Accepted Manuscript
Title: Review on the significance of chlorine for crop yield and
quality
Author: Christoph-Martin Geilfus
PII:
DOI:
Reference:
S0168-9452(17)30770-7
https://doi.org/10.1016/j.plantsci.2018.02.014
PSL 9757
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Plant Science
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Revised date:
Accepted date:
16-8-2017
29-12-2017
13-2-2018
Please cite this article as: Christoph-Martin Geilfus, Review on
the significance of chlorine for crop yield and quality, Plant
Science https://doi.org/10.1016/j.plantsci.2018.02.014
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Review on the significance of chlorine for
crop yield and quality
Christoph-Martin Geilfus
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C.-M. Geilfus; Controlled Environment Horticulture, Faculty of Life Sciences, Albrecht
Daniel Thaer-Institute of Agricultural and Horticultural Sciences, Humboldt-University of
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Berlin, Albrecht-Thaer-Weg 1, 14195 Berlin, Germany. E-mail: geilfusc@hu-berlin.de.
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Phone: +49(0) 30 2093 46475
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Graphical abstract
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Highlights
 Cl--salinity induces dysfunctions that hamper quality formation in crops.
 Starch partitioning, nutrient uptake, protein biosynthesis or photosynthesis are
impaired.
 Action is needed to stabilize yields and quality under Cl--salinity.
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 Thus, dietary quality of harvests is lowered by high tissue concentration of Cl-.
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 Restricted Cl--xylem loading or NO3-fertilization limit Cl- accumulation.
Abstract
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The chloride concentration in the plant determines yield and quality formation for two
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reasons. First, chlorine is a mineral nutrient and deficiencies thereof induce metabolic
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problems that interfere with growth. However, due to low requirement of most crops,
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deficiency of chloride hardly appears in the field. Second, excess of chloride, an event that
occurs under chloride-salinity, results in severe physiological dysfunctions impairing both
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quality and yield formation. The chloride ion can effect quality of plant-based products by
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conferring a salty taste that decreases market appeal of e.g. fruit juices and beverages.
However, most of the quality impairments are based on physiological dysfunctions that arise
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under conditions of chloride-toxicity: Shelf life of persimmon is shortened due to an
autocatalytic ethylene production in fruit tissues. High concentrations of chloride in the soil
can increase phyto-availability of the heavy metal cadmium, accumulating in wheat grains
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above dietary intake thresholds. When crops are cultivated on soils that are moderately
salinized by chloride, nitrate fertilization might be a strategy to suppress uptake of chloride by
means of an antagonistic anion-anion uptake competition. Overall, knowledge about proteins
that catalyse chloride-efflux out of the roots or that restrict xylem loading is needed to
engineer more resistant crops.
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Abbreviations: Chloride, Cl−.
Keywords: Chloride, Photosynthesis, Osmoregulation, Tonoplast-type H+-ATPase, BlossomEnd Rot, Crops, Yield, Quality, Fungal Infections.
Introduction
2.
Cl− as nutrient
Osmo- and turgor-regulation
2.2
Elongation growth and tonoplast-type H+-ATPase
2.3
Rhythmic movements
2.4
Action potentials as signals?
2.5
Enzyme activities
2.6
Photosynthesis
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2.1
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Cl− excess constrains yield formation
Inhibition of photosynthetic capacity
3.2
Retardation of root and tuber growth
3.3
The Cl−-sensitive potato
3.4
Antagonistic anion-anion effects
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3.1
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3.
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1.
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Tables of Contents
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4.
5.
Dysfunctions under Cl−-toxicity and implication for food quality and safety
4.1
Protein biosynthesis
4.2
Blossom-end rot
4.3
Ethylene production
4.4
Enhance cadmium uptake
4.5
Loss of quality of fruit juices and beverages in response to Cl−-toxicity
Cl− fertilization for fungal infection management
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6.
Concluding remarks
7.
Outstanding questions
1.
Introduction
Chloride (Cl−) is a nutrient and beneficial ion for higher plants [1,2]. The concentration of Cl−
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in the soil and its bulk solution mainly depends on bedrock material, depositions of airborne
Cl− via e.g. precipitation, or on inputs through fertilization or irrigation with Cl−-containing
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waters [3]. The average Cl− concentration in soils is 0.10 g kg-1 soil [4]. Cl− is barely adsorbed
to soil particles [5] and since it is highly water soluble [6], it is very mobile in soil solution.
The monovalent anion travels with soil water towards the root where it is taken up into the
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plant, a process that correlates well with water flow [7]. In the roots, Cl− moves
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predominantly via the symplastic pathway radially towards the vascular stele [8]. Before Cl−
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is acropetally translocated via xylem to the shoot, it needs to enter the root xylem. In
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Arabidopsis, this is partially mediated by the stelar-localized anion/H+ cotransporters protein
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NPF2.4 that facilitates the loading of Cl− into the root xylem [9]. For more molecular details
regarding Cl− uptake into the root cells or xylem loading and unloading, the reader is referred
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to recent works [10,11]. After Cl− is released in the shoot, it can be distributed via the phloem
[12], reaching the cytosol for e.g. storage in the vacuole [13] or incorporation in the oxygen-
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evolving complex of the photosystem II [14]. The Cl− concentration in the shoots of all major
glycophytic crop plants ranges from 1-20 mg g dw-1 [15-19]. This depends on species,
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genotype and the level of Cl− in the environment [20].
