Assessing the salt tolerance of four Algerian Opuntia species through morpho-physiological traits and mineral ion

Agrarian Academic Journal

doi: 10.32406/v7n6/2024/50-65/agrariacad

Assessing the salt tolerance of four Algerian Opuntia species through morpho-physiological traits and mineral ion. Avaliação da tolerância ao sal de quatro espécies Argelinas de Opuntia através de características morfo-fisiológicas e íon mineral.

Boubakr Hadj Kouider¹, Bahia Lallouche¹

^1- Laboratory of Biodiversity and Biotechnological Techniques of Plant Resource Development, Department of Agricultural Sciences, Faculty of Sciences, Mohamed Boudiaf University – M’Sila – Algeria. E-mails: boubakr.hadjkouider@univ-msila.dz, bahia.lallouche@univ-msila.dz

Abstract

This study investigated twenty parameters associated with mineral ion absorption and morpho-physiological traits to discern the unique characteristics of various Opuntia species exposed to different salt concentrations (200 mM, 400 mM, and 600 mM). The data revealed that under 200 mM and 400 mM NaCl stress, the most distinguishing traits were the Na⁺content in roots and cladodes, along with K⁺ content in cladodes. The species clustered into three groups, with O. amyclea and O. ficus indica demonstrating the highest salt tolerance. Under 600 mM salt stress, the content K⁺, Na⁺ and K⁺/ Na⁺ ratio of cladode, were identified as the most discriminant traits based on the calculated F-ratio. Biplot-based species analysis indicated that O. engelmannii and O. ficus indica exhibited the highest salt tolerance. Also, the cladode and root K⁺/ Na⁺ ration, K⁺, Na⁺ content of cladode and root Na⁺ content emerge as pivotal traits for assessing salt tolerance in Opuntia species.

Keywords: Opuntia. Salt stress. Morphological traits. Physiological traits. Mineral ions content.

Resumo

Este estudo investigou vinte parâmetros associados à absorção de íons minerais e características morfofisiológico para discernir as características únicas de várias espécies de Opuntia expostas a diferentes concentrações de sal (200 mM, 400 mM e 600 mM). Os dados revelaram que, sob estresse de NaCl de 200 mM e 400 mM, as características mais distintivas foram do conteúdo de Na⁺ nas raízes e cladódios, juntamente com o conteúdo de K⁺ nos cladódios. As espécies agruparam-se em três grupos, com O. amyclea e O. ficus indica demonstrando a maior tolerância ao sal. Sob estresse salino de 600 mM, o conteúdo de K⁺, Na⁺ e a razão K⁺/Na⁺ do cladódio foram identificados como as características mais discriminantes com base na razão F calculada. A análise de espécies baseada em Biplot indicou que O. engelmannii e O. ficus indica exibiram a maior tolerância ao sal. Além disso, a relação K⁺/Na⁺ do cladódio e da raiz, o conteúdo de K⁺, Na⁺ do cladódio e o conteúdo de Na⁺ da raiz emergem como características essenciais para avaliar a tolerância ao sal em espécies de Opuntia.

Palavras-chave: Opuntia. Estresse salino. Características morfológicas. Características fisiológicas. Conteúdo de íons minerais.

Introduction

In contemporary times, plants frequently confront a variety of abiotic stresses that can significantly affect agricultural productivity by up to 50%. These stresses initiate morphological and physiological changes that may ultimately lead to plant mortality (LALLOUCHE et al., 2017). Among these stressors, salinity stands out as one of the most destructive, causing profound alterations in morphological traits, physiological characteristics, and the proteomic and transcriptomic profiles of diverse plant species (LALLOUCHE et al., 2017; JAMSHIDI GOHARRIZI et al., 2020).

Salinity exerts its detrimental effects through ionic imbalance and osmotic reduction. Osmotic reduction results from salt in the soil solution, diminishing the plant’s water uptake capacity, leading to reduced nutrient absorption, stunted growth, and even cell death. Ionic imbalance occurs when an excess of salt enters the transpiration stream, causing damage to cells in transpiring leaves and potentially inhibiting growth (BALASUBRAMANIAM et al., 2023; CAI et al., 2023).

Potassium accumulation in plant tissues under saline conditions is implicated in osmotic adjustment, enzyme activation, regulation of membrane electric potential and overall growth and development (KUMARI et al., 2021).

Plants employ various mechanisms to defend against salt stress, including the synthesis of osmotic protectants such as proline, sugars, amino acids, and glycine betaine (YILDIZ et al., 2021). Mechanisms like salt compartmentalization in vacuoles, salt exclusion, and the accumulation of osmolytes play crucial roles in salt tolerance (ACOSTA-MOTOS et al., 2017). Increased inorganic ions, such as K⁺ concentration, have been reported in response to salinity stress, although their role in osmotic adjustment remains a topic of debate (ASSAHA et al., 2017; KUMAR et al., 2020).

Its influence extends to abiotic stress tolerance, particularly under salinity conditions, where K⁺ stimulates rapid and continuous alterations in genes controlling the response of phytohormones, influencing plant responses to salinity (ARIF et al., 2020).

