Halophytes have different ecophysiological and fungal root colonization traits in two saline soil conditions

doi:10.21203/rs.3.rs-6823575/v1

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Halophytes have different ecophysiological and fungal root colonization traits in two saline soil conditions

https://doi.org/10.21203/rs.3.rs-6823575/v1

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published 12 Nov, 2025

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Halophytes are considered a model for understanding plant salt-stress tolerance mechanisms because of their high interspecific biodiversity. However, little evidence shows how two cosmopolitan fungal root endorhizal fungi, arbuscular mycorrhizal fungi (AMF) and dark septate endophytes (DSE), influence these plants under salinity soil conditions. Hence, the ecophysiological response of six halophytes under two natural field salinity conditions and their relation with AMF and DSE were studied to increase the knowledge on their differences in plant salinity tolerance. The study was performed in the Colegio de Postgraduados research area in the former Lake Texcoco, Mexico. Under two salinity field conditions, ecophysiological responses regarding soil, foliar, root variables, and fungal root colonization were evaluated in six halophytes. This is the first report of simultaneous root colonization by these endorhizal fungi. Halophytes displayed different ecophysiological responses, and there was a plant-fungi relationship. S. torreyana was directly associated with colonization by DSE, foliar relative water content, and leaf succulence index. D. spicata and C. dactylon were linked to AMF colonization, proline concentration, and photosynthetic pigments. E. obtusiflora and B. salicifolia plants related to total root-glomalin related proteins (TR-GRP). Total-glomalin related soil proteins (T-GRSP) were lower with higher soil EC, but TR-GRP behaved contrarily. This study suggests, for the first time, the participation of TR-GRP in saline soils. Both types of GRP were related to soil calcium concentration and appear to be implicated in soil structure and stability, which suggests future research to increase evidence of the role of AMF in halophytes in saline soils.

arbuscular mycorrhizal fungi

dark septate endophytic fungi

glomalin

Plants capable of completing their life cycle in environments with high salt concentrations are known as halophytes and represent less than 2% of vascular plants (Flowers and Colmer 2008; Kumari et al. 2015). Halophytes have been mentioned as a new model of plant species for salt tolerance strategies, candidates for phytoremediation of saline soils (Mann et al. 2023; Sarath et al. 2021), and contributing to global food security and sovereignty (Karakas et al. 2020).

Halophytes use several biochemical and physiological mechanisms to adapt to soil salinity (Shabala et al. 2013; Shi 2013). For example: synthesis of compatible and osmoprotective solutes (Sánchez et al. 2008), control of radical absorption of ions (especially K) by roots and their transfer to leaves, accumulation or selective removal of ions, such as Na⁺ (Mahajan and Tuteja 2005), ions compartmentalization at the cellular level (Pang et al. 2010; Shabala and Mackay 2011), and efficiency in photosynthetic activity (Uzilday et al. 2015). However, little is known about fungal root endophytes naturally colonizing halophytes in field conditions and their influence on the ecophysiological response in natural saline soils.

The present research includes the importance of natural symbiotic associations with endophytic fungi. An eco-physiological approach suggested that the microbial community associated with halophytes may also be a critical factor in adaptation to saline soils (Yuan et al. 2016). For example, habitat-conditioned symbiosis refers to the adaptation of halophytes to saline conditions, establishing symbiotic associations with microorganisms such as arbuscular mycorrhizal fungi (AMF) and dark septate endophytic fungi (DSE). This fungal endophytic microbiome contributes to the complex ecological processes for halophyte adaptation to saline environments.

Parniske (2008) referred to AMF as fungi establishing “arbuscular mycorrhiza: the mother of plant root endosymbiosis”. These fungi, belonging to the Glomeromycota phylum, colonize roots up to 90% of plant species, and have several ecological/nutrient/adaptation benefits. DSE belong to a diverse group of Ascomycetes. DSE also colonize roots and facilitate plant growth and fitness; however, they need further clarification for their ecological functions (Hou et al. 2020). Research related to AMF has received much attention, and DSE lesser. Some studies indicate that DSE colonization might predominate over AMF in hostile environments (Hou et al. 2020; Huusko et al. 2017).

A better understanding of the ecophysiological responses of several halophytes influenced by salinity conditions may help to understand how soil-plant-endophyte fungal interactions improve soil management in sensitive salinity plants (glycophytes) and sustain plant productivity under salinity conditions. The hypothesis is that halophytes have different ecophysiological responses interconnected to the type of root fungal colonization. The objective of this field study was to identify the ecophysiological response of six common halophytes: Distichlis spicata, Suaeda torreyana, Eragrostis obtusiflora, Cynodon dactylon, Kochia scoparia, and Baccharis salicifolia under two salinity conditions and involving their fungal colonization by two key stone beneficial root endophytes, such as AMF and DSE.

