Optimization of Calcium and Magnesium Concentrations for Fertigation of Tomato with Desalinated Water

ISRAEL JOURNAL OF PLANT SCIENCES, 64 (2017) 3-4 https://doi.org/10.1080/07929978.2017.1288466

Optimization of calcium and magnesium concentrations for fertigation of tomato with desalinated water

Asher Bar-Tala, Uri Yermiyahub, Alon Ben-Galb, Amnon Schwartzc, Inna Faingoldb and Ron Seligmannc aInstitute of Soil, Water and Environmental Sciences, Agricultural Research Organization, Volcani Center, Rishon LeTsiyon, Israel; bGilat Research Center, Agricultural Research Organization, M.P. Negev, Israel; cThe Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

ABSTRACT ARTICLE HISTORY Desalinated water has become a legitimate alternative water resource for the irrigation of intensive Received 29 December 2016 Accepted 12 January 2017 crops in semiarid regions. The concentrations of calcium (Ca) and magnesium (Mg) in water (CCa and CMg, respectively) supplied from desalinated plants are much lower than the values typically KEYWORDS found in irrigation water resources in semiarid regions. blossom-end rot (BER), a physiological Calcium; magnesium; disorder at the blossom-end part of the fruit resulting in tissue disintegration and dehydration, is desalinated water; tomato; considered a Ca-related disorder and therefore the optimization of CCa has to consider not only blossom end rot total fruit production but also the occurrence of BER. There is a lack of information regarding the optimal CCa and CMg and Ca/Mg ratio in low-salinity water under Mediterranean conditions for high-quality yield of tomato fruits. The main objective of the research was to optimize CCa and CMg for the production of high tomato fruit yield with minimal occurrence of BER. A secondary objective was to determine critical levels of Ca, Mg and Ca/Mg ratio in leaves in relation to yield and the occurrence of BER. Tomato plants were grown in an inert media and fed with a wide range of CCa and CMg. Fruit yield ¡1 was shown to decrease signiﬁcantly when CCa was at or below 0.40 mmol l . In moderate CMg (1.4 mmol l¡1) treatment, BER was negatively correlated to Ca level up to and including 1.4 mmol l¡1 and was not manifested above that level under the prevailing conditions. Elevating ¡1 CMg above 0.25 mmol l enhanced BER occurrence. Concentrations of Ca and Mg in tomato organs increased with the respective mineral concentration in irrigation solution, whereas each element was reduced in organs as a function of the increased solution concentration of the other. The Ca concentration in diagnostic leaves (the diagnostic leaf is the fully developed youngest leaf) for optimal fruit yield with minimum BER was found to be 1.6%. The optimum CCa for high fruit yield with minimal BER occurrence was found to be in the range of 1.5–2.5 mmol l¡1 combined ¡1 with CMg at 0.25 mmol l .

Introduction value cash crops, such as greenhouse vegetables and flowers (Beltran et al. 2006). However, Yermiyahu et al. Desalinated water has recently become a legitimate (2007) reported that, when desalinated water was source for irrigation (Yermiyahu et al. 2007; Martinez- supplied to agriculture, magnesium (Mg) deficiency Alvarez et al. 2016). With an estimated 67% of global symptoms appeared on crops including tomatoes, water withdrawals and 87% of consumed water going basil and flowers, and that fertilization with Mg was to irrigation (Foley et al. 2011), freshwater resources necessary to alleviate the deficiency. Yermiyahu et al. may become insufficient to meet agricultural (2007) further warned that irrigation with desalinated demands. Desalination has recently become economi- water may also lead to deficiencies of other essential cally feasible and popular as a solution for irrigation elements, especially calcium (Ca) and sulfur. water, especially in dry regions where water produc- Calcium and Mg are essential macro-nutrients tion and delivery costs can be very high. While the required for plant growth (Hawkesford et al. 2012). costs of desalination may still be excessive for use by Calcium has essential roles in plants including (a) most irrigated agriculture, the use of desalinated responsibility for the structural and biochemical water has been validated at present prices with high-

CONTACT Asher Bar-Tal [email protected] This paper has been contributed in honor of Professor Uzi Kafkaﬁ. © Koninklijke Brill NV, Leiden, 2017

