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

The transport of ions across biological membranes is fundamental to diverse cellular functions such as energy production, nutrient uptake and distribution, growth, signalling, and osmoregulation. Ion influx and efflux must be coordinated to regulate osmotic potential, and to maintain charge balance within and across cellular compartments. Ion efflux out of cells contributes towards processes as varied as neuronal function in animals, heavy metal tolerance in bacteria, and salinity tolerance in plants. Ion efflux out of subcellular compartments is also critical for core cellular functions such as chloroplastic photosynthetic efficiency in plants (Correa Galvis et al., 2020).

Cation chloride cotransporters (CCCs) are cation and anion symporters that are present in all domains of life, whether archaea, animal, yeast, or plant. Chloride (Cl^-) is transported by CCCs electroneutrally across membranes with the cations of sodium (Na⁺) and/or potassium (K⁺). A single CCC exists in the archeaon, Methanosarcina acetivorans, which does not share a high degree of similarity to eukaryotic CCCs (Hartmann and Nothwang, 2015). In animals, CCCs have been separated into two subfamilies: the Cl^- and K⁺ efflux symporters (KCCs), and a second subfamily with two clades of CCC, the Cl^- and Na⁺/K⁺ influx symporters (NKCCs), and the Cl^- and Na⁺ influx symporters (NCCs). Vertebrates typically harbour several CCC isoforms from each subfamily. For example, humans (Homo sapiens) have seven CCC isoforms (4 KCC, 3 NKCC/NCCs) and zebrafish (Danio rerio) have 12 CCCs in total (Hartmann et al., 2014). In non-vascular plants there are two clades of CCC, CCC1 and CCC2, with some bryophytes, such as the moss Physcomitrium patens (formerly Physcomitrella patens) with up to seven isoforms (Henderson et al., 2018). In contrast, in flowering plants (angiosperms), CCCs are represented by only the CCC1 clade, with very few isoforms per plant. For instance, rice (Oryza sativa), contains two CCC1s, and Arabidopsis (Arabidopsis thaliana) has only one CCC1.

In vertebrates, CCCs are involved in diverse but specific cellular processes including osmoregulation in kidneys and neurons (regulation of cell volume), potassium secretion in muscles and regulation of Cl^– concentrations in neural tissue (Blaesse et al., 2009; Hartmann and Nothwang, 2015). NKCCs and NCCs drive influx of ions across the cell membrane, often by utilising large extracellular Na⁺ concentrations to drive transport of Cl^- and K⁺, or just Cl^- in the case of NCC, whereas KCCs utilise K⁺ gradients to mediate Cl^- efflux out of the cytosol (Blaesse et al., 2009; Arroyo et al., 2013). The importance of Cl^- management and osmoregulation for cell and organ function is highlighted by the large number of human diseases and conditions associated with CCC malfunction including schizophrenia, deafness, muscle spasticity, epilepsy, Andermans syndrome (neuropathy), and, Bartter and Gitelman syndrome (both characterised by kidney disfunction) (Simon et al., 1996; Kunchaparty et al., 1999; Howard et al., 2002; Boettger et al., 2002; Rivera et al., 2002; Boulenguez et al., 2010; Kim et al., 2012).

The single CCC1 protein in the model plant Arabidopsis also appears to have a crucial, but unexplained, role in plant function. When Arabidopsis CCC1 is genetically ablated, ccc1 plants exhibit complex and severe phenotypic defects which include a large reduction in overall plant size, a bushy appearance characterised by increased axillary shoot outgrowth, frequent stem necrosis, very low fertility, alterations in pathogen response, changes in cell wall composition, and changes in seed ion concentrations (Johnson et al., 2004; Colmenero-Flores et al., 2007; McDowell et al., 2013; Henderson et al., 2018; Han et al., 2020). Arabidopsis ccc1 also displays changes in ion distribution. Hydroponically grown ccc1 plants accumulate more Cl^- in shoots under both control and 50 mM NaCl conditions while soil-grown ccc1 plants accumulate more Cl^- in shoots when exposed to 50 mM Cl^- salts (Colmenero-Flores et al., 2007; Henderson et al., 2015). Similarly, roots of rice Osccc1.1 plants also had altered ion accumulation profiles under both control and saline conditions (Chen et al., 2016). While rice harbours two CCC1 proteins, Arabidopsis is the ideal system for investigating the role of CCCs in higher plants due to the presence of only a single CCC homologue, eliminating the possibility for functional redundancy (Henderson et al., 2018).

Plant, fungi, and animal CCC subcellular localisations are different. While many of the animals’ CCCs have been found on the cell membrane (plasma membrane [PM]), the yeast (Saccharomyces cerevisiae) CCC homologue, VHC1, is localised not on the exterior membrane of the cell, but on the yeast vacuolar membrane (Petrezselyova et al., 2013). Independent proteomic studies in Arabidopsis have revealed that the Arabidopsis CCC1 is highly abundant in the trans-Golgi network/early endosome (TGN/EE) (Sadowski et al., 2008; Drakakaki et al., 2012; Groen et al., 2014; Nikolovski et al., 2014), with the latest study defining CCC1 as a TGN/EE marker protein (Parsons et al., 2019). Heterologous expression studies in tobacco (Nicotiana benthamiana) epidermal cells also suggested an endomembrane localisation of the Arabidopsis CCC1 using a translational fluorescent protein fusion (Henderson et al., 2015). This raises the question of the role of CCC1 in this organelle. Several transport proteins in the TGN/EE have been identified, with mutants of the transport proteins involved in TGN/EE pH regulation exhibiting similar phenotypic aspects to ccc1 knockouts. CCC1 is therefore a candidate ion transporter that might contribute to TGN/EE pH regulation.