While previous studies have aimed to develop Opuntia species with increased salt tolerance, understanding the adaptive regulation, tolerance mechanisms under salt stress, the role of inorganic ions, and the optimal salt concentration for growth and development in Opuntia remain unclear. Opuntia species, belonging to the Cactaceae family, are increasingly cultivated in Mediterranean ecosystems for their edible fruits (FELKER; INGLESE, 2003; HADJKOUIDER et al., 2017). These species could prove beneficial for the restoration of natural protected areas. Opuntia, a commonly grown forage plant in semiarid areas, exhibits high water-use efficiency due to its CAM metabolism and serves as a potential reservoir of candidate genes for salt tolerance in plant breeding programs, given the frequent use of saline water in arid zone agriculture (MURILLO‐AMADOR et al., 2001; CHA-UM et al., 2013; SÁNCHEZ-PURIHUAMÁN et al., 2023; LALLOUCHE et al., 2015; FREIRE et al., 2018; LIMA et al., 2022).

This study’s objectives were to assess the contributions of morpho-physiological traits and mineral ions in four Opuntia species under salt stress, elucidate the accumulation of these molecules, and identify the optimal salt concentration for Opuntia growth and development. Clarity on these characteristics provides a valuable reference for a comprehensive exploration of salt tolerance mechanisms at both morphological and physiological levels.

Materials and methods

Plant material and salt stress application

The experiment was applied based on four Opuntia species (Opuntia ficus indica, Opuntia amyclea, Opuntia engelmannii and Opuntia streptacantha). Growing at differents arid and semi-arid regions of Algeria.

After the select on land, 60 young cladodes were collected, we chose 20 plants from each species and we took three (3) young cladodes from each plants. Thus, 60 young cladodes have been taken from each species.

The selected young cladodes are planted in the period of 2021 in 5 liter pots volume filled with sand and put under natural growing conditions. The experiment was adopted in the form of completely randomized design with fifteen replications per species per concentration. The pots were watered weekly by distilled water. Salinity stress was applied to the generated plants after the second year of culture. Opuntia plants were exposed to salinity treatments sixty (60) days. By using four levels of saline irrigation (0, 200, 400 and 600 mM).

Variation of tolerance to salt stress among the studied species was evaluated based on different morpho-physiological traits and mineral ions. After 60 consecutive day’s period under the salt stress, plant material samples were taken (roots, aged cladodes and young cladodes) for further analysis. For each species, 10 samples (roots, aged cladodes and young cladodes) per salinity level are intended from the analysis and another 5 samples from tracking the growth.

Morpho-physiological traits

The used of morpho-physiological traits in our study were the number of root (NR), aged cladode length (ACL), young cladode length (YCL), root length (RL), root fresh weight (RFW), aged cladode fresh weight (ACFW), young cladode fresh weight (YCFW), aged cladode and young cladode width (ACW, YCW) and the fresh weight root/ fresh weight cladode ratio (RFW/CFW).

The relative water content (RWC) was recorded at the end of the assay after 60 days. The RWC was calculated following the formula:

RWC (%) = (fresh weight − dry weight) × 100/ (turgid weight – dry weight) (TURNER, 1981)

Mineral ion traits

Measurement of ion concentration (Na⁺, K⁺, Ca²⁺, K⁺/Na⁺) for cladodes (CNa⁺, CK⁺, CCa⁺², CK⁺/CNa⁺ ratio) and roots (RNa⁺, RK⁺, RCa⁺², RK⁺/RNa⁺ ratio). Mineral ions in plant tissues were determined according to Allen et al. (1985).

Data analysis

Using the F ratio values, one-way ANOVA was performed on the data (Fast statistics v 2.0.4). The least amplitude significant differences (PPAS) test was used to determine the interaction between species and treatments (specie × salinity), and p < 0.05 was used to express significance.

To determine the discriminants morpho-physiological and mineralogical traits that cause significant differences among the Opuntia species under salt stress (0, 200, 400 and 600 mM NaCl), the multivariate analysis, clustering and ANOVA analysis was tested using XLSTAT software (https://www.xlstat.com/en/).

In PCA, the mean data from each NaCl concentration for each species were used to identify species groups and to determine the axes and the characters significantly contributing to the variation (HAMMER et al., 2009). In this procedure, the similarity matrix was used to generate eigen values and scores for the species. HCA was carried out using Ward’s minimum variance method as a clustering algorithm (WILLIAMS, 1976) and squared Euclidean distances as a measure of dissimilarity (WARD, 1963).

Results

Four levels of applied stress (control, 200 NaCl, 400 and 600 mM NaCl concentrations) were used to evaluate the effect of salinity on different morpho-physiological and mineralogical traits of Opuntia species.

Four species (O. ficus indica, O. amyclea, O. streptacantha and O. engelmannii) were used for the evaluation of salt tolerance (200, 400 and 600 mM), while the three species (O. ficus indica, O. streptacantha. and O. engelmannii) were used for the evaluation of salt tolerance at 600 mM. The species O. amyclea was not evaluated under salt stress 600 mM because it was totally affected by the third level of stress (600 mM).

Under stress 200 mM NaCl

Statistical analysis indicated significant differences between the species O.F.I., O.A., O.S., and O.E. under salt stress 200 mM NaCl at 60 days (P < 0.001; Table 1). The data of One-way ANOVA based on table 1, indicates a significant effect of salinity on the root number, length and fresh weight (N, L, RFW), aged and young cladodes length and fresh weight (ACL, ACFW, YCL, YCFW), fresh weight root/ fresh weight cladode ratio (RFW/CFW ratio), water content for aged and young cladode (ACRWC, YCRWC), Na⁺ and Ca²⁺ contents for cladodes, Ca²⁺, K⁺ for root and R K⁺/Na⁺ ratio.