Downloaded from Brill.com09/27/2021 09:46:37PM via free access 81 A. BAR-TAL ET AL. stability of plant tissue and membranes, (b) regulation White 2005). Imbalanced nutrition including high lev- of influx and efflux processes in cells and tissues, els of potassium (K) (Raleigh & Chucka 1944; Gerald- together with other substances, and (c) use as a fast son 1957; Bar-Tal & Pressman 1996), Mg (Raleigh signal transmitter to alert the plant to stress and initi- & Chucka 1944; Geraldson 1957; Chiu & Bold ate defense mechanisms (Hirschi 2004; Maathuis 1976; Hao & Papadopolus 2003) and ammonium 2009). Calcium deficiency can result in transpiration (Geraldson 1957; Ganmore-Neumann & Kafkafi 1980; losses, early ripening, increased susceptibility to bac- Bar-Tal et al. 2001a) also antagonize Ca uptake (Ho & terial and fungal diseases and induce pre- and post- White 2005). Plant growth promotors like indole acetic harvest physiological disorders, thus decreasing yield acid, abscisic acid and gibberellins additionally influ- and product quality and shortening its shelf life (Bar- ence BER through their interaction with Ca partition- Tal et al. 2001b; White & Broadley 2003; Yermiyahu ing and allocation in the whole plant and the et al. 2006; Bernstein et al. 2008). An important physio- fruit (Brown & Ho 1993; de Freitas et al. 2014; Barick- logical disorder in tomato and pepper fruits that is man et al. 2014). known to be affected by Ca nutrition is blossom-end Magnesium plays an important role in plant physi- rot (BER), a physiological disorder resulting in tissue ology, mainly in photosynthesis processes as an disintegration and dehydration with visual symptoms essential component in chlorophyll structure (Hawkes- shown first at the blossom-end part of the fruit (Ho ford et al. 2012). It also plays an important role in car- et al. 1993; Ho & White 2005). The occurrence of BER is bon partitioning and alleviating photo-oxidative known to lead to loss of quality and reduced market- damage (Cakmak & Kirkby 2008; Cakmak 2013) and in able yield of tomato crops in many parts of the world, crop quality (Cakmak 2013; Gerendas & Fuhrs 2013). ranging, for example, from 5% loss in the USA to 47% Magnesium is a common element in soils mainly as a loss in Brazil (Barrett et al. 2006; Loos et al. 2008). The component of clay minerals and in dolomite minerals factors affecting the appearance of BER were in calcareous soils and together with Ca are the domi- described in several reviews (Taylor & Locascio 2004; nant exchangeable cations in the complex of clays Ho & White 2005; Hocking et al. 2016). Saure (2005, and organic matter and in soil solution (Gerendas & 2014) raised questions about Ca deficiency as the Fuhrs 2013). In most soils the exchange isotherm of cause for BER, but most of the recent publications sup- Mg with Ca exhibits preference for Ca adsorption port the hypothesis of BER induced by local Ca defi- (Seyfried et al. 1989); therefore, Mg mobility in soil is ciency in the fruit tissue (Ho & White 2005; de Freitas higher than that of Ca (Gransee & Fuhrs 2013). This et al, 2011, 2014; Mestre et al. 2012; Barickman et al. property leads, on one hand, to easier transport of Mg 2014; Hocking et al. 2016). Factors known to reduce to the roots and uptake by plants and, on the other uptake, translocation and allocation of Ca to fruits hand, to Mg depletion of soils due to leaching include high light intensity, low humidity and salinity. (Gransee & Fuhrs 2013). Despite the importance of Mg Calcium is translocated from the root to the above- for plant nutrition, it has been practically overlooked ground organs in the xylem sap, with the transpiration in agriculture. Recently, Mg has been defined by Cak- stream, driven by diffusion and root pressure. During mak and Yazici (2010) as the “forgotten element in the day, most of the Ca is translocated to transpiring crop production” and Guo et al (2016) stated that Mg organs and only a small fraction to non-transpiring deficiency in plants is an urgent problem. Magnesium organs, whereas at night, solute movement is mainly uptake by plants is affected by competition with other driven by the pressure gradient between the root sys- cations, mainly ammonium, potassium, and calcium tem and the aboveground organs (Taylor & Locasio (Gransee & Fuhrs 2013). Recent studies showed spe- 2004). High light intensity, which promotes rapid fruit cific transporters for Mg uptake in plants, leading to expansion, causes a mismatch between Ca fruit efficient uptake under low Mg concentration, inde- demand to supply (Ho et al. 1993). Low humidity shifts pendent of Ca concentration. However, when the con- the balance of water, regarded as a Ca carrier, trans- centration of Mg in the solution is high, its uptake port to the leaves instead of to the fruits (Tadesse involves nonspecific pathways in competition with Ca et al. 2001; Guichard et al. 2005; Bar-Tal et al. 2006). (Gransee & Fuhrs 2013). Contrary to Ca, Mg is defined Salinity or high electrical conductivity in the feed solu- as an element having easy phloem movement in tion results in lower Ca uptake (Aktas et al. 2005;Ho& plants. Therefore, under conditions of Mg deficiency,