The plant TGN/EE is an organelle with a complex cellular role. One of its key roles is sorting and delivering proteins to the apoplast, PM, and vacuole (Dettmer et al., 2006; Viotti et al., 2010; Sze and Chanroj, 2018). Four TGN/EE Cl^- and K⁺ transporters have previously been identified: the H⁺/K⁺ antiporters NHX5 and NHX6, and the H⁺/Cl^- antiporters CLCd and CLCf. These antiporters import K⁺ and Cl^- into the TGN/EE in exchange for luminal protons and work in conjunction with the TGN/EE V-ATPase complex to regulate luminal pH (Bassil et al., 2011; Reguera et al., 2015; Scholl et al., 2021). Finely tuned luminal pH is required for the cellular function of the TGN/EE (Martinière et al., 2013; Luo et al., 2015; Reguera et al., 2015). Plants with reduced V-H⁺-ATPase activity (e.g. det3 mutants) have an elevated TGN/EE pH and exhibit severe developmental growth defects, which is accompanied by alterations in exocytosis of PM proteins, such as BRI1, defects in cell division and expansion and hypersensitivity to salt (Schumacher et al., 1999; Dettmer et al., 2006; Brüx et al., 2008; Krebs et al., 2010; Luo et al., 2015). Double nhx5/nhx6 mutants have similar, but not identical, growth defects to det3, with reduced cell length, a large decrease in overall plant size, and increased salt sensitivity of root growth and seed germination (Bassil et al., 2011; Reguera et al., 2015). As in det3, trafficking of BRI1 is altered in nhx5/nhx6; however, only recycling is affected while secretion to the PM is not (Dragwidge et al., 2019). In addition, the PM abundance of the membrane integrated proteins, PIN1 and PIN2, are reduced in nhx5/nhx6 (Dragwidge et al., 2018). However, in contrast to det3, the nhx5/nhx6 TGN/EE lumen is hyperacidic, consistent with the proposed role of NHX in exporting protons out of the TGN/EE (Luo et al., 2015; Reguera et al., 2015). The hyperacidity of nhx5/nhx6 TGN/EE lumen results in mis-sorting of vacuolar proteins due to altered binding of targets by the vacuolar sorting receptor VSR1;1 (Reguera et al., 2015). A clcld single knockout has a mild increase in pathogen sensitivity. The less severe phenotype of this knockout might be a result of the two TGN/EE resident CLC proteins, which are likely to exhibit functional redundancy similar to the two TGN/EE NHXs. Collectively, these observations demonstrate that a typical consequence of alterations in TGN/EE lumen pH regulation are defects in protein trafficking, particularly in protein exocytosis, changes in salt tolerance, and defects in cell elongation and division, resulting in severe impacts on plant growth.

The current model of TGN/EE pH regulation, as outlined above, is incomplete; it currently includes a proton pump (V-H⁺-ATPase) and anion- and cation-proton exchangers (CLC, NHX) (Sze and Chanroj, 2018), but a transport protein that mediates either cation or anion efflux has not yet been identified. Both import and export of ions are crucial components of dynamic cellular and organellar ion regulation. If both do not occur, cation and anion import into the TGN/EE would cease once the gradient becomes too high, which would inhibit the function of the antiporters. Plant CCC1s, with their cation and anion symport function and their residency in the TGN/EE, are ideal candidates to fill this missing role and complete the circuit through export of Cl^- and K⁺ from the TGN/EE.

Here, we characterised the role of Arabidopsis CCC1 in the TGN/EE. We demonstrate that TGN/EE-localised CCC1 rescues cellular defects of ccc1 knockouts in Arabidopsis, and that CCC1 impacts TGN/EE luminal pH and osmotic regulation. Genetic ablation of CCC1 function leads to defects in TGN/EE-dependent processes, specifically, ccc1 plants exhibit reduced rates of exocytosis and endocytic trafficking, typical of altered TGN/EE pH regulation. As such, we propose that CCC1 is a missing core component of the ion- and pH-regulating machinery of the TGN/EE.

In the TGN/EE, both an increase or a decrease of luminal pH leads to changes in endomembrane trafficking, cell expansion, and cell wall formation, which implies that the pH of the TGN/EE is finely regulated (Luo et al., 2015; Dragwidge et al., 2019). Here, we show that a functional CCC1 is localised in the TGN/EE in Arabidopsis, and that loss of this cation anion symporter leads to defects in establishing the typical, low pH in TGN/EE lumen. This makes CCC1 the first TGN/EE-localised transporter important for pH regulation that has not been shown to directly transport protons. Our results show that CCC1 is important for counteracting the cation-induced osmotic swelling of TGN/EE by monensin (Figure 7), consistent with this symporter being important for regulating luminal ion concentrations. pH measurements confirmed that ccc1 cells have a more alkaline pH in the TGN/EE lumen compared to wildtype. We therefore propose to update the current model of pH regulation, containing the V-H⁺-ATPase, NHX5 and NHX6, and CLCd (Sze and Chanroj, 2018), adding CCC1 (Figure 8).

Figure 8

Download asset Open asset

The function of CCC1 in the TGN/EE is consistent with CCC1 localisation to this organelle, as detected here and shown in earlier studies (Sadowski et al., 2008; Drakakaki et al., 2012; Groen et al., 2014; Nikolovski et al., 2014; Henderson et al., 2015; Parsons et al., 2019). We find no evidence that CCC1 was functional on any other membrane. The construction of a functional CCC1 with a tag was not trivial. Multiple attempts at tagging CCC1 failed and the construct used here, GFP-CCC1, did not give transformants if ubiquitously expressed under the control of its native promoter (Supplementary file 1a). We demonstrate cellular functionality through the ability of GFP-CCC1 to improve root hair and trichoblast elongation (Figure 3 and Figure 3—figure supplement 1), yet, the inability to express tagged CCC1 ubiquitously suggests that tagging does affect CCC1, potentially through modifying regulation or activity of the protein to create an overactive, embryo lethal variant. In another study, a CCC1-GFP construct expressed in pollen was predominantly localised to endomembranes, but was also suggested to localise to the PM (Domingos et al., 2019). This might indicate that in pollen, CCC1 might have other cellular localisation in addition to TGN/EE. However, the functionality of this construct was not shown through complementation of the pollen tube growth defect, and the PM signal might have been a result of overexpression of the construct through the tomato-derived Lat52 promoter or the C-terminal GFP-tag may have perturbed retention of the CCC1-GFP construct in the TGN/EE. Our results in root cells demonstrate that functional GFP-CCC1 localises to the TGN/EE and that loss of function of the symporter impacts TGN/EE luminal conditions, and results in phenotypes in line with disruption in TGN/EE luminal pH.

