Introduction

The production of fruit and vegetable crops has grown substantially in Mexico. Crops such as avocado, papaya, pepper, brassicas and berries have been produced for 10 years under a wide variety of climatic and soil conditions (^{Macías-Macías, 2010}; ^{Valencia-Sandoval, Duana, and Hernández, 2017}; ^{Fiscal, Restrepo, and Rodríguez, 2017}; ^{González-Razo et al., 2019}). The management of nutrients applied through fertigation is an important aspect to consider in maximizing yield and quality of fruits and vegetables (^{Maboko and Du Plooy, 2017}). Fertilizations are often used to increase the amount of salts in certain phenological stages with the purpose of improving some aspects of harvested products (^{Velos, Malabug, and Manuel, 2013}).

The technique of fertilization and fertigation are two of the most important techniques in crop production, mainly due to their positive impact on yield and quality of production (^{Incrocci, Massa, and Pardossi, 2017}). However, constant applications of fertilizer salts to soil have led to the contamination of surface and groundwater, as well as to the salinization of the soil itself (^{Moreira-Barradas, Abdelfattah, Matula, and Dolezal, 2015}; ^{Singh, 2020}). This corroborates the need for a better control of nutrition programs.

In many cases, the interaction between nutrients in soil solution as in plants, and nutrients balanced supply, have been shown to be more important than increasing certain elements (^{Cuquel, Motta, Tutida, and Mio, 2011}). For a better control of the nutritional contributions in crops, various methods of soil and plant tissue analysis have been implemented. Soil analysis allows the evaluation of the nutritional supply capacity for crops, and, on the other hand, its proper application leads to an improvement and a better planning of fertilization programs (^{Velos et al., 2013}; ^{Komosa, Roszyk, and Mieloch, 2017}). Soil analysis has been carried out using different monitoring techniques such as laboratory analysis, soil analysis or aqueous extract of substrates, and soil solution extractors (^{Incrocci et al., 2017}). This last technique allows a simple way of extracting the soil solution (SS) at different depths, and it is the fastest way of monitoring available ions (^{Falivene, 2008}). Likewise, by analyzing soil solution, the complex interaction between ions in the edaphic environment can be determined (^{Grattan and Grieve, 1998}).

Regarding the analysis of plant tissue, petiole cellular extract method (PCE) gives a way to determine the nutritional status of the plants. This method is carried out by collecting fresh plant material, which yields a quantitative evaluation of nutrients present in soluble inorganic forms in the plant tissue at the time of sampling (^{Llanderal et al., 2020}). To establish a nutritional diagnosis, it is necessary to make a comparison using sufficiency ranges obtained under different cultivation conditions, since it has been observed that nutritional variable values obtained from plants vary throughout the day and season of the year, among other factors (^{Salazar-García, Medina, Ibarra, and González, 2018}; ^{Menzel, 2018}; ^{Llanderal et al., 2020}).

There are several researches that propose wide sufficiency ranges through minimum and maximum values of important nutrients such as nitrate and potassium, mainly in dry foliar mass (^{Hochmuth et al., 2012}). However, there are few studies that explore the relationship between the composition of the SS and the PCE. In the present study, the results of the monitoring of the ions and nutritional variables in the SS and the PCE extract of 10 economically important crops of western Mexico are presented. The objective was to obtain ranges of mineral concentration from SS and PCE for crops, which in addition to providing basic information on this nutritional aspect can constitute an approximation to obtain sufficiency ranges based on the soil solution.

Materials and Methods

Field studies were conducted to determine the mineral concentration ranges and the interaction of ions in soil solution (SS) and petiole cellular extract (PCE) in 10 crops established in western Mexico (Table 1). The studied crops, located in agricultural fields in the states of Colima, Guanajuato and Jalisco, Mexico, were selected for their adequate agronomic management. According to the State Inventory of Forestry and Soil from the National Commission of Forestry (CONAFOR), on these lands predominate the following types of soil: Leptosol in Colima, Regosol in Jalisco and Vertisol in Guanajuato (^{CONAFOR, 2013a}, ^b, and ²⁰¹⁴). Weekly samplings were taken from May 2013 to March 2014. The collection of crop samples began after transplantation, except for avocado and blueberry, which were taken after 5 and 1 years after transplantation, respectively. Sampling for these two crops began in the bud differentiation stage in the middle of July 2013 when avocado plants were about 2 m high on average, while blueberry plants were about 0.4 m high.

