Specific Recruitment of Phosphoinositide Species to the Plant-Pathogen Interfacial Membrane Underlies Arabidopsis Susceptibility to Fungal Infection

Qin, Li; Zhou, Zhuqing; Li, Qiang; Zhai, Chun; Liu, Lijiang; Quilichini, Teagen D.; Gao, Peng; Kessler, Sharon A; Jaillais, Yvon; Datla, Raju; Peng, Gary; Xiang, Daoquan; Wei, Yangdou

doi:10.1105/tpc.19.00970

Cited by 55 publications

(51 citation statements)

References 118 publications

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“…The EHM was found to differ in its molecular composition from the conventional PM (Hückelhoven & Panstruga, 2011;Gil & Gay, 1977;Roberts et al, 1993;Micali et al, 2011;Koh et al, 2005). Remarkably, two recent studies reported that the EHM is enriched in PI(4,5)P 2 similarly as described in this study for the pollen endo-PM (Shimada et al, 2019;Qin et al, 2020). Future work on the pollen endo-PM needs to track the genesis of this special interface during male gamete differentiation and to investigate its functional significance.…”

Section: The Endo-pm Of the Pollen Vegetative Cell Is Enriched For Pisupporting

confidence: 68%

Lipid anchoring and electrostatic interactions target the phospholipase NOT-LIKE-DAD to pollen endo-plasma membrane

Laurine

Padula

Jacquier

et al. 2020

Preprint

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Phospholipases are ubiquitous enzymes that cleave phospholipids, one major constituent of membranes. They are thus essential for many developmental processes, including male gamete development. In flowering plants, mutation of phospholipase NOT-LIKE-DAD (NLD) leads to peculiar defects in sexual reproduction. Indeed, pollination of a wild-type female with mutant pollen generates haploid embryos containing solely maternal genetic information. Contrary to previous reports NLD does not localize to cytosol and plasma membrane (PM) of sperm cells but to the pollen endo-plasma membrane (endo-PM), a specific membrane derived from the PM of the pollen vegetative cell that encircles the two sperm cells. Pharmacological approaches coupled with targeted mutagenesis revealed that lipid anchoring together with electrostatic interactions between membrane and NLD are involved in the attachment of NLD to this atypical endo-PM. Membrane surface-charge and anionic lipid bio-sensors indicated that phosphatidylinositol-4,5-bisphosphate (PIP(4,5)P2) is enriched in the endo-PM as compared to the PM. Our results uncover a unique example of how membrane electrostatic properties can specify a unique polar domain (i.e. endo-PM), which is critical for plant reproduction and gamete formation.

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Section: The Endo-pm Of the Pollen Vegetative Cell Is Enriched For Pisupporting

confidence: 68%

Lipid anchoring and electrostatic interactions target the phospholipase NOT-LIKE-DAD to pollen endo-plasma membrane

Laurine

Padula

Jacquier

et al. 2020

Preprint

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“…PtdIns(4,5)P 2 accumulates in Arabidopsis plants at sites of pathogen infection (Shimada et al ., 2019; Qin et al ., 2020), and PtdIns(4,5)P 2 was identified as a susceptibility factor in Arabidopsis (Qin et al ., 2020). Therefore, the induction of StIPP, an enzyme hydrolyzing PtdIns(4,5)P 2 at the EHM, might be part of a defensive strategy of the host plant that involves limiting the availability of PtdIns(4,5)P 2 at infection sites.…”

Section: Discussionmentioning

confidence: 99%

“…A role for phosphoinositides in plant pathogen defense was recently proposed based on the observation that a fluorescent reporter for PtdIns(4,5)P 2 as well as a PI4P 5-kinase mediating the biosynthesis of PtdIns(4,5)P 2 accumulated in extra-invasive hyphal membranes upon infection of Arabidopsis thaliana with the pathogenic fungus Colletotrichum higginsianum (Shimada et al, 2019). Moreover, Qin et al (2020) recently identified PtdIns(4,5)P 2 as a susceptibility factor associating with the EHM after powdery mildew infection of Arabidopsis.…”

Section: Introductionmentioning

confidence: 99%

A phosphoinositide 5‐phosphatase from Solanum tuberosum is activated by PAMP‐treatment and may antagonize phosphatidylinositol 4,5‐bisphosphate at Phytophthora infestans infection sites