Na⁺ content in root and cladode and K⁺content in cladodes were found the most discriminant parameters, followed by ACRWC, RN, CCa²⁺, YCRWC, root K⁺/Na⁺ ratio, RFW, YCFW, ACFW, RFW/CFW, RL, RK⁺, RC²⁺ ACL and YCL (F ratio > F critical, Table 1). Aged cladode and young cladode width (ACW, YCW) and cladodes K⁺/ Na⁺ ratio were not so affected in all species (F ratio ˂ F critical, Table 1). The most discriminant trait root and cladode Na⁺ content and cladode K⁺ content were affected by salinity in all the examined species (Table 1).

Opuntia S. exhibited an increase in root Na⁺ content of 42.57%. Moreover, O.E., O.A. and O.F.I. exhibited an important increase in root Na⁺ content of 99.50%, 98.52% and 94.04%, respectively. We found that cladode Na⁺ content exhibited high increase. However, the increase was higher and faster in O. ficus indica and O. amyclea (from 9.9±1 in control plants to 24.9±1 in stressed plants and 10±1 in control plants to 26.1±1 in stressed plants), respectively. The matrix of correlations reveals the existence of a strong positive correlation of Na⁺ content in root with Na⁺ content in cladodes (r = 0.993).

Table 1 – Morpho-physiological and mineral ion traits for four Opuntia species after 60 days of experimental conditions and salt stress (0 and 200 mM NaCl). Values bearing the same letter in each line are not significantly different at p <0.05.

Traits

O. ficus indica (O.F.I.)

O. amyclea (O.A.)

O. engelmannii (O.E.)

O. streptacantha (O.S.)

One-way ANOVA

All genotypes under salinity

O.F.I. x salinity

O.A. x salinity

O.S. x salinity

O.E. x salinity

Control

200 mM

Control

200 NaCl

Control

200 mM l

Control

200 mM

F-ratio

F-critical

F-ratio > F-critical

Number of root

55±1b

47±1c

66±1a

31.2±1d

30±1d

31.5±1d

30.5±0.9d

869.65

4.06 Yes

Non

Root length (cm)

34±1b

22.6±2c

52±1a

49±1a

27.7±1c

25.5±1c

12.2±1d

9.2±1d

69.25

4.06 Yes

Non

Yes

Root fresh weight (g)

14.7±1b

11.3±1b

15±1b

12.4±0.9b

19.2±1a

16.9±1a

6.35±1c

4±1c

6237.9

4.06 Yes

Aged cladode length (cm)

20±1b

16±1c

24.5±1a

20±1b

19.5±1b

15±1c

19.5±1b

21.5±1b

29.18

4.06 Yes

Non

Aged cladode width (cm)

11±1na

9.5±1ns

9.7±1ns

8.5±1ns

10±1ns

8.7±1ns

7.7±1ns

3.0469

4.06 Non

Aged cladode fresh weight (g)

99±1c

87±1e

96±1d

81.3±1e

180.8±1a

168.7±1b

99.8±1c

68.3±1g

85.77

4.06 Yes

Young cladode length (cm)

18±1a

15±1b

14.5±1b

12±1c

10.5±1cd

9.5±1d

14.7±1b

14.29

4.06 Yes

Non

Yes

Young cladode width (cm)

6.6±1ns

6.63±0.9ns

6.5±1ns

5.5±1ns

7±1ns

5.5±1ns

6.6±1ns

5.7±1ns

1.66

4.06 Non

young cladode fresh weight (g)

53±1a

37.5±1c

51.7±1a

42±1b

40.54±1b

30.9±1d

31.9±1d

27.2±1e

130.4

4.06 Yes

Report fresh weight root/ fresh weight cladode

0.09±0.001b

0.09±0.002b

0.1±0.01a

0.09±0.001b

0.08±0.001b

0.04±0.01c

79.50

4.06 Yes

Non

Yes

Aged cladodes relative water content (%)

79.1±1a

69.5±1c

77.7±1a

72.7±1b

24±1g

37±1f

59±1d

48±1e

883.58

4.06 Yes

Young cladodes relative water content (%)

46.0±1b

24.4±1e

40.5±1c

32.7±1d

24±1e

34±1d

54±1a

47±1b

267.53

4.06 Yes

Cladodes Na⁺ (mg g^-1 DW)

9.9±1b

24.9±1a

10±1b

26.1±1a

5.11±1d

26.8±1a

7.5±1c

10.7±1b

131.77

4.06 Yes

Root Na⁺(mgg^-1 DW)

67.2±1d

130.4±1c

68±1d

135±1b

40.4±1g

57.6±1f

63.9±1e

162.6±1a

17730

4.06 Yes

Cladodes K⁺ (mgg^-1 DW)

12.6±1e

44.3±1b

13±1e

45±1b

16.9±1d

60.3±1a

29.9±1c

28.3±1c

5085.8

4.06 Yes

Non

Root K⁺ (mgg^-1 DW)

3.53±1d

4.2±1d

4.5±1d

34.73±1a

10.73±1c

13.92±1b

10.73±1c

45.56

4.06 Non

Yes

Non

Cladodes Ca²⁺ (mg g^-1 DW)

10.6±1e

40.2±1b

12.1±1e

41.5±1b

15.3±1d

56.2±1a

26.5±1c

25.5±1c

472.35

4.06 Yes

Non

Root Ca²⁺ (mgg^-1 DW)

