K<sup>+</sup> Efflux Antiporters 4, 5, and 6 Mediate pH and K<sup>+</sup> Homeostasis in Endomembrane Compartments

Zhu, Xiaoyan; Pan, Ting; Zhang, Xiao; Fan, Ligang; Quintero, Francisco J.; Zhao, Hong; Su, Xiaomeng; Li, Xiaojiao; Villalta, Irène; Mendoza, Irene; Shen, Jinbo; Jiang, Liwen; Pardo, José M.; Qiu, Quan‐Sheng

doi:10.1104/pp.18.01053

Cited by 72 publications

(68 citation statements)

References 71 publications

(53 reference statements)

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“…Other TGN/EE localised transport proteins together with the V-type H + -ATPase proton pump have been suggested to be critical for establishing optimal pH and ionic conditions in the TGN/EE, important for cargo delivery or pathogen resistance (Martinière et al, 2013; Shen et al, 2013; Guo et al, 2014; Luo et al, 2015). Currently, the model for ion and pH regulation consists of the V-H-ATPase, the cation proton antiporters NHX5, NHX6, KEA4, KEA5 and KEA6, and the chloride proton antiporter CLC-d (Guo et al, 2014; Sze and Chanroj, 2018; Zhu et al, 2018; Wang et al, 2019). It is suggested that the proton pump generates the H + gradient to establish the lower pH in the TGN/EE lumen compared to the cytosol, and that the ion proton antiporter contributes to fine-tuning the pH.…”

Section: Discussionmentioning

confidence: 99%

“…Among the few examples of characterised proteins are the TGN/EE and ER localised Arabidopsis sodium/potassium proton exchangers NHX5 and NHX6 and the potassium proton exchangers KEA4, KEA5 and KEA6. These proteins were shown to fulfil important roles in protein sorting to the vacuole, sorting of the auxin transporter PIN5, and potassium homeostasis; and the respective double or triple knockouts exhibit severely stunted growth (Bassil et al, 2011; Fan et al, 2018; Zhu et al, 2018; Wang et al, 2019). The cation proton exchanger CHX20 localises to the endomembrane system and was shown to be important for osmoregulation of stomatal guard cells (Sze et al, 2004; Padmanaban et al, 2007) and the ER localised soybean CHX protein, GmSALT3, was shown to be important for salinity tolerance (Guan et al, 2014; Liu et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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

McKay

McFarlane

et al. 2020

Preprint

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31The secretary and endocytic pathways intersect at the trans-Golgi network/Early Endosome 32 (TGN/EE). TGN/EE function depends on a careful balance of ions within this compartment, 33 and the electrochemical potential across its membrane. The identity of the proton pump 34 required for acidification and the transporters that catalyse cation and anion import into 35 endosome compartments are known. However, the protein needed to complete the transport 36 circuit, and that mediates cation and anion efflux from the TGN/EE has not been identified. 37Here, we characterize Cation Chloride Cotransporters (CCC1s) from Arabidopsis and rice. 38 We find that the AtCCC1 is localized to the TGN/EE, where it modulates important TGN 39 functions such as endocytosis, exocytosis, and cell wall synthesis/secretion. Loss of CCC1 40 results in severe, widespread phenotypes in both rice and Arabidopsis, including plant growth 41 and developmental perturbations, defects in root hair elongation and altered osmoregulation, 42 consistent with CCC performing a core cellular function. Complementation of the root hair 43 elongation phenotype of Atccc1 with root hair specific expression of GFP-AtCCC1 44 demonstrates CCC1 functions within the TGN/EE. Collectively, our results imply that CCC1 45 is a strong candidate for the missing component of the TGN/EE ion transportcircuit. 46 47 126 7including root hairs, and in the gynoecium, while GUS staining did not indicate expression in 127 these cells. This is likely due to the different sensitivities of the two methods. 128 129 ccc1 knockout mutants have a reduced root hair length and tip growth rate 130 As our expression analysis showed that AtCCC1 is expressed in root hairs (Fig. 1), we 131 examined whether root hair cells of the knockouts had an altered phenotype, and whether we 132 could use this model cell type to investigate the role of CCC1. Characterisation of the 133 knockouts showed that both Atccc1 and Osccc1.1 plants had a reduction in the overall length 134 of their root hairs compared to control plants (Fig. 2); and a complete lack of collet hairs in 135 Atccc1. Collet hairs are epidermal root hairs formed in some plant species in the transition 136 zone between the root and the hypocotyl (Fig. 2, Sliwinska et al., 2015). Atccc1 also had 137 branching and bulging of root hairs, although, at a low frequency, and root hairs of the 138 495 496 References 497 Balcerowicz, D., Schoenaers, S., and Vissenberg, K. (2015). Cell fate determination and 498 the switch from diffuse growth to planar polarity in Arabidopsis root epidermal cells. 499 Frontiers in Plant Science 6, 1163. 500 Bassil, E., and Blumwald, E. (2014). The ins and outs of intracellular ion homeostasis: 501 NHX-type cation/H + transporters. Current Opinion in Plant Biology 22, 1-6. 502 23 Bassil, E., Ohto, M.-a., Esumi, T., Tajima, H., Zhu, Z., Cagnac, O., Belmonte, M., Peleg, 503 Z., Yamaguchi, T., and Blumwald, E. (2011). The Arabidopsis intracellular Na + /H + 504 antiporters NHX5 and NHX6 are endosome associated ...

