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Article

Physiological Influence of Water Stress Conditions on Novel HLB-Tolerant Citrus Rootstocks

by
Juan M. Arjona-López
1,*,†,
Lidia Aparicio-Durán
1,†,
Frederick G. Gmitter, Jr.
2,
Estefanía Romero-Rodríguez
1,
Jude W. Grosser
2,
Aurea Hervalejo
1 and
Francisco J. Arenas-Arenas
1
1
Department of Agri-Food Engineering and Technology, Andalusian Institute of Agricultural and Fisheries Research and Training (IFAPA), “Las Torres” Center, Ctra. Sevilla-Cazalla de la Sierra km. 12.2, 41200 Seville, Alcalá del Río, Spain
2
Citrus Research and Education Center, Department of Horticultural Sciences, IFAS, University of Florida, Lake Alfred, FL 33850, USA
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2023, 13(1), 63; https://doi.org/10.3390/agronomy13010063
Submission received: 2 November 2022 / Revised: 16 December 2022 / Accepted: 20 December 2022 / Published: 24 December 2022
(This article belongs to the Special Issue Water Scarcity Management in Fruit Orchards: Potential Benefits on Fruit Quality and Long-Term Orchards Conservation)
Browse Figures
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Abstract

:
Citrus are one of the most relevant fruit crops in the Mediterranean basin, which is the second-highest citrus-growing region in the world. However, these crops are mainly grown under Mediterranean semi-arid conditions, characterized by long periods of drought and torrential rain. In this work, we have assessed the response of three promising HLB-tolerant citrus rootstocks (Orange-14, UFR-1, and B11R3T27) to the application of four water stress conditions (Control, Mild water stress, Drought, and Flooding), comparing them with Carrizo citrange. Aerial plant symptoms were recorded during the experimental period, whereas plant water parameters, including stomatal conductance, leaf water potential, and relative water content, were obtained at the end of the assay. For all assessed rootstocks and variables, drought treatment was the most limiting factor, with Carrizo citrange being the most suitable rootstock under this condition. Flooding was the second restrictive treatment, in which UFR-1 was the least affected rootstock. Mid-water stress with 50% water requirements did not differ from the Control treatment, which can help save water resources in semi-arid regions. This information can be helpful for the citrus industry to increase the efficiency of citrus crops subject to water stress in semi-arid regions.

1. Introduction

Citrus crops are one of the most financially and socially relevant fruit crops in the Mediterranean and subtropical regions. Thus, Mediterranean basin countries rank second in citrus production worldwide after China, with over 26 million tons [1]. In the Mediterranean region, citrus crops are grown chiefly under a semi-arid climate, and irrigation systems are thus required to obtain optimum production [2,3]. Under Mediterranean semi-arid conditions, the rainfall regime is characterized by a high temporal variability with long periods of drought in summer [4], which further aggravate soil desertification in this region [5,6]. In addition, because the soils mostly feature high clay content, a reduced drainage rate is also apparent [7,8].
Low water availability for plants is a major abiotic factor for agricultural production [9]. Specific to citrus, the crops are highly sensitive to long-term drought, which may severely affect their growth and development [10]. Drought induces complete stomatal closure, consequently reducing the transpiration rate/net CO2 assimilation rate. It may also cause increased cell respiration and thereby affect the internal leaf temperature [11,12]. First, citrus plants close their stomata under water scarcity, thus reducing stomatal conductance, water transpiration, and photosynthetic capacity [13,14]. Should this negative abiotic stress continue, the growth, fruit production and/or juice quality of citrus trees decreases [15,16].
Similarly, citrus crops are described as vulnerable to long-term flooding or waterlogging conditions, which can cause major financial losses [17]. This abiotic stress reduces the availability of root oxygen, diminishing plant growth, stomatal conductance, and photosynthesis [3,18]. Therefore, fruit production and quality can decrease under long-term flooding conditions.
In semi-arid regions, accurate irrigation water application is an essential practice due to the fact that water resources are limited and must be optimized. The application of a short water stress period (mild water stress) can improve fruit production on trees because they grow faster upon re-watering than those that are watered extensively as per crop requirements; the application of a water stress period in orange trees led to a growth that was higher than in those that are not subject to water stress [19,20,21,22].
Furthermore, citrus orchards in the Mediterranean basin are threatened by the occurrence risk of emerging diseases. Huanglongbing, or citrus greening disease (HLB), caused by three phytopathogenic and phloem-restricted bacteria from the “Candidatus Liberibacter” genus [23,24], has been reported as the most destructive citrus disease in the world [25]. HLB pathogens are chiefly and biologically transmitted by psyllid insects Trioza erytreae and Diaphorina citri [26,27,28,29]. Although none of these bacterial species have been identified in the Mediterranean basin countries [30,31], T. erytreae has been spreading across citrus trees in mainland Spain and Portugal since 2014 and 2015, respectively [32,33,34,35], whereas D. citri was identified on mandarin and orange orchards in Israel in August 2021 [31].
As with other woody crops, farmers often graft their different citrus cultivars in the most grown rootstock. In the case of Spain, the top citrus producer and exporter in the Mediterranean basin, Carrizo citrange is the most commonly used citrus rootstock [36]. Research into new planting materials, such as rootstocks, is described as a long-term effective and sustainable tool to fight abiotic and biotic factors in citrus orchards, [37] including water stress and HLB, respectively. Currently, citrus breeding programs are continuously obtaining new rootstocks to tackle these issues, and more recently address tolerance to HLB. However, this new plant material needs to undergo a preliminary assessment against typical and set abiotic disorders in Mediterranean countries. Hence, the aim of this study was to evaluate the physiological responsiveness of three novel citrus rootstocks to water stress conditions (drought, flooding, and mild water stress) compared with Carrizo citrange.