2.4±1d

3.1±1d

3.4±1d

30.6±1a

9.6±1c

12.8±1b

9.6±1c

45.56

4.06 Non

Yes

Cladodes K⁺/ Na⁺ ratio

1.2±1

1.7±1

2.3±1

1.7±1

3.5±1

2.2±1

3.8±1

2.6±1

0.5593

4.06 Non

Root K⁺/ Na⁺ ratio

0.05±0.001f

0.02±0.01h

0.061±0.01e

0.03±0.001g

0.82±0.001a

0.19±0.01c

0.21±0.01b

0.06±0.01a

512.34

4.06 Yes

In order to study the relationship among all the traits considering two levels of salt stress (control, 200 mM), multivariate analysis type PCA was performed based on two main components. Based on the Principal Component Analysis (PCA), special values of components 1 and 2 were 11.23 and 5.491, respectively, where 83.60% of total variation was explained. In this study, the first principal component had high positive correlation with RN, RL, ACW, ACFW, YCL, ACRWC, CNa⁺, RNa⁺, CK⁺, CCa²⁺ and had high negative correlation with RK⁺, YCW, RCa²⁺, CK⁺/Na⁺ ratio, and RK⁺/Na⁺ratio. So, the first component can be called the component of root and young cladode resistance. Second component had a high negative correlation with ACL, YCRWC, Thus, this component can be named aged and young cladode sensitivity. The PCA plots confirm root Na⁺ and cladode Na⁺ content as the most discriminant traits.

This analysis showed that the parameters, root Na⁺ content, cladode K⁺ and Ca²⁺ content and aged cladode fresh weight (ACFW) are correlated to the first axis inversely to what was noted at the control (0 mM) (Figure 1A, Figure 1B). The species distribution in the next representation of the two axes has kept the same grouping (Figure 3C).

The maximum Euclidean distance of 7.52 was observed between species O.A. and O.S. The lowest Euclidean distance was observed between O.A. and O.F.I. with only 4.55 also for O.E. and O.S. The Euclidean distance was moderate with 6.81, due to their genetic similarity.

In order to group the species based on 20 morpho-physiological traits, Cluster Analysis (CA) and Ward method were performed. This analysis led us to group the genotypes into three categories: C1 for the category of Highly Salt Tolerant (HST) species, it includes O. amyclea and O. ficus indica. C2 for Moderately Salt Tolerant (MST), it includes O. engelmannii and C3 Salt Tolerant (ST) for O. strepotacantha (Figure 1D). Clusters 2 and 3 had the lowest genetic distance (65.51). But cluster 1 and 2 had the highest genetic distance (127.19). Groups in cluster analysis were similar to the groups of two dimensional graphs in PCA. Thus, both analyses corroborated each other.

Under stress 400 mM NaCl

Statistical analysis showed significant differences between the species O.F.I., O.A., O.S., and O.E. under salt stress 400 mM NaCl at 60 days (Table 2). One-way ANOVA revealed a significant effect of salinity on the root number, length and fresh weight (RN, RL, RFW), aged cladode length, width and fresh weight (ACL, ACW, ACFW), YCL, YCFW, RFW/CFW, water content for aged cladode and young cladode (ACRWC, YCRWC), Na⁺, K⁺and Ca²⁺ content for root (RNa⁺, RK⁺, RCa²⁺), Ca²⁺ content for cladodes and RK⁺/Na⁺ ratio for root and cladodes.

Na⁺ and K⁺ content for cladodes were found to be the most discriminant traits (F ratio > F critical, Table 2).

RNa⁺, CCa²⁺, RK⁺/Na⁺ ratio, RL, RN, RFW, YCFW, RFW/CFW ratio, YCRWC, ACL, RK⁺, RCa²⁺, ACW and YCL also reflected G×T effects but the F-ratio were relatively low (Table 2). Young cladode width (YCW) and K⁺/Na⁺ratio concentration in cladode (C K⁺/Na⁺ ratio) were not affected by salinity in all species (F ratio ˂ F critical, Table 2).

The most discriminant parameters Na⁺ and K⁺ content for cladodes were affected by salinity in all species (Table 2). Furthermore, in all species plants Na⁺ and K⁺ content for cladodes showed significant increase. However, the increase was higher and faster in O.S. (from 5.11±1 in control plants to 18.6±1 in stressed plants). Moreover, in O.E., K⁺ content for cladode showed a high significant decrease (Table 2). Strong positive correlation (r=0.979) was revealed for this parameter with the fresh weight of root.

Table 2 – Morpho-physiological and mineral ion traits for four Opuntia species after 60 days of experimental conditions and salt stress (0 and 400 Mm NaCl). Values bearing the same letter in each line are not significantly different at p <0.05.

Traits

O. ficus indica (O.F.I.)

O. amyclea (O.A.)

O. engelmannii (O.E.)

O. streptacantha (O.S.)

One-way ANOVA

All genotypes under salinity

O.F.I. x salinity

O.A. x salinit

O.S. x salinit

O.E. x salinit

Control

400 mM

Control

400 mM

Control

400 mM

Control

400 mM

F-ratio

F-critical

F-ratio > F-critical

Number of root

55±1b

32±1d

66±1a

49±1c

31.2±1d

30.5±1d

31.5±1d

28.5±1e

267.50

4.06 Yes

Non

Yes

Root length (cm)

34±1c

23±1e

52±1a

42±0.95b

27.7±1d

22.06±1e

12.2±1f

9.7±0.9g

544.79

4.06 Yes

Root fresh weight (g)

14.7±1c

7.7±1de

15±1c

9.2±1d

19.2±1b

23±1a

6.3±1e

1.55±1e

245.80

4.06 Yes

Aged cladode length (cm)