Systematic analysis of soil salinity and its spatial distribution

The sampling site is located at the Colegio de Postgraduados in the east of the State of Mexico with the geographic coordinates 19.27° N, 98.54° W, and an altitude of approximately 2,236 masl (Fig. S1). This area is located in the former Lake Texcoco and characterized by natural salinity caused by weathering in the high regions of the basin (Valenzuela-Encinas et al. 2008). Systematic sampling was performed in February 2021. Thirty-eight rhizospheric soil samples were collected, dried in the shade, and sieved through a 2-mm stainless steel mesh. A saturated extract was obtained from the samples, in which the electrical conductivity (EC) was measured using a conductivity bridge (NOM-021-RECNAT-2000).

A spatial distribution map of the sampling site was generated according to the classification of saline soils proposed by the US Salinity Laboratory (Richards 1954). For this purpose, the EC data obtained were processed in the ArcGis v. 9.3 program, and the inverse distance weighted interpolator (IDW) method was applied. Therefore three areas with different salinity were identified (Fig. S1): 1) strongly saline soil (Zone 1; 8–16 dS m^-1), 2) moderately saline soil (Zone 2; 4–8 dS m^-1), and 3) slightly saline soil (green zone; 2–4 dS m^-1). Only soils and plants from Zones 1 and 2 were further studied due to their relevance for salinity conditions.

Selection, sampling, and identification of halophytes

Halophyte species were sampled during the dry season (February) to prevent rain from washing away salts and promote the germination, growth, and development of weed species less tolerant to salinity.

Halophyte species were selected based on their greater abundance and presence in Zones 1 and 2, as explained before, with high and moderate soil salinity (Table S1): Distichlis spicata, Cynodon dactylon, Eragrostis obtusiflora, Suaeda torreyana, Kochia scoparia, and Baccharis salicifolia. Solanum fructu-tecto was only identified in Zone 1. For all ecophysiological, soil, and fungal analysis, each halophyte was sampled for octupled (n = 8).

Rhizospheric chemical soil and foliar analyses

In rhizospheric soil (soil still root-adhered after a gentle hand-shaking), the chemical parameters analyzed in the saturation paste extract were electrical conductivity (EC) and concentration of soluble cations (Ca, Mg, K, and Na). EC was determined by conductimetry, while cations were determined as described in the Mexican standard NOM-021-RECNAT-2000. Na and K were quantified by flamometry, while Ca and Mg were analyzed by atomic absorption spectroscopy (Perkin Elmer 31000). The pH was measured with a potentiometer in the supernatant suspension of the soil:water mixture (2:1).

Foliar analysis included relative water content (RWC), leaf succulence index (LSI), and the concentration of photosynthetic pigment and proline. The RWC was estimated according to Mena-Petite et al. (1999). From each plant, 10 leaves with 8 replicates were used to determine the fresh weight (FW). Then, the leaves were placed in beakers with distilled water and refrigerated for 24 h. Excess moisture was removed with absorbent paper to determine the turgid weight (TW). Finally, dry weight (DW) was obtained by drying the leaves in an oven at 70°C until constant weight. This equation was used to calculate RWC (%) = FW – DW / TW-DW*100

The LSI was determined according to Medina et al. (2015). For this purpose, leaf area (LA) was obtained by scanning with the image analyzer IMAGEJ. The LSI was determined with this equation: LSI = (FW – DW) /LA

Five one-cm-long fresh leaf segments were randomly collected and placed in amber vials containing 5 mL of acetone (80%) to determine photosynthetic pigments. The vials were refrigerated for 12 d until the segments were decolorized. Absorbance was registered at 663.2 nm, 646.8 nm, and 470 nm to calculate the concentration of chlorophyll a, b, and total carotenoids, respectively. Pigment concentration (µg cm^− 2) was calculated according to Lichtenthaler (1987).

For proline concentration 50 mg of fresh leaf tissue from each halophyte was placed in glass tubes, and 2 mL of an ethanol-water mixture (40:60) was added, then kept at 4°C overnight, then macerated and centrifuged at 4,000 rpm for 10 min. A 100 µL aliquot of the extract was mixed with 1 mL of 1% ninhydrin solution diluted in 60% acetic acid, then vortexed and incubated in a water bath at 95°C for 20 min. After cooling, the chromogen (organic phase) was extracted with 3 mL of toluene and absorbance was read at 520 nm using a calibration curve with a proline standard solution (Rosales et al. 2012). The foliar analysis of P, Na, K, Ca, and Mg was performed on the solution obtained from the digestion of 0.5 g of leaves with a mixture of HClO₄ and H₂SO₄ (1:4) (Walinga et al. 1995).

Root fungal colonization and total glomalin concentration in soil and root

The fine roots of each halophyte were washed and cut into 1 cm segments. The segments were placed in 3% KOH for 12 d until root pigmentation was removed (Guzmán-Cornejo et al. 2023). The segments were immersed in 3% HCl for 15 min and stained for 3 d with 0.5% trypan blue dissolved in 50% glycerol. Colonization frequency (expressed as a percentage) by AMF and DSE was determined by the method described by Gonzalez-Chavez et al. (2002).

