Deciphering the drought tolerance mechanisms in citrus rootstocks

Authors

  • Muhammad SOHAIL Department of Horticulture, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan-60800 (PK)
  • Hossam S. EL-BELTAGI Agricultural Biotechnology Department, College of Agriculture and Food Sciences, King Faisal University, Al-Ahsa 31982; Biochemistry Department, Faculty of Agriculture, Cairo University, Giza 12613 (SA)
  • Sajjad HUSSAIN Department of Horticulture, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan-60800; Citrus Center, Texas A&M University Kingsville, Weslaco 78596, Texas (US)
  • Altaf HUSSAIN Directorate of Agriculture Research, Sibi, Balochistan (PK)
  • Ehsan ALI Department of Forestry and Range Management, Faculty of Agricultural Sciences, Bahauddin Zakariya University, Multan 60800 (PK)
  • Shakeel AHMAD Institute of Agronomy, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan 60800 (PK)
  • Muhammad N. SHAH Department of Agriculture, Government College University, Lahore (PK)
  • Vicent ARBONA Departament de Biologia, Bioquímica i Ciències Naturals, Universitat Jaume I, Castelló de la Plana (ES)
  • Muhammad F. KHALID Environmental Science Centre, Qatar University, Doha 2713 (QA)

DOI:

https://doi.org/10.15835/nbha52414124

Keywords:

antioxidant defense, citrus rootstocks, osmotic adjustment, transpiration, water deficit

Abstract

An increasing amount of land is becoming unsuitable for citrus cultivation, mainly due to water scarcity. This study evaluated the physiological and biochemical performance of trifoliate orange (Poncirus trifoliata) and rough lemon (Citrus jambhiri) seedlings subjected to water deficit for 12 days. Under these conditions, trifoliate orange was more sensitive than rough lemon and exhibited significant changes in LRWC (64.8% vs 36.7%), gas exchange parameters (71.7% vs 54.3% on average), leaf surface area (18.2% vs 4.9%), chlorophyll fluorescence in dark- and light-adapted leaves (44.5% vs 33.3% on average) and non-photochemical quenching (94.3% vs 28.2%). Moreover, oxidative stress indicators, such as malondialdehyde or hydrogen peroxide, indicated significantly higher values in trifoliate orange than in rough lemon seedlings. They also showed lower antioxidant defense activation. Other biochemical parameters, such as proline, glycine betaine, antioxidant capacity, phenolic content, and total soluble proteins, showed higher levels in rough lemon than in trifoliate orange seedlings. Overall, the better performance of rough lemon in arid conditions could be attributed to its improved ability to prevent water loss and maintain tissue water content. In addition, rough lemon has a more robust antioxidant defense to keep production of reactive oxygen species at low levels.

References

Alipour H, HoseinBeyki A, Jahed M, Rahnama H, Sharifnia M (2013). A review on citrus production and export marketing strategies in Mazandaran province, Iran. Middle-East of Scientific Research 14(10):1375-1380. https://doi.org/10.5829/idosi.mejsr.2013.14.10.3558

Arbona V, Zandalinas SI, Manzi M, González-Guzmán M, Rodriguez PL, Gómez-Cadenas A (2017). Depletion of abscisic acid levels in roots of flooded Carrizo citrange (Poncirus trifoliata L. Raf. × Citrus sinensis L. Osb.) plants is a stress-specific response associated to the differential expression of PYR/PYL/RCAR receptors. Plant Molecular Biology 93:623-640. https://doi.org/10.1007/s11103-017-0587-7

Arnon DI (1949). Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24(1):1-15. https://doi.org/10.1104/pp.24.1.1

Asada K (1999). The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Biology 50(1):601-639. https://doi.org/10.1146/annurev.arplant.50.1.601

Balal RM, Khan MM, Shahid MA, Mattson NS, Abbas T, Ashfaq M, Garcia-Sanchez F, Ghazanfer U, Gimeno V, Iqbal Z. (2012). Comparative studies on the physiobiochemical, enzymatic, and ionic modifications in salt-tolerant and salt-sensitive citrus rootstocks under NaCl stress. Journal of the American Society for Horticultural Science 137(2):86-95. https://doi.org/10.21273/JASHS.137.2.86

Bates LS, Waldren RA, Teare ID (1973). Rapid determination of free proline for water-stress studies. Plant and Soil 39(1):205-207. https://doi.org/10.1007/BF00018060

Bjorkman O, Demming B (1987). Photon yield of oxygen evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origin. Planta 170:489-504. https://doi.org/10.1007/BF00402983

Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72(1-2):248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Chance B, Maehly AC (1955). Assay of catalases and peroxidases. Methods in Enzymology 2:764-775. http://dx.doi.org/10.1016/S0076-6879(55)02300-8