2. Materials and Methods

2.1. Plant Material and Experimental Conditions

The response of a total of 128 plants from four citrus rootstocks (non-grafted) included Orange-14 (Citrus reticulata ‘Nova’ + C. maxima HBP × C. reticulata ‘Cleopatra’ + Poncirus trifoliata) [38], UFR-1 (C. reticulata ‘Nova’ + C. maxima HBP × C. reticulata ‘Cleopatra’ + P. trifoliata) [39,40,41] and B11R3T27 (P. trifoliata ‘Flying dragon’ × C. paradisi ‘Duncan’), [42] as well as the standard-comparative rootstock Carrizo citrange (C. sinensis ‘Washington’ × P. trifoliata) [43], which is commercially available in Spain under register number 16690003 [44], were evaluated. As far as the ploidy levels are concerned, Carrizo citrange and B11R3T27 are diploid hybrids, while Orange-14 and UFR-1 are tetraploid hybrids. Citrus plants obtained from in vitro culture conditions by Agromillora Group Nursery (Subirats, Barcelona, Spain), were provided at the age of six-month-old. Once the plant material was received, each citrus plant was transferred to a 1.6-L pot with peat moss Sphagnum substrate (Organic matter over dry matter = 85–90%; Electrical conductivity = 0.5 mS cm−1; pH = 6.5–7; N = 1%; P2O5 = 0.2%; and K2O = 0.9%). All plants were subsequently maintained over a fortnightly acclimation period under greenhouse conditions, during which all were irrigated thrice a week depending on water requirements (100% irrigation), and a nutritive solution was not applied because the peat moss substrate contained sufficient nutrients to support plant growth in a short experiment of duration. The experiment was performed in a greenhouse located in “Las Torres” center of the Andalusian Institute of Agricultural and Fisheries Research and Training (IFAPA), Alcalá del Río municipality, Seville, Spain (37°30′43.3′′ N; 5°57′47.4′′ W) in the spring-summer season (May–June) of 2021 (28.60 °C and 64.90%, averaged temperature and relative humidity, respectively).