The total GRSP (T-GRSP) concentration was determined in 1 g of rhizospheric soil from each halophyte. To each sample, 8 mL of 50 mM sodium citrate (pH = 8.0) was added, shaken, and placed in an autoclave at 121°C for 1 h, then cooled and centrifuged at 5000 rpm for 15 min. The volume of the supernatant was measured and stored at 4°C. The extraction was repeated (8 mL of citrate, autoclave, and centrifugation) until the reddish-brown color in the sample disappeared. All the supernatants from each sample were stored in the same bottle, measuring the total volume at the end of the extraction process, and then kept at 4°C until measurement. Quantification was performed by using a standard curve prepared with bovine serum albumin (BSA) (Wright and Upadhayaya 1996). The same procedure was performed to analyze the concentration of total glomalin in roots (TR-GRP) using 1 g of root. Plant tissue samples were mineralized by Zasoski and Burau´s (1977) method to quantify sodium and nutrient content based on dry weight.

Statistical analyses

For all variables data normality and variance homogeneity were confirmed by Shapiro-Wilk and Bartlett’s tests, respectively, both at p ≤ 0.05. The data were analyzed with descriptive statistics, ANOVA (p ≤ 0.05), and Tukey’s test for comparison of means (p ≤ 0.05) using R statistical software version 4.0.5. Multivariate analysis (PCA = principal component analysis) was performed with the R package Factoextra version 4.0.5.

Chemical soil analysis

The rhizospheric soil pH of halophytes in both zones was alkaline, with similar values between plants and zones (Table 1). The lowest pH and EC were observed in the rhizosphere of B. salicifolia in Zone 1. The average EC of the rhizospheric soil of all Zone 1 plants significantly differed from those of Zone 2, except for B. salicifolia. The highest EC was in D. spicata (29.3 dS m^− 1) in Zone 1, while the lowest was in B. salicifolia (5.2 dS m^− 1 and 4.4 dS m^− 1 in Zone 1 and 2, respectively). D. spicata of Zone 1 also had the highest sodium adsorption ratio (SAR), while in Zone 2, it was S. torreyana. The soil SAR of all Zone 1 plants differed from that of Zone 2, except for K. scoparia.

Table 1

Chemical properties of the rhizosphere soil of halophytes
Halophyte	Zone 1			Zone 2
	pH	EC (dS m^− 1)	SAR (mmol L^− 1)	pH	EC (dS m^− 1)	SAR (mmol L^− 1)
Distichlis spicata	9.8 ± 0.28a	29.3 ± 2.58a*	60.4 ± 2.34a*	9.3 ± 0.31A	13.2 ± 2.33A	15.0 ± 1.58B
Kochia scoparia	9.6 ± 0.24a	18.5 ± 2.69b*	9.5 ± 2.67e	9.4 ± 0.28A	9.4 ± 2.58A	10.8 ± 2.06C
Eragrostis obtusiflora	9.2 ± 0.27a	22.4 ± 2.23b*	24.3 ± 2.14c*	9.6 ± 0.24A	8.5 ± 2.63B	7.6 ± 1.06CD
Cynodon dactylon	9.4 ± 0.27a	14.6 ± 2.06c*	22.7 ± 2.08c*	9.2 ± 0.22A	5.2 ± 1.85B	15.3 ± 2.12B
Suaeda torreyana	9.8 ± 0.24a	14.7 ± 2.10c*	51.2 ± 2.82b*	9.4 ± 0.26A	7.6 ± 2.13B	20.9 ± 2.35A
Baccharis salicifolia	8.7 ± 0.26b	5.2 ± 2.20d	14.1 ± 2.56d*	9.1 ± 0.20A	4.4 ± 2.02B	7.5 ± 1.02D
Solanum fructu-tecto	9.4 ± 0.23a	14.3 ± 2.38c	14.2 ± 2.53d
Means and standard deviation are shown, n = 8. Identical lowercase letters indicate no statistical difference in pH, EC, and SAR between the plants in Zone 1 (Tukey, α = 0.05). Identical capital letters present no statistical difference in pH, EC, and SAR between plants in Zone 2 (Tukey, α = 0.05). (*) Shows a significant difference in pH, EC, and SAR in the same plant when comparing Zone 1 and Zone 2 (Tukey, α = 0.05). EC = Electrical conductivity, and SAR = Sodium adsorption ratio.

In Zone 1, the soluble P soil concentration ranged from 24 to 14 mg kg^− 1, while in Zone 2 from 10 to 11 mg kg^− 1 of soil (data not shown). No differences in P soil concentration were found between zones of the same halophyte. The soil Na⁺ concentration range in Zone 1 was 124–524 mM, whereas, in Zone 2, the range was 94–447 mM (Fig. 1a). Soil Na⁺ concentration was similar between zones of the same halophyte species (Fig. 1a). The highest soil Na⁺ concentration was observed in S. torreyana. The average soil K concentration was 34.21 mM and 16.32 mM for Zones 1 and 2, respectively. In Zone 1, the highest K concentration was observed in the rhizosphere of D. spicata. In Zone 2, all plants had similar soil K concentration (Fig. 1b). The average rhizospheric Ca concentration was 3.19 mM in Zone 1 and 3.04 mM in Zone 2. In both zones, the concentration was similar between plants. When comparing the Ca concentration between zones in the same plant, only C. dactylon showed a difference (Fig. 1c). In Zone 1, the range of Mg concentration in the soil was 0.60–1.02 mM, while in Zone 2, the range was 0.28–0.59 mM. The average concentration was similar between zones, 0.80 mM in Zone 1 and 0.59 mM in Zone 2 (Fig. 1d).