Soil solution samples were extracted using (model SSAT-LT-300, Irrometer^® Co. Riverside, Calif.) lysimeters following the installation procedure described by ^{Granados et al. (2005)}. Briefly, the lysimeters were inserted immediately after irrigation at a depth of 20 cm and 20 cm away from the stem of the plants. A suction force of 70 kilopascals was applied to each lysimeter using a manual vacuum pump. Soil water samples were collected one day after establishing the vacuum. The nutritional variables and ions analyzed in the soil solution and petiole cellular extract are shown in Table 1.

The petiole cellular extract samples were obtained according to the procedure suggested by ^{Cadahía-López (2008)}. Briefly, petioles of youngest fully developed leaves number 3, 4 and 5 (numbered from the apex) of plants were collected. The samples were taken from plants close to soil solution sampling point when air temperature ranged from 20 to 30 °C. Each plant was randomly selected. The petiole cellular extract samples were obtained by placing the petioles, separated from the leaf blades, in a press to break the tissues. The resulting cellular juice was collected using a plastic syringe and then discharged into a polyethylene bag.

Sampling for nutritional variables was carried out following the procedure described by ^{Leyva-Ruelas et al. (2005)}. The ions and nutritional variables in the SS and the CPE were analyzed using a portable equipment. Electrical conductivity (EC) was measured using a (Horiba Spectrum Cardy Twin) conductivimeter, pH, using a (Hanna HI98130) potentiometer, and Ca²⁺, NO₃ ^-, K⁺, and Na⁺ minerals were analyzed with (Horiba) ion selective electrodes using different models according to B751, B743, B731, and B722 ions, respectively. PO₄ ^3-, Mg²⁺, Fe³⁺, and Zn²⁺ were analyzed using the Spectroquant^® NOVA 60A analytical test. For those elements, a colorimetric test was performed in MERCK^® cuvettes. Aiming to know the preliminary effect of ions on the vegetal tissue qualitative parameter levels, total soluble solids (TSS) readings were included using an OTAMA refractometer.

Results and Discussion

Table 2 shows the EC range of variation, pH values, and mineral concentration in SS in crops under study. The EC levels ranged from 0.4 to 2.0 dS m^-1 and the pH values were found in a range of 5.5 to 8.0. Conductivity levels registered for agronomic variables were between the recommended levels by some authors. ^{Cadahía-López (2005)} recommends a limit of 2.7 dS m^-1 for many cultures in fertigation. However, in strawberry, lettuce and pepper crops, registered values of EC were higher than those proposed by ^{Tanji (1990)} who suggests values of 0.9, 1.4, and 1.5 dS m^-1, respectively, for the above-mentioned crops or otherwise a significant reduction in growth and yield may occur. On the other hand, there has been reported that CE from SS are in response to the technique used for their extraction. CE extracted from SS using vacuum lysimeters are found at high levels as compared to those collected with techniques which do not use vacuum generation (^{Cabrera-Corral et al., 2016}). The pH values fall within the limits of availability of most essential elements in soil for various crops (^{Liu and Hanlon, 2012}). The conductivity and pH recorded suggest normal values for the studied crops.

With the purpose of estimating the level of nutritional sufficiency of registered SS, a comparison between mineral concentration ranges of the SS and the reference levels for different types of soil reported by ^{Cadahía-López (2005)} and other authors was made.

The concentration range of the NO₃ ^- anion in soil solution was recorded in a variable range from 40 to 620 mg L^-1. Most changing values were recorded in the pepper crop, 220-620 mg L^-1 during the flowering-fruiting stage and 40-70 mg L^-1 in the pre-harvest stage, which can be considered acceptable compared to the one found (396.8-1178 mg L^-1) by ^{Llanderal et al. (2020)} throughout the pepper crop cycle. ^{Rodríguez et al. (2020)} propose a nitrate sufficiency value of 5 mmol L^-1 (310 mg L^-1) for soil-established pepper crops; however, this value only applies to vegetative growth. In lettuce crops, maximum values of 225‑267 mg L^-1 were recorded. These values are higher than the optimum found in some brassicas (150 mg L^-1) (^{Altamimi et al., 2013}). The wide variability observed in nitrate concentrations in this study may be due to imprecise applications of nitrogen fertilizers or, to their excessive amounts, which frequently incur in high lixiviation. ^{Yanai et al. (1998)}, observed that in a sandy loam soil of the cambisol type, the application of (NH₄)₂SO₄ ^- allows NO₃ ^- loss reduction in the first 20 days after its addition to the soil as compared to Ca(NO₃)₂. This is due mainly because nitrification in ammonia fertilizers is slow.