Downloaded from Brill.com09/27/2021 09:46:37PM via free access ISRAEL JOURNAL OF PLANT SCIENCES 82 symptoms and lower concentrations of Mg appear tomato production is estimated to be 7.5/2.1–3.3 mainly in the older leaves (Cakmak & Yazici 2010). molar ratio. The Mg concentration may be started at Very few publications report on optimal concentra- 2.1 mmol l¡1 and gradually increased to 3.3 mmol l¡1 tions of Ca and Mg in the irrigation of soilless green- towards the end of the season, to improve plant house-grown tomato-bearing fruits. Probably the growth and fruit firmness. In another study in the win- earliest published related research was conducted by ter similar results were obtained (Hao & Papadopolus Raleigh and Chucka (1944), who reported competition 2004). However, the lowest Ca level in these studies between Ca and Mg and antagonistic effects on BER was high above recommended Ca and Mg concentra- occurrence. Unfortunately, they used very high tion for vegetables and greenhouse-grown tomato concentrations of Ca (3–50 mmol l¡1) and Mg (Silber & Bar-Tal 2008). The climate conditions in the (2–33 mmol l¡1), much higher than the average con- Canadian fall and winter do not induce high occur- centrations in the natural water used for irrigation in rence of BER; therefore, the observed maximum level Israel (Yermiyahu et al. 2007). of BER affected fruits was 22.5% in the early season Schwartz and Bar-Yosef (1983) investigated Ca and before 1 November and only as high as 7.1% in the Mg uptake by tomato plants in a solution culture with winter study. various Mg and Ca concentrations. They fit the There is a lack of information on the response of Michaelis–Menten equation to the observed flux of Ca fruit-bearing tomato plants to concentrations of Ca uptake as a function of solution Ca concentration. The and Mg and their ratio in high-quality water under equation include two parameters; Fmax is the maximal Mediterranean climate conditions or the effect of

ﬂux (quantity/(root unit £ time)) and Km is the con- these on the occurrence of BER-affected fruits. The centration at which the ﬂux is half of Fmax. They found hypothesis of this research is that fertilization with Ca –1 that enhanced Ca (2.5 vs. 1 meq l ) decreased Fmax and Mg is required in intensive soilless culture-grown and KM of Mg. This effect was attributed to stimulation crops irrigated with desalinated water. Calcium and by Ca of selective ion uptake (related to KM) and a magnesium cannot be simply independently competitive effect on carrier sites which reduced Fmax. regarded; their interactions with one another and Increased Mg values had no appreciable effect on with other nutrients make changes in their concentra-

Fmax of Ca but they enhanced KM. Root and canopy tions and ratio particularly important for plant growth, growth rates were appreciably retarded at solution fruit yield and the occurrence of BER. Mg and Ca concentrations of 0.05 and 0.10 meq l–1, The main objective of the research was to optimize respectively, relative to those at higher Mg and Ca Ca and Mg concentrations in the irrigation water for concentrations. At the initial appearance of deficiency production of high yield with minimal occurrence of symptoms, Mg and Ca concentrations in the shoots BER and to characterize the interactive effects of Ca were 0.13% and 0.11%, respectively. Unfortunately, and Mg on tomato plant growth and fruit yield. A sec- Schwartz and Bar-Yosef (1983) terminated their exper- ondary objective was to determine critical levels of iment before fruit-bearing, therefore providing no Ca, Mg and Ca/Mg ratio in leaves in relation to yield information on the combined effects of Ca and Mg on and the occurrence of BER. fruit yield, BER occurrence or on mature plants. Hao and Papadopolus (2003) reported that plants Materials and methods grown at 0.8 mmol l–1 Mg started to show leaf chloro- Experiment I sis on both the middle and bottom leaves 8 weeks after planting. Leaves with moderate chlorosis lost A field experiment was set up in a large, semicommer- about 50% of their photosynthetic capacity. Fruit yield cial net house situated in the Ramat Negev research in the late growth stage decreased at 0.8 mmol station in the south of Israel (30590N, 34430E). l–1 Mg. BER incidence increased linearly with increas- Tomato plants (Solanum lycopersicum L., Var. Ikram; ing Mg concentration from 0.8 to 4.6 mmol l–1 in the Zeraim Gedera, Israel) were received as seedlings early growth stage at low Ca (3.75 mmol l¡1), but BER (Hishtil Nurseries, Israel) and were transplanted on 21 incidence at high Ca (7.5 mmol l¡1) was not affected Feb 2006 into polystyrene containers (100 l £ 50 W £ by Mg concentration. Therefore, for a fall greenhouse 20 H cm; Polybid, Israel), filled with Perlite (Perlite #2; tomato crop, the optimum Ca/Mg concentration for Agrekal Habonim Ind., Israel). Each plot included three

