Phosphatidylinositol 4-Phosphate Negatively Regulates Chloroplast Division in Arabidopsis

Okazaki, Kumiko; Miyagishima, Shin-ya; Wada, Hajime

doi:10.1105/tpc.115.136234

Cited by 31 publications

(25 citation statements)

References 54 publications

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“…These findings suggest that increased levels of membrane PI4P and PI(4,5)P 2 could also disrupt thylakoid formation and grana assembly during chloroplast development in rice. Interestingly, this result coincides with reported evidence whereby inhibition of PI4P synthesis accelerates chloroplast division, supporting the idea that PI4P negatively regulates chloroplast division in Arabidopsis (Okazaki et al, 2015). Taken together, these findings suggest that the massive accumulation of membrane PI4P and PI(4,5)P 2 resulting from terminated GH1 production could disturb organelle development and cytoarchitecture.…”

Section: Resultssupporting

confidence: 90%

A SAC phosphoinositide phosphatase controls rice development via hydrolyzing phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate

Guo¹,

Chen²,

Lü

et al. 2019

Preprint

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30Phosphoinositides (PIs) as regulatory membrane lipids play essential roles in multiple 31 cellular processes. Although the exact molecular targets of PIs-dependent modulation 32 remain largely elusive, the effects of disturbed PIs metabolism could be employed to 33 propose regulatory modules associated with particular downstream targets of PIs. 34 Here, we identified the role of GRAIN NUMBER AND PLANT HEIGHT 1 (GH1), 35 which encodes a suppressor of actin (SAC) domain-containing phosphatase with 36 unknown function in rice. Endoplasmic reticulum-localized GH1 specifically 37 dephosphorylated and hydrolyzed phosphatidylinositol 4-phosphate (PI4P) and 38 phosphatidylinositol 4,5-bisphosphate [PI(4,5)P2]. Inactivation of GH1 resulted in 39 massive accumulation of both PI4P and PI(4,5)P2, while excessive GH1 caused their 40 depletion. Notably, superabundant PI4P and PI(4,5)P2 could both disrupt actin 41 cytoskeleton organization and suppress cell elongation. Interestingly, both PI4P and 42 PI(4,5)P2 inhibited actin-related proteins 2 and 3 (Arp2/3) complex-nucleated actin 43 branching networks in vitro, whereas PI(4,5)P2 showed more dramatic effect in a 44 dose-dependent manner. Overall, the overaccumulation of PI(4,5)P2 resulted from 45 dysfunction of SAC phosphatase possibly perturbs Arp2/3 complex-mediated actin 46 polymerization, thereby disordering the cell development. These findings imply that 47 Arp2/3 complex might be the potential molecular target of PI(4,5)P2-dependent 48 modulation in eukaryotes, thereby providing new insights into the relationship 49 between PIs homeostasis and plants growth and development. 50 51 Phosphoinositides (PIs) as a minor component of cell membranes and phosphorylated 52 derivatives of phosphatidylinositol are known to liberate the second messengers, 53 inositol 1,4,5-triphosphate and diacylglycerol in response to activation of cell surface 54 receptors (Boss and Im, 2012). Nevertheless, emerging evidence suggests that PIs also 55 play crucial roles as signaling molecules, functioning as regulatory lipids in various 56 fundamental cellular processes (Heilmann, 2016). A new detection approach further 57 confirmed that phosphatidylinositol 4-phosphate (PI4P) and phosphatidylinositol 58 4,5-bisphosphate [PI(4,5)P2] are the most abundant PIs in the cells (Balla, 2013; 59 Kielkowska et al., 2014). PI4P is phosphorylated by phosphatidylinositol phosphate 60 kinases, resulting in the production of PI(4,5)P2, while conversely PI(4,5)P2 is 61 dephosphorylated by PI phosphatases to generate PI4P, supporting the hypothesis that 62 turnover and dynamic formation of PIs is necessary for plant development (Gerth et 63 al., 2017).64 65 The plant actin cytoskeleton plays essential roles in cell morphogenesis, and the 66 dynamics of actin cytoskeleton drives the membrane deformation and trafficking, 67 which is required for polar cell growth and movement of vesicles and organelles 68 (Pleskot et al., 2014; Wang et al., 2017). This dynamic remodeling is controlled by 69 diverse actin-bin...