Interestingly, endomembrane localisation of CCCs is not restricted to Arabidopsis CCC1. Yeast CCC, called VHC1, is the only functionally characterised CCC outside of plants and animals. Similar to Arabidopsis CCC1, VHC1 is found on an intracellular membrane; and like many animal CCCs, and CCC1 from plants, VHC1 is involved in osmoregulation (Petrezselyova et al., 2013). Intracellular organelles such as the TGN/EE (or the yeast vacuole) are kept in osmotic equilibrium with the cytosol, which is akin to the adjustment animal cells conduct with their extracellular fluid. Unlike animal cells, plants maintain steep osmotic gradients across their plasma membranes, enabled by the presence of a cell wall and the establishment of turgor pressure. Therefore, proteins involved in osmoregulation localised on the PM of animal or plant cells are likely to require different characteristics and this may explain the difference in localisation of CCC proteins in animals as compared to organisms with a cell wall. Interestingly, also for CLC proteins, many animal CLCs are localised to the plasma membrane, but all investigated plant CLCs are localised to internal membranes, with no PM localisation detected (De Angeli et al., 2009).

CCC1 is an electroneutral anion cation symporter, which, like other CCCs, fixes the stoichiometry of exported anions and cations at 1:1 (Colmenero-Flores et al., 2007). In animals, this stoichiometry either consists of the electroneutral transport of 2Cl^-:1Na⁺:1K⁺ in NKCCs, or 1Cl^-:1K⁺ and 1Cl^-:1Na⁺ in KCCs and NCCs, respectively. As Arabidopsis plants can be grown in the near absence of Na⁺ (50 nM) without showing a ccc1 knockout phenotype, it is likely that CCC1 is functional in the absence of Na⁺. This supports the hypothesis that CCC1 can function as a 1Cl^-:1K⁺ symporter, which could be validated through further experimentation in heterologous systems (e.g. Colmenero-Flores et al., 2007; Henderson et al., 2015; van Delden et al., 2020).

In the TGN/EE, a 1:1 K⁺:Cl^- ion export ratio of plant CCCs would tightly connect the activities of the colocalised ion exchangers NHX5 and NHX6 with CLCd, which contribute to the strict but dynamic regulation of pH. In addition, other transporters such as the potassium efflux antiporters KEA4, KEA5, and KEA6 might also contribute to luminal pH regulation in planta; yet their roles are currently less understood since triple kea4/kea5/kea5 knockouts show a much less severe phenotype compared to nhx5/nhx6, det3, or ccc1 (Dettmer et al., 2006; Colmenero-Flores et al., 2007; Bassil et al., 2011; Zhu et al., 2019).

Functional pH regulation and endomembrane transport has a vital role in many cellular processes, including cell wall formation, nutrient acquisition, and the establishment of hormone gradients (Guo et al., 2014; Adamowski and Friml, 2015; Sinclair et al., 2018). In agreement with this, ccc1 mutant plants display very severe phenotypic alterations compared to wildtype. We found that CCC1 is ubiquitously expressed, and its function is required for cell elongation, which might be a contributing cause of the reduced overall growth of the mutants (Figures 1 and 2). Cell elongation is also reduced in nhx5/nhx6 and clcd/amiR-clcf mutants; with reduced root hair elongation speed in both and reduced root epidermal cell and root hair length in clcd/amiR-clcf (Bassil et al., 2011; Scholl et al., 2021). Reduced root hair elongation could be the result of reduced rates of endomembrane trafficking, which have been observed in nhx5/nhx6 causing reduced delivery of cargo important for cell expansion such as cell wall components. Phenotypic defects in ccc1 are not restricted to cell elongation, we found that trichoblast patterning was also altered in ccc1 roots (Figure 2—figure supplement 1), which hints at a role of TGN/EE ion and pH regulation in early cell development. ccc1 plants further exhibit highly increased shoot branching, which gives the knockout plants a bushy appearance (Henderson et al., 2018). One cause for this might be defects in auxin transport regulation in shoots. We found alterations in PIN2 exocytosis in ccc1 roots, suggesting that similar defects could exist in shoot cells (Figure 5).

Previous work has revealed a link between endomembrane trafficking, the TGN/EE and salt tolerance in plants. Knockouts of the Arabidopsis Rab GTPase ARA6, involved in TGN/EE to PM trafficking, result in salt-sensitive plants. Likewise, knockouts of VACUOLAR PROTEIN SORTING 4 (VPS4), involved in sorting of proteins for vacuolar degradation, result in salt-sensitive plants. Similarly, both det3 plants and RNAi knockdowns of the TGN/EE V-H⁺-ATPase display a stronger reduction in primary root growth in response to 50 mM NaCl compared with wildtype plants (Batelli et al., 2007; Krebs et al., 2010). nhx5/nhx6 plants exhibit severe reductions in growth when transferred to media containing 100 mM NaCl and germination of nhx5/nhx6 seeds, with a reduced TGN/EE luminal pH is almost completely abolished on media containing 100 mM NaCl (Bassil et al., 2011). CCC1 appears to play a contrasting role to NHX5/NHX6, as here, we found that the germination of ccc1 seeds was more tolerant to salt and osmotic stress than wildtype (Figure 4). The contrasting roles in osmotic tolerance may be explained by the contrasting roles of the proteins in the TGN/EE. nhx5/nhx6 knockouts have a lower TGN/EE pH and are more resistant to monensin, while ccc1 knockouts have a higher TGN/EE pH and are hypersensitive to monensin. NHX5 and NHX6 import K⁺ from the cytosol and therefore knockouts are likely to have a reduced accumulation of K⁺ in the TGN/EE whereas we find here that CCC1 is likely to export K⁺ and therefore knockouts likely have an increased accumulation of K⁺. The elevated TGN/EE luminal pH in ccc1 under control condition might further prime them for osmotic shock treatments that induce plasmolysis, as luminal pH is as high in ccc1 under control conditions as it is in wildtype in response to osmotic shock.

CCC1 is important for root hair growth under standard conditions, but ccc1 knockout root hair growth occurred at the same rate as wildtype at an elevated osmolarity. The greater germination rate of ccc1 seeds on media with a higher osmolarity may be the result of a combination of factors, including changes in TGN/EE luminal pH and multiple downstream factors. Changes in the cell wall composition of ccc1 knockouts have been observed (Han et al., 2020), so ccc1 plants might have a weaker cell wall and potentially a weaker seed coat, which might require a smaller water uptake for the necessary seed swelling and seed coat rupture to occur.

Knockouts of ccc1 require higher concentrations to induce plasmolysis of root epidermal cells. This increased tolerance to plasmolysis could occur if ccc1 knockouts were able to regulate their internal osmolarity faster than wildtype. It is possible that ccc1 root epidermal cells could influx external osmolytes faster, due to altered PM localisation of osmolyte transporters, to more rapidly match the external osmolarity. Supporting this, nutrient uptake and ion translocation have been shown to be affected in ccc1 plants, with altered total shoot K⁺, Na⁺, and Cl^- accumulation compared to the wildtype (Colmenero-Flores et al., 2007; Henderson et al., 2015). Interestingly, Osccc1.1 roots have a lower cell sap osmolality, but an increase in biomass was reported when plants grown in saline conditions compared to control conditions (Chen et al., 2016). The model we propose for Arabidopsis CCC1 might therefore be similar in rice, suggesting a conserved function.