2.2. Treatments of Water Stress and Experimental Design

Reference evapotranspiration was first recorded and obtained from the greenhouse station three days a week, and citrus crop evapotranspiration was calculated in order to apply precise irrigation on Monday, Wednesday, and Friday (Table 1). Hence, four water stress treatments were applied to this experiment: Control (plants were irrigated at 100% crop evapotranspiration), Mild water stress (MWS, plants were irrigated at 50% crop evapotranspiration), Drought (plants were not irrigated during the experiment), and Flooding (plants were placed under waterlogged conditions in planter boxes under waterlogged conditions). All plants were arranged using a random design, and eight replicates (n = 8) were used per treatment and rootstock, with each plant being the experimental unit and resulting in 16 treatment combinations. The experiment started following the acclimation period and on the first day of treatment application (D1) and was completed 30 days later (D30). We carried out deep periodical assessments of aerial symptoms and at the end of the experiment, we obtained the response of plant water relation parameters such as stomatal conductance, leaf water potential, and relative water content considering a previous preliminary work [45].

2.3. Assessment of Aerial Plant Symptoms

For each plant, above-ground symptoms on leaves were recorded to estimate the effect of irrigation treatments using a 0 to 4: symptoms scale: 0, plants without symptoms; 1, plants with 25% leaves affected by chlorosis; 2, plants with 50% leaves affected by chlorosis; 3, plants with over 50% leaves affected by chlorosis; and 4, fully desiccated and dead plants. This assessment process was performed on days 1, 10, 19, 22, 26, and 30, from the first water stress treatment application until the end of the experiment. All data obtained in this assessment process were used to calculate the standardized area under the abiotic stress progress curve (SAUASPC) [46], using the following equations:
AUASPC = ∑ i − 1 n − 1 y i + y i + 1 2 × ( t i + 1 − t i )
where yi is an assessment of aerial plant symptoms at the corresponding evaluation day (i), and n is the total number of observations days.
SAUASPC = A U A S P C ∑ t
where ∑ t is the total number of assessment days.

2.4. Assessment Plant Water Relation Parameters

2.4.1. Stomatal Conductance

On the last day of the experiment (D30), stomatal conductance (gs) was measured from two leaves per plant for a total of three plants. For this, a Leaf Porometer SC-1 was used (Deacon Devices, Pullman, WA, USA) [47].

2.4.2. Leaf Water Potential

Leaf water potential (LWP) was recorded at D30 from one leaf per plant for a total of three plants. For this assessment process, a Pump-Up Scholander chamber (PMS Instrument Company, Albany, OR, USA) [48] was used.

2.4.3. Relative Water Content

Relative water content (RWC) was obtained from leaves on four plants per rootstock and treatment at the end of the experiment (D30). The assessment process was carried out on two leaves per plant, collecting two discs 1 cm in diameter per leaf. The group of four discs per plant was weighed using a digital precision electronic scale Series 5134 IN (Nahita, Columbus, OH, USA). All groups of discs were covered with distilled water for 4 h in dark conditions at room temperature and weighed again. Each group of discs was subsequently placed in a labeled paper envelope and dried at 80 °C for 24 h in an oven and weighed again. Finally, the RWC was calculated using the following equation [49]:
R W C = ( W − D W ) ( T W − D W ) × 100
where W is the fresh weight of the four discs per each citrus rootstock and treatment; TW is the weight of the four turgent discs after 4 h in distilled water; DW is the dry weight of the four discs under oven conditions.

2.5. Statistical Analysis

All data obtained to calculate SAUASPC and stomatal conductance were analyzed by two-way ANOVA (Analysis of variance), and LWP and RWC data were analyzed by one-way ANOVA using the free software R version 4.1.2 [50]. Mean separations were obtained using the LSD-Fisher test (p < 0.05) [51] through the “agricolae” package [52]. The figures were also plotted with the same free software version, using the “ggplot2” package [53].

3. Results

3.1. Plant Symptoms

Plant symptoms response with the SAUASPC reported statistical differences among citrus rootstocks and treatments. No citrus rootstock displayed any symptoms in the control treatment during the experiment assessment. Similarly, Carrizo citrange and UFR-1 showed the same response in the MWS treatment and control. A low symptoms incidence was identified in Orange-14 and B11R3T27 under MWS, without significant differences compared with the control response. Under drought conditions, Orange-14 displayed the highest symptoms rate compared with other citrus rootstocks and treatments, followed by UFR-1 and B11R3T27. On the contrary, the lowest symptoms incidence was shown by Carrizo citrange, with statistical differences compared with Orange-14 under drought conditions. Conversely, Carrizo was statistically on par with Orange-14 under flooding conditions (Table 2).