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

McKay

McFarlane

et al. 2020

Preprint

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“…In vivo calibration was achieved from the same protoplasts expressing the PRpHluorin for pH measurement. Protoplasts were incubated in WI protoplast buffer (0.5 M mannitol and 20 mM KCl) with 25 μM nigericin, 60 mM KCl, and 10 mM MES/HEPES Bis-Tris-propane adjusted to different pH values ranging from 5.0 to 8.0 for each calibration point [33,37,38,[47][48][49]. Fluorescence was observed using a confocal laser scanning microscope (Leica TCS-SP8).…”

Section: Ph Measurementsmentioning

confidence: 99%

OsNHX5-mediated pH homeostasis is required for post-Golgi trafficking of seed storage proteins in rice endosperm cells

et al. 2019

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Background: As the major storage protein in rice seeds, glutelins are synthesized at the endoplasmic reticulum (ER) as proglutelins and transported to protein storage vacuoles (PSVs) called PBIIs (Protein body IIs), where they are cleaved into mature forms by the vacuolar processing enzymes. However, the molecular mechanisms underlying glutelin trafficking are largely unknown. Results: In this study, we report a rice mutant, named glutelin precursor accumulation6 (gpa6), which abnormally accumulates massive proglutelins. Cytological analyses revealed that in gpa6 endosperm cells, proglutelins were mis-sorted, leading to the presence of dense vesicles (DVs) and the formation paramural bodies (PMBs) at the apoplast, consequently, smaller PBII were observed. Mutated gene in gpa6 was found to encode a Na + /H + antiporter, OsNHX5. OsNHX5 is expressed in all tissues analyzed, and its expression level is much higher than its closest paralog OsNHX6. The OsNHX5 protein colocalizes to the Golgi, the trans-Golgi network (TGN) and the prevacuolar compartment (PVC) in tobacco leaf epidermal cells. In vivo pH measurements indicated that the lumens of Golgi, TGN and PVC became more acidic in gpa6. Conclusions: Our results demonstrated an important role of OsNHX5 in regulating endomembrane luminal pH, which is essential for seed storage protein trafficking in rice.

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“…The CPA2 family, which includes the K + efflux antiporters (KEAs) and cation/H + exchangers (CHXs), was found in bacteria, fungi and plants, but rarely seen in metazoans [7]. KEA 4 family genes were homologous to bacteria K + efflux transporters (EcKefB and EcKefC) [16], characterized as K + / H + reverse transporter, which promotes K + homeostasis and plays a role in maintaining pH and ion homeostasis in intimal network [20,21]. KEAs in plants were first identified in Arabidopsis and named AtKEA1-6 [15].…”

Section: Introductionmentioning

confidence: 99%

Monovalent cation/proton antiporters (CPAs) in moso bamboo (Phyllostachys edulis): genome-wide identification, molecular evolutionary and functional description

Wang

Liu

Gao

et al. 2020

Preprint

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Background: Plant monovalent cation/proton enantiomer (CPA) family is a type of transmembrane transporters that plays an important role in resistance to plant abiotic stresses such as salt, drought and osmotic stress. Results: In this study, 32 CPA family members were firstly identified from moso bamboo, and divided into two subfamilies, including 8 in CPA1 and 24 in CPA2. Members of the same group shared similar structures and subcellular localization predictions. Gene duplication analysis found that the expansion of the CPA genes in moso bamboo may depend on whole genome duplication (WGD) event approximately 11.18 million years ago (MYA). Gene Ontology (GO) analysis revealed that PheCPA proteins are ion transporter localized on the membrane, and the post-translational modifications (PTMs) prediction indicated there are many PTMs sites may be involved in regulating CPA protein functions. Promoter analysis revealed various cis-acting elements related to abiotic and biotic stresses, plant growth and development and phytohormone responses. The significant change of expression levels of eight PheNHXs, which belong to CPA1, under the treatment of ABA, NaCl and PEG, suggesting that they may have played an important role in moso bamboo response to these abiotic stresses. Additionally, PPI prediction reveals potential interaction proteins of PheNHX subfamily members. Conclusions: The results suggested that the CPA family may plays an important role in plant responses to stress conditions. The comprehensive identification and analysis of PheCPAs indicated that PheCPAs, particularly those genes encoding PheNHXs, might serve as valuable genetic resources for the improvement of moso bamboo growth and resistance to abiotic stress.

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K⁺ Efflux Antiporters 4, 5, and 6 Mediate pH and K⁺ Homeostasis in Endomembrane Compartments

Cited by 72 publications

References 71 publications

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

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

OsNHX5-mediated pH homeostasis is required for post-Golgi trafficking of seed storage proteins in rice endosperm cells

Monovalent cation/proton antiporters (CPAs) in moso bamboo (Phyllostachys edulis): genome-wide identification, molecular evolutionary and functional description

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K+ Efflux Antiporters 4, 5, and 6 Mediate pH and K+ Homeostasis in Endomembrane Compartments

Cited by 72 publications

References 71 publications

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

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

OsNHX5-mediated pH homeostasis is required for post-Golgi trafficking of seed storage proteins in rice endosperm cells

Monovalent cation/proton antiporters (CPAs) in moso bamboo (Phyllostachys edulis): genome-wide identification, molecular evolutionary and functional description

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K⁺ Efflux Antiporters 4, 5, and 6 Mediate pH and K⁺ Homeostasis in Endomembrane Compartments