Phosphatase and tensin homolog (PTEN) is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens.

Abstract

Phosphatase and tensin homolog deleted on chromosome 10 (PTEN) is a lipid phosphatase implicated in cellular proliferation and survival. In animal cells, loss of PTEN leads to increased levels of phosphatidylinositol (3,4,5)-trisphosphate, stimulation of glucose and lipid metabolism, cellular growth, and morphological changes (related to adaptation and survival). Intriguingly, in plants, phosphatidylinositol (3,4,5)-trisphosphate has not been detected, and the enzymes that synthesize it were never reported. In this study we performed a genetic, biochemical, and functional characterization of the moss Physcomitrella patens PTEN gene family. P. patens has four PTENs, which are ubiquitously expressed during the entire moss life cycle. Using a knock-in approach, we show that all four genes are expressed in growing tissues, namely caulonemal and rhizoid cells. At the subcellular level, PpPTEN-green fluorescent protein fusions localized to the cytosol and the nucleus. Analysis of single and double knockouts revealed no significant phenotypes at different developmental stages, indicative of functional redundancy. However, compared with wild-type triple and quadruple pten knockouts, caulonemal cells grew faster, switched from the juvenile protonemal stage to adult gametophores earlier, and produced more rhizoids. Furthermore, analysis of lipid content and quantitative real-time polymerase chain reaction data performed in quadruple mutants revealed altered phosphoinositide levels [increase in phosphatidylinositol (3,5)-bisphosphate and decrease in phosphatidylinositol 3-phosphate] and up-regulation of marker genes from the synthesis phase of the cell cycle (e.g. P. patens proliferating cell nuclear antigen, ribonucleotide reductase, and minichromosome maintenance) and of the retinoblastoma-related protein gene P. patens retinoblastomarelated protein1. Together, these results suggest that PpPTEN is a suppressor of cell growth and morphogenic development in plants.

Evolutionary insights into FYVE and PHOX effector proteins from the moss Physcomitrella patens

“…PtdIns3P and PtdIns(3,5)P 2 are minor PPIs in P. patens, which closely agrees with what is observed in other organisms (Saavedra et al 2009, Saavedra et al 2015, Leprince et al 2014, Meijer et al 1999. In this study, we performed a genome wide analysis of the FYVE and PHOX gene families in P. patens.…”

KCH kinesin drives nuclear transport and cytoskeletal coalescence for tip cell growth

“…Apical tip growth was severely suppressed in the KCH KO line. Based on previous studies, this phenotype could be attributed to defects in the actin cytoskeleton, MT cytoskeleton, and/or lipid biogenesis at the tip (van Gisbergen et al, 2012;Vidali and Bezanilla, 2012;Hiwatashi et al, 2014;Saavedra et al, 2015). Defects in general housekeeping processes such as protein translation would also perturb cell growth.…”

Phosphoinositide signaling in plant development

“…For instance, the overexpression of PI-synthase in maize results in altered drought tolerance (Liu et al, 2013). Work on petunia, tobacco and the moss Physcomitrella patens supports an important role for PIs in the control of polar tip growth (Dowd et al, 2006;Helling et al, 2006;Saavedra et al, 2011Saavedra et al, , 2015. Although some of the reported phenotypes are severe, the molecular mechanisms underlying PI functions in plants remain mostly unclear.…”