1-InsP7, respectively. Further, VIH1/2 use 5-InsP7 as substrate to generate InsP8. The isomer identity of InsP8 remains unresolved but presumably represents the 1,5 and/or the 3,5-InsP8 isomer. VIH1/2 are also able to dephosphorylate 1/3,5-InsP8 and 1/3-InsP7 to InsP6. At low adenylate charge, the ITPK1 kinase domain also catalyzes the reverse reaction from 5-InsP7 to InsP6 in the presence of ADP to locally generate ATP. The gray arrows and question marks denote alternative routes of 1/3-InsP7 and 1/3,5-InsP8 synthesis, and the responsible enzymes, respectively. (B) Schematic representation of ITPK1, ITPK2, VIH1 and VIH2 architectures. Kinase domains are shown in dark gray, phosphatase domains in light gray.

FIGURE 2

Model for the ITPK1-dependent phosphorylation of InsP6 and 5-InsP7 removal and possible link of ITPK1 with VIHs and phosphate homeostasis. Upon Pi-deficiency, ATP levels drop and stimulate ITPK1 to transfer the P-phosphate from 5-InsP7 to ADP, leading to the local generation of ATP and decreased 5-InsP7 levels. Additionally, low ATP/ADP ratios (i.e., low adenylate charge) and low Pi levels cause the switch from kinase to phosphatase activity of VIH proteins to hydrolyze InsP8. Lacking PP-InsPs, the interaction between PHR1 and SPX1 is destabilized, which promotes the binding of PHR1 to the P1BS motif in the promoter region of PSI genes. As a result, the Pi starvation response is activated. When plant cells regain sufficient Pi, ATP levels increase and the kinase activity of ITPK1 is activated, leading to the generation of 5-InsP7, which further serves as substrate for the kinase-activated VIH proteins to produce InsP8. Consequently, the accumulation of PP-InsPs facilitates the binding of SPX proteins to PHR1 to suppress Pi starvation responses.

FIGURE 3

PP-InsPs and their kinases are involved in different abiotic and biotic stress responses in plants. PP-InsPs’ involvement in Pi homeostasis, hormone perception and regulation is depicted. Purple arrows indicate the kinase/phosphatase activity of the respective enzymes on InsPs and PP-InsPs. Gray arrows and red question marks depict a putative effect of XopH on PP-InsPs. Red arrows and T-shaped line indicate promotion and suppression of specific InsPs and PP-InsPs in regulating stress responses, respectively. Green arrows depict the interplay between plant hormones auxin, JA and SA, respectively. ITPK1 phosphorylates InsP6 to 5-InsP7. The latter serves as precursor for InsP8, which plays a crucial role in adaption to changing Pi levels. Additionally, InsP6 is degraded by XopH to potentially release Pi for the pathogen’s nutritional benefit. ITPK1 and VIH2 interaction is needed to maintain Pi homeostasis. Higher PP-InsPs are also involved in hormone perception and regulation. The ITPK1-generated 5-InsP7 is speculated to be involved in auxin and SA signaling. The VIH2- generated InsP8 has been proposed to represent a critical co-ligand of the JA receptor complex and is also assumed to regulate SA signaling. The bacterial type III effector XopH displays 1- phytase activity but may also have hydrolytic activities against PP-InsPs that might disrupt hormone-regulated defense mechanisms.