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Table 1. Experiment I treatments with respective Ca and Mg con- Table 2. Experiment II treatments with respective Ca and Mg centrations in the irrigating solutions. concentrations in the irrigating solutions. Concentration (mmol l¡1) Molar ratio Concentration (mmol l¡1) Molar ratio Treatment Ca Mg2C Ca/Mg Treatment Ca Mg2C Ca/Mg 1 0.2 1.4 0.14 1 0.50 0.25 2.0 2 0.4 1.4 0.29 2 1.00 0.25 4.0 3 1.4 1.4 1.00 3 2.50 0.25 10.0 4 2.6 1.4 1.86 4 5.00 0.25 20.0 5 5.4 1.4 3.86 5 0.50 2.50 0.2 6 1.4 0.4 3.50 6 1.00 2.50 0.4 7 1.4 0.7 2.00 7 2.50 2.50 1.0 8 1.4 2.8 0.50 8 5.00 2.50 2.0

containers and each container was populated with within the container, the irrigation solution dose was ﬁve plants in two rows with each row lined with a drip adjusted to allow an excess of up to 40% of the water line (Netaﬁm, Israel). The distance between the cen- consumed by evapotranspiration. ters of two adjutant plots was 2.0 m.

Five treatments of Ca (Cca) under the same Mg con- Experiment II centration (C ) and four treatments of C with fixed Mg Mg A second experiment following the same methodol- C (Table 1) were introduced via lines with integral ca ogy as the first experiment. Four treatments of C drippers of 1.6 l h–1, 20 cm between drippers, one line ca under two treatments of C in a complete factorial for each row, two lines for each container. The lines of Mg design (Table 2) experiment was carried out starting each treatment were fed from a separate 5000-l tank with transplanting on 10 Sep 2006 and the experi- containing complete solution. Solutions were pre- ment lasted until 12 April 2007. pared by filling the tanks with desalinized water from a small-scale, on-site reverse osmosis plant (Argad, Measurements Israel) and later adding concentrated fertilizer solutions (Fertilizers & Chemicals Ltd, Israel) and salts from For irrigation management five containers of selected various suppliers to fulfill treatment specifications. All treatments were situated on weighing platforms fertilizers were added one by one into the solution (Model 1041, 100 kg max., C3 resolution; Vishay, tank, where the solution was mixed by a pump that Israel). As plant weight was supported by above-can- circulated the water from the bottom to the top of the opy wires, changes in weight represented storage of tank. The basic fertigation solution delivered the fol- water in the containers and served to quantify water lowing elemental concentrations: 6.43 mmol l¡1 N, of uptake by the plant. The weight measurements were which NH4-N was between 10% and 20% of the total recorded continuously by a data-logger (Model 21X; ¡1 N and the rest was NO3-N, 0.56 mmol l P, 5.12 mmol Campbell Scientific, UT, USA). The data were collected l¡1 K, 0.81 mmol l¡1 S, 1.4 mmol l¡1 Mg, 17.9 mmol l¡1 remotely every week via a cellular modem (Model Fe, 9.1 mmol l¡1 Mn, 3.8 mmol l¡1 Zn, 0.57 mmol l¡1 TC35i; Siemens, Germany) and analyzed using Excel Cu, 0.21 mmol l¡1 Mo and 27.7 mmol l¡1 B. Complete software (Microsoft Corporation, WA, USA). Momen- solution pH was adjusted between 5.5 and 6.0 using tary combined container evaporation and whole-plant either phosphoric acid or potassium hydroxide, water uptake was calculated by a numerical derivative depending on real-time on-site need (details of measured container weight. Each week, irrigation following). frequency and amount per treatment were adjusted Treatments were distributed according to a statisti- following evaporation and uptake trends. Water drain- cal design of randomized blocks and were repeated ing from the containers was also collected weekly and six times (blocks). Irrigation started on day of trans- analyzed for electrical conductivity (EC) and pH and planting and was applied 4–6 times daily depending the trend of the latter was used to readjust the grow- on actual water consumption (details following). Ferti- ing medium pH by changing the NO3-N to NH4-N ratio gation was initiated three weeks later and lasted in the feed solution, raising or lowering it when drain throughout the season. To avoid salt accumulation pH decreased or increased, respectively.