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Section: Resultssupporting

confidence: 90%

A SAC phosphoinositide phosphatase controls rice development via hydrolyzing phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate

Guo¹,

Chen²,

Lü

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…Only one study has detected PIP by radiolabeling experiments and found it, preferentially, in the outer leaflet of the chloroplast envelope (70). Mutants lacking enzymes for PI4P synthesis have more chloroplasts per cell, suggesting that PI4P negatively regulates chloroplast division (71). PI4P might also be a minor lipid in the chloroplast inner envelope membrane, where it could be bound by stromal proteins such as CPSFL1 and VIPP1 (56,57).…”

Section: Discussionmentioning

confidence: 99%

A Sec14 domain protein is required for photoautotrophic growth and chloroplast vesicle formation in Arabidopsis thaliana

Hertle

García-Cerdán

Armbruster

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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In eukaryotic photosynthetic organisms, the conversion of solar into chemical energy occurs in thylakoid membranes in the chloroplast. How thylakoid membranes are formed and maintained is poorly understood. However, previous observations of vesicles adjacent to the stromal side of the inner envelope membrane of the chloroplast suggest a possible role of membrane transport via vesicle trafficking from the inner envelope to the thylakoids. Here we show that the model plant Arabidopsis thaliana has a chloroplast-localized Sec14-like protein (CPSFL1) that is necessary for photoautotrophic growth and vesicle formation at the inner envelope membrane of the chloroplast. The cpsfl1 mutants are seedling lethal, show a defect in thylakoid structure, and lack chloroplast vesicles. Sec14 domain proteins are found only in eukaryotes and have been well characterized in yeast, where they regulate vesicle budding at the trans-Golgi network. Like the yeast Sec14p, CPSFL1 binds phosphatidylinositol phosphates (PIPs) and phosphatidic acid (PA) and acts as a phosphatidylinositol transfer protein in vitro, and expression of Arabidopsis CPSFL1 can complement the yeast sec14 mutation. CPSFL1 can transfer PIP into PA-rich membrane bilayers in vitro, suggesting that CPSFL1 potentially facilitates vesicle formation by trafficking PA and/or PIP, known regulators of membrane trafficking between organellar subcompartments. These results underscore the role of vesicles in thylakoid biogenesis and/or maintenance. CPSFL1 appears to be an example of a eukaryotic cytosolic protein that has been coopted for a function in the chloroplast, an organelle derived from endosymbiosis of a cyanobacterium.

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“…Based on these and other results, the authors proposed that PDV1 interaction with PI4P in the chloroplast envelope alters PDV1 affinity for DRP5B, which may alter the rate of chloroplast division. These findings implicate phosphoinositide signaling in the regulation of chloroplast division (Okazaki et al, 2015).…”

Section: Regulation Of Chloroplast Divisionmentioning

confidence: 63%

“…Recently, Okazaki et al (2015) reported that the phosphoinositide phosphatidylinositol 4-phosphate (PI4P) negatively regulates chloroplast division in Arabidopsis. Inhibition of phosphatidylinositol 4-kinase to reduce PI4P levels in chloroplast membranes accelerated chloroplast division, producing a larger population of smaller chloroplasts, similar to overexpression of PDV proteins (Okazaki et al, 2009).…”

Section: Regulation Of Chloroplast Divisionmentioning

confidence: 99%

The Molecular Machinery of Chloroplast Division

et al. 2017

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Phosphatidylinositol 4-Phosphate Negatively Regulates Chloroplast Division in Arabidopsis

Cited by 31 publications

References 54 publications

A SAC phosphoinositide phosphatase controls rice development via hydrolyzing phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate

A SAC phosphoinositide phosphatase controls rice development via hydrolyzing phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate

A Sec14 domain protein is required for photoautotrophic growth and chloroplast vesicle formation in Arabidopsis thaliana

The Molecular Machinery of Chloroplast Division

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