Water stress effect on grafted Pistacia vera L. in field conditions

Abstract

Pistacia atlantica Desf. is adapted to arid and semi-arid environments and is considered the best rootstock for Pistacia vera L. The physiological mechanisms responsible for the efficiency of P. atlantica as rootstock, compared to P. vera, are unknown. This study evaluated the effect of water stress and pistachio rootstock (Pistacia vera L. and Pistacia atlantica Desf.) on water status, highlighting the physiological aspects of the scion-rootstock interaction in Pistacia vera L. and Pistacia atlantica Desf. at the seedling stage under water stress. Individuals of Pistacia vera L. were grafted on Pistacia vera and Pistacia atlantica for 2 years, and subjected to two water regimes: irrigation and water stress for 7 weeks. Water status parameters (relative water content (RWC) and soil water content (SWC)), leaf gas exchange parameters (stomatal conductance, net photosynthesis, and transpiration rate), chlorophyll fluorescence transient (OJIP), maximum photosynthetic yield (Fv/Fm), and total chlorophyll content were measured weekly. The results revealed that although soil water content decreased significantly, both rootstocks maintained a high level of hydration, slightly reduced leaf gas exchange, and a stable maximum photosynthetic yield during the water stress, with no clear differences between them. These results suggest that Pistacia vera L. grafted on Pistacia vera L. and Pistacia atlantica Desf. tolerates water stress at the seedling stage in field conditions. These findings are very important in agriculture, and we recommend the investigation of drought stress effect at the tree stage and for a long duration of water stress.

Keywords:
Arid regions; Chlorophyll fluorescence; Photosynthesis; Pistachio; Rootstocks; Water stress

Introduction

Grafting is a plant propagation technique applied since antiquity in various parts of the world. It consists of the development of a new plant through the combination of a root part called the rootstock and an aerial part named the shoot scion (Cookson et al., 2014). This technique is primarily used for vegetative propagation of uniform genetic material, and secondarily to overcome a large number of problems related to constraining climatic conditions (cold, wet, or dry environments, low or high radiation, salinity, and the incidence of pests and diseases) (Ioannou, 2001; Bletsos et al., 2003; Rivero et al., 2003; Estan et al., 2005; Tavallali et al., 2008; Dayal et al., 2014; Jogaiah et al., 2014; Melnyk & Meyerowitz, 2015; Ramírez-Gil et al., 2017; Jimenes et al., 2018; Zhou et al., 2018; Rasool et al., 2020; Ranjbar & Imani, 2022). The use of grafted plants in the production of tree crops is very common compared to the use of grafting in vegetable crops (Martínez-Ballesta et al., 2010). Different plants have been propagated by grafting, such as olive, orange, apple, citrus, grape, and prunes (Atkinson et al., 2003; Fabbri et al., 2004; Moreno et al., 2014; He et al., 2018).

The use of rootstocks is now considerably broadened for a variety of reasons: to improve plant vigor and yield through the efficiency of water and soil mineral uptake, the effectiveness of their uses, and their adaptation to environmental stresses (Storey & Walker, 1999; Tavallali et al., 2008; Yin et al., 2010; Jogaiah et al., 2014; Dayal et al., 2014; Kumari et al., 2015; Ranjbar & Imani, 2022). Indeed, grafted plants absorb higher amounts of water and mineral nutrients compared to non-grafted plants. This is a consequence of the vigorous root system, used as rootstock. In addition, grafting allows the extension of time of collection and the enhancement of yield production (Nguyen & Yen, 2018).

Several studies have revealed the influence of rootstock on improving scion vigor (Cohen & Naor, 2002; Weibel et al., 2003). Some mechanisms involved in improving the growth rate of the shoot scion have been suggested by Rogers and Beakbane (1957), Lochard and Schneider (1981), and Webster (1995). This resides in the effects of rootstock on mineral nutrition (Jones, 1971), water status, and phytohormones. Solari et al. (2006) confirmed the involvement of water relations in improving scion vigor, partly related to differences in hydraulic conductance.