In broccoli, cauliflower, and lettuce crops established between San Luis de la Paz and Celaya, Guanajuato, PO₄ ^3- was found in a range of 17-66 mg L^-1. About this, three field experiments conducted in Central Mexico from 1996 through 1998 on clay loam to clay soils near Celaya, these soils contained 11 to 20 mg L^-1 (^{Castellanos et al., 1999}). In this regard, ^{Cadahía-López (2005)} mention that for most rainfed soils, normal levels are found between 9 to 35 mg L^-1, while the highest levels of phosphorus are for highly irrigated crops on clay soil with a maximum range of 61 to 96 mg L^-1. According to these reports, the registered values can be considered acceptable.

The K⁺ levels in all cultures were recorded in a range of 3.0 to 377 mg L^-1. The lowest values were recorded in pepper, broccoli, cauliflower and lettuce crops, while the highest value was recorded in the blueberry crop. The maximum K⁺ values recorded in blueberry crop during the differentiation and flowering stages were above the optimum (150 mg L^-1) found by ^{Hart, Strik, White, and Yang (2006)} and ^{Komosa et al. (2017)}. ^{Castellanos et al. (1999)} reported values between 600 to 900 mg L^-1 in vertisol-type clay loam soils in the central region of Guanajuato, Mexico; high yields of broccoli are achieved in this place. ^{Altamimi et al. (2013)} observed optimal yields at levels of 13 to 123 mg L^-1. The low content of K in SS recorded in some crops may be due to the low retention of this element by the soil. In this regard, ^{Lao et al. (2003)}, mention that ion concentration in soil solution varies according to depth. That is, at 25 cm depth, higher concentrations of cations such as Mg²⁺ and Na⁺ are found, compared to those found at depths closer to surface.

Levels of Ca²⁺, Mg²⁺, Na⁺, Fe³⁺ and Zn²⁺ in soil solution were recorded in the ranges of 27-533, 10‑53, 15.3-500, 0.5-1.8 and 2.8-7.4 mg L^-1, respectively (Table 2). According to several authors (^{Cadahía-López, 2005}; ^{Robin et al., 2008}; ^{Smith, Fisher, and Argo, 2004}), levels of microelements such as Mg²⁺, Fe³⁺ and Zn²⁺ were within plant required range for optimal growth in soil and substrate. However, elements such as Ca²⁺, Mg²⁺, and Na⁺ were recorded at high concentrations. Maximum levels of calcium in papaya crop were twice the optimal values (240 mg L^-1) recommended by ^{Madani et al. (2013)}. Similarly, the maximum values recorded for Ca²⁺ in strawberry crop were higher than the limit value (465 mg L^-1) recommended by ^{Choi, Latigui, and Lee (2013)}. The before mentioned values show evidence of high availability of calcium in the different soils related to this study. Na⁺ was found in values higher than the maximum tolerable recommended for irrigation water for both open field and greenhouse crops (<100 mg L^‑1) (^{Breś, Kleiber y Trelka, 2010}). ^{Grattan and Grieve (1998)} mentions that high concentrations of Na⁺ in the soil solution can decrease the ionic strength of other nutrients and cause nutritional disorders in plants. In this regard, ^{Lao et al. (2003)} mention that ion concentration in soil solution varies according to depth. That is, at 25 cm depth, higher concentrations of cations such as Mg²⁺ and Na⁺ are found, compared to those found at depths closer to surface.

