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

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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 accesses here: https://doi.org/10.25909/17256545 https://doi.org/10.25909/17256515 https://doi.org/10.25909/17256467 https://doi.org/10.25909/17256428.

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Author details

1. W Daniel 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. E Heather 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

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