Under conditions of excess of Cl− in the environment, tissue concentrations can exceed toxic
levels in our crops, whereupon yield and quality are reduced. Not much is known about how
toxic level of Cl− are mechanistically linked with processes that impair quality formation.
There is a dearth of published data and the few information are scattered. Here, the historic
and the recent literature is reviewed and novel hypotheses are developed that led to the
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suggestion of novel experiments that are urgently needed to bring the topic forward. The first
part in this review is meant to provide a survey about functions of Cl− as nutrient. Then,
aspects related to the accumulation of excess of Cl− are discussed with special emphasis on
toxicity-related constraints for quality formation. Recommendations to produce yields with a
2.
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high quality are worked out.
Cl− as nutrient
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Most glycophytic crop plants (plants that will only grow in soils with a low content of salts)
contain 1-20 mg Cl− g dw-1 [15,16]. However, deficiency symptoms are observed only at
much lower concentrations. Thresholds for deficiency strongly depend on the crop species.
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Rice (Oryza sativa) is deficient at Cl− concentrations below 3 mg g shoot dw-1, wheat
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(Triticum aestivum) and barley (Hordeum vulgare) at concentrations below 1.2-4.0 mg g dw-1,
spinach (Spinacia oleracea) and lettuce (Lactuca sativa) at concentrations below 0.14 mg g
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dw-1, and maize (Zea mays) when Cl− falls below a concentrations of 0.05-0.11 mg Cl− g dw-1
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[3]. By assuming a minimal requirement of 1 mg Cl− g dw-1, it was calculated that rainfall at
inland sites would deposit the required Cl−, which amounts to 4-8 kg ha-1 [16]. Thus, despite
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rare exceptions [21], a Cl− deficiency in the field is considered an unlikely event that might
only be observed when plants with a high Cl− requirement such as palm trees (Elaeis spp.) (6
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mg Cl− g leaf dw-1) or kiwifruit (Actinida deliciosa) that require at least 60 µM g-1 leaf DW
[22] are cultivated in highly leached soils without any Cl− inputs (Marschner, 2011). For
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instance, it was calculated that one ton of dried tomato plants requires only a minimum of 200
grams of chlorine [1]. However, lack of Cl− can be studied under laboratory conditions in
hydroponic cultivation systems and these studies revealed that Cl− deficiency symptoms
include leaf growth reduction and wilting, which can be followed by chlorosis and necrosis
[1]. Although Cl− has a high mobility in the plant, Cl− deficiency symptoms are generally first
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observed in young leaves [23]. Functions of Cl− as a micronutrient or beneficial element will
be discussed next.
2.1
Osmo- and turgor-regulation
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Cl− is a micronutrient [24] but, during its function in osmo- and turgor-regulation, it can
accumulate in the vasculature, in guard cells or in expanding tissues reaching, at some
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instances, a final concentration of up to 150 mM in the vacuole [2,16]. Here, Cl− serves as an
osmoticum [25,26] that drives the water flow. In result, turgor increases which facilitates
compound movement [27], effects source-sink partitioning and influences turgor-driven
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movements. In the guard cells during stomatal aperture adjustments, Cl− has a similar function
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as malate. It counterbalances influx of potassium during stomata opening [28]. Accumulation
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of Cl− together with potassium and malate decreases guard cell water potential in vacuoles,
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whereupon water streams in, causing the guard cells to swell [29,30]. In guard cells, this
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potassium-counterbalancing role is dominantly exercised by malate [31], but Cl− is also
functional when malate is present [32-34]. It was found that the vacuolar chloride channel
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AtALMT9 controls the stomatal aperture via facilitating Cl− fluxes, whereby this channel is
activated by malate [13]. In agreement, it was shown for field bean (Vicia faba) that Cl− is
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sequestered in the vacuole of guard cell through the action of a kinase-dependent vacuolar
chloride channel, whereby this Cl− influx is required for stomatal opening [35]. Based on the
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general relevance for osmo-regulation and control of stomatal aperture, a debate has emerged
over the assumption that Cl− is relevant for water- and nitrogen use efficiencies in crops
[2,11].
2.2
Elongation growth and tonoplast-type H+-ATPase
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Cl− stimulates the activity of the tonoplast-type H+-translocating ATPase [36,37]. By this, it
contributes to the maintenance of the pH gradient between the slightly alkaline cytosol (pH =
7.2-7.5; [28]) and the acidic vacuole (pH = 5.0-5.5; [38,39]). This establishes a positive
membrane potential over the tonoplast [40], a potential that can reach +86 mV inside the
vacuole of the bubble algae (Valonia ventricosa) [41]. This difference of membrane potentials
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favours the intrusion of anions (e.g. nitrate) into the vacuole, where they serve as an
osmoticum. In consequence, water accumulates within the vacuoles and turgor pressure
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increases, which is thought to give rise to turgor-driven cell expansion in shoot and root tissue
[42,43,44]. In this way, Cl− is thought to be instrumental for facilitating elongation growth via
effects exerted through the V-type H+-ATPase on turgor [45]. Of note, the establishment of a
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positive membrane potential inside the vacuole wills also favours the influx of Cl− along its
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electrical gradient into the vacuole. The observation that the addition of 10 mM Cl− into a
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nutrient solutions of corn (Zea mays) and tomato (Lycopersicon esculentum) had a positive
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effect on growth [46], together with the fact that vacuoles can accumulate the osmotically
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active Cl−, gives rise to the idea that Cl− tolerant crops such as chard (Beta vulgaris subsp.