Here, we show the TGN/EE pH of epidermal root cells increases in response to both salt and osmotic shock, which has not been reported previously. Modulation of the TGN/EE pH in response to abiotic stress may enable wildtype plants to rapidly regulate protein trafficking and abundance. det3, nhx5/nhx6, and ccc1 plants all exhibit TGN/EE pH differences compared to the wildtype of around 0.3 units (Luo et al., 2015; Reguera et al., 2015; Dragwidge et al., 2018; Dragwidge et al., 2019), very similar to what we consistently found for ccc1. All three genotypes exhibit altered responses to salt and osmotic treatments, suggesting that a dynamic but tight regulation of TGN/EE luminal pH is an important factor for plant response to these abiotic stresses.

In conclusion, our research here demonstrates that CCC1 has a central function in plant cells and fills a gap in our understanding of how endomembrane luminal pH is regulated through the identification of a novel ion efflux component of the TGN/EE ion transport network.

Data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 2-7. Original images files can be accessed on figshare.

1. 1. McKay D
   2. Wege S
   3. Gilliham M

   (2021) figshare

   Tissue specific expression CCC1 promoter.

   https://doi.org/10.25909/17256545.v1
2. 1. McKay D
   2. Gilliham M
   3. Wege S

   (2021) figshare

   Root hair branching examples.

   https://doi.org/10.25909/17256515.v1
3. 1. McKay D
   2. Wege S
   3. Gilliham M

   (2021) figshare

   Monensin experiment.

   https://doi.org/10.25909/17256467.v1
4. 1. McKay D
   2. Wege S
   3. Gilliham M

   (2021) figshare

   Cell File Organisation.

   https://doi.org/10.25909/17256428.v1

1. 1. Adamowski M
   2. Friml J

   (2015) PIN-dependent auxin transport: action, regulation, and evolution

   The Plant Cell 27:20–32.

   https://doi.org/10.1105/tpc.114.134874

   • PubMed
   • Google Scholar
2. 1. Arroyo JP
   2. Kahle KT
   3. Gamba G

   (2013) The SLC12 family of electroneutral cation-coupled chloride cotransporters

   Molecular Aspects of Medicine 34:288–298.

   https://doi.org/10.1016/j.mam.2012.05.002

   • PubMed
   • Google Scholar
3. 1. Barberon M
   2. Zelazny E
   3. Robert S
   4. Conéjéro G
   5. Curie C
   6. Friml J
   7. Vert G

   (2011) Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants

   PNAS 108:E450–E458.

   https://doi.org/10.1073/pnas.1100659108

   • PubMed
   • Google Scholar
4. 1. Bassil E
   2. Ohto M
   3. Esumi T
   4. Tajima H
   5. Zhu Z
   6. Cagnac O
   7. Belmonte M
   8. Peleg Z
   9. Yamaguchi T
   10. Blumwald E

   (2011) The Arabidopsis intracellular Na⁺/H⁺ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development

   The Plant Cell 23:224–239.

   https://doi.org/10.1105/tpc.110.079426

   • PubMed
   • Google Scholar
5. 1. Batelli G
   2. Verslues PE
   3. Agius F
   4. Qiu Q
   5. Fujii H
   6. Pan S
   7. Schumaker KS
   8. Grillo S
   9. Zhu JK

   (2007) SOS2 promotes salt tolerance in part by interacting with the vacuolar H⁺-ATPase and upregulating its transport activity

   Molecular and Cellular Biology 27:7781–7790.

   https://doi.org/10.1128/MCB.00430-07

   • PubMed
   • Google Scholar
6. 1. Blaesse P
   2. Airaksinen MS
   3. Rivera C
   4. Kaila K

   (2009) Cation-chloride cotransporters and neuronal function

   Neuron 61:820–838.

   https://doi.org/10.1016/j.neuron.2009.03.003

   • PubMed
   • Google Scholar
7. 1. Boettger T
   2. Hübner CA
   3. Maier H
   4. Rust MB
   5. Beck FX
   6. Jentsch TJ

   (2002) Deafness and renal tubular acidosis in mice lacking the K-Cl co-transporter Kcc4

   Nature 416:874–878.

   https://doi.org/10.1038/416874a

   • PubMed
   • Google Scholar
8. 1. Bolte S
   2. Cordelières FP

   (2006) A guided tour into subcellular colocalization analysis in light microscopy

   Journal of Microscopy 224:213–232.

   https://doi.org/10.1111/j.1365-2818.2006.01706.x

   • PubMed
   • Google Scholar
9. 1. Boulenguez P
   2. Liabeuf S
   3. Bos R
   4. Bras H
   5. Jean-Xavier C
   6. Brocard C
   7. Stil A
   8. Darbon P
   9. Cattaert D
   10. Delpire E
   11. Marsala M
   12. Vinay L

   (2010) Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury

   Nature Medicine 16:302–307.

   https://doi.org/10.1038/nm.2107

   • PubMed
   • Google Scholar
10. 1. Boursiac Y
    2. Boudet J
    3. Postaire O
    4. Luu DT
    5. Tournaire-Roux C
    6. Maurel C

    (2008) Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization

    The Plant Journal 56:207–218.

    https://doi.org/10.1111/j.1365-313X.2008.03594.x

    • PubMed
    • Google Scholar
11. 1. Brüx A
    2. Liu T-Y
    3. Krebs M
    4. Stierhof Y-D
    5. Lohmann JU
    6. Miersch O
    7. Wasternack C
    8. Schumacher K

    (2008) Reduced V-ATPase activity in the trans-Golgi network causes oxylipin-dependent hypocotyl growth Inhibition in Arabidopsis

    The Plant Cell 20:1088–1100.

    https://doi.org/10.1105/tpc.108.058362

    • PubMed
    • Google Scholar
12. 1. Che-Othman MH
    2. Millar AH
    3. Taylor NL

    (2017) Connecting salt stress signalling pathways with salinity-induced changes in mitochondrial metabolic processes in C3 plants

    Plant, Cell & Environment 40:2875–2905.