20±1b

22.3±1c

24.5±1a

15.95±1d

19.5±1c

19±1c

19.5±1c

23.5±1ab

34.8

4.06 yes

Yes

Non

Yes

Aged cladode width (cm)

11±1ab

10.7±1ab

9.7±1bc

8±1c

8.5±1bc

12.5±1a

8.7±1bc

7.5±1c

16.56

4.06 Non

Yes

Non

Aged cladode fresh weight (g)

99±1c

80±1e

96±1d

70.4±1f

180.8±1a

156.4±1b

99.8±1c

81.33±1e

37.67

4.06 Yes

Young cladode length (cm)

18±1ba

13.5±1bc

14.5±1b

12±1cd

10.5±1de

13±1bc

9.5±1e

8.75±1e

13.67

4.06 Yes

Non

Young cladode width (cm)

6.6±1ns

5.8±1ns

6.5±1ns

5.3±1ns

7±1ns

6.5±1ns

6.6±1ns

4.75±1ns

1.6619

4.06 Non

young cladode fresh weight (g)

53±1a

34.2±1c

51.7±1a

27.6±1e

40.54±1b

41.4±1b

31.9±1d

20.3±1f

244.38

4.06 Yes

Non

Yes

Report fresh weight root/ fresh weight cladode

0.09±0.01bc

0.06±0.01d

0.10±0.01b

0.09±0.01c

0.11±0.01a

0.04±0.01e

0.01±0.01f

200.26

4.06 Yes

Aged cladodes relative water content (%)

79.1±1a

62.4±1b

77.7±1a

61.5±1b

24±1e

29±1d

59±1c

16.1±1f

1280.0

4.06 Yes

Young cladodes relative water content (%)

46.03±1b

17.8±1f

40.5±1c

14.8±1g

24±1e

26±1d

54±1a

16±1bg

76.59

4.06 Yes

Non

Yes

Cladodes Na⁺ (mg g-1 DW)

9.9±1c

13.9±1b

10±1c

14±1b

5.11±1e

18.6±1a

7.5±1d

9.9±1c

4770.4

4.06 Yes

Root Na⁺ (mg g-1 DW)

67.2±1e

166.7±1c

68±1e

169±1b

40.4±1g

162.6±1d

63.9±1f

207±1a

1274.7

4.06 Yes

Cladodes K⁺ (mg g-1 DW)

12.6±1e

45.5±1b

13±1e

45±1b

16.9±1d

61.5±1a

29.9±1c

12.3±1e

1635.9

4.06 Yes

Root K⁺ (mg g-1 DW)

3.5±1e

2.7±1e

4.2±1e

4.1±1e

34.7±1a

9.9±1c

13.9±1b

7.1±1d

31.02

4.06 Non

Yes

Cladodes Ca2⁺ (mg g-1 DW)

10.6±1f

42.02±1c

12.11±1f

44.7±1b

15.3±1e

58.4±1a

26.5±1d

10.7±1f

1216.6

4.06 Yes

Root Ca2⁺ (mg g-1 DW)

2.4±1e

2.6±1e

3.15±1e

3.2±1e

30.6±1a

8.8±1c

12.8±1b

6.03±1d

24.64

4.06 Non

Yes

Cladodes K⁺/ Na⁺ ratio

1.2±1ns

3.2±1ns

2.3±1ns

3.2±1ns

3.5±1ns

3.1±1ns

3.8±1ns

1.2±1ns

2.891

4.06 Non

Yes

Root K⁺/ Na⁺ ratio

0.05±0.01d

0.02±0.01g

0.06±0.01c

0.025±0.01f

0.82±0.01a

0.06±0.01c

0.21±0.01b

0.03±0.01e

994.0

4.06 Yes

PCA revealed that the first and second principal components accounted for 59.137 and 31.464 % of the variation that existed among the traits, respectively. The first component comprised of RFW, ACW, ACFW, YCL, YCW, YCFW, RFW/CFW ratio YCRWC, CNa⁺, CK⁺, CCa²⁺ RK⁺/RNa⁺ ratio, CK⁺/Na⁺ ratio, RNa⁺ and aged cladode length. Therefore, this component can be called the component of young cladode and root resistance. The second component involved NR, RL and ACRWC, respectively, so, this component can be named root sensitivity. The PCA plots confirmed that Na⁺ content for cladodes is the most discriminant parameter.

This analysis showed that the traits, root fresh weight (RFW), aged cladode length and fresh weight (ACL, ACFW), young cladode width and relative water content (YCW, YCRWC), report fresh weight root/ fresh weight cladode (RFW/CFW ratio), CK⁺, CCa²⁺ concentration for cladodes, CK⁺/Na⁺ ratio and RK⁺/Na⁺ ratio are correlated to the first axis, while the number (NR) and length (RL) of root and aged cladodes relative water content (ACRWC) parameter is correlated to the second axis inversely to what was noted at the control (0 mM) (Figure 1A, Figure 1B). The distribution of species in the next representation of the two axes has not kept the same grouping (Figure 1E).

The maximum Euclidean distance was observed between species O. streptacantha and O. engelmannii (8.42). The lowest Euclidean distance was observed between species O. ficus indica and O. amyclea (3.57), which described their genetic similarity. In order to group the species by considering all the attributes, Cluster analysis and Ward method were performed. This analysis generated three clusters of genotypes: C1 for HST (O. engelmannii), C2 for ST (O. ficus indica and O. amyclea) and C3 for MST (O. streptacantha) (Figure 1F). Clusters 2 and 3 had the highest genetic distance (117.44). Groups in cluster analysis were similar to the groups of two dimensional graphs in PCA, Thus, both analyses corroborated each other.