vulgaris) or clover (Trifolium repens) could be fertilized by moderate doses of Cl− in order to
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promote expansion growth. What is needed are experiments with increasing Cl− supply to test
for a dose that increases turgor-driven expansion growth without inducing cellular damages
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associated with Cl−-toxicities. The idea that uptake of Cl− favours expansion growth is
supported by the finding that the ꞌacid-growthꞌ-controlling phytohormone auxin [47]
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stimulates Cl− uptake by oat coleoptiles [48]. Moreover, it was found that a Cl− fertilization at
a rate of 44.83 kg ha-1 increases yield of corn and grain sorghum (Sorghum vulgare) when
applied to a soil that contains less than 22.42 kg ha-1 (0 - 60-cm depth) [49]. The fertilization
of winter wheat with Cl−, given as NH4Cl, markedly increased fresh weight yield and kernel
weight over those yields obtained by (NH4)2,SO4 fertilization (sulfate was sufficiently added
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to the NH4Cl-treated plots). Cl− was discussed to cause these yield increases by increasing leaf
turgor potential for the facilitation of expansion growth [50].
V-ATPases are also expressed in the endomembrane systems of the endoplasmic reticulum or
the Golgi vesicles [50]. Here, via the generation of potentials across the membranes, VATPase are implicated in a wide range of ion and metabolite transport processes and in
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secretory and endocytic trafficking [51,52]. In other words, it can be assumed that Cl− is
indirectly involved in all those processes but it is an open question what will happen if the
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cellular Cl− homeostasis cannot be maintained under conditions of e.g. Cl−-toxicity. Are VATPases-facilitated trafficking processes influenced?
Rhythmic movements
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2.3
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The rhythmic leaf movement of the pink silk tree (Albizzia julibrissin) is mediated by
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potassium influxes that are counterbalanced by Cl− influxes [53]. Influx of these ions
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increases turgor by decreasing the osmotic potential, which drives water influx. Besides
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functions in nastic movements, pulvinar movements are also influenced by Cl − activities. For
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more insights, the reader is referred to a recent work [2].
Action potentials as signals?
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There is some indication that Cl− fluxes between subcellular compartments generate action
potentials [54] that are suggested to be relevant for cellular communication [55,56]. More
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work is required to verify this and it would be interesting to know if this could be related to
signalling the onset of Cl−-salinity. During Cl−-salinity, cellular Cl−-concentrations can
accumulate up to the millimolar-range, a concentration that might be sufficient to generate
action potentials when channelled across (endo)membranes.
2.5
Enzyme activities
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The stimulating function of the activity of the tonoplast-type H+-ATPase was discussed
above. Besides, a link between Cl− and glutamine utilization for asparagine synthesis was
vaguely reported [57]: In the annual yellow-lupin (Lupinus luteus) Cl− acts as an allosteric
activator that increases the affinity of the glutamine-dependent asparagine synthetase to
glutamine by up to 50-fold. A glance to mammalian- or bacterial systems reveals the
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existence of more of such interactions. Cl− is known to regulate the activity of the
angiotensin-converting enzyme in human somatic cells [58] or the activity of the alpha-
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amylase in the proteobacteria Alteromonas haloplanctis [59]. It is an intriguing observation
that Cl− can act as allosteric enzyme activator. Upon binding, Cl− increases activity of the αamylase from the bacteria Pseudoalteromonas haloplanktis via positive allosteric modulation.
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Cl− binding is not mandatory for the proper enzyme folding but enhances the enzyme
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reactivity and the structural stability of this bacterial α-amylase [60]. It is not fully resolved
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whether Cl− has such an in vivo effect on the activity of α-amylase in plants. There is only a
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very early study on potato (Solanum tuberosum) that reports that Cl− accelerates and stabilizes
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the activity of the α-amylase [61]. The Starch content is a key quality determinant for
potatoes. Thus, it remains to be elucidated as to whether starch content in potatoes can be
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(substantially) increased by a slight supply of Cl− (the reader is referred to chapter 3.3 where
the sensitivity of potato to Cl− is discussed).
Photosynthesis
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2.6
Cl− has a major function in the photosynthetic light reaction. In the year 1946, a Cl−-depended
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stimulation of the Hill reaction was demonstrated [62]. It was then reasoned that Cl− indirectly
stimulates the oxygen evolution system by protecting chloroplastic components from being
destroyed by light [63]. This led to the suggestion that Cl− has a structural function in the
photosynthetic electron transport chain during the Hill reaction [64]. In vitro experiments on
isolated chloroplasts from sugar beet (Beta vulgaris) have shown that Cl− content can be
decreased by washing them with the Cl− chelator ethylenediaminetetraacetic acid [65]. When
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Cl− was added again, a 10-fold stimulation of the photosynthetic activity was observed. Later,
it was found that Cl− protects peptides of the photosystem II from dissociation and it was
concluded that Cl− has a structural role, which is to stabilize polypeptides from this
photosystem, thereby enabling the oxidation of water [66]. Crystal structure analysis of the
oxygen-evolving complex of the photosystem II indicated a role of Cl− in the structural
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organization of the Mn4CaO5-cluster [14]. The finding that Cl− binding sites near this
Mn4CaO5-cluster are exposed to the luminal bulk solution gave rise to the idea that Cl− is an
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integral compound of structures that function either as a proton exit channel or water inlet
channel [14]. It was proposed that the binding of Cl− near the oxygen-evolving complex
avoids the formation of a salt bridge between aspartic acid and lysine [59]. The formation of
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such a bridge might otherwise result in a conformational shift that lowers the pKa of this
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residue, being unfavourable for the ability to accept protons during the S-state cycle of the
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Cl− excess constrains yield formation
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3.