Table 3 shows ranges of variation for ion concentration in PCE, pH, and total soluble solids (TSS) by phenological stage. In general, a decrease in the concentration of the ions was observed according to the different stages, which agrees with that observed by ^{Hochmuth et al. (2012)} in eleven horticultural crops. The ranges of concentrations for NO₃ ^-, K⁺, and Ca²⁺ in PCE in crops under study were within the frequent value ranges found by ^{Cadahía-López (2008)}, in the PCE analysis of horticultural crops. In specific, the NO₃ ^- concentration ranges obtained are similar to sufficiency ranges reported for strawberry (200-900 mg L^-1) and pepper (500-1600 mg L^-1) crops, however, they differ for broccoli (500-1600 mg L^-1), cauliflower (290‑740 mg L^-1), lettuce (350-600 mg L^-1), and cantaloupe (700-1200 mg L^-1) crops (^{Hochmuth et al., 2012}). K⁺ concentration was found within sufficiency ranges for broccoli (2200-6500 mg L^-1), strawberry (1500-3500 mg L^-1), and cantaloupe (3000-5000 mg L^-1) crops, while in pepper crop the concentration obtained was higher (2000-3500 mg L^-1) than the sufficiency range (^{Hochmuth et al., 2012}). It is worth mentioning that the reference ranges of Ca²⁺ levels in PCE in horticultural crops are not reported in the literature. However, a comparison with respect to the total Ca²⁺ content in leaf tissue reported by ^{Hochmuth et al. (2012)}, shows that broccoli, lettuce, and cantaloupe crops have higher content Ca²⁺ compared to that of strawberry and pepper crops, which agrees with the PCE content of this study. Regarding ion concentration on different crop stages, in general, it is observed that the highest concentrations were found in the first phenological stages. In this regard, it has been reported that the concentrations of some elements such as nitrate, tend to be higher in early (vegetative) stages in fruit crops; in later stages, a pronounced decline is observed, which is even higher in fruit formation and growth stages. This decline in K⁺ levels is due to the increase in the mineral translocation from leaves towards fruits (^{Wira, Jamil, and Armizatul, 2013}).

On the other hand, high concentrations of Na⁺ in PCE were recorded mainly in broccoli, cauliflower, lettuce, and pepper crops (Table 3). It should be noticed that, in the first three cultures, these values were in correspondence to the concentration of this element in SS, however, this was not the case for pepper crop (Table 2). In this regard, it has been documented that, regardless of Na⁺ supply, there are several crops that translocate low concentrations of this non-essential element to reproductive or storage structures, such as seeds, fruits, or storage roots, or other consumable portions of many staple crops. In contrast, vegetative structures, such as leaves and petioles subject to greater transpiration and greater xylem flux, tend to accumulate Na⁺ at reasonably high levels without adversely affecting fruit productivity or quality. This occurs at the expense of a low concentration of K⁺ in the soil solution. This has been observed mainly in vegetative stage of growing vegetables (^{Subbarao, Ito, Berry, and Wheeler, 2003}), such as lettuce and some brassicas.

Table 4 shows correlations between the SS ions and PCE variables. In general, it can be observed that EC showed positive correlations with most of the ions recorded, but particularly with anion NO₃ ^-. The pH showed positive correlations with the Ca²⁺ and NO₃ ^- ions, however, it showed negative correlations with K⁺, Na⁺ and PO₄ ^3- in several crops, which suggests the impact of pH on the bioavailability of these ions. The decrease of pH in soil solution, associated with a higher concentration of P, has been observed by ^{Choi et al. (2013)}, who attribute this acidification to the reaction of H₂PO₄ anion with Ca²⁺, delivering calcium monophosphate with the consequent release of H⁺ ions. The correlation between pH and K⁺ may be a function of N present in solution. ^{Gratieri, Cecílio, Barbosa, and Pavani (2013)} observed that, by increasing the concentration of K⁺ with respect to N, this led to an increase in the pH of the fertigation solution. The lowest pH value (4.7) resulted from fertigation with a solution containing 20 and 6 mmol L^-1 of N and K⁺, respectively, while the highest pH (5.7) resulted from 12.6 and 10 mmol L^-1 of N and K⁺ concentrations, respectively.

Highly significant positive correlations were also recorded between NO₃ ^- and K⁺ ions, and NO₃ ^- and Ca²⁺ in SS, mainly in broccoli, cauliflower, blueberry, raspberry, and lettuce crops. Likewise, highly significant positive correlations between NO₃ ^- and Zn²⁺ were observed. These results allow us to verify important interactions of NO₃ ^- with several of the cations present in the soil solution. The foregoing suggests that the NO₃ ^- anion has a determining effect on the concentration of cations in the soil solution, primarily attributable to the ion exchange and electrochemical equilibrium processes that NO₃ ^- undergoes as it is weakly adsorbed at the exchange sites of soil (^{Yanai et al., 1998}), but also due to its anionic dominance in the nutrient medium (^{Yanai et al., 1996}).