Rausche¹,

Stenzel²,

Stauder³

et al. 2020

New Phytologist

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Potato (Solanum tuberosum) plants susceptible to late blight disease caused by the oomycete Phytophthora infestans display enhanced resistance upon infiltration with the pathogen-associated molecular pattern (PAMP), Pep-13. Here, we characterize a potato gene similar to Arabidopsis 5-phosphatases which was identified in transcript arrays performed to identify Pep-13 regulated genes, and termed StIPP. Recombinant StIPP protein specifically dephosphorylated the D5-position of phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P 2) in vitro. Other phosphoinositides or soluble inositolpolyphosphates were not converted. When transiently expressed in tobacco (Nicotiana tabacum) pollen tubes, a StIPP-YFP fusion localized to the subapical plasma membrane and antagonized PtdIns(4,5)P 2-dependent effects on cell morphology, indicating in vivo functionality. Phytophthora infestans-infection of N. benthamiana leaf epidermis cells resulted in relocalization of StIPP-GFP from the plasma membrane to the extra-haustorial membrane (EHM). Colocalizion with the effector protein RFP-AvrBlb2 at infection sites is consistent with a role of StIPP in the plant-oomycete interaction. Correlation analysis of fluorescence distributions of StIPP-GFP and biosensors for PtdIns (4,5)P 2 or phosphatidylinositol 4-phosphate (PtdIns4P) indicate StIPP activity predominantly at the EHM. In Arabidopsis protoplasts, expression of StIPP resulted in the stabilization of the PAMP receptor, FLAGELLIN-SENSITIVE 2, indicating that StIPP may act as a PAMP-induced and localized antagonist of PtdIns(4,5)P 2-dependent processes during plant immunity.

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“…In previous studies, a contribution of phosphoinositides to the regulation of important physiological processes has also been reported for the vegetative portion of plants. These studies describe roles for phosphoinositides in clathrin recruitment (König et al, 2008;Ischebeck et al, 2013); the polarization of auxin efflux carriers of the PIN-FORMED (PIN)-family (Mei et al, 2012;Ischebeck et al, 2013; Tejos et al, 2014), of D6P-kinases (Barbosa et al, 2016) and of BRX and PAX proteins (Marhava et al, 2020); the control of cytokinesis (Lin et al, 2019); cell wall deposition (Rodriguez-Villalon et al, 2015), and roles in membrane trafficking during plant pathogen interactions (Shimada et al, 2019;Qin et al, 2020). While these reports together may suggest the presence of PtdIns(4,5)P 2 in membrane nanodomains occupied by phosphoinositides, in Arabidopsis hypocotyl cells we detected such nanodomains by SD only upon application of salt (Supplemental Fig.…”

Section: Ptdins(45)p 2 Nanodomains Only In Pollen Tubes and Other Opmentioning

confidence: 99%

Plasma membrane nano-organization specifies phosphoinositide effects on Rho-GTPases and actin dynamics in tobacco pollen tubes

Fratini

Krishnamoorthy

Stenzel

et al. 2020

Preprint

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Pollen tube growth requires coordination of cytoskeletal dynamics and apical secretion. The regulatory phospholipid, phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) is enriched in the subapical plasma membrane of pollen tubes and can influence both actin dynamics and secretion. How alternative PtdIns(4,5)P2-effects are specified is unclear. Spinning disc microscopy (SD) reveals dual distribution of a fluorescent PtdIns(4,5)P2-reporter in dynamic plasma membrane nanodomains vs. apparent diffuse membrane labelling, consistent with spatially distinct coexisting pools of PtdIns(4,5)P2. Several PI4P 5-kinases (PIP5Ks) can generate PtdIns(4,5)P2 in pollen tubes. Despite localizing to one membrane region, AtPIP5K2 and NtPIP5K6 display distinctive overexpression effects on cell morphologies, respectively related to altered actin dynamics or membrane trafficking. When analyzed by SD, AtPIP5K2-EYFP associated with nanodomains, whereas NtPIP5K6-EYFP localized diffusely. Chimeric AtPIP5K2 and NtPIP5K6 variants with reciprocally swapped membrane-associating domains evoked reciprocally shifted effects on cell morphology upon overexpression. Overall, PI4P 5-kinase variants targeted to nanodomains stabilized actin, suggesting a specific function of PtdIns(4,5)P2-nanodomains. A distinct role of nanodomain-associated AtPIP5K2 in actin regulation is further supported by proximity to and interaction with the Rho-GTPase NtRac5, and by functional interplay with elements of ROP-signalling. Plasma membrane nano-organization may thus aid the specification of PtdIns(4,5)P2-functions to coordinate cytoskeletal dynamics and secretion in pollen tubes.

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Specific Recruitment of Phosphoinositide Species to the Plant-Pathogen Interfacial Membrane Underlies Arabidopsis Susceptibility to Fungal Infection

Abstract: Plant biotrophic and hemibiotrophic pathogens modulate cellular distribution of host phosphoinositides and recruit PI(4,5)P 2 to the plant-pathogen interfacial membrane as a susceptibility factor for disease development.

Cited by 55 publications

References 118 publications

Lipid anchoring and electrostatic interactions target the phospholipase NOT-LIKE-DAD to pollen endo-plasma membrane

Lipid anchoring and electrostatic interactions target the phospholipase NOT-LIKE-DAD to pollen endo-plasma membrane

A phosphoinositide 5‐phosphatase from Solanum tuberosum is activated by PAMP‐treatment and may antagonize phosphatidylinositol 4,5‐bisphosphate at Phytophthora infestans infection sites

Plasma membrane nano-organization specifies phosphoinositide effects on Rho-GTPases and actin dynamics in tobacco pollen tubes

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