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Vegetative and productive performance was mea- Statistical analysis sured throughout the seasons. Sampling of whole Statistical analysis was done with JMP12 Software plants was conducted in experiment I on two dates (SAS Institute Inc., NC, USA). Following the random- (42 and 109 days after transplanting (DAT)) and in ized complete block design, one-way analysis of vari- experiment II on 110 DAT with one plant per plot sam- ance was carried out. The measured values of plant pled. At each sampling date leaves were separated parts weight, their nutrient concentrations and the from the main stem and then split into three age various yield parameters were analyzed by treatment groups according to location along the main stem. In and block with means comparison done for all pairs experiment II, diagnostic leaves were sampled 119 using the Tukey–Kramer HSD test. Differences with a DAT, where the diagnostic leaf is the fully developed probability larger than 95% were deemed significant. youngest leaf. All plant parts were weighed immedi- ately for fresh matter, washed with distilled water, dried in a ventilated oven at 60 C, weighed again for Results dry matter, and stored pending chemical analysis. Experiment I Yield measurements took place throughout the season with ripe fruits that had reached 80% red color Plant vegetative growth selectively harvested weekly, weighed, their number Responses to Cca were clearly pronounced during the fi recorded and their quality evaluated by commercial rst growing season, when treatments included standards with specific attention given to BER symp- very low Ca concentrations. At the lowest Cca of ¡1 toms. Mineral concentrations of Ca and Mg in the dif- 0.20 mmol l in the irrigation water, in comparison to ferent plant parts was analyzed in the sampled plants other higher Ca treatments, plants were stunted, had and in red ripe fruits. The dry tissue (DW) of plant short nodes and their leaves were small, dark, stiff and organs was ground to pass a 20-mesh sieve, and 100- fragile to touch. Dry weights of the stem and leaves harvested on two sampling dates, 42 and 109 DAT, mg samples were wet digested with HClO4-HNO3 and analyzed for Ca and Mg in an atomic absorption spec- are shown in Figure 1. On the early sampling date no fi trophotometer (model AAnalyst 800, Perkin Elmer, signi cant effect of Ca concentration on stem and Waltham, MA, USA). leaves was obtained, but on the later date, stem and

Figure 1. Dry weight of tomato plants leaves and stem as a function of Ca or Mg in the irrigation solution at 42 (left) and 109 (right) days after transplanting, experiment I. Different letters above symbols indicate signiﬁcant differences between irrigating treatments at P < 0.05.

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¡1 leaves dry weights increased three times as Cca 5.4 mmol l had no signiﬁcant effect. Magnesium con- increased from 0.2 to 0.4 mmol l¡1 and a slight centration had no signiﬁcant effect on the total number decrease was obtained with further increase of Ca of fruits and fruit weight; however, increasing CMg con- concentration above 0.4 mmol l¡1. It should be noted centration from 0.7 to 2.8 mmol l¡1 caused an increase that stem weight was the highest with plants growing in the fraction of BER-affected fruits from 54% to 67% at 0.4 mmol l¡1 Ca and declined thereafter. On the (number basis) or from 42% to 49% (weight basis). other hand, leaves showed approximately the same Calcium concentration in leaves and fruits increased weight across the range (excluding, as said, the lowest with Cca (Figures 3 and 4). Fruit Ca concentration was

Ca treatment). No signiﬁcant effect of CMg on the dry much lower than that in the leaves, while Ca in the weights of leaves and stem in the studied range of 0.4 leaves followed their age, being highest in the lower to 2.8 mmol l¡1 was obtained. “old” leaves and lowest in the upper young ones. The initial increase in Ca concentration in plant organs with Tomato yield and quality increasing Cca was steep and it approached maximum ¡1 Both yield and quality responded to Ca treatment value at Cca of 2.6 mmol l (Figures 3 and 4). ¡1 Magnesium concentration in the leaves and fruits (Figure 2). For Cca at and below 0.4 mmol l , the total number of fruits and their weights were less than 10% increased with CMg (Figures 3 and 4). Like Ca, Mg con- of the other treatments. Note that the low fruit yield at centrations in the leaves, followed their age being ¡1 highest in the lower “old” leaves and lowest in the Cca 0.4 mmol l was in contrast to the maximum stem and leaf biomass at this concentration. The high- upper young ones. The initial increase in Mg concen- est number and weight of fruits manifesting BER symp- tration in plant organs with increasing CMg was steep ¡1 toms were found for the 1.4 mmol l Ca treatment. and it approached maximum value at CMg of ¡1 However, as total fruit number was very low at 0.2 and 1.4 mmol l (Figures 3 and 4). 0.4 mmol l¡1 Ca, it can be seen that the fraction of BER Magnesium concentration in the leaves and fruits fruits decreased from 100% to 38% (number basis) or decreased with increase in CCa (Figures 3 and 4). The effect of C on Mg concentration was stronger in the from 100% to 19% (weight basis) as Cca increased from Ca 0.2 to 2.6 mmol l¡1, but a further increase to old compared to the young leaves and the slope was