Foliar physiological characteristics of halophytes

Foliar RWC values were between 46% and 92% (Fig. 2a). The average RWC of Zone 1 plants was 80%, and that of Zone 2 was 66%. The highest RWC from Zone 1 was observed in leaves of S. torreyana (92%), whereas B. salicifolia had the highest RWC (85%) in Zone 2 (Fig. 2a). D. spicata and K. scoparia had higher RWC in Zone 1 than in Zone 2. The other plants showed no statistical difference in RWC between the two zones.

The LSI of halophytes in this study was between 0.04% and 1.87%. Similar to what was observed in RWC, S. torreyana presented the highest LSI, 1.87% and 1.29% in Zones 1 and 2, respectively, while C. dactylon had the lowest LSI. No differences were observed when comparing LSIs of the same plant between zones (Fig. 2b).

In Zone 1, S. fructu-tecto had the highest leaf proline concentration, although it was similar in E. obtusiflora, D. spicata, and C. dactylon. For Zone 2, the proline concentration in leaves of D. spicata (1,312 µg g^− 1 DW) and C. dactylon (1,045 µg g^− 1 DW) was different from that in the other plants (Fig. 2c). The proline concentration was similar when comparing the same plant between zones with different EC.

The highest chlorophyll a concentration was observed in D. spicata (476 µg cm^− 2) from Zone 1. Regardless of the zone, the other plants had low chlorophyll a concentrations; B. salicifolia (47 µg cm^− 2) and K. scoparia (48 µg cm^− 2) from Zone 2 had the lowest concentration (Fig. S2a). Only D. spicata and B. salicifolia showed differences in chlorophyll a between zones.

The chlorophyll b concentrations varied from 6 to 247 µg cm^− 2, values lower than the chlorophyll a concentration. Like chlorophyll a concentration, D. spicata had the highest chlorophyll b concentration (247 µg cm^− 2) in Zone 1 (Fig. S2b). Chlorophyll b concentration only differed between zones in K. scoparia and B. salicifolia.

The concentration range of total carotenoids fluctuated between 3,909 µg cm^− 2 and 37,640 µg cm^− 2. D. spicata and C. dactylon presented the highest concentration of total carotenoids (Fig. S2c). No differences in carotenoid concentration were observed between zones.

Foliar concentration and nutrient ratios in halophytes

The foliar Na concentration in halophytes ranged from 4 to 39 g kg^− 1 (Fig. 3a). S. torreyana had the highest foliar concentration in both zones, 39 g kg^− 1 in Zone 1 and 29 g kg^− 1 in Zone 2. In contrast, the lowest Na concentration was observed in Zone 2, in C. dactylon and B. salicifolia, with 3 g kg^− 1 and 3.75 g kg^− 1, respectively. The foliar K concentration ranged from 3 to 66 g kg^− 1. In Zone 2, all plants had a similarly low K concentration, approximately 11 g kg^− 1. S. torreyana had the highest foliar concentration of K when established in Zone 1 (Fig. 3b). The foliar Ca concentration in the halophytes from Zone 1 ranged between 2 and10 g kg^− 1. B. salicifolia and Solanum fructo-tecto had the highest Ca concentration in Zone 1 (10 g kg^− 1). In Zone 2, plants had lower Ca concentrations (2–5 g kg^− 1), and no difference was observed between plants (Fig. 3c). Only K. scoparia had different K concentrations when comparing Zone 1 and Zone 2. In Zone 1, E. obtusiflora, C. dactylon, and Solanum fructu-tecto had the highest Mg concentrations, with 6.53, 6.39, and 7.19 g kg^− 1, respectively. In Zone 2, the range of foliar Mg concentration was between 1.53–7.19 g kg^− 1, and C. dactylon had the highest Mg concentration (Fig. 3d).

The foliar P concentration in the halophytes was from 6 to 12 g kg^− 1 (Fig. S3). The highest concentration was observed in B. salicifolia (12.2 g kg^− 1) and S. fructo-tecto (12.4 g kg^− 1) from Zone 1, while the lowest was in C. dactylon (6.8 g kg^− 1) also from Zone 1. All plants from Zone 2 had similar foliar P concentrations (average 10.3 g kg^− 1). Comparing zones, only K. scoparia and C. dactylon had different foliar P concentrations.

