Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development

Abstract

Recent evidence highlights novel roles for intracellular Na(+)/H(+) antiporters (NHXs) in plants. The availability of knockouts and overexpressors of specific NHX isoforms has provided compelling genetic evidence to support earlier physiological and biochemical data which suggested the involvement of NHX antiporters in ion and pH regulation. Most plants sequenced to date contain multiple NHX members and, based on their sequence identity and localization, can be grouped into three distinct functional classes: plasma membrane, vacuolar, and endosomal associated. Orthologues of each functional class are represented in all sequenced plant genomes, suggesting conserved and fundamental roles across taxa. In this review we seek to highlight recent findings which demonstrate that intracellular NHX antiporters (i.e. vacuolar and endosomal isoforms) play roles in growth and development, including cell expansion, cell volume regulation, ion homeostasis, osmotic adjustment, pH regulation, vesicular trafficking, protein processing, cellular stress responses, as well as flowering. A significant new discovery demonstrated that in addition to the better known vacuolar NHX isoforms, plants also contain endosomal NHX isoforms that regulate protein processing and trafficking of cellular cargo. We draw parallels from close orthologues in yeast and mammals and discuss distinctive NHX functions in plants.

In Vivo Intracellular pH Measurements in Tobacco andArabidopsisReveal an Unexpected pH Gradient in the Endomembrane System

“…As found previously, the EE/TGN fraction of VSR organelles was more acidic than the PVC ( Figure 8E; Tukey test, P value < 0.001). Recently, it was proposed that endosomal NHX antiporters are also necessary for regulating endosomal pH and required for proper vacuolar sorting (Bassil et al, 2011b(Bassil et al, , 2012. Consequently, we coexpressed pH-VSR with NHX5-RFP and found that 23% of pH-VSR colocalized with NHX5-RFP ( Figures 8C and 8D).…”

“…Monensin, bafilomycin A, and concanamycin A induce massive changes in Golgi morphology with an increase of saccules and an accumulation of vesicles at the trans face of the Golgi (Dettmer et al, 2006;Scheuring et al, 2011). Recently, endosomal NHX-type Na + /H + antiporters have been proposed to play a role in maintaining pH homeostasis (Bassil et al, 2011a(Bassil et al, , 2012, as other cation/H + exchangers do (reviewed in Chanroj et al, 2012). In mammalian cells, NHX-type antiporters have been suggested to function as proton leaks to counterbalance luminal acidification generated by V-ATPases (Demaurex, 2002;Orlowski and Grinstein, 2007).…”

Ectopic expression of Arabidopsis thaliana Na+(K+)/H+ antiporter gene, AtNHX5, enhances soybean salt tolerance

“…However, the major cause of damage is the toxic effect of excessive Na + and K + ions in the cytoplasm (Golldack et al, 2014). Research has shown that a protein called Na + (K + )/H + antiporter (NHX) plays important roles in maintaining the proper ion homeostasis in the cytoplasm (Mahajan and Tuteja, 2005;Bassil et al, 2012 Skou, 1957), while the first plant homolog was found in barley in 1976 (Ratner and Jacoby, 1976). Since then, Na…”

Role of Ion Transporters in Salinity Resistance in Plants

“…Plant cells employ primary active transport, mediated by H -ATPase, and secondary transport mediated by channels and co-transporters in order to maintain high concentrations of K and low concentrations of Na in the cytosol. The overall sub cellular compartmentation of Na into the vacuole and other organelles, such as mitochondria and plastids also lowers Na concentration in the cytoplasm and at the same time contributes to osmotic adjustment in order to maintain water uptake under salt conditions and the AtNHX family of Na /H antiporters which localized in the tonoplast membrane here play an important role in Na compartmentation using the H gradient as a driving force across the membrane under salinity stress (Blumwald, 2000;Bassil et al, 2012). The first functionally-characterized member of this gene family, AtNHX1, contributes to Na and monovalent cation sequestration in plant vacuoles.…”