Pistacia vera is often propagated by grafting. This taxon can be grafted on the same species or other species of the genus Pistacia and their interspecific hybrids, according to the culture zone. Thus, the main rootstocks are P. vera, P. atlantica, P. integerrima J.L.Stewart, P. terebinthus L., and Pistacia. integerrima × Pistacia atlantica hybrids (Guerrero, 2011). The use of Pistacia atlantica as rootstock for Pistacia vera has shown a better adaptation to the environmental conditions of this species. Pistacia atlantica is of great ecological and medicinal importance. Moreover, it is adapted to arid and semi-arid environments (Ben Hamed et al., 2016; 2021; 2022; 2023). Unfortunately, it is threatened with disappearance due to its low germination capacity and human activities (Yousefi, 2016; Amara et al., 2017).

This study aims to i) compare the effect of water stress and rootstocks (Pistacia vera and Pistacia atlantica) on water status. ii) highlight the physiological aspects of rootstock-scion interaction in Pistacia vera and Pistacia atlantica; and iii) study the influence of Pistacia atlantica rootstock on Pistacia vera scion at the seedling stage.

Materials and methods

Experimental site, plant material, and treatment

The experiment was conducted under field conditions in Gafsa, Tunisia, during the period of June-July 2014. Germination was carried out directly at the experimental site after seed scarification in September 2012 on sandy soil. After one year of growth, the grafting of Pistacia vera on P .vera and P. atlantica was carried out in June 2013. In this study, specimens ofPistacia atlanticaandPistacia verawere collected from Tunisian arid zones, and deposited as voucher specimens in the herbarium of the Faculty of Sciences of Sfax, University of Sfax (Sfax, Tunisia). The corresponding voucher specimen is cataloged under the reference number R02-24. This collection is accessible to the public, providing researchers with access to reference material for further studies. The climate was Mediterranean, with an average annual rainfall of 165 mm. The minimum and maximum temperatures during the experimental period (June-July 2014) ranged between 30 °C and 40 °C.

Pistacia vera grafted on rootstocks of P. vera and P. atlantica were divided into two groups: The first group was composed of 12 irrigated seedlings with a drip irrigation system for daily irrigation (20ml/h). The second group was water-stressed (12 repetitions for each rootstock) by ceasing irrigation for 35 days. The treatments were: 1) P. vera grafted on P. vera irrigated; 2) P. vera grafted on P. vera water-stressed; 3) P. vera grafted on P. atlantica irrigated; 4) P. vera grafted on P. atlantica water-stressed.

Soil water content

The soil water content was estimated each week at six replicates per treatment. For each treatment, a soil sample was taken at 30 cm and 60 cm depths. For each measurement, the soils sampled were weighed in the fresh state (FW) and then dried in an oven at 105 °C for 48 hours (DW). This parameter was estimated just before the start of treatment and after 1, 2, 3, 4, 5, 6, and 7 weeks of the water withholding as follows: SWC (%) = [(FW (g) − DW (g))/(DW (g))] × 100.

Relative water content

This parameter was estimated on six leaves for each treatment, just before the start of treatment and after 1, 2, 3, 4, 5, 6, and 7 weeks of the water withholding. For each measurement, leaves were freshly weighted (FW) and in a turgid state (TW), then dried (DW).RWC = [(FW−DW)/(TW−DW)] × 100

Leaf gas exchange parameters

Leaf gas exchange was measured on six leaves of the same physiological age, the third leaf after the first leaf of emergency of the same age, on sunny days from 9-11 a.m. using the portable LCi Pro+ photosynthesis unit (ADC BioScientific Ltd.), at the PAR (1000 µmol m⁻²s⁻¹). These parameters were estimated just before the start of treatment, after 1, 2, 3, 4, 5, 6, and 7 weeks of water stress.

Chlorophyll fluorescence

A portable chlorophyll fluorometer (OS-30P; Opti Science, Inc., NH, USA) was used to estimate chlorophyll fluorescence on the same leaves that were used for leaf gas exchange measurements. The device was calibrated by fixing the duration of measurement (30 s) and the light intensity (700 μS). The mode OJIP gives the fluorescence kinetics of multiphase transitions O, J, I, and P, minimal, intermediate, and maximal fluorescence levels respectively. Measurements were conducted under actinic light and after a 30-minute dark adaptation period. Fv/Fm parameters were also measured. Six measurements were taken in both states. These measurements were taken immediately after the leaf gas exchange measurements, just before the beginning of treatment, and after 1, 2, 3, 4, 5, 6, and 7 weeks of water stress.