In Zone 1, only S. torreyana, D. spicata, and K. scoparia had a ratio Na/K higher than 1. In Zone 2, all halophytes had this ratio higher than 1, except C. dactylon (Fig. 4a). S. torreyana, E. obtusiflora, and B. salicifolia had a higher ratio in Zone 2 than in Zone 1. The ratio Na/Ca was in the range of 0.5 to 9.6. Only S. torreyana in both zones and K. scoparia from Zone 2 (Fig. 4b) had a high ratio Na/Ca (> 9). A difference in the ratio between zones was observed in K. scoparia. S. torreyana and K. scoparia established in both zones had a ratio higher than 5, and different from the ratio observed in the rest of the halophytes. S. torreyana had the highest Na/K and Na/Mg ratios in both zones (Fig. 4c and 4d).

Colonization frequency by AMF and DSE

All plant roots simultaneously had colonization by AMF and DSE structures. AMF formed in roots, coiled hyphae, vesicles, and arbuscules (Fig. S4). Total mycorrhizal colonization (14% − 48%) was higher in Zone 1 than in Zone 2 for all plants. D. spicata had the highest percentage of AMF colonization in both zones. S. torreyana had the lowest percentage of AMF in both zones (Fig. S5a). Colonization by arbuscules was between 6% and 16% (Fig. S5b), and by vesicles was from 2–9% (Fig. S5c). Roots of D. spicata and E. obtusiflora had the highest arbuscular colonization in Zone 1. In Zone 1, the highest colonization by vesicles was in the roots of D. spicata (8.4%), K. scoparia (8.9%), and B. salicifolia (9.8%). In Zone 2, all halophytes had similar vesicle colonization percentages.

DSE structures were observed in the roots of all halophytes as dark-colored septate hyphae and microsclerotia with intracellular growth in the root cortex (Fig. 5Sd). Average colonization by DSE in halophytes from Zone 1 was between 16–48%, and in Zone 2, 14–38%. S. torreyana had the highest percentage of DSE colonization in both zones (Fig. S5d). In D. spicata, colonization by DSE was lower than by AMF in both zones. The roots of S. torreyana, K. scoparia, and B. salicifolia had a higher percent colonization by DSE when established in Zone 1 than in Zone 2 (Fig. S5d).

Concentration of total glomalin in soil (T-GRSP) and roots (TR-GRP)

The range of T-GRSP concentration in Zone 1 was 0.08–0.12 mg g^− 1, whereas Zone 2 had 0.02–0.15 mg g^− 1 (Fig. 5a). In Zone 1, the highest T-GRSP concentration was observed in the rhizosphere of D. spicata (0.12 mg g^− 1) and S. fructo-tecto (0.13 mg g^− 1). In contrast, in Zone 2, the rhizosphere of K. scoparia had the highest concentration (0.15 mg g^− 1). A higher concentration of T-GRSP at major ECs had C. dactylon and E. obtusiflora.

The average TR-GRP concentration was higher than T-GRSP. In Zone 1, the average TR-GRP was 0.25 mg g^− 1, and in Zone 2, it was 0.18 mg g^− 1 (Fig. 5b). The C. dactylon roots had the highest TR-GRP concentration in both zones. E. obtusiflora, D. spicata, and C. dactylon had higher TR-GRP in Zone 1 than in Zone 2.

Principal component and correlation analysis

The first two components of the PCA explained 58.6% of the total accumulated variance (Fig. 6a). PC1 accumulated 39.3% of the variance and the most significant variables in the upper right quadrant were colonization by AMF, Na/K, Na/Ca, Na/Mg ratios, leaf proline concentration, chlorophyll a and b, carotenoid concentration, EC, soil Ca and K concentration, and leaf Mg concentration. The most significant variables in the lower right quadrant were colonization by DSE, the LSI and RWC, leaf K and Na concentration, and rhizospheric soil Na concentration (Fig. 6a). PC2 explained 19.3% of the variance, and the most influential variables were leaf Mg, P, and Ca concentration, rhizospheric soil P, Mg, and Ca concentration, T-GRSP, and TR-GRP (Fig. 6a).

The PCA also showed that D. spicata, C. dactylon, and S. torreyana plants from the two zones clustered in PC1, whereas K. scoparia and E. obtusiflora clustered in PC2 (Fig. 6b). B. salicifolia from the two zones were part of PC, but grouped in different quadrats. Several significant correlations were observed, these are presented in Table S2.

Chemical properties of the rhizospheric soil of halophytes

The average soil P concentration in Zone 1 was 19 mg kg^− 1 and in Zone 2 10.5 mg kg^− 1. Lower soil P concentrations were observed by Xie et al. (2022) in a saline soil with EC of 20 dS m^− 1 (2 mg kg^− 1) and Mahmood et al. (2013) in two saline soils with EC of 6.6 and 4.2 dS m^− 1 (2.9 and 2.8 mg kg^− 1, respectively). In this study, in all halophytes, the P concentration was lower than the average normal P soil concentration in non-saline soils (25 to 50 mg kg^− 1) and lower than the suboptimal soil P concentration (< 20 mg kg^− 1). According to Shenoy and Kalagudi (2005), soil salinity may cause P deficiency in plants; however, it did not occur in the halophytes studied (see below).