Figure 2. Fruit yield and blossom-end rot (BER) affected fruits (number of fruits and fresh weight per plot, left and right, respectively) as function of solution Ca (top) and Mg (bottom) concentration in the irrigating solution, experiment I. Different letters above columns indicate signiﬁcant differences at P < 0.05. Numbers above columns are percentage of BER of total fruits.

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Figure 3. Calcium and Mg concentrations in leaves of different heights on plant (high, middle and low) as a function of their concentration in the irrigation solution. Plant sampled 109 days after transplanting, experiment I. Vertical bars are the standard deviations.

steeper for lower CCa. Calcium concentration in the between the first and second experiments is probably leaves and fruits also decreased with increase in CMg the different range of Ca concentrations. Experiment I and the effect was stronger in the old compared to included two treatments of extreme low Ca concen- the young leaves (Figures 3 and 4). However, the rela- tration, 0.2 and 0.4 mmol l¡1, whereas the lowest Ca ¡1 tive effect of CMg on leaves and fruit Ca was much concentration in experiment II was 0.5 mmol l . The smaller than the effect of CCa on leaf Mg. lowest Mg treatments in the first and second experiments were 0.4 and 0.25 mmol l¡1; both concentrations had no significant effect on tomato vegetative Experiment II biomass production. Plant vegetative growth Dry weight of plant vegetative organs did not show Fruit yield significant difference between treatments (data not The total fruit weight and number of fruits in most shown). The reason for the difference in response studied treatments were similar but the combination

Figure 4. Calcium and Mg concentrations in fruits as a function of their concentration in the irrigation solution, experiment I. Vertical bars are the standard deviations.

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Figure 5. Total fruit yield by weight (A), blossom-end rot (BER)-affected fruits by weight (B), total fruit yield by number (C), BER-affected fruits by number (D), the percentage of BER affected fruits by weight (E), and the percentage of BER-affected fruits by number (F) in the varying Ca treatments within the two Mg treatments, experiment II.

¡1 of high Mg (2.5 mmol l ) with the lowest Ca treat- leaf Mg was enhanced significantly as CMg was ele- ¡1 ¡1 ment (0.5 mmol l ) yielded significantly lower weight vated from 0.25 to 2.5 mmol l . Increasing CCa led to and number of fruits (Figure 5). Both the number and a reduction in diagnostic leaf Mg with stronger impact weight of BER-affected fruits were significantly at the high CMg (Figure 6). The pattern of response of affected by CCa and CMg. Considerable number and red fruit Ca and Mg to CCa and CMg was very similar to weight of BER-affected fruits were obtained at the two that of the diagnostic leaf Ca and Mg concentrations ¡1 lowest CCa of 0.5 and 1.0 mmol l . At these CCa, when and thus a linear relationship with high correlation ¡1 CMg increased 10-fold (from 0.25 to 2.5 mmol l ), was obtained between red fruit and diagnostic leaf Ca BER-affected fruit number was much higher. and Mg, respectively (Figure 7).

Ca and Mg concentrations in plant organs Discussion The pattern of the response of Ca and Mg concentration in the leaves and fruits to CCa in experiment II Comparing Ca levels in leaves and fruits clearly were very similar to those obtained in experiment I. presents the known pattern relating Ca transport and

Nonlinear increases in diagnostic leaf Ca versus CCa allocation to the transpiration stream (Gilliham et al. were obtained (Figure 6). Lower diagnostic leaf Ca 2011). Leaves, being the ﬁnal location for Ca trans- concentrations were obtained with the 10-fold ported by transpiration, had high levels of accumu- ¡1 increase in CMg from 0.25 to 2.5 mmol l . Diagnostic lated Ca while fruits had much lower Ca

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Figure 6. Concentration of Ca (left) and Mg (right) in diagnostic leaves as a function of Ca concentration in the irrigation water under low or high Mg concentration in the irrigation water, experiment II. Vertical bars denote standard deviations and, when unnoticed, are smaller than the marker. concentration, which is not surprising, as they have Rose (Rosa hybrida) (Bar-Tal et al. 2001b) and Beach only very low rates of transpiration, are hydraulically Morning Glory (Ipomoea pes-capae) (Suarez 2010), are isolated due to reduced xylem functionality (Malone & apparently a result of insufficient Ca levels reaching Andrews 2001), and employ hydraulic barriers protect- the plant cells, presumably causing loss of membrane ing fruit embryos from water stress (Van Ieperen et al. integrity as well as cell wall weakness (Ho & White ¡1 2003). Fruits therefore are particularly sensitive to 2005; Proseus & Boyer 2006). At CCa of 0.4 mmol l potential Ca deficiency-related disorders. the final vegetative biomass was not different than