The total chlorophyll content was measured using a chlorofluorometer (CCM 200, Chlorophyll Content Meter). The measurements were made on six leaves for each treatment of the same age, the fourth leaf after the first leaf at the emergence stage.

Statistical analysis

The data were analyzed using analysis of variance (ANOVA), according to a factor model with fixed factors. These factors were: day, treatment, and species/rootstocks. These analyses were performed using SPSS statistical software 11.5 (Statistical Package for the Social Sciences, SPSS Institute Inc., Cary, NC, USA). The SigmaPlot version 8.0 software was used to develop the different figures. The averages are represented with their standard deviations, and the significance is expressed at p <0.05.

Results

Figure 1 illustrates the variation in soil water content as a function of the duration of water stress, rootstock (Pistacia vera or Pistacia atlantica), and soil depth (30 and 60 cm). Control individuals maintained this parameter at high values throughout the experiment. On the other hand, the soil water content in water-stressed individuals gradually decreased by increasing the degree of stress (Fig. 1 A-B ). This decrease was remarkable at the end of the period of water stress (seven weeks). At the end of the test, the soil was almost dry for both depths (30 and 60 cm).

Fig. 1
Soil water content at 30 cm (A) and 60 cm (B), relative water content (C), stomatal conductance (D), net photosynthesis (E), transpiration rate (F), maximal quantum yield of PSII (FV/FM) (G) and total chlorophyll content (H) in Pistacia vera L. grafted on Pistacia atlantica Desf. irrigated (●); Pistacia vera L. grafted on Pistacia atlantica Desf. water-stressed (○); Pistacia vera L. grafted on Pistacia vera L. irrigated (▼); and Pistacia vera L. grafted on Pistacia vera L. water-stressed (▽). Bars denote the standard error. Values are means of 6 measurements.

Irrigated individuals of Pistacia vera and Pistacia atlantica rootstocks maintained leaf RWC at high and stable values during the experiment (Fig. 1 C ). Similarly, RWC remained invariable in water-stressed individuals during the first three weeks of water stress. After 21 days, the RWC decreased in both rootstocks. At the end of the water stress period, this reduction was approximately 20%.

Gs remained invariable in irrigated seedlings of both rootstocks during the test. However, the water-stressed individual of both rootstocks maintained a gs value similar to irrigated ones during the first five weeks (Fig. 1 D ). Beyond five weeks, it decreased with the increase in the water stress period. It reached 0.05 μmol m^-2s^-1 after seven weeks of water stress. The difference between rootstocks was not remarkable during the seven weeks of water stress.

As shown for the RWC and the gs, the variation of the net photosynthesis remained stable for the two rootstocks in the irrigated regime during the experimentation. In contrast, water-stressed individuals from both rootstocks maintained comparable values to controls during the first three weeks. From the third week of the applied water stress, a decrease was observed in both species by approximately 50% (Fig. 1 E ). The difference between rootstocks was not significant.

As shown in Fig. 1 F , the rate of transpiration remained invariable during the experiment in irrigated individuals of both rootstocks. On the other hand, E decreased with increasing water stress from the fourth week of irrigation withholding. This reduction was approximately 40% by the end of the water stress period, with no clear difference between the two rootstocks.

The polyphasic OJIP transient curves show that there was no clear difference between the two rootstocks throughout the experiment. The effect of water stress and the difference between the two rootstocks were not significant, neither in light-adapted nor in dark-adapted leaves (Fig. 2).

Fig. 2
Effect of water stress on chlorophyll fluorescence transient (OJIP) in dark-adapted leaves of Pistacia vera L. grafted on Pistacia atlantica Desf. irrigated (black); Pistacia vera L. grafted on Pistacia atlantica Desf. water-stressed (red); Pistacia vera L. grafted on Pistacia vera L. irrigated (green) and Pistacia vera L. grafted on Pistacia vera L. water-stressed during two months (yellow). Values are means of six measurements.

