Inositol Polyphosphate 5-Phosphatase7 Regulates the Production of Reactive Oxygen Species and Salt Tolerance in Arabidopsis      

Abstract

Plants possess remarkable ability to adapt to adverse environmental conditions. The adaptation process involves the removal of many molecules from organelles, especially membranes, and replacing them with new ones. The process is mediated by an intracellular vesicle-trafficking system regulated by phosphatidylinositol (PtdIns) kinases and phosphatases. Although PtdIns comprise a fraction of membrane lipids, they function as major regulators of stress signaling. We analyzed the role of PtdIns 5-phosphatases (5PTases) in plant salt tolerance. The Arabidopsis (Arabidopsis thaliana) genome contains 15 At5PTases. We analyzed salt sensitivity in nine At5ptase mutants and identified one (At5ptase7) that showed increased sensitivity, which was improved by overexpression. At5ptase7 mutants demonstrated reduced production of reactive oxygen species (ROS). Supplementation of mutants with exogenous PtdIns dephosphorylated at the D5# position restored ROS production, while PtdIns(4,5)P 2 , PtdIns(3,5)P 2 , or PtdIns(3,4,5)P 3 were ineffective. Compromised salt tolerance was also observed in mutant NADPH Oxidase, in agreement with the low ROS production and salt sensitivity of PtdIns 3-kinase mutants and with the inhibition of NADPH oxidase activity in wild-type plants. Localization of green fluorescent protein-labeled At5PTase7 occurred in the plasma membrane and nucleus, places that coincided with ROS production. Analysis of salt-responsive gene expression showed that mutants failed to induce the RD29A and RD22 genes, which contain several ROS-dependent elements in their promoters. Inhibition of ROS production by diphenylene iodonium suppressed gene induction. In summary, our results show a nonredundant function of At5PTase7 in salt stress response by regulating ROS production and gene expression.

Phosphoinositide signaling in plant development

“…In recent years, PIs have emerged as central regulators of plant function and development, and a number of important and severe plant phenotypes have been reported when plant PI metabolism is perturbed Nelson, 2009, 2004;Chen et al, 2008;Ercetin et al, 2008;Golani et al, 2013;Gunesekera et al, 2007;Ischebeck et al, 2008Ischebeck et al, , 2011Ischebeck et al, , 2013Kaye et al, 2011;Kusano et al, 2008;Löfke et al, 2008;Mei et al, 2012;Novakova et al, 2014;Parker et al, 2000;Preuss et al, 2006;Rodriguez-Villalon et al, 2015;Sousa et al, 2008;Stenzel et al, 2008;Tejos et al, 2014;Wang et al, 2012;Williams et al, 2005;Zhong et al, , 2005. The perturbation of PI signaling components in Arabidopsis, for example, gives rise to a variety of phenotypes affecting multiple tissue types and aspects of plant development (summarized in Table 1).…”

A Critical Role of Lyst-Interacting Protein5, a Positive Regulator of Multivesicular Body Biogenesis, in Plant Responses to Heat and Salt Stresses

“…A number of studies have shown that NADPH oxidase-dependent ROS was induced by salt stress in Arabidopsis seedling roots and functioned as a positive regulator of salt tolerance by signaling salt stress responses. Mutations of genes involved in phosphatidylinositol signaling, which regulates vesicle trafficking, not only compromised salt tolerance but also the saltinduced intracellular production of ROS by NADPH oxidases (Kaye et al, 2011). Although NADPH oxidases normally reside in the plasma membrane, they can also be targeted by endocytosis and assembled into active forms in the internal membranes, and endosomal ROS production plays critical roles in a number of biological processes, including preinflammatory immune responses (Rubinek and Levy, 1993;Casbon et al, 2009).…”

“…When compared with wild-type plants, lip5 mutants accumulate increased levels of ubiquitinated protein aggregates, suggesting a possible role of LIP5-regulated MVB trafficking as a critical route for the degradation of heat-damaged proteins. Compromised salt tolerance of the lip5 mutants was associated with an increased accumulation of cellular NaCl but reduced levels of cellular reactive oxygen species (ROS), which have been implicated in the signaling of salt stress responses (Kaye et al, 2011;Xie et al, 2011). The roles of LIP5 and its phosphorylation by MPK3/6 in plant responses to heat and salt stresses were also investigated.…”

Reactive oxygen species and stress signaling in plants

“…геном арабидопсиса содержит 10 предста-вителей семейства генов мембраносвязанной субъединицы RBOH (Respiratory Burst Oxidase Homologs), обозначаемых как AtRboh (A, B, C, D, E, F, G, H, J, L) [37][38]. В геноме риса выявле-но девять генов, кодирующих каталитическую субъединицу NADPHоксидазы.…”