3.2. Plant Water Relation Parameters

3.2.1. Stomatal Conductance

Statistical differences were detected among citrus rootstocks and treatments assayed. The highest stomatal conductance values were achieved by Carrizo citrange in the treatment control, MWS and flooding, and by B11R3T27 under control conditions. The second highest response group was found in the rootstocks B11R3T27 under MWS and flooding conditions, and Orange-14 under control conditions. This response was followed by UFR-1 under control and MWS conditions, and Orange-14 under MWS conditions. Finally, the lowest significant stomatal conductance values were achieved under drought conditions for all rootstocks, and under flooding conditions for Orange-14 (Table 3).

3.2.2. Leaf Water Potential

For all citrus rootstocks, the lowest LWP response was obtained under the drought treatment followed by flooding treatment, but only statistical differences were found among the treatments in Carrizo citrange and Orange-14. Carrizo citrange showed the highest significant rate with MWS compared with the drought and flooding treatments, and without significant differences compared with the control. For Orange-14, the highest statistical LWP rate was achieved by control and MWS, compared with the lowest response, which was obtained in the drought and flooding treatments. UFR-1 and B11R3T27 did not show statistical differences among the treatments, and the highest response was accomplished in the MWS treatment for both rootstocks. Thus, Carrizo citrange, UFR-1, and B11R3T27 displayed higher values of LWP under MWS than control conditions (Figure 1).

3.2.3. Relative Water Content

Statistical differences were found in the relative water content results for each citrus rootstock. In all, the lowest significant RWC response was achieved by the drought treatment compared with the highest rate. Thus, Carrizo citrange, Orange-14, and UFR-1 displayed the two highest RWC results under the control and MWS conditions, without statistical differences between these conditions. In the case of B11R3T27, the highest statistical RWC rate was obtained under control conditions compared with the three other treatments assayed. An intermediate response was found for all rootstocks under flooding conditions, with significant differences with control and the MWS rate, except for Carrizo citrange, whereas the lowest statistical RWC result was achieved under drought conditions per citrus rootstocks compared with the other treatments, except in Carrizo citrange, which did not differ with the flooding treatment (Figure 2).

4. Discussion

In this work, we have characterized the physiological effect of four irrigation treatments on three new and one commercial citrus rootstocks, including flooding and drought conditions. In our study, drought and flooding treatment showed the highest symptom rate for all citrus rootstocks, except for Carrizo citrange, which was not significantly affected by the drought treatment. However, this comparative rootstock reported the highest symptoms under flooding treatment, during which UFR-1 was not significantly affected. In the literature, Carrizo citrange is reported to be an optimal candidate under drought conditions and provides an intermediate response under flooding conditions [54,55]. In addition and to our knowledge, the remaining rootstocks have not previously been tested against water stress conditions [54]. Nevertheless, previous research carried out by this group in the summer of 2020 pointed out that B11R5T60, another citrus rootstock obtained by the CREC, reported a better response under the application of water stress treatments than Carrizo citrange [45].
As with symptoms, the lowest stomatal conductance response was found under drought conditions for all rootstocks, followed by flooding treatment. Nevertheless, Carrizo citrange and B11R3T27 did not close completely their stomata under flooding conditions, probably this is an avoiding mechanism to tolerate flooding conditions.
Regarding LWP and RWC results, the drought condition was again the most limiting factor in all rootstocks for symptoms and stomatal conductance, as described above. In line with the results obtained for stomatal conductance, all rootstocks reduced their values of LWP under severe water deprivation; thus closing the stomata very rapidly [56]. Concerning RWC, this parameter could provide plant cell water status information [57,58]. Thus, all rootstocks displayed the lowest value under drought conditions; however, Carrizo citrange accomplished a higher rate of water content at this limiting water treatment than the others citrus rootstocks.
On the other hand, the mild water stress treatment did not negatively affect the development of citrus rootstocks and showed statistically comparable results to those of the control in all parameters. This incidence could be beneficial in semi-arid regions to save water in agriculture production, where irrigation requirements are a limiting factor for citrus crops in Spain [59].