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water oxidizing process.
Cl− toxicity can result in chlorotic discolorations and later in necrotic leaf edges. Growth of
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glycophytes is sizeably reduced [67]. Visual toxicity symptoms can start with chlorosis at the
leaf edges, which might precede leaf tip burn [68] or in extreme situations leaf abscission.
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However, such Cl−-injuries are not only a thread to global food security, they are also
problematic for ornamental crops such as roses (Rosa ×fortuniana or R. odorata), because
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they reduce the aesthetic appearance and thus consumer acceptance and marketable yield [69].
High concentration of Cl− in the tissue, particular in the cytosol or chloroplast, are thought to
limit the growth of a wide range of glycophytic plants [46,70-74]. Reasons for this are not
fully resolved. It can be differentiated between Cl−-sensitive crops such as bird's-foot trefoil
[75] (Lotus corniculatus,), Citrus rootstocks [76], or grapevine (Vitis vinifera, [74]), that show
toxicity symptoms in the shoots at concentrations ranging from 4-7 mg g dw-1, whereas less10
sensitive crops show symptoms only at concentrations between 15-33 mg g dw-1 [3]. Sugar
beet (Beta vulgaris) has halophytic ancestors (halophyte; plant that survives to reproduce
when salt concentration is around 200 mM NaCl or more; [77,78]) and, here, Cl− is only toxic
at concentrations higher than 50 mg g dw-1. Of note, halophytes such as grey mangrove
(Avicennia marina) require much higher Cl− levels for photosynthetic light reaction [79].
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Thus, halophytes accumulate more Cl− than glycophytes when cultivated with less than 1 mM
Cl− [80].
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A descriptive modelling approach was used to calculate that grain yield will be reduced by
10% when the subsoil Cl− concentration reaches 490 mg kg-1 (calculated for chickpea
production; Cicer arietinum), 662 mg kg- 1 (durum wheat; Triticum durum), 854 mg kg-1
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(bread wheat, Triticum aestivum), 980 mg kg-1 (canola; Brassica spp.) or 1012 mg kg-1
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(barley, Hordeum vulgare) [81]. These data are based on a vertisol, a soil type that is
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dominated by the phyllosilicate clay montmorillonite [82]. Thresholds are anticipated to be
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lower in loamy soils that adsorbs less Cl−. Physiological reasons of the underlying
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dysfunctions have not been very well resolved and toxicity symptoms are deceptive because
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visual appearance can be similar under conditions of other nutrient deficiencies [3].
Inhibition of photosynthetic capacity
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Photosynthetic capacity of glycophytes is affected by the excessive accumulation of Cl− in the
chloroplasts [73]. In Cl−-stressed field bean (Vicia faba L.), leaf chlorotic symptoms were
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ascribed to high chloroplastic Cl− concentrations being responsible for a reduction in
chlorophyll content [83]. In accordance, it was reported about a chlorophyll degradation in
Cl−-stressed field bean that was associated with a concomitant reduction in photosynthetic
capacity, quantum yield and growth [84]. This was discussed to be the result of a Cl−-induced
disturbance of the structural organization of the photosystem II that is likely to occur under
Cl−-salinity since the chloroplast envelope has a high permeability for Cl− [85]. Cl−
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concentrations ranging from 250-300 mM have been found in the stroma of the chloroplasts
in Cl−-stressed common bean (Phaseolus vulgaris, [86]). A disturbance of the photosynthesis
by too high concentrations of Cl− in the chloroplast is likely to be a reason why plants show
stunted growth. A lack in assimilates and energy equivalents (i.e. ATP and NADH+H+) might
account for a reduced anabolic activity, limiting growth of glycophytes. If this is true, Cl−-
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toxicities may also impair the quality of crops by lowering the carbohydrate content.
Carbohydrate content is a major quality attribute of our starchy crops. Besides cereals, species
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such as banana (Musa ×paradisiaca), pea (Pisum sativum), lentil (Lens culinaris) or cassava
(Manihot esculenta) belong to the carbohydrate-rich crops that are globally important for
providing an energy-rich diet to people in developing countries. What is needed are
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investigations that estimate if and how Cl−-toxicities will reduce the energy density of those
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Retardation of root and tuber growth
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3.2
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foods and feeds.
