Trends in Plant Science
Volume 24, Issue 2, February 2019, Pages 142-151
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Opinion
Friend or Foe? Chloride Patterning in Halophytes

https://doi.org/10.1016/j.tplants.2018.11.003Get rights and content

Highlights

Interest in the Cl aspect of salinity tolerance has traditionally focused on non-halophytes.

Knowledge of Cl regulation in ‘salt-loving’ halophytes is limited, even though these plants thrive and survive at much higher external Cl than non-halophytes and use Cl for osmoregulation.

Proteins catalysing root Cl transport have recently been characterised in non-halophytes, but this knowledge needs to be extended to halophytes. Of interest is that single amino acid polymorphisms in halophytic transporters alter their function compared to their non-halophytic homologues.

Our understanding of post-translational regulation of anion channels in stomata is fairly advanced, but that of root Cl transport remains elusive.

The calcineurin B-like protein (CBL)–CBL-interacting protein kinase (CIPK) network regulates several ion transport systems in plants. Does it also modulate Cl transport?

In this opinion article, we challenge the traditional view that breeding for reduced Cl uptake would benefit plant salinity tolerance. A negative correlation between shoot Cl concentration and plant biomass does not hold for halophytes – naturally salt tolerant species. We argue that, under physiologically relevant conditions, Cl uptake requires plants to invest metabolic energy, and that the poor selectivity of Cl-transporting proteins may explain the reported negative correlation between Cl accumulation and crop salinity tolerance. We propose a new paradigm: salinity tolerance could be achieved by improving the selectivity of some of the broadly selective anion-transporting proteins (e.g., for NO3 > Cl), alongside tight control of Cl uptake, rather than targeting traits mediating its efflux from the root.

Section snippets

Chloride – A Toxin or a Beneficial Osmoticum?

The physiological and molecular mechanisms conferring plant salinity tolerance have been intensively studied over the past four decades. Most investigations have focused on Na+, but the past few years have witnessed a ‘renaissance period’ for Cl research. This interest is mainly driven by the need to fully understand the role of Cl as a nutrient and its conflicting role in limiting plant growth in saline soils 1, 2, 3, 4, 5. However, this current attention on the role of Cl in plant salinity

Should Chloride Be Excluded?

In non-halophytes, the current notion is that Cl exclusion from the shoot (either from the root epidermis or the xylem) is crucial for salt tolerance 1, 3, 7, 8, 9, 10, 11, 12. These arguments are supported by findings in some salt-sensitive species that high shoot Cl levels correlate with severe physiological dysfunctions that not only affect the yield but also the quality and edibility of non-halophytic crops 4, 13, 14. Nonetheless, tissue Cl concentrations in halophytes can exceed 500 mM 15

Energetics of Chloride Transport

The cellular targets for Cl toxicity remain elusive, but high Cl concentrations have been found to interfere with root NO3 uptake [31], stomatal regulation, and leaf photosynthetic capacity 11, 32. Thus, using Cl for osmotic adjustment comes with the risk of overaccumulation and potential toxicity to cellular functions. In most plant cells, the large central vacuole serves as a storage reservoir where, during salt stress, cytotoxic Cl and Na+ are sequestered away to maintain optimal

Do Chloride Transporters Differ between Halophytes and Non-Halophytes?

The mechanisms of Cl uptake at the root PM in halophytes remain to be discovered. In non-halophytes, the molecular identity of transporters likely to catalyse Cl transport at the root PM has recently been revealed (Box 1), and these putative Cl transport systems could also occur in halophytes. However, the picture is far from complete. More in-depth phylogenetic and functional analyses of these transporter/channel families are required both in halophytes and non-halophytes. Recent evidence

How Is Chloride Transport Regulated?

Compared to their non-halophytic relatives, halophytes have enhanced constitutive expression of specific gene families involved in ion transport (e.g., NHXs, HKTs, SLAHs, and AHAs 57, 58, 59, 60). Nevertheless, salt-induced changes in protein activity are not always associated with changes in transcriptional regulation, emphasising the important role of post-translational regulation 33, 35, 39, 57, 58. Anion transport is controlled by many cytosolic factors 61, 62, and it is plausible that the

Concluding Remarks and Future Perspectives

Regulation of Cl uptake and translocation in plants is a significant issue, even more so under saline conditions where Cl toxicity potentially comes into play. We argue here that, under saline conditions, halophytes: (i) require Cl as an osmoticum for cell turgor and growth, (ii) invest metabolic energy for Cl uptake by roots, and (iii) regulate Cl influx rather than relying on efflux to tightly control net root Cl uptake. The ability of halophytes to limit Cl influx over the long term

Acknowledgments

N.B. is a recipient of a Marie Curie Fellowship (grant 700001).

Glossary

Active ion transport
movement of ions across a membrane against the electrochemical gradient, thus requiring energy. Passive ion transport does not require energy input.
Calcineurin B-like protein (CBL)–CBL-interacting protein kinase (CIPK) network
a signalling network that acts in diverse plant stress responses. In plants, different environmental stimuli generate specific Ca2+ signatures. The CBL proteins are one of the plant sensors that perceive these Ca2+ signatures and then interact with and

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