The soil concentration of Na ranged between 94 and 524 mM in the two zones under study. Greenway and Munns (1980) classified as true halophytes those plants optimally developed with soil Na concentrations between 100–300 mM. Therefore, D. spicata, S. torreyana, and K. scoparia behaved as true halophytes.

D. spicata had 30% and 40% higher soil K concentrations, when established in Zones 1 and 2, respectively (Fig. 1b), than the normal soil K concentration (6 mM) which is the ideal concentration to plant demand (Sardans and Peñuelas 2021). The average Ca concentration in the saline soil of the present study was 99% higher than the normal concentration (0.1 mM) or the optimal to meet plant requirements (2–3 mM) as referred Wood et al. (2005) and Jones et al. (1976), respectively. The range of soil Mg concentration was between 0.3 to 1.0 mM. These concentrations were low comparing to the average normal soil concentration of 8.5 mM reported by Karley and White (2009). However, foliar Mg deficiency did not occur in the halophytes from the present study (see further down).

Foliar ecophysiological traits in halophytes

The average RWC of plants from Zone 1 was higher than in Zone 2. RWC values may be from 60–95% in halophytes (Calone et al. 2022). However, higher values may be characteristic of some halophytes for maintaining the osmotic potential in plant cells as observed for S. torreyana with the highest value (92%).

The LSI observed in halophytes (3% − 18%) is similar to values reported for Suaeda aegyptiaca (5.3%) and 6.1% in Suaeda glauca (Yepes et al. 2018 and Zhang et al. 2020, respectively) when established under greenhouse conditions. However, lower (< 1%) values were observed in S. maritima, Jaumea carnosa and Kandelia candel (Grigore and Toma 2017). RWC and LSI correlated each other (r = 0.94) and simultaneously with soil Na concentration (0.92, 0.90), foliar Na (0.94 and 0.92) and foliar K concentrations (0.88 and 0.89), respectively, which related RWS and LSI with Na and K as protective osmolites.

Several authors, under pot experimental conditions, observed that proline concentration enhanced when EC increases (Elnaggar et al. 2020; Ghanem et al. 2021; Wiszniewska et al. 2021). In the present study, it did not occurred, proline concentration varied among halophytes, but no difference observed between zones. Proline concentration had high correlation with foliar Mg concentration (0.98). It is possible that Mg functions as cofactor during proline synthesis; however, it must be confirmed.

Flexas and Carriquí (2020) indicated that the average concentration of chlorophyll a in vascular plants varied among species from 300 to 1,500 µg cm^− 2. In the present research only D. spicata of Zone 1 had chlorophyll a concentration between these ranges. The rest of the plants had low chlorophyll a concentrations, which can be due to the low soil Mg and high soil Na concentrations, which may directly or indirectly harm photosynthetic productivity and chlorophyll synthesis (Sharavdorj et al., 2022). Chlorophyll a correlated with EC (0.78), soil K concentration (0.80), and Na/K ratio (0.82). Although Mg is a key component of chlorophyll, there was no correlation between these variables in this study.

Chlorophyll b's concentration was low in the six halophytes under study in the field compared to the concentrations observed by Rabhi et al. (2012) in Sesuvium portulacastrum and Tecticornia indica (2,740 µg cm^− 2 and 835 µg cm^− 2, respectively). There were no differences between zones, except in B. salicifolia. Chlorophyll b correlated with soil K concentration (0.82) and N/K ratio (0.87). K may be influencing chlorophyll b due to its osmoprotector role, influencing photosynthesis and cellular metabolism, but the high soil Na concentration decreases chlorophyll b production in most halophytes. D. spicata and C. dactylon had the highest carotenoid concentration, which is a distinctive feature of the Poaceae family halophytic species (Atia et al. 2019). However, the concentration of carotenoids was similar when comparing between zones.

Foliar concentration and nutrient ratio in the halophytes

Levinsh et al. (2021) found a range of foliar Na concentration from 8 to 30 g kg^− 1 in 102 halophytes; which correspond to results observed in the present research where S. torreyana had the highest foliar Na concentration (average 34 g kg^− 1). However all plants may be Na-hyperaccumulators having foliar Na concentration higher than 4 g kg^− 1 (Shahrokh et al. 2022).

In Zone 1, S. torreyana had the highest foliar concentration of K (64 g kg^− 1). Ibraheem et al. (2022) in Suaeda species, under natural saline conditions at Red Sea east coast, observed leaf K concentration between 10–80 g kg^− 1. In general, plants contain between 1 to 5 g kg^− 1 of foliar Ca concentration (Marschner 1995). In the present research, plants had Ca in this range, except B. salicifolia and S. fructu-tecto with twice this concentration when established in Zone 1. Marschner and Cakmak (1989) reported that normal foliar Mg concentration in plants is between 2–8 g kg^− 1. In the present study, all plants had concentrations within this range, except E. obtusiflora and D. spicata from Zone 2 (1.5 g Mg kg^− 1).