Chaves MM, Flexas J, Pinheiro C (2009). Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103(4):551-560. https://doi.org/10.1093/aob/mcn125

Colmenero-Flores JM, Arbona V, Morillon R, Gómez-Cadenas A 2020. In: Talon Manuel (ed.), Caruso Marco (ed.), Gmitter Fred (ed.). The genus Citrus. Amsterdam: Elsevier, pp 291-309. https://doi.org/10.1016/B978-0-12-812163-4.00014-0

Demiral T, Türkan I (2005). Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environmental and Experimental Botany 53(3):247-257. https://doi.org/10.1016/j.envexpbot.2004.03.017

dos Santos IC, de Almeida AA, Pirovani CP, Costa MG, da Conceição AS, dos Santos Soares Filho W, Coelho Filho MA, Gesteira AS (2019). Physiological, biochemical and molecular responses to drought conditions in field-grown grafted and ungrafted citrus plants. Environmental and Experimental Botany 162:406-420. https://doi.org/10.1016/j.envexpbot.2019.03.018

El‐Beltagi HS, Eshak NS, Mohamed HI, Bendary ESA, Danial AW (2022a). Physical characteristics, mineral content, and antioxidant and antibacterial activities of Punica granatum or Citrus sinensis peel extracts and their applications to improve cake quality. Plants 11:1740. https://doi.org/10.3390/plants11131740

El-Beltagi HS, Ahmad I, Basit A, Shehata WF, Hassan U, Shah ST, … Mohamed HI (2022b). Ascorbic acid enhances growth and yield of sweet peppers (Capsicum annum) by mitigating salinity stress. Gesunde Pflanzen 74:423-433. https://doi.org/10.1007/s10343-021-00619-6

El-Beltagi HS, Ahmad I, Basit A, Abd El-Lateef HM, Yasir M, Tanveer SS, Ullah I, Elsayed MMM, Ali I, Ali F, Ali S, Aziz I, Kandeel M, Ikram MZ (2022c). Effect of Azospirillum and Azotobacter species on the performance of cherry tomato under different salinity levels. Gesunde Pflanzen 74: 487. https://doi.org/10.1007/s10343-022-00625-2

El-Beltagi HS, El-Naqma KA, Al-Daej MI, El-Afry MM, Shehata WF, El-Nady MF, … Metwaly MMS (2024). Effects of zinc nanoparticles and proline on growth, physiological and yield characteristics of pea (Pisum sativum L.) irrigated with diluted seawater. Cogent Food & Agriculture 10:2348695. https://doi.org/10.1080/23311932.2024.2348695.

FAOSTAT (2020). Available online at: FAOSTAT (accessed Jan 10, 2022).

Foyer CH, Halliwell B (1976). The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21-25. https://doi.org/10.1007/BF00386001

Giannopolitis CN, Ries SK (1977). Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59(2):309-314. https://doi.org/10.1104/pp.59.2.309

Gowda VR, Henry A, Yamauchi A, Shashidhar HE, Serraj R (2011). Root biology and genetic improvement for drought avoidance in rice. Field Crops Research 122(1):1-13. https://doi.org/10.1016/j.fcr.2011.03.001

Grieve CM, Grattan SR (1983). Rapid assay for determination of water-soluble quaternary ammonium compounds. Plant and Soil 70(2):303-307. https://doi.org/10.1007/BF02374789

Harborne JB (1973). Phenolic compounds. In: Harborne JB (Ed). Phytochemical Methods, Springer, Amsterdam, pp 33-88. https://doi.org/10.1007/978-94-009-5921-7

Heath RL, Packer L (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125(1):189-198. https://doi.org/10.1016/0003-9861(68)90654-1

Hu H, Xiong L (2014). Genetic engineering and breeding of drought-resistant crops. Annual Review of Plant Biology 65:715-741. https://doi.org/10.1146/annurev-arplant-050213-040000

Hussain S, Khalid MF, Ali MA, Ahmed N, Hasanuzzaman M, Ahmad S (2022). Citrus Production: Technological Advancements and Adaptation to Changing Climate. CRC Press. https://doi.org/10.1201/9781003119852

Hussain S, Khalid MF, Saqib M, Ahmad S, Zafar W, Rao MJ, Morillon R, Anjum MA (2018). Drought tolerance in citrus rootstocks is associated with better antioxidant defense mechanism. Acta Physiologiae Plantarum 40:135. https://doi.org/10.1007/s11738-018-2710-z