    https://doi.org/10.1111/pce.13034

    • PubMed
    • Google Scholar
13. 1. Chen ZC
    2. Yamaji N
    3. Fujii-Kashino M
    4. Ma JF

    (2016) A cation-chloride cotransporter gene is required for cell elongation and osmoregulation in rice

    Plant Physiology 171:494–507.

    https://doi.org/10.1104/pp.16.00017

    • PubMed
    • Google Scholar
14. 1. Clough SJ
    2. Bent AF

    (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana

    The Plant Journal 16:735–743.

    https://doi.org/10.1046/j.1365-313x.1998.00343.x

    • PubMed
    • Google Scholar
15. 1. Colmenero-Flores JM
    2. Martínez G
    3. Gamba G
    4. Vázquez N
    5. Iglesias DJ
    6. Brumós J
    7. Talón M

    (2007) Identification and functional characterization of cation-chloride cotransporters in plants

    The Plant Journal 50:278–292.

    https://doi.org/10.1111/j.1365-313X.2007.03048.x

    • PubMed
    • Google Scholar
16. 1. Correa Galvis V
    2. Strand DD
    3. Messer M
    4. Thiele W
    5. Bethmann S
    6. Hübner D
    7. Uflewski M
    8. Kaiser E
    9. Siemiatkowska B
    10. Morris BA
    11. Tóth SZ
    12. Watanabe M
    13. Brückner F
    14. Höfgen R
    15. Jahns P
    16. Schöttler MA
    17. Armbruster U

    (2020) H⁺ transport by K⁺ EXCHANGE ANTIPORTER3 promotes photosynthesis and growth in chloroplast ATP synthase mutants

    Plant Physiology 182:2126–2142.

    https://doi.org/10.1104/pp.19.01561

    • Google Scholar
17. 1. Cutler SR
    2. Ehrhardt DW
    3. Griffitts JS
    4. Somerville CR

    (2000) Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency

    PNAS 97:3718–3723.

    https://doi.org/10.1073/pnas.97.7.3718

    • PubMed
    • Google Scholar
18. 1. De Angeli A
    2. Monachello D
    3. Ephritikhine G
    4. Frachisse JM
    5. Thomine S
    6. Gambale F
    7. Barbier-Brygoo H

    (2009) Review CLC-mediated anion transport in plant cells

    Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 364:195–201.

    https://doi.org/10.1098/rstb.2008.0128

    • PubMed
    • Google Scholar
19. 1. Dejonghe W
    2. Kuenen S
    3. Mylle E
    4. Vasileva M
    5. Keech O
    6. Viotti C
    7. Swerts J
    8. Fendrych M
    9. Ortiz-Morea FA
    10. Mishev K
    11. Delang S
    12. Scholl S
    13. Zarza X
    14. Heilmann M
    15. Kourelis J
    16. Kasprowicz J
    17. Nguyen LSL
    18. Drozdzecki A
    19. Van Houtte I
    20. Szatmári AM
    21. Majda M
    22. Baisa G
    23. Bednarek SY
    24. Robert S
    25. Audenaert D
    26. Testerink C
    27. Munnik T
    28. Van Damme D
    29. Heilmann I
    30. Schumacher K
    31. Winne J
    32. Friml J
    33. Verstreken P
    34. Russinova E

    (2016) Mitochondrial uncouplers inhibit clathrin-mediated endocytosis largely through cytoplasmic acidification

    Nature Communications 7:11710.

    https://doi.org/10.1038/ncomms11710

    • PubMed
    • Google Scholar
20. 1. Dettmer J
    2. Hong-Hermesdorf A
    3. Stierhof YD
    4. Schumacher K

    (2006) Vacuolar H⁺-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis

    The Plant Cell 18:715–730.

    https://doi.org/10.1105/tpc.105.037978

    • PubMed
    • Google Scholar
21. 1. Domingos P
    2. Dias PN
    3. Tavares B
    4. Portes MT
    5. Wudick MM
    6. Konrad KR
    7. Gilliham M
    8. Bicho A
    9. Feijó JA

    (2019) Molecular and electrophysiological characterization of anion transport in Arabidopsis thaliana pollen reveals regulatory roles for pH, Ca²⁺ and GABA

    The New Phytologist 223:1353–1371.

    https://doi.org/10.1111/nph.15863

    • PubMed
    • Google Scholar
22. 1. Dragwidge JM
    2. Ford BA
    3. Ashnest JR
    4. Das P
    5. Gendall AR

    (2018) Two Endosomal NHX-Type Na⁺/H⁺ Antiporters are Involved in Auxin-Mediated Development in Arabidopsis thaliana

    Plant & Cell Physiology 59:1660–1669.

    https://doi.org/10.1093/pcp/pcy090

    • PubMed
    • Google Scholar
23. 1. Dragwidge JM
    2. Scholl S
    3. Schumacher K
    4. Gendall AR

    (2019) NHX-type Na⁺(K⁺)/H⁺ antiporters are required for TGN/EE trafficking and endosomal ion homeostasis in Arabidopsis

    Journal of Cell Science 132:226472.

    https://doi.org/10.1242/jcs.226472

    • PubMed
    • Google Scholar
24. 1. Drakakaki G
    2. van de Ven W
    3. Pan S
    4. Miao Y
    5. Wang J
    6. Keinath NF
    7. Weatherly B
    8. Jiang L
    9. Schumacher K
    10. Hicks G
    11. Raikhel N

    (2012) Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis

    Cell Research 22:413–424.

    https://doi.org/10.1038/cr.2011.129

    • PubMed
    • Google Scholar
25. 1. Geldner N
    2. Friml J
    3. Stierhof YD
    4. Jürgens G
    5. Palme K

    (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking

    Nature 413:425–428.

    https://doi.org/10.1038/35096571

    • PubMed
    • Google Scholar
26. 1. Gilles JF
    2. Dos Santos M
    3. Boudier T
    4. Bolte S
    5. Heck N

    (2017) DiAna, an ImageJ tool for object-based 3D co-localization and distance analysis

    Methods 115:55–64.

    https://doi.org/10.1016/j.ymeth.2016.11.016

    • PubMed
    • Google Scholar
27. 1. Groen AJ
    2. Sancho-Andrés G
    3. Breckels LM
    4. Gatto L
    5. Aniento F
    6. Lilley KS

    (2014) Identification of trans-golgi network proteins in Arabidopsis thaliana root tissue

    Journal of Proteome Research 13:763–776.