Foliar P concentration in all halophytes (6 to 12 g kg^− 1) was higher than the normal range (0.5 to 5 g kg^− 1) according to Wieczorek et al. (2022). Even with low soil P concentrations, all halophytes established in both zones under study had superior P foliar concentration than those of Phragmites communis, Suaeda salsa, and Aeluropus sinensis (1.2, 1.6, and 1.2 g kg^− 1, respectively) established in soil with moderate salinity (Zhao et al., 2022). As mentioned earlier, the key role of endorhizal fungi in improving plant P uptake is strongly recognized; however, only colonization by DSE correlated with foliar P concentration (r = 0.64). This is in agreement with that DSE influences uptake P in plants (Barrow and Osuna 2002; Huertas et al. 2024); however, the mechanism may differ from this in AMF. DSE may decompose organic matter and then increase P uptake. Further studies should elucidate how AMF and DSE, when colonizing simultaneously, influence P and other nutrient uptake in halophytes.

A high foliar ratio of Na/K is a common characteristic of tolerance to salinity in halophytes (Jouyban 2012). In the current study, S. torreyana had the highest ratio, especially in Zone 2, which was nearly as high as that in the halophyte Cakile maritima (3), which was irrigated with a nutrient solution containing 400 mM Na. A high ratio means that the plant can accumulate Na in leaves, particularly in vacuoles for osmotic adjustment (Houmani et al. 2023).

A high ratio Na/Ca (> 5) is an index to predict optimum uptake, transport, and foliar Ca concentration in halophytes (Genc et al. 2010), which was only observed in S. torreyana in both EC conditions analyzed and in K. scoparia in Zone 1. Low ratio (< 5) suggests a deficient Ca uptake due to high Na concentrations, which occurred in this study in E. obtusiflora, D. spicata, C. dactylon, B. salicifolia, and S. fructu-tecto. Houmani et al. (2023) observed in the halophyte C. maritima a ratio of 6.

S. torreyana and K. scoparia had a foliar ratio of Na/Mg > 5, which may predict salinity tolerance and efficient Mg uptake, translocation and foliar concentration in halophytes. The rest of halophytes had a low ratio, which means that Mg is totally or partially displaced by Na present in the soil, and this may negatively influence Mg root absorption.

Root colonization by AMF and DSE

Although the microbiome associated with halophyte roots is crucial for promoting plant resistance to abiotic stresses, such as salinity (Calvo et al. 2014), few studies have addressed it. D. spicata was the halophyte with the highest colonization by AMF, similar to 34% reported by Kim and Weber (1985) in the same plant species in the field. In contrast, S. torreyana (average 15%) had the lowest total root colonization. This plant species belongs to the Chenopodiaceae family, which is considered non-mycorrhizal (Wang and Qiu 2006), but low (< 20%) mycorrhizal colonization was also reported in other members of this family (Hildebrandt et al., 2001; Landwehr et al., 2002). In the present study, roots of all halophytes (average 15%) were colonized by arbuscules, except in S. torreyana (Fig. S5b), as also observed in Salicornia europea (Demars and Boerner 1996; Wilde et al. 2009). S. torreyana presented the lowest percentage of vesicles (2%), similar to the observation of Lugo et al. (2024) in the roots of the halophyte fern Acrostichum aureum. Mycorrhizal colonization was correlated with foliar Mg concentration (r = 0.89). This may be relevant as foliar Mg concentration is a crucial mechanism for keeping ionic homeostasis in response to saline stress in plants (Ahmed et al. 2023).

This is the first study to suggest the involvement of DSE in halophytes' physiology. In contrast to colonization by AMF, colonization by DSE was correlated with soil Na (r = 0.92), soil K concentrations (r = 0.82), foliar K (r = 0.82), and P concentrations (0.64). It may be that DSE colonization may be less influenced by plant P concentration, as occurs in AMF.

The roots of S. torreyana had the highest DSE colonization (> 30%). Sonjak et al. (2009) observed low colonization by DSE in Suaeda maritima (0.4%), Salicornia europea (0.7%) and Atriplex portulacoides (14%). Despite the evidence that DSE can colonize the roots of halophytes (Toju et al. 2018; Vandenkoornhuyse et al. 2002), the ecological importance of these associations has not been fully explored as mentioned before.

Concentration of total glomalin in soil (T-GRSP) and roots (TR-GRP)

Limited information is available on the effect of soil salinity on soil T-GRSP concentration, even knowing that its production can add carbon to saline soils and mitigate effects under a global change climate scenario (Banegas et al. 2022). In the present study, the concentration of T-GRSP was low (0.02 and 0.15 mg g^− 1). The average T-GRSP concentration was similar between zones. Banegas et al. (2022) reported that the T-GRSP concentration in saline soil was as low as 0.07 and a maximum of 1.2 mg g^− 1, while Hammer and Rilling (2011) quantified under in vitro conditions 0.9 mg g^− 1. T-GRSP correlated with soil Ca concentration (0.93), which is in agreement with Son et al. (2024), who mentioned that the adsorption of cations such as Ca to GRSP assists soil aggregation because this soil element promotes not only the stability and functionality of GRSP but also helps flocculation of clay particles. Therefore, Ca and GRSP may work together, favoring soil stability.