Jacquemond C, Blondel L (1986). Contribution to the study of citrus rootstocks: Poncirus trifoliata. Part 1.: study of botanical characters. Fruits (France). 41(5):303-339. https://revues.cirad.fr/index.php/fruits

Khalid MF, Hussain S, Anjum MA, Morillon R, Ahmad S, Ejaz S, Hussain M, Jaafar HZ, Alrashood ST, Ormenisan AN (2021). Physiological and biochemical responses of Kinnow mandarin grafted on diploid and tetraploid Volkamer lemon rootstocks under different water-deficit regimes. PloS One 16(4):e0247558. https://doi.org/10.1371/journal.pone.0247558

Khalid MF, Shafqat W, Khan RI, Abbas M, Ahmed T, Ahmad S, Hussain S (2022). Citrus Responses and Tolerance against Temperature Stress. In Citrus Production: Technological Advancements and Adaptation to Changing Climate. CRC Press. 149-155. https://doi.org/10.1201/9781003119852-10

Khalid MF, Vincent C, Morillon R, Anjum MA, Ahmad S, Hussain S (2021). Different strategies lead to a common outcome: different water-deficit scenarios highlight physiological and biochemical strategies of water-deficit tolerance in diploid versus tetraploid Volkamer lemon. Tree Physiology 41(12):2359-2374. https://doi.org/10.1093/treephys/tpab074

Khoshbakht D, Asghari MR, Haghighi M (2018). Effects of foliar applications of nitric oxide and spermidine on chlorophyll fluorescence, photosynthesis and antioxidant enzyme activities of citrus seedlings under salinity stress. Photosynthetica 56(4):1313-1325. https://doi.org/10.1007/s11099-018-0839-z

López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2008). Relationship between salt tolerance and photosynthetic machinery performance in citrus. Environmental and Experimental Botany 62(2):176-184. https://doi.org/10.1016/j.envexpbot.2007.08.002

Merah O (2001). Potential importance of water status traits for durum wheat improvement under Mediterranean conditions. The Journal of Agricultural Science 137(2):139-145. https://doi.org/10.1017/S0021859601001253

Miranda MT, Espinoza-Núñez E, Silva SF, Pereira L, Hayashi AH, Boscariol-Camargo RL, … Ribeiro RV (2022). Water stress signaling and hydraulic traits in three congeneric citrus species under water deficit. Plant Science 319:111255. https://doi.org/10.1016/j.plantsci.2022.111255

Mittler R (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7(9):405-410. https://doi.org/10.1016/S1360-1385(02)02312-9

Nakano Y, Asada K (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22(5):867-880. https://doi.org/10.1093/oxfordjournals.pcp.a076232

Nilsen ET, Freeman J, Grene R, Tokuhisa J (2014). A rootstock provides water conservation for a grafted commercial tomato (Solanum lycopersicum L.) line in response to mild-drought conditions: a focus on vegetative growth and photosynthetic parameters. PLoS One 9(12):e115380. https://doi.org/10.1371/journal.pone.0115380

Noctor G, Foyer CH (1998). Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Biology 49(1):249-279. https://doi.org/10.1146/annurev.arplant.49.1.249

Osório ML, Osório J, Vieira AC, Gonçalves S, Romano A (2011). Influence of enhanced temperature on photosynthesis, photooxidative damage, and antioxidant strategies in Ceratonia siliqua L. seedlings subjected to water deficit and rewatering. Photosynthetica 49(1):3-12. https://doi.org/10.1007/s11099-011-0001-7

Oustric J, Quilichini Y, Morillon R, Herbette S, Luro F, Giannettini J, Berti L, Santini J (2019). Tetraploid citrus seedlings subjected to long-term nutrient deficiency are less affected at the ultrastructural, physiological and biochemical levels than diploid ones. Plant Physiology and Biochemistry 135:372-384. https://doi.org/10.1016/j.plaphy.2018.12.020

Özgen M, Scheerens JC, Reese RN, Miller RA (2010). Total phenolic, anthocyanin contents and antioxidant capacity of selected elderberry (Sambucus canadensis L.) accessions. Pharmacognosy Magazine 6(23):198. https://doi.org/10.4103/0973-1296.66936

Pérez-Pérez JG, Robles JM, Tovar JC, Botía P (2009). Response to drought and salt stress of lemon ‘Fino 49’under field conditions: water relations, osmotic adjustment and gas exchange. Scientia Horticulturae 122(1):83-90.