A wide range of recommended values of CCa, from under sufficient Ca level; however, yield performance ¡1 ¡1 1 to 5 mmol l , has been reported (Bar-Tal & Press- was extremely low. Increasing CCa to 1.4 mmol l and man 1996; Hao & Papadopolus 2003, 2004) for tomato above resulted in a good vegetative performance as fertigation. The use of desalinized water and an intact well as acceptable marketable fruit production. growth substrate in the current study allowed build- Results from the current investigation of the impact of ing complete and stable Ca and Mg levels and mainte- Ca and Mg on tomato plant reproductive performance nance of ratios between the elements in the irrigation were likely highly sensitive to the environmental con- solutions without risk of interference from basal conditions under which it was conducted. The hot, dry centrations. Under the conditions prevailing in the environment, even in protected structures at the ¡1 current study, CCa of 0.2 mmol l during experiment I experimental station in Israel’s Negev Highlands, favor was shown to stunt and limit vegetative growth of the presence of and distribution of the Ca-related dis- tomato plants. The symptoms observed, including order BER. The percentage of fruits manifesting BER chlorosis and leaf necrosis, similar to those reported symptoms increased dramatically with decreasing CCa. for other plants exposed to severe Ca deficiencies, i.e. BER is known to be a Ca deficiency-related disorder;

Figure 7. Correlation between diagnostic leaf Ca and red fruit Ca (left) and between diagnostic leaf Mg and red fruit Mg (right). Empty and full symbols, respectively, stand for 0.25 and 2.50 mmol l¡1 Mg concentration in the irrigation solution. Diagnostic leaves and red fruits were sampled on 119 and 185 days after transplanting, respectively, experiment II.

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¡1 however, it does not always materialize due to a com- combined with CMg at 0.25 mmol l . It should be bination of climatic conditions and growers’ practices noted that in the present study Mg deﬁciency thresh- under which BER is not manifested (Ho & White 2005; old values were not obtained and that further investi-

Bar-Tal et al. 2006). It seems that in view of the good gation with lower CMg values is required for growing practices that were well maintained through- optimizing the required Mg in desalinated water out the experiment including (a) frequent and ade- under Mediterranean climate conditions. quate irrigation, (b) well-aerated growing medium, (c) As BER is not known to be a Mg-related disorder, it low ammonium to nitrate ratio, and (d) reasonable is assumed that an indirect effect of Ca level suppres- water salinity levels, the trigger for BER appearance sion by imbalanced Mg level exists (Taylor & Locascio under low CCa was the local prevalent climatic condi- 2004; Ho & White 2005). This assumption is supported tions, which included high light intensity, high tem- in the current research by the relationships found peratures and low humidity. between the observed fraction of BER-affected fruits

In experiment II, CCa levels started at a higher level and the concentrations of Ca and Mg in diagnostic (0.5 mmol l¡1) and did not result in significant effects leaf (Figure 8). A high correlation between BER on vegetative or productive performance differences. The occurrence of BER in similar Ca treatments in experiment II was lower than in experiment I because it was planted in the fall with the main fruit production occurring under the relatively mild conditions of the winter and spring, in contrast to fruit production during the harsher late spring and summer in the first experiment. As in the previous season, BER-exhibiting fruits were collected at higher numbers at both CMg levels in the low CCa treatments. However, increasing ¡1 CMg from 0.25 to 2.50 mmol l , a relatively high level, significantly raised the number of BER fruits. It can be concluded that under climatic conditions which promote the onset of BER, and when Ca levels in the irrigation water are low and/or when high Mg levels suppress Ca uptake, related yield loss of tomato is expected. Irrigation with rainwater which is low in Ca usually occurs in countries where climatic conditions are mild. Contrarily, the use of desalinized water lacking in Ca, in many cases resulting from a shortage of other fresh water sources, will typically occur in hot and dry regions. Such situations require that attention is paid to Ca nutrition and to evading Ca-related disorders by careful fertilization and irrigation management (Yermiyahu et al. 2007) and, where possible, by manipulating meteorological conditions (Tadesse et al. 2001; Guichard et al. 2005; Bar-Tal et al. 2006). The results in the current study indicate that the required CCa and CMg are both much lower than the recommended values of 7.5 mmol Ca l¡1 and 2–3 mmol Mg l¡1 by Hao and Papodopous (2003, 2004). Under the high temperatures of the late spring and summer under Mediterranean climate conditions, Figure 8. BER occurrence as a function of the diagnostic leaf Ca the required CCa for high fruit yield with minimal BER (A) and Mg (B) (sampled 119 days after transplanting) and the ¡ occurrence is in the range of 1.5–2.5 mmol l 1 molar ratio of Ca/Mg (C) in the irrigation solution, experiment II.