5. Conclusions

Our work provides preliminary information for citrus growers selecting rootstocks in those regions with drought and flooding problems, such as semi-arid regions, where saving water resources is a priority. Under drought and flooding conditions, the optimal choice is Carrizo citrange and UFR-1, respectively. In addition, all these four rootstocks are suitable for adapting to mild water stress periods, reporting similar behavior as those with 100% water requirements, except for B11R3T27 for RWC. Thus, new citrus rootstocks are a preliminary option for saving water resources in semi-arid regions and increasing rootstock diversity to combat biotic factors, such as HLB, in those areas with this problem or its risk of occurrence. Consequently, all these citrus rootstocks need further characterization regarding their water requirements, fruit yield, and quality under field conditions.

Author Contributions

Conceptualization, F.J.A.-A.; methodology, L.A.-D. and F.J.A.-A.; software, J.M.A.-L.; validation, J.M.A.-L., L.A.-D. and F.J.A.-A.; formal analysis, J.M.A.-L., L.A.-D. and E.R.-R.; investigation, J.M.A.-L., L.A.-D. and E.R.-R.; resources, F.G.G.J., J.W.G. and F.J.A.-A.; data curation, J.M.A.-L., L.A.-D. and E.R.-R.; writing—original draft preparation, J.M.A.-L. and L.A.-D.; writing—review and editing, F.G.G.J., J.W.G., A.H. and F.J.A.-A.; visualization, J.M.A.-L. and L.A.-D.; supervision, F.J.A.-A.; project administration, F.J.A.-A.; funding acquisition, F.J.A.-A. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the research contract CEM 38/2018 from Agromillora Catalana.

Data Availability Statement

Not applicable.