Ramadan KMA, El-Beltagi HS, El-Mageed TAA, Saudy HS, Al-Otaibi HH, Mahmoud MAA (2023). The changes in various physio-biochemical parameters and yield traits of faba bean due to humic acid plus 6-benzylaminopurine application under deficit irrigation. Agronomy 13,1227. https://doi.org/10.3390/agronomy13051227

Rao MJ, Zuo H, Xu Q (2021). Genomic insights into citrus domestication and its important agronomic traits. Plant Communications 2(1):100138. https://doi.org/10.1016/j.xplc.2020.100138

Ruiz-Sánchez MC, Domingo R, Savé R, Biel C, Torrecillas A (1997). Effects of water stress and rewatering on leaf water relations of lemon plants. Biologia Plantarum 39:623-631. https://doi.org/10.1023/A:1000943218256

Sambrook J, Russell DW (2006). In vitro mutagenesis using double-stranded DNA templates: selection of mutants with DpnI. Cold Spring Harbor Protocols. https://doi.org/10.1101/pdb.prot3813

Santos IC, Almeida AA, Anhert D, Conceição AS, Pirovani CP, Pires JL, Valle RR, Baligar VC (2014). Molecular, physiological and biochemical responses of Theobroma cacao L. genotypes to soil water deficit. PLoS One 9(12):e115746. https://doi.org/10.1371/journal.pone.0115746

Seday U, Gulsen O, Uzun AY, Toprak GÜ (2014). Response of citrus rootstocks to different salinity levels for morphological and antioxidative enzyme activities. Journal of Animal & Plant Sciences 24(2):512-520.

Shafqat W, Jaskani MJ, Maqbool R, Khan AS, Ali Z (2019). Evaluation of citrus rootstocks against drought, heat and their combined stress based on growth and photosynthetic pigments. International Journal of Agriculture and Biology 22(5):1001-1009. https://doi.org/10.17957/IJAB/15.1160

Shalaby TA, Taha NA, Rakha MT, El-Beltagi HS, Shehata WF, Ramadan KMA, El-Ramady H, Bayoumi, YA (2022). Can Grafting Manage FusariumWilt Disease of Cucumber and Increase Productivity under Heat Stress? Plants 11:1147. https://doi.org/10.3390/plants11091147

Simova-Stoilova L, Demirevska K, Petrova T, Tsenov N, Feller U (2008). Antioxidative protection in wheat varieties under severe recoverable drought at seedling stage. Plant, Soil and Environment 54(12):529-536. https://doi.org/10.17221/427-PSE

Smirnoff N (1993). The role of active oxygen in the response of plants to water deficit and desiccation. New Phytologist 125(1):27-58. https://doi.org/10.1111/j.1469-8137.1993.tb03863.x

Sulistiawati NP, Rai IN, Ign S, Astarini IA (2014). Phenophyology studies in efforts produced off season citrus (Citrus nobilis var, microcarpa). International Journal on Advanced Science, Engineering and Information Technology 4:56-61. https://doi.org/10.18517/ijaseit.4.6.462.

Syvertsen JP, Garcia-Sanchez F (2014). Multiple abiotic stresses occurring with salinity stress in citrus. Environmental and Experimental Botany 103:128-137. https://doi.org/10.1016/j.envexpbot.2013.09.015

Tudela D, Primo-Millo E (1992). 1-Aminocyclopropane-1-carboxylic acid transported from roots to shoots promotes leaf abscission in Cleopatra mandarin (Citrus reshni Hort. ex Tan.) seedlings rehydrated after water stress. Plant Physiology 100(1):131-137. https://doi.org/10.1104/pp.100.1.131

Velikova V, Yordanov I, Edreva AJ (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science 151(1):59-66. https://doi.org/10.1016/S0168-9452(99)00197-1

Verslues PE, Agarwal M, Katiyar‐Agarwal S, Zhu J, Zhu JK (2006). Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal 45(4):523-539. https://doi.org/10.1111/j.1365-313X.2005.02593.x

Yahmed JB, Costantino G, Amiel P, Talón M, Ollitrault P, Morillon R, Luro F (2015). Diversity in the trifoliate orange taxon reveals two main genetic groups marked by specific morphological traits and water deficit tolerance properties. The Journal of Agricultural Science 154: 495-514. https://doi.org/10.1017/S0021859615000234

Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A (2017). Modulation of antioxidant defense system is associated with combined drought and heat stress tolerance in citrus. Frontiers in Plant Science 8:953. https://doi.org/10.3389/fpls.2017.00953

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Published

2024-11-04

How to Cite

SOHAIL, M., EL-BELTAGI, H. S., HUSSAIN, S., HUSSAIN, A., ALI, E., AHMAD, S., SHAH, M. N., ARBONA, V., & KHALID, M. F. (2024). Deciphering the drought tolerance mechanisms in citrus rootstocks. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 52(4), 14124. https://doi.org/10.15835/nbha52414124

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DOI: 10.15835/nbha52414124

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