Under stress 600 mM NaCl

Statistical analysis showed significant differences between the species O.F.I., O.A., O.S., and O.E. under salt stress 600 mM NaCl at 60 days (Table 3).

The data of One-way ANOVA based on table 3, indicates a significant effect of salinity on the Na⁺, K⁺and Ca²⁺ concentration for root (RK⁺, RCa²⁺), K⁺ and Ca²⁺ concentration for cladodes (CK⁺, CCa²⁺), YCP, RFW/CFW ratio, RK⁺/Na⁺ ratio, aged cladode length, width and fresh weight (g) (ACL, ACW, ACFW), root length (RL), CK⁺/Na⁺ratio, young cladode length (YCL), water content for aged (ACRWC) and root number (RN) were found to be significantly affected (Table 3).

K⁺ and K⁺/Na⁺ for cladodes (CK⁺, CK⁺/Na⁺) were found to be the most discriminants traits (F ratio> F critical, Table 3). The RFW, CCa²⁺, YCRWC, RFW/CFW ratio, ACRWC, YCFW, RK⁺/Na⁺, ACL, RL, RCa²⁺, YCL, ACW, RN and potassium content in the roots (RK⁺) also reflected G×T effects but the F-ratio was relatively low (Table 3). Young cladode width (YCW) was not so affected in all species (F ratio ˂ F critical, Table 3).

K⁺ content cladode for cladodes (CK⁺) was affected by salinity in all species (Table 3) O.F.I. and O.S. exhibited a significant increase compared to the control (Table 3), where K⁺ content for cladode was decreased to 74.86% in O. engelmannii. Strong positive correlation (r=0.1) was revealed for this parameter with root length and root fresh weight.

In order to study the relationship among all the parameters in two levels of salt stress (control, 600 mM).

Table 3 – Morpho-physiological and mineral ion traits for three Opuntia species after 60 days of experimental conditions and salt stress (0 and 600 nM NaCl). Values bearing the same letter in each line are not significantly different at p <0.05.

Traits

O. ficus indica (O.F.I.)

O. engelmanii (O.E.)

O. streptacantha (O.S.)

One-way ANOVA

All genotypes under salinity

O.F.I. x salinity

O.S. x salinity

O.E. x salinity

Control

600 mM

Control

600 mM

Control

600 mM

F-ratio

F-critical

F-ratio > F-critical

Number of root

55±1a

27±1c

31.25±1b

25±1d

31.5±1b

28.5±1c

9.25

5.14 Yes

Root length (cm)

34±1a

22±1c

27.75±1b

23.5±1c

12.25±1d

13.2±1d

91.93

5.14 Yes

Non

Root fresh weight (g)

14.7±1b

5.2±1d

19.2±1a

8.95±1c

6.35±1d

2.5±1e

4713.18

5.14 Yes

Aged cladode length (cm)

20±1b

23±1a

19.5±1bc

17.5±1c

19.5±1bc

11.5±1d

99.25

5.14 Yes

Non

Yes

Aged cladode width (cm)

11±1a

8.5±1a

10.2±1a

8.75±1a

6±1b

13.39

5.14 Yes

Non

Yes

Aged cladode fresh weight (g)

99±1c

65.9±1d

180.8±1a

133.07±1b

99.8±1c

63.02±1e

31.47

5.14 Yes

Young cladode length (cm)

18±1a

6.1±1c

10.5±1b

9.75±1b

9.5±1b

10.25±1b

15.39

5.14 Yes

Non

Young cladode width (cm)

6.6±1ns

4±1ns

7±1ns

4.5±1ns

6.66±1ns

6±1ns

3.25

5.14 Yes

Non

young cladode fresh weight (g)

53±1a

7±1f

40.5±1b

24.25±1e

31.9±1c

28.5±1d

388.93

5.14 Yes

Report fresh weight root/ fresh weight cladode

0.095±0.001a

0.071±0.001c

0.092±0.001b

0.05±0.001d

0.04±0.001e

0.02±0.001f

1501

5.14 Yes

Aged cladodes relative water content (%)

79.1±1a

50.8±1c

24±1d

19±1e

59±1b

12.8±1f

1246.84

5.14 Yes

es

Young cladodes relative water content (%)

46.03±1b

15±1e

24±1c

17±1d

54±1a

12.8±1f

12951.01

5.14 Yes

Cladodes Na⁺ (mg g^-1 DW)

9.9±1b

17.2±1a

5.11±1d

5.91±1cd

7.53±1c

11.5±1b

95.59

5.14 Yes

Non

Yes

Root Na⁺(mg g^-1 DW)

67.2±1d

336±1a

40.4±1f

215±1c

64±1e

231.2±1b

313.24

5.14 Yes

Cladodes K⁺ (mg g^-1 DW)

12.6±1e

44.3±1b

16.9±1d

51.5±1a

29.92±1c

7.52±1f

1671.04

5.14 Yes

Root K⁺ (mg g^-1 DW)

3.53±1d

4.33±1d

34.7±1a

6.73±1c

13.92±1b

4.33±1d

5.76

5.14 Non

Yes

Cladodes Ca²⁺ (mg g^-1 DW)