The concentration of NO₃ ^- in the PCE with respect to the concentration in the SS showed positive correlations in the broccoli and cauliflower crops. This suggests that an increase in soil solution concentrations corresponds to higher assimilation by plants. However, statistically significant negative correlations were found in raspberry, cantaloupe, and pepper crops, suggesting that higher application rates do not reflect higher assimilations. About this, it has been found that the concentration of nutrients in the PCE is a function of the level of demand of ions for some physiological processes, such as nutrient uptake, bioassimilation, and storage (^{Llanderal et al., 2020}), while decrease in ions in soil solution, generally is due to leaching towards lower depths, or to high assimilation by plants in certain phenological stages (^{Komosa et al., 2017}). The foregoing supposes the occurrence of a negative correlation when high mineral applications are combined with periods of low plant demand. There is evidence that some plant species, mainly forest species, show a blockage in nitrate uptake when its concentration is significantly high in the presence of ammonium; the blockage is attributed to the inhibitory effects of ammonia (^{Gessler et al., 1998}). The exact explanation for such a response in horticultural species is still an area of opportunity.

In contrast, significant positive correlations were recorded between the concentration of K⁺ in the SS with respect to K⁺ in the PCE in crops such as avocado, blueberry, papaya, and pepper, while highly significant positive correlations between levels of K⁺ in the SS and TSS in the PCE were registered in blueberry, pepper, papaya, strawberry and raspberry crops. In some crops, this above shows a high K⁺ uptake response by increasing the soil concentration of the element. However, crops such as broccoli, cauliflower and lettuce did not show higher assimilation even when SS increased (Table 2). ^{Voogt (2002)} mentions that is important distinguish between the composition of the nutrient solution to be supplied to a crop and the composition of the root environment. Like in hydroponics, it is the solution in the growing media, or in soil the soil solution. This author indicates that the nutrient solution composition must reflect the uptake ratios of individual elements by the crop and as the demand between species differs. In this regard, it has been documented that when a nutrient solution is applied continuously, plants can take up the ions in very low concentrations, likewise, it has been reported that, under these same conditions, high proportions of the nutrients are not used by plants or their assimilation does not impact their productivity (^{Trejo-Téllez and Gómez-Merino, 2012}). On the other hand, a negative correlation was registered between the pH of SS and the concentration of K⁺ in PCE in the blueberry crop, while negative correlations between TSS and pH in SS were observed in avocado, blueberry, raspberry, and pepper crops (Table 4). The negative effect of soil acidity on foliar K⁺ levels has been documented in blueberry crops in different types of soil (^{Hart et al., 2006}). Positive impact of potassium fertilization on the yield and quality of some crops, like berries, has been reported (^{Hart et al., 2006}). K⁺ is attributed a fundamental role in the discharge of sucrose from phloem in vine crops (Vitis vinifera L.) (^{Rogiers et al., 2017}). In papaya fruits sprayed with K⁺ from 3% on, TSS levels were significantly increased and the severity of fruit damage caused by Fusarium moniliforme was reduced (^{Rathnayake, Sarananda, and Abesekara, 2010}). The effect of K⁺ on pH of tomato, blueberry and raspberry fruits is also reported (^{Fontes, Sampaio, and Finger, 2000}). The previous results show the importance of considering pH levels as they affect the K concentration levels in soil, and these in turn, TSS concentration.

In Table 4, a statistically significant positive correlation is found between the concentration of Ca²⁺ present in SS and its content in PCE for all crops. The highest statistical significance was registered in lettuce, raspberry, strawberry, papaya, and cantaloupe crops, while in broccoli, blueberry and pepper crops no significant difference was observed. This suggests an important correspondence between levels of Ca²⁺ applied to the soil with assimilation levels in several crops under study. In this regard, ^{Dayod, Tyerman, Leigh, and Gilliham (2010)} mention that, regardless of the available amount of Ca in the soil, the movement of Calcium within plants is subject to other factors, including transpiration, which is variable among plant species and is a function of weather. This would explain the low positive correlation registered in some crops.

Conclusions

The previous results constitute a first approximation to sufficiency values for NO₃ ^-, PO₄ ^3-, K⁺, Ca²⁺, Mg²⁺, Fe³⁺ and Zn²⁺ ions in soil solution (SS) and petiole cellular extract (PCE) for crops studied in the summer-winter in western Mexico. The foregoing is clear from the fact that, in general, the concentration ranges of the ions in the SS and PCE were within acceptable ranges. Na⁺ levels were found at relatively high levels for some crops; however, no significant interactions were observed with the remaining elements that make up SS or PCE. The correlations between ions in SS suggest important interactions of NO₃ ^- anions with cations such as Ca²⁺, K⁺ and Zn²⁺ in the SS, while correlations between ions that make up the SS and PCE content, show negative correlations of NO₃ ^- anions in some crops, but positive in the remaining ions. It is worth noticing the positive correlation between K⁺ of SS with the levels of TSS in PCE in some crops.