Plant Endomembrane Dynamics: Studies of K⁺/H⁺ Antiporters Provide Insights on the Effects of pH and Ion Homeostasis

Abstract

Plants remodel their cells through the dynamic endomembrane system. Intracellular pH is important for membrane trafficking, but the determinants of pH homeostasis are poorly defined in plants. Electrogenic proton (H) pumps depend on counter-ion fluxes to establish transmembrane pH gradients at the plasma membrane and endomembranes. Vacuolar-type H-ATPase-mediated acidification of the trans-Golgi network is crucial for secretion and membrane recycling. Pump and counter-ion fluxes are unlikely to fine-tune pH; rather, alkali cation/H antiporters, which can alter pH and/or cation homeostasis locally and transiently, are prime candidates. Plants have a large family of predicted cation/H exchangers (CHX) of obscure function, in addition to the well-studied K(Na)/H exchangers (NHX). Here, we review the regulation of cytosolic and vacuolar pH, highlighting the similarities and distinctions of NHX and CHX members. In planta, alkalinization of the trans-Golgi network or vacuole by NHXs promotes membrane trafficking, endocytosis, cell expansion, and growth. CHXs localize to endomembranes and/or the plasma membrane and contribute to male fertility, pollen tube guidance, pollen wall construction, stomatal opening, and, in soybean (), tolerance to salt stress. Three-dimensional structural models and mutagenesis of Arabidopsis () genes have allowed us to infer that AtCHX17 and AtNHX1 share a global architecture and a translocation core like bacterial Na/H antiporters. Yet, the presence of distinct residues suggests that some CHXs differ from NHXs in pH sensing and electrogenicity. How H pumps, counter-ion fluxes, and cation/H antiporters are linked with signaling and membrane trafficking to remodel membranes and cell walls awaits further investigation.

Pathogen‐inducedpHchanges regulate the growth‐defense balance in plants

“…The alteration of cellulose synthase activity in response to extra‐ and intracellular signals is vital for growth modification under dynamic environmental conditions. Changes in pH within distinct cell compartments, including the apoplast/cell wall, act as messengers to transfer such signals (Felle, ; Sze & Chanroj, ). Plants and fungi primarily regulate pH across the plasma membrane via the activity of proton pumps, such as plasma membrane H + ‐ATPases.…”

Pathogen-induced pH changes regulate the growth-defense balance of plants

“…The alteration of cellulose synthase activity in response to extra-and intracellular signals is vital for growth modification under dynamic environmental conditions. Changes in pH within distinct cell compartments, including the apoplast/CW, act as messengers to transfer such signals (Felle, 2001;Sze & Chanroj, 2018) . Plants and fungi primarily regulate pH at across the PM via the activity of proton pumps, such as PM H + -ATPases.…”

Plant Trans-Golgi Network/Early Endosome pH regulation requires Cation Chloride Cotransporter (CCC1)

“…Cellular function is dependent upon ion transport across endomembranes (Sze and Chanroj, 2018). Organisms lacking key endomembrane ion transporters often exhibiting severe phenotypic defects (Maresova and Sychrova, 2005; Colmenero-Flores et al, 2007; Jentsch and Pusch, 2018).…”