10.6±1e

42±1b

15.3±1d

58.26±1a

26.53±1c

5.43±1f

1908.45

5.14 Yes

Root Ca²⁺ (mg g^-1 DW)

2.4±1d

3.22±1d

30.6±1a

8.86±1c

12.83±1b

3.23±1d

31.75

5.14 Non

Yes

Cladodes K⁺/ Na⁺ ratio

1.27±0.9c

2.56±1bc

3.5±0.9b

8.73±1a

3.88±1b

0.65±0.01c

80.24

5.14 Non

Yes

Root K⁺/ Na⁺ ratio

0.05±0.001c

0.012±0.001f

0.82±0.001a

0.03±0.001d

0.21±0.001b

0.018±0.001e

283.0

5.14 Yes

PCA representation was performed based on the two main components. According to the data from analysis of the principal component, special values of components 1 and 2 were 11.74 and 8.25, respectively, which overall, 100% of total variations was explained.

In this study, the first principal component had high, positive and negative correlation with RL, RFW, ACW, ACFW, YCW, YCRWC, CK⁺, RK⁺, RCa²⁺, CCa²⁺and CK⁺/Na⁺ ratio. Therefore, the first component can be called the component of young cladode and root resistance.

Second component had a high, positive correlation with report fresh weight root/ fresh weight cladode (RFW/CFW), RNa⁺ and CK⁺. Consequently, this component can be named young cladode and root sensitivity. The PCA plots confirm K⁺ content for cladodes (YCRWC) the most discriminant parameter.

This analysis showed that the parameters, root number and fresh weight (RN, RFW), aged cladode fresh weight (ACFW), water content for young cladode (YCRWC), Ca²⁺ and K⁺ concentration for cladodes and root (CK⁺, CCa²⁺) and K⁺/Na⁺ ratio for cladodes (CK⁺/Na⁺) are correlated to the first axis, while the Na⁺ concentration for root and cladode (RNa⁺), aged cladode relative water content and length (ACRWC, ACL) parameter are correlated to the second axis inversely to what was noted at the control (0 mM) (Figure 1A, Figure 1B). The distribution of species in the next representation the two axes has not kept the same grouping (Figure 1G).

The maximum Euclidean distance was observed between species O. streptacantha and O. engelmannii (6.852), the lowest Euclidean distance was observed between species O. engelmannii and O. ficus indica (6.010), which described their genetic similarity. In order to grouping of species based on all attributes, it was performed by using a cluster analysis and Ward method. This analysis led us to group the genotypes into three categories such as highly salt tolerance, C1 (O. engelmannii), salt tolerant, C2 (O. ficus indica) and salt moderately tolerant, C3 (O. streptacantha) (Figure 1H). Clusters 2 and 3 had the lowest genetic distance (101.58). But cluster 1 and 2 had the highest genetic distance (145.09). Groups in cluster analysis were similar to the groups of two-dimensional graphs in PCA.

Figure 1 – Left: Biplot display of Opuntia species according to the first and second PCA components under salt stress conditions (control, 200, 400 and 600 mM of NaCl). Right: Cluster analysis using 20 morpho-physiological traits.

Discussion

The calculated F-ratio for root and cladode Na⁺, cladode K⁺ and cladode K⁺/cladode Na⁺ ratio, were found to be the most discriminant traits. Moreover, the matrix of correlations reveals the existence of a strong positive correlation of K⁺ content in cladode with root length (r=1) and K⁺/Na⁺ ratio content in cladodes with root fresh weight (r = 0.980).

The mineral ion absorption response, analyzed through the expression of the accumulation of Na⁺ content (root and cladodes), K⁺ content (cladodes) and K⁺/Na⁺ ratio content (cladodes) of O. ficus indica, O. amyclea, O. engelmannii and O. streptacantha in salt stress condition with (NaCl), 200, 400 and 600 mM, show that the plants accumulate these compounds in different organs. This accumulation varied from one organ to another, from one species to another, it depends directly to the degree of the applied salt stress concentration.

In O. ficus indica and O. amyclea the accumulation of Na⁺, K⁺ content, K⁺/Na⁺ ratio is in the direction of root, cladodes, the same in control plants toward stressed plants with different concentrations. In the cladodes, that K⁺ content predominated over Na⁺ content, also the K⁺ content of cladode predominated over K⁺ content of root. These results are in conformity with the study of Lima et al. (2022) on prickly pear cactus (Opuntia stricta Haw.), Franco-Salazar; Veliz, (2007) on Opuntia ficus indica and Hernández et al. (2018) on Vicia sativa L. Indeed, in the Opuntia ficus indica stressed by NaCl (200, 400 and 600 mM) and O. amyclea stressed by NaCl (200 and 400 mM) K⁺and K⁺/Na⁺ ratio concentration are increasing much more in cladodes comparatively to root, also the K⁺ content in root declined significantly in relation to concentration of salt stress. These results are in conformity with the study of Franco-Salazar; Veliz (2007) on cactus pear (Opuntia ficus indica Mill.), and Cha-Um et al. (2013) in Echinopsis calochlora.

In addition, in O. engelmannii Na⁺and K⁺ concentration of both root and cladode, also the K⁺/Na⁺ ratio concentration showed a significant increase in the control and under salt stress at 200, 400 and 600 mM. However, it was observed that this species showed the maximum increase in Na⁺, K⁺ and K⁺/Na⁺ ratio concentration under salt stress. In the cladodes, the K⁺ and K⁺/Na⁺ ratio concentration predominated the K⁺ and K⁺/Na⁺ ratio concentration of root.