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In contrast to aspects of Cl−-toxicity in the shoot, literature bearing on mechanistic reasons for
linking Cl−-toxicity with root development is barely available. In Cl−-stressed pea (Pisum
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sativum L.), the respiration in root tips has been found to be depressed because of a shift from
the glycolysis to the pentose phosphate pathway, a shift thought to interfere with the energy
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supply [87]. In another study, Cl−-salinity has been reported to dampen the root growth of
avocado (Persea americana L) resulting in problems regarding water supply [88]. The
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mechanisms behind this root growth retardation were never studied with a focus on Cl−associated effects. The addition of 100 mM NaCl to the roots of Arabidopsis that grew in agar
media resulted in a quiescent phase in lateral roots that retarded growth for several days [89].
This growth suppression is controlled by abscisic acid signalling at the endodermis, which
serves as an important site for sensing NaCl-stress. These results are very thrilling, but the
experimental design does not allow concluding as to whether this retardation in growth was
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induced either by the sodium, by Cl−, or by the osmotic stress component of NaCl-stress.
Further work is appreciated to advance our understanding of how toxic Cl− concentrations in
the soil are mechanistically linked to physiological dysfunctions leading to root growth
reductions. Knowledge with regard to this would be significant because many of our starchy
food plants are root and tuber crops. These include besides potato and cassava (Manihot
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esculenta) also bulb and tuberous Allium and Beta vulgaris subspecies vegetables such as
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onion, garlic or beets.
The Cl−-sensitive potato
Caution is needed when Solanum tuberosum is fertilized with Cl−-containing mineral or
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organic fertilizers. Fertilization of 400 kg Cl− ha-1 via KCl decreases tuber yield, retards crop
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growth and slows down emergence [90]. However, an application of 400 kg of potassium
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would be higher than required (180-240 kg K+ ha-1 for table potato; 110-180 kg K+ ha-1 for
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starch potato). However, since the addition of 210 kg total N ha-1 year-1 via pig slurry
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amendments (finishers) carries a concomitant input of > 450 kg Cl− ha-1 year-1 [91], the abovedescribed scenario might become true. The physiological reasons for the tuber yield reduction
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are unclear. Besides the possibility of a Cl−-induced quiescent phase in roots or maybe
stolons, as speculated in section 3.2, tuber yield reduction could be the result of an impaired
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uptake of nitrate or an inhibited photosynthesis [92]. High amounts of Cl− (e.g. 6.1 g Cl− per
pot) decrease leaf chlorophyll content and result in a reduction of the photosynthesis [93]. In
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result, the total sum of carbohydrates decreases in the leaves while starch content increases.
The latter is indicative for an impaired carbohydrate partitioning. The leaves that accumulated
starch grew better compared to the tubers [93,94]. Trying to explain this divergent growth
between the shoot and the tubers, a hypothesis was expressed [94]: It was suggested that Cl−
accumulates in the vacuoles of the leaf cells, which decreases the leaf osmotic potential,
driving water inflow in shoots. Shoot turgor pressure increases, ultimately favouring turgor13
driven cell expansion and shoot growth. The growing shoot is then thought to act as a strong
sink for assimilates, having a sink strength that dominates over, or at least competes with, the
sink strength of the tubers. Assimilates such as starch are preferably delivered into the
expanding tissues of the shoot, and not to the tubers. This reduction of the carbohydrate
delivery to the tubers may delay tuber development and growth. This theory has to be tested
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C tracer experiments to elucidate carbon translocation rates and allocation
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by using in situ
patterns between shoot and tuber. For this, leaves have to be labelled with
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[C]-sugar
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molecules that are brushed on abraded zones of leaves. Partitioning of labelled sugar
molecules between donor leaves and sink organs (root, youngest immature leaves) can be
monitored. Different Cl−- and sodium-accompanying counter ions have to be used that allow
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Antagonistic anion-anion effects
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3.4
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testing for Cl−-specific effects.
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Antagonistic ion-ion uptake interactions are attributable for nutrient deficiency that are
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induced by Cl−-salinity. When the external Cl− concentrations is very high, an antagonism
between Cl− and nitrate uptake has been reported in Brassica rapa [95] and Citrus [96]. This
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phenome may be based on an inhibition of nitrate transporters, as shown for the Arabidopsis
thaliana nitrate transporter 1/peptide transporter NPF7.3. NPF7.3 is located in the root
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pericycle cells where it catalyzes xylem loading of nitrate [97]. However, when concentration
of Cl− increase in the environment and subsequently in the roots, it was observed that nitrate
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concentration increase in the roots but decrease in the shoot, while increasing amounts of Cl−
are loaded into the xylem being delivered to the shoot [98]. It is thought that NPF7.3 leaks Cl−
at too high concentrations because NPF7.3 cannot discriminate nitrate over Cl−, by this
displacing nitrate from being quantitatively taken up [10,11]. Such a competitive uptake effect
is thought to induce a lack of nitrogen in the shoot, finally hampering growth and yield [2,67]
as shown for wheat (Triticum aestivum L.; [99]), grapevine (Vitis sp.; [100]), or tomato
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(Solanum lycopersicum; [101]); with exception for Zea mays L. [102]. For the tomato
(Lycopersicon esculentum Mill), it was shown that the nitrate dose needs to be increased to
ensure an adequate N supply [103] under conditions of excess of external Cl−. This is an
interesting observation that is worth being tested as strategy to cope with the problem of
excess accumulation of Cl− in the shoot. Is a nitrate fertilization, supplied either to the soil or
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via foliar application, instrumental in decreasing toxic shoot concentrations of Cl−?