    https://doi.org/10.1021/pr4008464

    • PubMed
    • Google Scholar
28. 1. Guo W
    2. Zuo Z
    3. Cheng X
    4. Sun J
    5. Li H
    6. Li L
    7. Qiu JL

    (2014) The chloride channel family gene CLCd negatively regulates pathogen-associated molecular pattern (PAMP)-triggered immunity in Arabidopsis

    Journal of Experimental Botany 65:1205–1215.

    https://doi.org/10.1093/jxb/ert484

    • PubMed
    • Google Scholar
29. 1. Hachez C
    2. Veljanovski V
    3. Reinhardt H
    4. Guillaumot D
    5. Vanhee C
    6. Chaumont F
    7. Batoko H

    (2014) The Arabidopsis abiotic stress-induced TSPO-related protein reduces cell-surface expression of the aquaporin PIP2;7 through protein-protein interactions and autophagic degradation

    The Plant Cell 26:4974–4990.

    https://doi.org/10.1105/tpc.114.134080

    • PubMed
    • Google Scholar
30. 1. Han BD
    2. Jiang YH
    3. Cui GX
    4. Mi JN
    5. Roelfsema MRG
    6. Mouille G
    7. Sechet J
    8. Al-Babili S
    9. Aranda M
    10. Hirt H

    (2020) Cation-chloride co-transporter (CCC1) mediates plant resistance against Pseudomonas Syringae

    Plant Physiology 182:1052–1065.

    https://doi.org/10.1104/pp.19.01279

    • Google Scholar
31. 1. Hartmann AM
    2. Tesch D
    3. Nothwang HG
    4. Bininda-Emonds ORP

    (2014) Evolution of the cation chloride cotransporter family: ancient origins, gene losses, and subfunctionalization through duplication

    Molecular Biology and Evolution 31:434–447.

    https://doi.org/10.1093/molbev/mst225

    • PubMed
    • Google Scholar
32. 1. Hartmann AM
    2. Nothwang HG

    (2015) Molecular and evolutionary insights into the structural organization of cation chloride cotransporters

    Frontiers in Cellular Neuroscience 8:470.

    https://doi.org/10.3389/fncel.2014.00470

    • PubMed
    • Google Scholar
33. 1. Henderson SW
    2. Wege S
    3. Qiu J
    4. Blackmore DH
    5. Walker AR
    6. Tyerman SD
    7. Walker RR
    8. Gilliham M

    (2015) Grapevine and arabidopsis cation-chloride cotransporters localize to the golgi and trans-golgi network and indirectly influence long-distance ion transport and plant salt tolerance

    Plant Physiology 169:2215–2229.

    https://doi.org/10.1104/pp.15.00499

    • PubMed
    • Google Scholar
34. 1. Henderson SW
    2. Wege S
    3. Gilliham M

    (2018) Plant cation-chloride cotransporters (CCC): evolutionary origins and functional insights

    International Journal of Molecular Sciences 19:E492.

    https://doi.org/10.3390/ijms19020492

    • PubMed
    • Google Scholar
35. 1. Howard HC
    2. Mount DB
    3. Rochefort D
    4. Byun N
    5. Dupré N
    6. Lu J
    7. Fan X
    8. Song L
    9. Rivière JB
    10. Prévost C
    11. Horst J
    12. Simonati A
    13. Lemcke B
    14. Welch R
    15. England R
    16. Zhan FQ
    17. Mercado A
    18. Siesser WB
    19. George AL
    20. McDonald MP
    21. Bouchard JP
    22. Mathieu J
    23. Delpire E
    24. Rouleau GA

    (2002) The K-Cl cotransporter KCC3 is mutant in a severe peripheral neuropathy associated with agenesis of the corpus callosum

    Nature Genetics 32:384–392.

    https://doi.org/10.1038/ng1002

    • PubMed
    • Google Scholar
36. 1. Jefferson RA
    2. Kavanagh TA
    3. Bevan MW

    (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants

    The EMBO Journal 6:3901–3907.

    https://doi.org/10.1002/j.1460-2075.1987.tb02730.x

    • PubMed
    • Google Scholar
37. 1. Johnson MA
    2. von Besser K
    3. Zhou Q
    4. Smith E
    5. Aux G
    6. Patton D
    7. Levin JZ
    8. Preuss D

    (2004) Arabidopsis hapless mutations define essential gametophytic functions

    Genetics 168:971–982.

    https://doi.org/10.1534/genetics.104.029447

    • PubMed
    • Google Scholar
38. 1. Kim JY
    2. Liu CY
    3. Zhang F
    4. Duan X
    5. Wen Z
    6. Song J
    7. Feighery E
    8. Lu B
    9. Rujescu D
    10. St Clair D
    11. Christian K
    12. Callicott JH
    13. Weinberger DR
    14. Song H
    15. Ming G

    (2012) Interplay between DISC1 and GABA signaling regulates neurogenesis in mice and risk for schizophrenia

    Cell 148:1051–1064.

    https://doi.org/10.1016/j.cell.2011.12.037

    • PubMed
    • Google Scholar
39. 1. Krebs M
    2. Beyhl D
    3. Görlich E
    4. Al-Rasheid KAS
    5. Marten I
    6. Stierhof YD
    7. Hedrich R
    8. Schumacher K

    (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation

    PNAS 107:3251–3256.

    https://doi.org/10.1073/pnas.0913035107

    • PubMed
    • Google Scholar
40. 1. Kunchaparty S
    2. Palcso M
    3. Berkman J
    4. Velázquez H
    5. Desir GV
    6. Bernstein P
    7. Reilly RF
    8. Ellison DH

    (1999) Defective processing and expression of thiazide-sensitive Na-Cl cotransporter as a cause of Gitelman’s syndrome

    The American Journal of Physiology 277:F643–F649.

    https://doi.org/10.1152/ajprenal.1999.277.4.F643

    • PubMed
    • Google Scholar
41. 1. Luo Y
    2. Scholl S
    3. Doering A
    4. Zhang Y
    5. Irani NG
    6. Rubbo SD
    7. Neumetzler L
    8. Krishnamoorthy P
    9. Van Houtte I
    10. Mylle E
    11. Bischoff V
    12. Vernhettes S
    13. Winne J
    14. Friml J
    15. Stierhof YD
    16. Schumacher K
    17. Persson S
    18. Russinova E

    (2015) V-ATPase activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis

    Nature Plants 1:15094.

    https://doi.org/10.1038/nplants.2015.94

    • PubMed
    • Google Scholar
42. 1. Luu D-T
    2. Martinière A
    3. Sorieul M
    4. Runions J
    5. Maurel C