In O. streptacantha K⁺ and K⁺/Na⁺ ratio content in root showed high significant reduction for the control under salt stress at 200, 400 and 600 mM NaCl. However, K⁺/Na⁺ ratio concentration in root showed a higher percentage of reduction when compared to K⁺ in cladodes. In comparison with the control, at 200, 400 and 600 mM we registered a decrease in K⁺content in cladode with 5.35%, 58.86% and 74.86%, respectively.

The accumulation of K⁺ and K⁺/Na⁺ ratio occurs significantly in cladode than in roots under normal conditions (control) or under salt stress (200, 400 and 600 mM NaCl) in all species Opuntia.

Our results regarding an increase in Na⁺, K⁺, K⁺/Na⁺ in root and cladodes agree with what Sleimi et al. (2015) reported, that the exposure of Plantago maritima to (0, 50, 100, 200, 300, 400 and 500 mM NaCl) of sodium chloride led to the increase in Na⁺ content. Freire et al. (2018) observed that increasing the salinity level of irrigation water increased Na⁺ content in the cactus (Nopalea cochenillifera Salm Dyck), and there was a significant interaction between irrigation frequency and irrigation water salinity. Cha-Um et al. (2013) in their study on Cactus (Echinopsis calochlora), Lima et al. (2022) in their study on prickly pear cactus (Opuntia stricta Haw.) reported that Na⁺ content in root and cladodes increase with the increase of salt concentrations. Supporting results also include what Murillo‐Amador et al. (2001) in prickly pear (Opuntia ficus-indica), Sánchez-Purihuamán et al. (2023) on Opuntia sp. “prickly pear”, Schuch; Kelly (2008) in three cactus species (Echinocactus grusonii, Fouquieria splendens and Carnegiea gingantea). Demonstrate that salinity stress of sodium chloride caused an increase in Na⁺, K⁺ and K⁺/Na⁺ in root and cladodes.

A NaCl induced increase in root and cladodes Na⁺ content, and in cladodes K⁺ content and K⁺/Na⁺ ratio were accompanied by a decrease in cladodes K⁺ content and K⁺/Na⁺ ratio in response to salinity stress is a widely interpreted phenomenon, with numerous papers published on this subject which led to regulation of cell turgor.

Additionally, potassium plays an important role in alleviating salinity stress by recasting key processes of plants (ASSAHA et al., 2017; KUMARI et al., 2021). In this sense, it has been reported that K⁺and K⁺/Na⁺ ratio acquisition, transportation and accumulation also serve as the perquisite trait to establish salt tolerant mechanism (FAKHRFESHANI et al., 2015). Recently, plant growth regulators (PGRs) and other signaling molecules have also been found several implications in plants with respect to their roles in mediating K⁺ homoeostasis during salinity stress in plants (YANG et al., 2014; CAI; GAO, 2020).

In another study, Aranda et al. (2021); Sarraf et al. (2022) attributed the increase in NaCl concentration significantly to impair the uptake of some elements such as K⁺and the ability to maintain high K⁺and Na⁺ concentrations in the tissues, thus proving to be one of the key mechanisms of tolerance to saline environments. Therefore, with the higher concentration of Na⁺ in the roots and in the cladode (aged and young), the Opuntia favored the higher concentration of K⁺ in the cladodes comparatively to root to maintain the ideal level of this element in the cladodes tissues. It follows from these studies that high K⁺ and K⁺/Na⁺ availability ameliorates plant growth under salt stress, but under low K⁺ and K⁺/Na⁺ salt stress is devastating. These results reflect firstly, the variability of metabolism of all Opuntia species under salt stress (SHABALA; POTTOSIN, 2014) and secondly, express their ability to accumulate the Na⁺, K⁺ and K⁺.Na⁺ ratio content in different organs. In addition, salinity tolerance was significantly negatively correlated with inorganic ion (Na⁺, K⁺) contents in leaves or roots (except for root K⁺ content) but positively correlated with K⁺/Na⁺ ratio in leaves or roots (CAI; GAO, 2020).

The results of these parameters in the present study suggest that a low-level uptake of Na⁺of cladodes, high uptake of K⁺ and K⁺/Na⁺ ratio in cladodes in O. streptacantha and O. ficus indica under salt stress 200, 400 and 600 mM NaCl might be due of these antiporters and membrane transporters, which can help to stand against the high salt stress.

Conclusion

In this investigation, we assessed the salt tolerance of four Algerian Opuntia species by subjecting them to varying NaCl concentrations (0, 200, 400, and 600 mM) and analyzing their morpho-physiological traits and mineral ion. O. streptacantha exhibited the least sensitivity to salinity stress, followed by O. ficus indica. Through the analysis of discriminant parameters, we determined that O. engelmannii displayed high salt tolerance, while O. ficus indica demonstrated moderate salt tolerance. Our findings highlight the effectiveness of root Na⁺ content, cladode K⁺ content, and cladodes K⁺/Na⁺ ratio as indicators of salt tolerance in Opuntia species. Additionally, our study enhances the understanding of the pivotal changes in mineral ion absorption under salinity stress in Opuntia.

Interest conflicts

There was no conflict of interest among the authors.

Authors’ contribution

Boubakr Hadj Kouider – original idea, reading and interpretation of works and writing; Bahia Lallouche – original idea, writing and corrections.

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Received on February 22, 2024

Returned for adjustments on January 7, 2025

Received with adjustments on January 11, 2025

Accepted on February 3, 2025