There is also increasing indication for such Cl− antagonistic effects on the uptake and
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translocation of phosphate [101,104] and sulphate [105]. A literature review reveals a dearth
of published data on this topic and it is hardly known as to whether this antagonistic effect is
either based on a specific competition for binding site at the phosphate or sulphate transport
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protein or as to whether Cl− is simply leaking through these protein pores, quantitatively
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displacing phosphate or sulphate. The latter would indicate an unspecific competition between
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the Cl− and the anions. This and other open points, as for example the molecular identification
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of the involved phosphate and sulphate transport proteins, await clarification. Work is also
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needed to clarify how this process can be better controlled to avoid macronutrient deficiency
under Cl−-salinity. This topic is relevant because nitrogen, phosphate and sulphur are
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nutrition.
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important ingredients in plant-based foods that determine the nutritional value for human
4.
Dysfunctions under Cl−-toxicity and implication for food quality and safety
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It is a little known fact that excess of Cl− in the environment interferes with the formation of
quality of plant-based foods (and feeds) (Table 1). The interplay between Cl−-toxicities and
quality-related aspects is reviewed in this chapter.
4.1
Protein biosynthesis
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Ribosomal enzymes that catalyse protein synthesis are inhibited by high concentration of Cl −.
Addition of 80 mM Cl− was inhibitory for the in vitro translation of RNA from the leaves of
sugar beet (Beta vulgaris), wheat (Triticum aestivum), barley (Hordeum vulgare) or pea
(Pisum sativum) [106]. This is one reason why plants need to avoid accumulation of Cl− in the
cytoplasm when growing under Cl−-salinity [107]. Taking into account that synthesis of
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ribosomes and proteins correlates closely with growth, it can be hypothesized that high
cytoplasmic concentrations of Cl− restricts growth and development because a myriad of
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enzymes and structural proteins may be affected in their abundance. It is worse testing as to
whether the pattern of storage proteins of wheat (Triticum aestivum) changes under Cl−salinity. Wheat grain storage proteins such as glutenins and gliadins are important for food
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quality for two reasons. First, they determine the backing quality of the dough [108] and,
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second, they are cause of the food-related celiac disease [109]. Environmental stimuli such as
A
availability of nitrogen or sulphur have pronounced effects on the storage protein pattern
M
[110,111]. What about Cl−? It was very recently shown that Cl– fertilization on soils with low
ED
Cl– content can influence the protein concentration in the grain, which, however, is cultivarspecific [112]. A second link between supply of Cl– and protein synthesis was shown after
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treating maize with a stressful dose of Cl–: Abundances of 44 leaf proteins increased [113].
This effect was mediated via a Cl−-induced increase of the pH of the apoplast [17] that
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transiently alkalinized in distant leaves upon the onset of Cl−-salinity [114]. Our
understanding of why the apoplastic pH rises upon exposure to Cl−-stress is as rudimentary
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[115], however, this Cl−-induced pH event increases abundances of more than 40 proteins.
Among them are proteins that function in protein biosynthesis, sucrose catabolism or the
phenylpropanoid pathway, which determines sensory quality of plant-based foods [116].
Experiments are anticipated to investigate the effect of Cl−-stress on backing quality and other
quality determining features.
16
4.2
Blossom-end rot
Blossom-end rot is a disorder that occurs on the fruits of tomato (Lycopersicon esculentum
Mill.), eggplant (Solanum melongena), or pepper (Capsicum annuum). First, a water-soaked
spot appears which may expand before it dries, flattens and darkens. Calcium deficiency is
associated with the establishment of this a physiological disorder [117]. It is thought that
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calcium demand in fast growing fruits exceeds its delivery, leading to a weakening of the cell
wall and disturbed membrane integrity [118,119]. Studies on pepper [120] and tomato [46]
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show that toxic concentrations of Cl− can initiated blossom-end rot. Here, a hypothesis for the
induction of blossom-end in fruits is suggested under conditions of Cl−-salinity: It is known
that Cl−, when given together with sodium, accumulates in the tissue where it weakly
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associates to the oxygen of the lipid head-groups of the lipid membrane bilayers. In result, the
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dipole moment that is normally created by the polarized water under non-saline conditions
A
switches, causing both, (i) alterations in the electrostatic potential and (ii) a thickening of the
M
membrane [121,122]. These salt-induced structural changes in the bilayer might induce
ED
problems during cell expansion, because, as a cell grows, its plasma membrane must expand
but should not thicken. Since under Cl−-salinity, blossom-end rot is almost exclusively
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observed in the expanding tissues of the fruits, it is hypothesized that structural plasma
CC
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membrane impairments contribute to the formation of this disorder.
4.3
Ethylene production
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It was reported for persimmon fruits (Dyospiros lotus L.) that Cl− stress affects the
postharvest quality via effects exerted on ethylene production. Cl− accumulation in the fruit
calyces (sepal) resulted in necrotic lesions and was correlated with increased ethylene
production in the calyx. Calyx ethylene production stimulated autocatalytic ethylene
production in fruit tissues diminishing fruit firmness by accelerating fruit maturity. As a
17
result, postharvest period is shortened due to reduced shelf life [123]. Knowledge with regard
to the regulatory molecules downstream of Cl− and upstream of ethylene is lacking.