    (2012) Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress

    The Plant Journal 69:894–905.

    https://doi.org/10.1111/j.1365-313X.2011.04841.x

    • PubMed
    • Google Scholar
43. 1. Marquès-Bueno MDM
    2. Morao AK
    3. Cayrel A
    4. Platre MP
    5. Barberon M
    6. Caillieux E
    7. Colot V
    8. Jaillais Y
    9. Roudier F
    10. Vert G

    (2016) A versatile Multisite Gateway-compatible promoter and transgenic line collection for cell type-specific functional genomics in Arabidopsis

    The Plant Journal 85:320–333.

    https://doi.org/10.1111/tpj.13099

    • PubMed
    • Google Scholar
44. 1. Martinière A
    2. Bassil E
    3. Jublanc E
    4. Alcon C
    5. Reguera M
    6. Sentenac H
    7. Blumwald E
    8. Paris N

    (2013) In vivo intracellular pH measurements in tobacco and Arabidopsis reveal an unexpected pH gradient in the endomembrane system

    The Plant Cell 25:4028–4043.

    https://doi.org/10.1105/tpc.113.116897

    • PubMed
    • Google Scholar
45. 1. McDowell SC
    2. Akmakjian G
    3. Sladek C
    4. Mendoza-Cozatl D
    5. Morrissey JB
    6. Saini N
    7. Mittler R
    8. Baxter I
    9. Salt DE
    10. Ward JM
    11. Schroeder JI
    12. Guerinot ML
    13. Harper JF

    (2013) Elemental concentrations in the seed of mutants and natural variants of Arabidopsis thaliana grown under varying soil conditions

    PLOS ONE 8:e63014.

    https://doi.org/10.1371/journal.pone.0063014

    • PubMed
    • Google Scholar
46. 1. McFarlane HE
    2. Young RE
    3. Wasteneys GO
    4. Samuels AL

    (2008) Cortical microtubules mark the mucilage secretion domain of the plasma membrane in Arabidopsis seed coat cells

    Planta 227:1363–1375.

    https://doi.org/10.1007/s00425-008-0708-2

    • PubMed
    • Google Scholar
47. 1. Moseyko N
    2. Feldman LJ

    (2001) Expression of pH-sensitive green fluorescent protein in Arabidopsis thaliana

    Plant, Cell & Environment 24:557–563.

    https://doi.org/10.1046/j.1365-3040.2001.00703.x

    • PubMed
    • Google Scholar
48. 1. Nikolovski N
    2. Shliaha PV
    3. Gatto L
    4. Dupree P
    5. Lilley KS

    (2014) Label-free protein quantification for plant Golgi protein localization and abundance

    Plant Physiology 166:1033–1043.

    https://doi.org/10.1104/pp.114.245589

    • PubMed
    • Google Scholar
49. 1. Parsons HT
    2. Stevens TJ
    3. McFarlane HEM
    4. Vidal-Melgosa S
    5. Griss J
    6. Lawrence N
    7. Butler R
    8. Sousa MML
    9. Salemi M
    10. Willats WGT
    11. Petzold CJ
    12. Heazlewood JL
    13. Lilley KS

    (2019) Separating Golgi proteins from cis to trans reveals underlying properties of cisternal localization

    The Plant Cell 31:2010–2034.

    https://doi.org/10.1105/tpc.19.00081

    • Google Scholar
50. 1. Petrezselyova S
    2. Kinclova-Zimmermannova O
    3. Sychrova H

    (2013) Vhc1, a novel transporter belonging to the family of electroneutral cation-Cl(-) cotransporters, participates in the regulation of cation content and morphology of Saccharomyces cerevisiae vacuoles

    Biochimica et Biophysica Acta 1828:623–631.

    https://doi.org/10.1016/j.bbamem.2012.09.019

    • PubMed
    • Google Scholar
51. 1. Reguera M
    2. Bassil E
    3. Tajima H
    4. Wimmer M
    5. Chanoca A
    6. Otegui MS
    7. Paris N
    8. Blumwald E

    (2015) pH Regulation by NHX-type antiporters is required for receptor-mediated protein trafficking to the vacuole in arabidopsis

    The Plant Cell 27:1200–1217.

    https://doi.org/10.1105/tpc.114.135699

    • PubMed
    • Google Scholar
52. 1. Rivera C
    2. Li H
    3. Thomas-Crusells J
    4. Lahtinen H
    5. Viitanen T
    6. Nanobashvili A
    7. Kokaia Z
    8. Airaksinen MS
    9. Voipio J
    10. Kaila K
    11. Saarma M

    (2002) BDNF-induced TrkB activation down-regulates the K⁺-Cl^- cotransporter KCC2 and impairs neuronal Cl- extrusion

    The Journal of Cell Biology 159:747–752.

    https://doi.org/10.1083/jcb.200209011

    • PubMed
    • Google Scholar
53. 1. Sadowski PG
    2. Groen AJ
    3. Dupree P
    4. Lilley KS

    (2008) Sub-cellular localization of membrane proteins

    Proteomics 8:3991–4011.

    https://doi.org/10.1002/pmic.200800217

    • PubMed
    • Google Scholar
54. 1. Sato T

    (1968)

    A modified method for lead staining of thin sections

    Journal of Electron Microscopy 17:158–159.

    • PubMed
    • Google Scholar
55. 1. Schindelin J
    2. Arganda-Carreras I
    3. Frise E
    4. Kaynig V
    5. Longair M
    6. Pietzsch T
    7. Preibisch S
    8. Rueden C
    9. Saalfeld S
    10. Schmid B
    11. Tinevez J-Y
    12. White DJ
    13. Hartenstein V
    14. Eliceiri K
    15. Tomancak P
    16. Cardona A

    (2012) Fiji: an open-source platform for biological-image analysis

    Nature Methods 9:676–682.

    https://doi.org/10.1038/nmeth.2019

    • PubMed
    • Google Scholar
56. 1. Scholl S
    2. Hillmer S
    3. Krebs M
    4. Schumacher K

    (2021) ClCd and ClCf act redundantly at the trans-Golgi network/early endosome and prevent acidification of the Golgi stack

    Journal of Cell Science 134:jcs258807.

    https://doi.org/10.1242/jcs.258807

    • PubMed
    • Google Scholar
57. 1. Schumacher K
    2. Vafeados D
    3. McCarthy M
    4. Sze H
    5. Wilkins T
    6. Chory J