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occurrence and leaf Ca independently of CMg treat- concentration and NO3:NH4 ratio on yield, fruit shape, and ment was obtained, whereas no correlation was found the incidence of blossom-end rot in relation to plant mineral – with leaf Mg. The occurrence of BER decreased sharply composition. HortScience. 36:1244 1251. Bar-Tal A, Aloni B, Arbel A, Barak M, Karni L, Oserovitz J, Hazan from 40% to 10% as diagnostic leaf Ca increased from A, Gantz S, Avidan A, Posalski I, et al. 2006. Effects of evapo- 0.9% to 1.6% and decreased moderately with further rating cooling system on the incidence of blossom-end rot increase in diagnostic leaf Ca (Figure 8a). The occur- and fruit cracking in bell pepper (Capsicum annuum L.). J rence of BER increased as leaf Mg concentration in the Hort Sci Biotech. 81:599–606. diagnostic leaves increased but different relations Bar-Tal A, Baas R, Ganmore-Neumann R, Dik A, Marissen N, Silber A, Davidov S, Hazan A, Kirshner B. Elad Y. 2001b. Rose were obtained for the low and high CMg treatments. flower production and quality as affected by Ca concentra- These results indicate that the incidence of BER is tion in the petal. Agronomie. 21:393–402. related directly to Ca status in the plant rather than Ca Bar-Tal A, Pressman E. 1996. Root restriction and K and Ca solu- concentration in the solution. Elevating CMg leads to tion concentration affect dry matter production, cation reduction of Ca concentration in leaves and fruits uptake, and blossom end rot in greenhouse tomato. J Am resulting in increased incidence of BER. This finding Soc Hort Sci. 121:649–655. Beltran JM, Koo-Oshima S, Steduto P. 2006. Introductory paper: shows that there is a combined effect of CCa and CMg desalination of saline waters. In Beltran JM, Koo-Oshima S, on BER occurrence. However, presenting the occur- editors. Water desalination for agricultural applications. FAO rence of BER as a function of the ratio CCa/CMg showed Land and Water Discussion Paper, no. 5. p. 5–11. Rome: that for similar values of the ratio, higher BER occur- FAO. Available from: http://www.fao.org/3/a-a0494e.pdf rence was obtained for higher CMg. Therefore, we Bernstein N, Luria G, Bruner M, Nishri Y, Dori I, Matan E, Ioffe M. conclude that the diagnostic leaf Ca can be used 2008. Development of “stem-topple” disorder in Ranunculus as indicator for BER occurrence, whereas the ratio asiaticus is related to localised disturbances in tissue calcium levels. J Hort Sci Biotech. 83:525–531. C /C was found useless. Ca Mg Brown MM, Ho LC. 1993. Factors affecting calcium transport and basipetal IAA movement in tomato fruit in relation to Acknowledgments blossom-end rot. J Exp Bot. 44:1111–1117. We would like to thank S. Cohen, T. Shemer, R. Golan, M. Ami- Cakmak I. 2013. Magnesium in crop production, food quality hai, M. Levy and A. Hizkiyahu from Ramat Negev R&D Israel for and human health. Plant Soil. 368:1–4. technical assistance in conducting the experiments. Cakmak I, Kirkby EA. 2008. Role of Mg in carbon partitioning and alleviating photooxidative damage. Physiol Plant. 133:692–704. Disclosure statement Cakmak I, Yazici AM. 2010. Magnesium: a forgotten element in fl No potential con ict of interest was reported by the authors. crop production. Better Crops Plant. 94:23–25. Chiu TF, Bold C. 1976. Effects of shortage of calcium and other Funding cations on 45Ca mobility, growth and nutritional disorders This research was supported by the Fund of the Chief Scientist of tomato plants (Lycopersicon esculentum). J Sci Food Agric. of the Ministry of Agriculture and Rural Development in Israel 27:969–977. [grant number 301-0527-07]. De Freitas ST, McElrone AJ, Shackel KA, Mitcham EJ. 2014. 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