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Title: Overexpression of Arabidopsis thaliana PTEN caused accumulation of autophagic bodies in pollen tubes by disrupting phosphatidylinositol 3-phosphate dynamics

item ZHANG, YAN - Shandong Agricultural University
item LI, SHA - Shandong Agricultural University
item ZHOU, LIANG-ZI - Shandong Agricultural University
item FOX, EMILY - University Of California
item PAO, JAMES - University Of California
item SUN, WEI - University Of California
item ZHOU, CHAO - Shandong Agricultural University
item McCormick, Sheila

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/22/2011
Publication Date: 10/10/2011
Citation: Zhang, Y., Li, S., Zhou, L., Fox, E., Pao, J., Sun, W., Zhou, C., Mccormick, S.M. 2011. Overexpression of Arabidopsis thaliana PTEN caused accumulation of autophagic bodies in pollen tubes by disrupting phosphatidylinositol 3-phosphate dynamics. Plant Journal. 68:1081-1092.

Interpretive Summary: PTEN is a lipid and protein phosphatase (i.e. a protein that removes phosphate groups from other proteins or from lipids). In plants PTEN is a pollen-specific protein. This work showed that overexpression of PTEN in pollen caused the pollen to develop autophagic (self-eating) bodies and led to male sterility. PTEN overexpression had these effects by changing the dynamics of a signaling lipid called PI3P.

Technical Abstract: Autophagy is a pathway in eukaryotes by which nutrient remobilization occurs through bulk protein and organelle turnover. Autophagy not only aides cells in coping with harsh environments but also plays a key role in many physiological processes that include pollen germination and tube growth. Most autophagic components are conserved among eukaryotes, but phylum-specific molecular components also exist. We show here that Arabidopsis thaliana PTEN, a protein and lipid dual phosphatase homologous to animal PTENs (phosphatase and tensin homologs deleted on chromosome 10), regulates autophagy in pollen tubes by disrupting the dynamics of phosphatidylinositol 3-phosphate (PI3P). The pollen-specific PTEN bound PI3P in vitro and was localized at PI3P-positive vesicles. Overexpression of PTEN caused accumulation of autophagic bodies and resulted in gametophytic male sterility. Such an overexpression effect was dependent upon its lipid phosphatase activity and was inhibited by exogenous PI3P or by expression of a class III phosphatidylinositol 3-kinase (PI3K) that produced PI3P. Overexpression of PTEN disrupted the dynamics of autophagosomes and a subpopulation of endosomes, as shown by altered localization patterns of respective fluorescent markers. Treatment with wortmannin, an inhibitor of class III PI3K, mimicked the effects by PTEN overexpression, which implied a critical role for PI3P dynamics in these processes. Despite sharing evolutionarily conserved catalytic domains, plant PTENs contain regulatory sequences that are distinct from those of animal PTENs, which might underlie their differing membrane association and thereby function. Our results show that PTEN regulates autophagy through phylum-specific molecular mechanisms.