Phosphorylation dynamics of membrane proteins from Arabidopsis roots submitted to salt stress

Abstract

An excess of NaCl in the soil is detrimental for plant growth. It interferes with mineral nutrition and water uptake and leads to accumulation of toxic ions in the plant. Understanding the response of roots to NaCl stress may facilitate the development of crops with increased tolerance to this and other stresses. Since controls achieved at the posttranslational level are of critical importance for regulating protein function, the present work used a robust label-free quantitative proteomic methodology to quantify phosphorylation events that affect root membrane proteins in Arabidopsis, in response to short-term (up to 2 h) NaCl treatments. This work identified 302 proteotypic phosphopeptides including 77 novel phosphorylated sites. NaCl treatment significantly altered the abundance of 74 phosphopeptides, giving novel insights into the regulation of major classes of membrane proteins, including ATPases, sodium transporters, and aquaporins. The data provide a unique access to phosphorylation reprogramming of ionic equilibrium in plant cells under NaCl stress. The use of predictive bioinformatic tools for kinase motifs suggested that root membrane proteins are substrates of cAMP-dependent protein kinase, cGMP-dependent protein kinase, and protein kinase C families, also called AGC kinases, arguing for an important role of lipid signaling in abiotic stress responses. It also pointed to cross-talks between protein kinase families during NaCl stress.

Novel Aquaporin Regulatory Mechanisms Revealed by Interactomics

“…Thus, we hypothesize that a reduced physical interaction between PLD␦ and PIP2;1 upon H 2 O 2 treatment would result in a decreased PA binding to PIP2;1, thereby altering PIP2;1 function. Such a role for lipid signaling in PIP2;1 function is consistent with the suggested role of lipid-mediated signaling in the transduction of stress signals arising from the soil (89).…”

Role of the Plasma Membrane in Saline Conditions: Lipids and Proteins

“…The authors also demonstrate that the PM proteins are the target of different protein kinases in response to NaCl stress, and also point out to an important role for lipid signaling in salt stress responses in plants. Other PM proteins that have been shown to be upregulated under salt stress, and correlate with salt tolerance are aquaporins (Mansour, 2014, Vialaret et al, 2014. Aquaporins are mainly involved in water absorption under salinity.…”

“…This results in enhancing the activity of the PM Na + /H + antiporter of salt adapted cells; Na + /H + antiporters are known to play a key role in Na + exclusion under high salt. Vialaret et al (2014) identified PM proteins from Arabidopsis roots that upregulated in response to NaCl treatment. These proteins include PM transport proteins and protein kinases, which are involved in ion homeostasis and signal perception.…”

“…Many studies demonstrated alterations of the PM proteome in plant species/genotypes contrasting in salt sensitivity under saline conditions (Singh et al, 1985;Hurkman et al, 1988Hurkman et al, , 1989Kononowicz et al, 1994;Kerkeb et al, 2001;Goncalo et al, 2003;Salama et al, 2007;Katz et al, 2007;Sengupta & Majumder, 2009;Zamani et al, 2010;Zhang et al, 2012b;Huang et al, 2012;Mansour, 2013). These studies report that several of the salt responsive PM proteins Cochlearia hollandica Na + /H + antiporter Na + extrusion Nawaz et al (2014) Dunaliella salina 60-KD protein Ion homeostasis Fisher et al (1994) Porteresia coarctata Cellulose synthase Cell wall synthesis Sengupta and Majumder (2009) Puccinella tenuiflora PutPMP3 PM hyperpolarization reserving Chang-Qing et al (2008) Oryza sativa 14-3-3 protein H + -ATPase regulator Malakshah et al (2007) Oryza sativa OsRPK1 Signal transduction Cheng et al (2009) Fragaria ananassa Osmotin PM protectant Husaini and Abdin (2008) Glycine max GmPIP1;6 Water transporter Zhou et al (2014) Dunaliella salina 150-KD protein PM permeability Sadka et al (1991) Triticum aestivum 14-3-3 protein H + -ATPase regulator Wang et al (2008b) Arabidopsis thaliana AtLTL1 Releasing fatty acids from PM Naranjo et al (2006) Musa paradisiaca Dehydrin PM protectant Shekhawat et al (2011) Chlorella vulgaris CvFAD2 Fatty acid unsaturation Lu et al (2009) Avicennia officinalis ABC transporters Ion detoxification Krishnamurthy et al (2014) Kandelia candel 14-3-3-like protein H + -ATPase regulator Wang et al (2014) Oryza sativa Protein kinases Signal transduction Vialaret et al (2014) Avicennia officinalis H + -ATPases Energy source for secondary ion transporters Krishnamurthy et al (2014) produced in salt tolerant species/cultivars improve their salt tolerance, and hence may pl...…”

Nitrogen Nutrition, Its Regulation and Biotechnological Approaches to Improve Crop Productivity

“…The N & C-terminals of NRT2.1 contain many protein kinase recognition motifs. Like NRT1.1, NRT2.1 is regulated by a phosphorylation/dephosphorylation mechanism under high nitrogen conditions [377] [378] NRT2.1 gene expression is induced by light and sugars. Sugar and nitrate are coupled by glucose metabolism by oxidative pentose phosphate pathway (OPPP) [379].…”