Acknowledgments

We are highly thankful to Agromillora Group for providing the plant material, including Mariàngela Mestre and Joan Torrent.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 13 00063 g001 550
Figure 1. Mean leaf water potential (LWP; MPa) on four citrus rootstocks (Carrizo citrange, Orange-14, UFR-1, and B11R3T27) under four water conditions treatments (Control, MWS, Drought, and Flooding) at the end of the experiment. Values in columns with different letters denote statistical differences among the treatments per citrus rootstock by LSD-Fisher’s test (p < 0.05). MWS: Mild water stress; ns: not significant differences.
Figure 1. Mean leaf water potential (LWP; MPa) on four citrus rootstocks (Carrizo citrange, Orange-14, UFR-1, and B11R3T27) under four water conditions treatments (Control, MWS, Drought, and Flooding) at the end of the experiment. Values in columns with different letters denote statistical differences among the treatments per citrus rootstock by LSD-Fisher’s test (p < 0.05). MWS: Mild water stress; ns: not significant differences.
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Agronomy 13 00063 g002 550
Figure 2. Mean relative water content (RWC; %) on four citrus rootstocks (Carrizo citrange, Orange-14, UFR-1, and B11R3T27) under four water conditions treatments (Control, MWS, Drought, and Flooding) at the end of the experiment. Values in columns with different letters denote statistical differences among the treatments per each citrus rootstock by LSD-Fisher’s test (p < 0.05). MWS: Mild water stress.
Figure 2. Mean relative water content (RWC; %) on four citrus rootstocks (Carrizo citrange, Orange-14, UFR-1, and B11R3T27) under four water conditions treatments (Control, MWS, Drought, and Flooding) at the end of the experiment. Values in columns with different letters denote statistical differences among the treatments per each citrus rootstock by LSD-Fisher’s test (p < 0.05). MWS: Mild water stress.
Agronomy 13 00063 g002
Table
Table 1. Crop coefficients for irrigation water calculation during the experimental period.
Table 1. Crop coefficients for irrigation water calculation during the experimental period.
TimeEto (mm Day−1)KcEtc (mm Day−1)
D15.850.452.63
D35.360.452.41
D55.750.452.59
D96.780.453.05
D127.550.453.40
D156.700.453.02
D194.800.452.16
D224.130.451.86
D245.950.452.68
D267.200.453.24
D297.380.453.32
Eto: Reference evapotranspiration; Kc: crop coefficient; Etc: crop evapotranspiration
Table
Table 2. Mean standardized area under the abiotic stress progress curve (SAUASPC) during the 30-day of assessment.
Table 2. Mean standardized area under the abiotic stress progress curve (SAUASPC) during the 30-day of assessment.
Treatment
RootstockControlMWSDroughtFlooding
Carrizo citrange0.00 ± 0.00 h0.00 ± 0.00 h0.20 ± 0.04 fg0.50 ± 0.08 cd
Orange-140.00 ± 0.00 h0.03 ± 0.03 h0.98 ± 0.08 a0.66 ± 0.10 bc
UFR-10.00 ± 0.00 h0.00 ± 0.00 h0.77 ± 0.11 b0.26 ± 0.06 ef
B11R3T270.00 ± 0.00 h0.03 ± 0.03 gh0.78 ± 0.10 b0.41 ± 0.07 de
Values with different letters denote statistical differences among citrus rootstocks and treatments by LSD-Fisher’s test (p < 0.05). MWS: Mild water stress.
Table
Table 3. Mean stomatal conductance values (mmol m−2 s−1) on four citrus rootstocks (Carrizo citrange, Orange-14, UFR-1, and B11R3T27) under four water conditions treatments (Control, MWS, Drought, and Flooding) at the end of the experiment.
Table 3. Mean stomatal conductance values (mmol m−2 s−1) on four citrus rootstocks (Carrizo citrange, Orange-14, UFR-1, and B11R3T27) under four water conditions treatments (Control, MWS, Drought, and Flooding) at the end of the experiment.
Treatment
RootstockControlMWSDroughtFlooding
Carrizo citrange205.32 ± 20.82 a184.33 ± 12.77 ab43.32 ± 7.60 f172.63 ± 34.21 ab
Orange-14123.23 ± 15.02 cd98.00 ± 1.98 de41.67 ± 3.28 f36.23 ± 1.54 f
UFR-1102.00 ± 17.67 de97.87 ± 7.95 de46.17 ± 10.15 f69.35 ± 22.10 fe
B11R3T27187.28 ± 16.39 ab158.75 ± 13.46 bc44.93 ± 4.67 f117.48 ± 0.83 cd
Values with different letters denote statistical differences among citrus rootstocks and treatments by LSD-Fisher’s test (p < 0.05). MWS: Mild water stress.
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MDPI and ACS Style

Arjona-López, J.M.; Aparicio-Durán, L.; Gmitter, F.G., Jr.; Romero-Rodríguez, E.; Grosser, J.W.; Hervalejo, A.; Arenas-Arenas, F.J. Physiological Influence of Water Stress Conditions on Novel HLB-Tolerant Citrus Rootstocks. Agronomy 2023, 13, 63. https://doi.org/10.3390/agronomy13010063

AMA Style

Arjona-López JM, Aparicio-Durán L, Gmitter FG Jr., Romero-Rodríguez E, Grosser JW, Hervalejo A, Arenas-Arenas FJ. Physiological Influence of Water Stress Conditions on Novel HLB-Tolerant Citrus Rootstocks. Agronomy. 2023; 13(1):63. https://doi.org/10.3390/agronomy13010063

Chicago/Turabian Style

Arjona-López, Juan M., Lidia Aparicio-Durán, Frederick G. Gmitter, Jr., Estefanía Romero-Rodríguez, Jude W. Grosser, Aurea Hervalejo, and Francisco J. Arenas-Arenas. 2023. "Physiological Influence of Water Stress Conditions on Novel HLB-Tolerant Citrus Rootstocks" Agronomy 13, no. 1: 63. https://doi.org/10.3390/agronomy13010063

APA Style

Arjona-López, J. M., Aparicio-Durán, L., Gmitter, F. G., Jr., Romero-Rodríguez, E., Grosser, J. W., Hervalejo, A., & Arenas-Arenas, F. J. (2023). Physiological Influence of Water Stress Conditions on Novel HLB-Tolerant Citrus Rootstocks. Agronomy, 13(1), 63. https://doi.org/10.3390/agronomy13010063

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