The variation in maximum photosynthetic yield of PSII as a function of water stress (Fig. 1 G ) showed that this parameter remained stable for the different applied treatments and the two rootstocks during the seven weeks of increasing water stress.

The control individuals maintained high and invariable levels of total chlorophyll content during the experiment (Fig 1 H ). Under water stress, the two rootstocks decreased this parameter, starting after four weeks of stress compared to the controls. This reduction was about 40% in PV/PVS and PV/PAS, with no notable difference between the two rootstocks.

Discussion

The comparative study of the effect of water stress and rootstock on soil water content, plant water status, leaf gas exchanges, total chlorophyll content, and maximum photosynthetic yield of PSII showed that the soil water content decreased in water-stressed individuals from the second week of water withholding compared to controls. The soil became almost dry after seven weeks without any clear difference in the identity of the rootstock. On the contrary, the water status of the plant, as visualized by the monitoring of the RWC, showed that the water-stressed individuals of the two rootstocks maintained a stable water status until three weeks of water withholding. Even at the end of the water stress period, the reduction in RWC in water-stressed individuals remained low. A high level of hydration of the plant, despite the reduction in soil water content, may indicate some mechanisms, including osmotic adjustment through the accumulation of compatible solutes (Verbeke, 2022), the limitation of transpiration, and the control of stomatal conductance (Jafari et al., 2018). The latter mechanism was observed in our results. Maintaining a high water status may be due to effective control of stomatal opening (Kholova et al.,2010) or improvement of the water status of the scion via the efficiency of water uptake by the rootstock (Solari et al., 2006; Jafari et al., 2018; Liu et al., 2019; Fullana-Pericàs et al., 2020). Also, root volume and K content may influence the relative water content of scion leaves (Jafari et al., 2018). According to Del Carmen et al. (2010), slight turgor reduction under water stress maintains Pistacia atlantica growth compared to the hybrid and P. terebinthus rootstock. Also, the recovery was faster in Pistacia atlantica.

The leaf gas exchanges were slightly reduced, with no remarkable difference between the rootstocks. In agreement with the results found by Germana (1997) who reported that Pistacia atlantica as rootstocks have higher transpiration and photosynthesis than P. terebinthus, especially in water-stressed plants, which could make them more adapted to water stress. Memmi et al. (2016) showed that P. atlantica may be a suitable rootstock for water deficit conditions compared to P. terebinthus and P. integerrima. The mechanism implicated is an efficient stomatal regulation. The maximum photosynthetic yield confirms these results. Indeed, фmax PSII was kept stable until seven weeks of water stress. On the contrary, this parameter is reduced by 3 weeks in Prunus mongolica under gradual water stress (Guo et al., 2015). The difference between rootstocks may be clear only in the long term. In this regard, Jackson (2000) and Somkuwar et al. (2015) suggest that the interaction between the scion and the rootstock usually results from the mutual translocation of nutrients and growth regulators between the graft and the rootstock. Probably, the degree of water stress imposed in this study may not be strong enough to affect physiological parameters, as shown by Del Carmen et al. (2010).

Pistacia vera grafted on P. vera L. and P. atlantica subjected to water stress at the seedling stage in field conditions, maintained a high level of hydration, slightly reduced leaf gas exchanges, and a stable maximum photosynthetic yield during the water stress period. However, there were no significant differences between the two used rootstocks under drought stress. This finding is probably due to the early age of the tested individual or to the duration of water stress. Based on our results, we recommend the investigation of other hypotheses to explain the performance of Pistacia atlantica compared to Pistacia vera rootstock.

Acknowledgments

We sincerely thank the editor and reviewers for taking the time to review our manuscript. This research has received grant funding from the Tunisian Ministry of High Education and Scientific Research.

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• Data Availability
  The datasets related to this article will be available upon request to the author

Edited by

• Editor Chef:
  Thais Almeida

• Associate Editor:
  Marina Scalon

Data availability

The datasets related to this article will be available upon request to the author

Publication Dates

• Publication in this collection
  28 Nov 2025
• Date of issue
  2025

History

• Received
  25 July 2023
• Accepted
  30 Dec 2024