Enhance cadmium uptake
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4.4
High Cl−-concentrations in nutrient solution were found to result in an enhanced accumulation
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of cadmium in brown mustard (Brassica juncea; [124]). Similar results were reported for soils
when chloro-complexation of cadmium increased the plant availability of cadmium [125,126].
This can be a problem for the quality of crops as shown for wheat. High inputs of Cl− increase
U
wheat grain cadmium levels above the dietary intake limits [127]. These examples shows that
Loss of quality of fruit juices and beverages in response to Cl−-toxicity
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4.5
M
A
increase fertility of soils that are rich in cadmium.
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Cl− enriched fertilizers such as KCl, manures [91] or sewage sludge should not be used to
Most grapevine varieties (Virti vinifera) are sensitive to Cl−-salinity because Cl− is loaded
PT
excessively into the root xylem and travels towards the shoot [74], where it accumulates and
causes cellular damage [128]. Apparently, the Cl− is also streaming into the berries. This is a
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little known fact. A screening of Australian grape juices revealed a mean concentration of Cl−
in the juices of 140 mg/L [129]. The content of Cl− in grape juice will reflect that of the wine
A
[130] which is a negative because Cl− confers an unwanted salty taste. A few Australian
viticultural regions contain such high soil Cl− concentrations that the mean concentration of
Cl− in the juices were, according to the Australian food law, too high for selling the wine on
the Australian market. In this case, wine makers may blend their product in order to sell it
[129]. Not only the terroir but also the grape variety influences the concentration of Cl−- in the
wine. The Syrah variety is prone to accumulate the highest amounts, giving the wine an
18
undesirable salty taste, which decreases its market appeal [131,132]. Besides salty taste, soapy
attributes were correlated and associated with increasing Cl− concentrations in Chardonnay
wines as it was found by a whole-mouth gustatory descriptive sensory evaluation conducted
by a trained panel [133].
Cl− influx into the plants and particular into the fruits is also a problem for citrus (Citrus)
IP
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cultivation. Citrus production is particular limited by Cl−-salinity because oranges, grapefruits
and lemons decrease fruit yield upon the accumulation of Cl− [134,135]. It was reported that
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irrigation with Cl−-containing water reduced branch growth and increased Cl− levels in citrus
leaves causing leaf damage [136]. Citrus also accumulates Cl− in fruit juices when irrigated
with Cl−-containing waters [137], which is an unwanted product feature (salty taste).
U
Although there is improvement in our understanding of the molecular uptake mechanisms of
N
Cl− into the vegetative tissues of the root or leaf [10,11,34,72-74,138], there is lack of
A
information about the molecular mechanisms that facilitate transfer of Cl− into the fruits of our
M
crops. Which transport proteins are involved? What controls these proteins? Information
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about this may be useful for engineering trees that are able to exclude Cl− from being loaded
5.
PT
into the fruits.
Cl− fertilization for fungal infection management
CC
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Crops may benefit from Cl− fertilization via a Cl−-induced disease repression [139].
Knowledge with regard to this is relevant as a fungal contamination of plant-based foods
A
constraints quality. The severity of take-all root rot (caused by Gaeumannomyces graminis
var. tritici) has been decreased in winter wheat in response to the Cl− fertilization. This was
discussed to be attributable to a Cl−-induced change in plant water potential as the growth of
G. graminis tritici declines with declining water potential [140]. Such a general effect on
water availability may also be the reason why foliar application of Cl−, sprayed as KCL,
inhibits the spore germination of Septori tritici and Blumeria graminis f. sp. tritici on winter
19
wheat [141]. Beside foliar disease, a positive role of Cl− in supressing soil born diseases has
also been shown for rhizoctonia disease in sugar beet [142]. More examples for the
suppression of fungal disease by Cl−-containing salts are given elsewhere [143]. Based on this
it can be assumed that a Cl− fertilization of infected plants may increases yields via the
repression of fungal colonisations rather than being the direct result of an improved nutrition
IP
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with Cl−. There is a huge gap in our understanding about the molecular mechanisms that link
Cl− fertilization with an enhanced tolerance towards fungal infections. The question raises as
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to whether a Cl− foliar application modulates genetic networks that may convey a tolerance. A
recent study demonstrated the link between supply of a stressful dose of Cl− and the
Concluding remarks
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6.
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accumulation of the plant defence-compounds glucosinolates [144].
A
Cl− is a nutrient that is indispensable for photosynthesis and relevant for other processes such
M
as osmo- and turgor-regulation. Moreover, fertilization of Cl− can (i) improve fruit quality, as
ED
shown for strawberry [145], (ii) influence protein concentration in the grains of wheat [112],
or (iii) may increases yields via the repression of fungal leaf infections [139-142].
PT
Deficiencies, however, do not occur in most agricultural production systems because traces of
Cl− in soil and rainwater are enough to fulfil requirement of nearly all major crops. In
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contrast, excess of Cl− under conditions of Cl−-salinity induces severe physiological
dysfunctions that hamper yield formation and affect quality-related attributes. For instance,
A
potato tuber development is impaired having low starch content, tomatoes suffer under Cl−induced nitrogen deficiency, grape juices and derived wines taste salty and post-harvestattributes such as shelf life of persimmon fruits is impaired by interactions between Cl−salinity and ethylene production (Figure 1). Surprisingly, the physiological and molecular
reasons behind these toxicity symptoms are only poorly understood or, with respect to roots,
almost not studied. Accumulation of excess of Cl− into the shoots might be avoided by
20
engineering crops that have either mechanism that facilitate Cl−-efflux from the roots
[146,147] or that restrict xylem loading [9,148]. More research is necessary to identify the
rate-limiting transport proteins in the diverse crop species and experiments are needed to
understand how they are controlled. Improvements in knowledge should be utilized in
breeding efforts to engineer crops that can grow in environments with high Cl−-concentrations
IP
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without showing impairments in quality or yield. When soils are only modestly contaminated
with Cl−, it might be a strategy to fertilize mineral nitrate because this anion can supress the
7.