The concentration of TR-GRP (from 0.10 to 0.40 mg g^− 1) was 5 and 2.6 times higher than the T-GRSP range. Wu et al. (2016) observed lower values of TR-GRP from mycorrhizal orange roots (0.08 mg g^− 1) in non-saline soils and mentioned that the function of this fraction of glomalin in soil-plant systems has yet to be explored. Different correlations were observed in the present study between fungal colonization by AMF and TR-GRP (r = 0.94); TR-GRP and EC (0.84), TR-GRP and soil Ca concentration (0.96). This latter correlation is stronger than the one observed with T-GRP. These proteins are glomalin-related and complement the participation of mycorrhizal roots and the external mycelium, influencing soil structure, which may be the differential role between AMF and DSE in saline soils. This requires further experimental analysis to increase the functional understanding of AMF in saline soils.

Principal component and correlation analysis

The accumulated variance (58.6%) is meaningful as only two components a significant portion of the variability explained, integrated and selected several plant and soil variables analyzed in this soil saline field study involving the influence of two keystone fungi inhabiting their rhizosphere (Table S3). It is clear that 41.4% remains be explained, therefore, more soil samples should be analyzed regarding other soil variables (carbonates, organic matter, cation exchange capacity, mineralogy, etc.) and ecophysiological plant variables (more nutrients, environmental aspects or seasonality). EC was an important variable that significantly modified the physiology of the halophytes D. spicata and C. dactylon.

The six halophytes studied showed different salinity coping strategies in the field associated with their ecophysiological traits and preferentially related to halophyte-fungal root colonization. The salinity tolerance of D. spicata and C. dactylon, from the family Poaceae, was linked to AMF colonization, proline accumulation, and photosynthetic pigments. B. salicifolia, E. obtusiflora, and S. fructu-tecto, T-GRSP, TR-GRP, leaf Ca concentration, and soil Ca and Mg concentrations were associated in these halophytes. In contrast, S. torreyana was mostly colonized by DSE and related to RWC, LSI, and leaf concentration of K and Na, ions that participate as osmotic adjusters. This is the first research with halophytes that relates several ecophysiological traits to two key beneficial fungal groups —HMA and DSE—under natural salinity conditions. Both fungi play important but distinct functions in supporting halophytes in saline soils. Therefore, deeper research may elucidate the importance of these natural symbiotic associations in halophytes established in the field under different salinity conditions. Of special interest is the finding of glomalin fractions and their correlation with soil Ca concentration, both linked to soil stability/structure and potential carbon soil sequestration, relevant aspects related to the mitigation effects under the global climate change scenario. Future research should rely on molecular genetics and functional genomics to generate a better understanding of the mechanisms involved in salinity tolerance in halophytes without neglecting the symbiosis with AMF and DSE.

Supplementary materials

The online version contains supplementary material available at XXX

Conflict of interest

The authors have no competing interests to declare

Funding

The authors declare that no funds, grants or other support were received during the preparation of this manuscript.

Acknowledgments

The authors thank Heike Vibrans Lindemann from the Posgrado de Botánica, Colegio de Postgraduados, Campus Montecillo, for the taxonomical identification of halophytes.

Authorship contributions JABG: Conceptualization, Data curation, Formal analysis, Investigation, Original draft, and writing-review and editing. RCG: Methodology, Resources, Validation, Visualization, Original draft, and writing-review and editing. JECS: Formal analysis, and validation. YEKR: Investigation, Visualization, Original draft and writing-review, and editing, MCGC: Investigation, Funding acquisition, Resources, Supervision, Original draft and writing-review, and editing.

Data availability

All data produced are presented in this document.

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Halophytes have different ecophysiological and fungal root colonization traits in two saline soil conditions

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Abstract

Figures

Introduction

Materials and methods

Systematic analysis of soil salinity and its spatial distribution

Selection, sampling, and identification of halophytes

Rhizospheric chemical soil and foliar analyses

Root fungal colonization and total glomalin concentration in soil and root

Statistical analyses

Results

Chemical soil analysis

Foliar physiological characteristics of halophytes

Foliar concentration and nutrient ratios in halophytes

Colonization frequency by AMF and DSE

Concentration of total glomalin in soil (T-GRSP) and roots (TR-GRP)

Discussion

Chemical properties of the rhizospheric soil of halophytes

Foliar ecophysiological traits in halophytes

Foliar concentration and nutrient ratio in the halophytes

Root colonization by AMF and DSE

Concentration of total glomalin in soil (T-GRSP) and roots (TR-GRP)

Conclusion

Declarations

Supplementary materials

Funding

Acknowledgments

Data availability

References

Supplementary Files

Status:

Journal Publication

Version 1