    (1999) The Arabidopsis det3 mutant reveals a central role for the vacuolar H(+)-ATPase in plant growth and development

    Genes & Development 13:3259–3270.

    https://doi.org/10.1101/gad.13.24.3259

    • PubMed
    • Google Scholar
58. 1. Shen J
    2. Zeng Y
    3. Zhuang X
    4. Sun L
    5. Yao X
    6. Pimpl P
    7. Jiang L

    (2013) Organelle pH in the Arabidopsis endomembrane system

    Molecular Plant 6:1419–1437.

    https://doi.org/10.1093/mp/sst079

    • PubMed
    • Google Scholar
59. 1. Simon DB
    2. Karet FE
    3. Hamdan JM
    4. DiPietro A
    5. Sanjad SA
    6. Lifton RP

    (1996) Bartter’s syndrome, hypokalaemic alkalosis with hypercalciuria, is caused by mutations in the Na-K-2Cl cotransporter NKCC2

    Nature Genetics 13:183–188.

    https://doi.org/10.1038/ng0696-183

    • PubMed
    • Google Scholar
60. 1. Sinclair R
    2. Rosquete MR
    3. Drakakaki G

    (2018) Post-Golgi Trafficking and Transport of Cell Wall Components

    Frontiers in Plant Science 9:1784.

    https://doi.org/10.3389/fpls.2018.01784

    • PubMed
    • Google Scholar
61. 1. Sliwinska E
    2. Mathur J
    3. Bewley JD

    (2015) On the relationship between endoreduplication and collet hair initiation and tip growth, as determined using six Arabidopsis thaliana root-hair mutants

    Journal of Experimental Botany 66:3285–3295.

    https://doi.org/10.1093/jxb/erv136

    • PubMed
    • Google Scholar
62. 1. Spurr AR

    (1969) A low-viscosity epoxy resin embedding medium for electron microscopy

    Journal of Ultrastructure Research 26:31–43.

    https://doi.org/10.1016/s0022-5320(69)90033-1

    • PubMed
    • Google Scholar
63. 1. Sze H
    2. Chanroj S

    (2018) Plant endomembrane dynamics: studies of K⁺/H⁺ antiporters provide insights on the effects of pH and ion homeostasis

    Plant Physiology 177:875–895.

    https://doi.org/10.1104/pp.18.00142

    • PubMed
    • Google Scholar
64. 1. van Delden SH
    2. Nazarideljou MJ
    3. Marcelis LFM

    (2020) Nutrient solutions for Arabidopsis thaliana: a study on nutrient solution composition in hydroponics systems

    Plant Methods 16:72.

    https://doi.org/10.1186/s13007-020-00606-4

    • PubMed
    • Google Scholar
65. 1. Viotti C
    2. Bubeck J
    3. Stierhof Y-D
    4. Krebs M
    5. Langhans M
    6. van den Berg W
    7. van Dongen W
    8. Richter S
    9. Geldner N
    10. Takano J
    11. Jürgens G
    12. de Vries SC
    13. Robinson DG
    14. Schumacher K

    (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle

    The Plant Cell 22:1344–1357.

    https://doi.org/10.1105/tpc.109.072637

    • PubMed
    • Google Scholar
66. 1. Wendrich JR
    2. Yang B
    3. Vandamme N
    4. Verstaen K
    5. Smet W
    6. Van de Velde C
    7. Minne M
    8. Wybouw B
    9. Mor E
    10. Arents HE
    11. Nolf J
    12. Van Duyse J
    13. Van Isterdael G
    14. Maere S
    15. Saeys Y
    16. De Rybel B

    (2020) Vascular transcription factors guide plant epidermal responses to limiting phosphate conditions

    Science 370:eaay4970.

    https://doi.org/10.1126/science.aay4970

    • PubMed
    • Google Scholar
67. 1. Xu J
    2. Scheres B

    (2005) Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity

    The Plant Cell 17:525–536.

    https://doi.org/10.1105/tpc.104.028449

    • PubMed
    • Google Scholar
68. 1. Zhang GF
    2. Driouich A
    3. Staehelin LA

    (1993)

    Effect of monensin on plant Golgi: re-examination of the monensin-induced changes in cisternal architecture and functional activities of the Golgi apparatus of sycamore suspension-cultured cells

    Journal of Cell Science 104 ( Pt 3):819–831.

    • PubMed
    • Google Scholar
69. 1. Zhu X
    2. Pan T
    3. Zhang X
    4. Fan L
    5. Quintero FJ
    6. Zhao H
    7. Su X
    8. Li X
    9. Villalta I
    10. Mendoza I
    11. Shen J
    12. Jiang L
    13. Pardo JM
    14. Qiu QS

    (2019) K⁺ Efflux Antiporters 4, 5 and 6 mediate pH and K⁺ homeostasis in endomembrane compartments

    Plant, Cell & Environment 178:1657–1678.

    https://doi.org/10.1104/pp.18.01053

    • PubMed
    • Google Scholar

Author details

1. Daniel W McKay

   School of Agriculture, Food and Wine, Waite Research Institute, ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Waite Campus, Adelaide, Australia

   Contribution

   Formal analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9743-4961

2. Heather E McFarlane

   1. School of Biosciences, University of Melbourne, Melbourne, Australia
   2. Department of Cell and Systems Biology, University of Toronto, Toronto, Canada

   Contribution

   Investigation, Methodology, Visualization, Writing – review and editing

   Competing interests

   Reviewing editor, eLife

   "This ORCID iD identifies the author of this article:" 0000-0001-5569-5151

3. Yue Qu

   School of Agriculture, Food and Wine, Waite Research Institute, ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Waite Campus, Adelaide, Australia

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0101-1097

4. Apriadi Situmorang

   School of Agriculture, Food and Wine, Waite Research Institute, ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Waite Campus, Adelaide, Australia

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1879-3355

5. Matthew Gilliham

   School of Agriculture, Food and Wine, Waite Research Institute, ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Waite Campus, Adelaide, Australia

   Contribution

   Conceptualization, Funding acquisition, Methodology, Resources, Supervision, Validation, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0666-3078

6. Stefanie Wege

   School of Agriculture, Food and Wine, Waite Research Institute, ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Waite Campus, Adelaide, Australia

   Contribution

   Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Writing – original draft, Writing – review and editing

   For correspondence

   stefanie.wege@adelaide.edu.au

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7232-5889

• 1,922

  views

• 347

  downloads

• 11

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.