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uptake of Cl− by means of antagonistic uptake competition.
Outstanding questions
 Based on the finding that ribosomal enzymes are inhibited by high concentration of
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Cl−, it would be important to know as to whether the pattern of the seed storage
A
proteins is also affected. Wheat storage proteins such as glutenins and gliadins
M
determine the baking quality of the dough. Changes thereof are also relevant for the
potential of wheat products to cause celiac disease.
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 Fruit juices and derived wines can be enriched in Cl−, which confers an unwanted salty
and soapy taste. The elucidation of the transporter proteins that facilitate uptake of Cl−
PT
from the vegetative tissues into the berry flesh would be helpful to engineer fruit crops
that can exclude Cl− from the pulp.
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 Blossom-end rot is a disorder that frequently coincidences with Cl−-toxicity. How are
toxic concentrations of Cl− mechanistically linked with these dark spots on the fruits?
A
Are membrane damages involved?
21
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Figure legend
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Figure 1. Cl−-salinity induces physiological dysfunctions in many crops constraining both
yield and quality formation. Potatoes produce smaller tubers with lower starch content, grape
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juices and derived wines taste salty and post-harvest-attributes such as shelf life of persimmon
fruits is impaired by interactions between Cl−-salinity and autocatalytic ethylene production.
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Figure file
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Figure 1
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I
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Table 1. Physiological dysfunctions under Cl−-toxicity and implication for food quality and yield
Crop
Symptom and implication for food quality
Reference
[46]
Medicago sativa
Avocado tree
Persea americana
Shoot growth depression
Dampened root growth impairs water supply, reduced fruit production possibly due to dehydration, leaf necrosis and premature leaf
abscission
Barley
Hordeum vulgare
Burned leaf tips, yield loss, potentially inhibitory for translation of RNA
[46,81,106]
Canola
Brassica spp
Yield loss
[81]
Chickpea
Cicer arietinum
Yield loss
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Alfalfa
[88,149,150]
[81]
−
Citrus spp.
Yield loss, reduced leaf and branch growth, leaf yellowing, leaf bronzing, burned tips, leaf abscission, accumulation of Cl in fruit juices
[46,135,137,151]
Common bean
Phaseolus vulgaris
Leaf burning and abscission
[46]
Corn
Zea may
Cotton
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Citrus
[46]
Gossypium hirsutum
Shoot growth depression
[46]
Field bean
Vicia faba
[83,84]
Grapevine
Vitis vinifera
Shoot growth depression, chlorophyll degradation, reduction in photosynthetic capacity and quantum yield
Growth reduction, lack of nitrogen in the shoot, accumulation of Cl− in berries which confers salty taste
Kiwifruit
Actinida deliciosa
Leaf scorch, leaf drop, reduction of phosphor and nitrogen leaf content
[22,152]
Mango
Mangifera indica L.
Chloride accumulates in fruits, defoliation due to chloride burn
[153,154]
Pisum sativum
Growth reduction, lack of nitrogen in the shoot, depression of mitochondrial respiration in root
[87,105,106]
Pepper
Capsicum annuum
Decreased fruit yield and fruit size, blossom-end rot results in fewer marketable fruits
[120]
Persimmon fruits
Dyospiros lotus
Necrotic lesions, ethylene production in the calyx reduces fruit firmness and shelf life
[123,155]
Potato
Solanum tuberosum
Decreased tuber yield, retarded shoot growth and emergence, decline in photosynthesis, impaired nitrogen uptake
[90,92,93]
Rose
Rosa odorata
Shoot growth reduction and detracted aesthetic appearance
[69]
Sorghum
Sorghum vulgare
Leaf burning and leaf-edge necrosis
[46]
Soybean
Glycine max
Leaf scorch and yield reduction
[103,156]
Strawberry
Fragaria ananassa
[158]
Tomato
Lycopersicon esculentum
Increased total fruit yield and fruit firmness.
Restricted growth and impaired fruit setting, lack of shoot nitrogen, increased defoliation, blossom-end rot, reduced fruit water content,
putative positive aspect on aromatic compounds in fruits.
Tobacco
Nicotiana tabacum
Light green leaves and leaf margins curled upwards, lowering of burning quality, ash shows black colour, aroma and taste aggravate.
[159]
Wheat
Triticum aestivum
Yield loss, lack of nitrogen in the shoot, potentially inhibitory for translation of RNA
[81,90,106]
Wheat
Triticum durum
Yield loss
[81]
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A
Pea
PT
Burned leaf tips and growth reduction
[74,100,131]
[1,3,46,101,157]
39
This research did not receive any specific grant from funding agencies in the public,
commercial, or not-for-profit sectors.
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Conflicts of interest: none
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