Inositol hexakisphosphate biosynthesis underpins PAMP‐triggered immunity to Pseudomonas syringae pv. tomato in Arabidopsis thaliana but is dispensable for establishment of systemic acquired resistance

Abstract

Phytic acid (inositol hexakisphosphate, InsP6) is an important phosphate store and signal molecule necessary for maintenance of basal resistance to plant pathogens. Arabidopsis thaliana (‘arabidopsis’) has three genes encoding myo‐inositol phosphate synthases (IPS1–3), the enzymes that catalyse conversion of glucose‐6‐phosphate to InsP, the first step in InsP6 biosynthesis. There is one gene for inositol‐(1,3,4,5,6)‐pentakisphosphate 2‐kinase (IPK1), which catalyses the final step. Previously, we showed that mutation of IPS2 and IPK1 but not IPS1 increased susceptibility to pathogens. Our aim was to better understand the InsP6 biosynthesis pathway in plant defence. Here we found that the susceptibility of arabidopsis (Col‐0) to virulent and avirulent Pseudomonas syringae pv. tomato was also increased in ips3 and ips2/3 double mutants. Also, ipk1 plants had compromised expression of local acquired resistance induced by treatment with the pathogen‐derived molecular pattern (PAMP) molecule flg22, but were unaffected in other responses to flg22, including Ca2+ influx and the oxidative burst, seedling root growth inhibition, and transcriptional up‐regulation of the PAMP‐triggered genes MITOGEN‐ACTIVATED PROTEIN KINASE (MPK) 3, MPK11, CINNAMYL ALCOHOL DEHYDROGENASE 5, and FLG22‐INDUCED RECEPTOR‐LIKE KINASE 1. IPK1 mutation did not prevent the induction of systemic acquired resistance by avirulent P. syringae. Also, ips2 and ips2/3 double mutant plants, like ipk1, were hypersusceptible to P. syringae but were not compromised in flg22‐induced local acquired resistance. The results support the role of InsP6 biosynthesis enzymes in effective basal resistance and indicate that there is more than one basal resistance mechanism dependent upon InsP6 biosynthesis.

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

“…These results indicate that the enhanced susceptibility of ips2 and ipk1 is not related to low SA levels, but could be caused by the disruption of InsP 6 biosynthesis ( Murphy et al, 2008 ). Further studies of the ipk1 mutant and of loss-of-function mutants of another IPS isoform ( IPS3 ) confirmed an involvement of InsP 6 in basal pathogen responses ( Poon et al, 2020 ). While displaying a higher susceptibility to Pst than wild-type plants, when the ips2 , ips3 , and ipk1 mutants were assessed for SAR acquirement, no impairment was detected.…”

“…This is because studies showing an involvement of InsPs and PP-InsPs in SA-dependent immunity have in part contradictory outcomes. Arabidopsis mutants disrupted in InsP 6 biosynthesis, for instance, showed increased susceptibility to bacterial, fungal and viral infections ( Murphy et al, 2008 ; Poon et al, 2020 ), as well as to cyst nematode infestation ( Jain, 2015 ). In fact, the Arabidopsis ips2 and ipk1 mutants defective in the activities of enzymes for the first and last steps in InsP 6 biosynthesis, respectively, were similarly susceptible to microbial pathogens than NahG -transgenic lines and to sid2 mutants, both of which are unable to accumulate normal levels of SA ( Murphy et al, 2008 ).…”

“…While displaying a higher susceptibility to Pst than wild-type plants, when the ips2 , ips3 , and ipk1 mutants were assessed for SAR acquirement, no impairment was detected. Besides, all mutants except ipk1 presented flg22-induced resistance to Pst , indicating that PTI was inhibited in ipk1 only ( Poon et al, 2020 ). In this case, however, disruption of InsP 6 synthesis in ipk1 did not affect typical responses to flg22, such as Ca 2+ influx, oxidative burst, root growth inhibition and activation of PAMP-triggered genes.…”

Arabidopsis inositol polyphosphate kinases IPK1 and ITPK1 modulate crosstalks between SA-dependent immunity and phosphate-starvation responses

“…Murphy et al (2008) however did not find noticeable change either in the basal SA levels or its increase upon avirulent pathogen challenge in ipk1-1 . Further, although Poon et al (2020) did not measure the endogenous expression levels of FRK1 or other PTI markers, their induction upon PAMP-treatment was not affected in ipk1-1 . Ma et al (2017) in contrast showed impaired induction of FRK1 and other PTI responses in ipk1-1 (also in mips1 and mips2 ) with PAMP-exposure.…”

“…Defenses against the cyst nematode is also reduced in the ipk1-1 plants (Jain, 2015). Recently, it was shown that while ipk1-1 plants remain deficient in induction of local resistance, PTI hallmarks such as intracellular Ca 2+ spike, ROS production, and upregulated expression of responsive markers remained comparable to wild-type plants (Poon et al ., 2020). An earlier study though contrastingly claimed that induction of PTI markers upon PAMP-treatment are deficient in ipk1-1 (Ma et al ., 2017).…”