Abstract
The aim of the present study is to investigate the contribution of mycorrhization to the resilience of olive trees to drought. One-year-old olive plants were inoculated (Myc+) or not (Myc−) with arbuscular mycorrhizal fungi (AMF), and subjected to a 40-day-drought period. At regular intervals of the watering-off period and after rehydration period, water relations and gas exchanges parameters were measured. Similarly, the total soluble sugars, proline, and mineral nutrients concentrations were determined. The results revealed that Myc+ plants were less affected by drought than Myc− plants proving the involvement of the AMF in the alleviation of drought impact on olive tree. In fact, the turgor potential (Ψp) in Myc+ plants exhibited positive values during the whole treatment period, while Ψp in Myc− plants was negative mainly under severe stress intensity. Moreover, the stomatal function of Myc+ plants was less affected by drought compared to Myc− plants. The maximum of mycorrhizas relative drought alleviation rate (RDAR) was estimated to be 40% for Ψpd and RWC, 36% for the osmotic potential (ΨS), 86% for Ψp, 16% for gs, and 27% for E. The osmotic adjustment by proline was earlier in Myc+ plants than in Myc− ones. The inoculation with AMF also improved mineral uptake (K, N, Zn, and Fe). After 40 days of drought, Myc+ plants survive but not Myc− ones. In addition, the restoration of the irrigation permitted the Myc+ plants to recuperate from severe drought stress. To sum up, inoculation of young olive trees with the AMF improved their resilience to drought.
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Abbreviations
- RDAR:
-
Relative drought alleviation rate
- \( {\text{DI}}_{{{\text{Myc}}^{ - } }} \) :
-
Drought impact in non-mycorrhizal plants
- \( {\text{DI}}_{{{\text{Myc}}^{ + } }} \) :
-
Drought impact in mycorrhizal plants
References
Abbaspour H, Saeidi-Sar S, Afshari H, Abdel-Wahhab MA (2012) Tolerance of Mycorrhiza infected Pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J Plant Physiol 169:704–709
Abohatem M, Chakrafi F, Jaiti F, Dihazi A, Baaziz M (2011) Arbuscular mycorrhizal fungi limit incidence of Fusarium oxysporum f.sp. albedinis on date palm seedlings by increasing nutrient contents, total phenols and peroxidase activities. Open Hortic J 4:10–16
Allen JW, Shachar-Hill Y (2009) Sulfur transfer through an arbuscular mycorrhiza. Plant Physiol 149:549–560
Arnould P, Hotyat M (2003) Eau et environnement: Tunisie et milieux méditerranéens. ENS ed., Lyon
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42
Augé RM, Schekel KA, Wample RL (1986) Osmotic adjustment in leaves of VA mycorrhizal and non-mycorrhizal rose plants in response to drought stress. J Plant Physiol 82:765–770
Augé RM, Foster JG, Loescher WH, Stodola AW (1992) Symplastic sugar and free amino acid molality of Rosa roots with regard to mycorrhizal colonization and drought. Symbiosis 12:1–17
Azcon-Aguilar C, Barea JM (1997) Appling mycorrhiza biotechnology to horticulture: significance and potentials. Sci Hortic 68:1–24
Azcón-Aguilar C, Barea JM (2015) Nutrient cycling in the mycorrhizosphere. J Soil Sci Plant Nutr 25(2):372–396
Barea JM, Palenzuela J, Cornejo P, Sánchez-Castro I, Navarro-Fernández C, Lopéz-García A, Estrada B, Azcón R, Ferrol N, Azcón-Aguilar C (2011) Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. J Arid Environ 75:1292–1301
Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1559
Bhosale KS, Shinde BP (2011) Influence of arbuscular mycorrhizal fungi on proline and chlorophyll content in Zingiber officinale Rosc grown under water stress. Ind J Fundam Appl Life Sci 1(3):172–176
Bompadre MJ, Rios De Molina MC, Colombo RP, Fernandez Bidondo L, Silvani VA, Pardo AG, Ocampo JA, Godeas AM (2013) Differential efficiency of two strains of the arbuscular mycorrhizal fungus Rhizophagus irregularis on olive (Olea europaea) plants under two water regimes. Symbiosis 6:105–112
Boomsma CR, Vyn TJ (2008) Maize drought tolerance: potential improvements through arbuscular mycorrhizal symbiosis? Field Crop Res 108:14–31
Boudiche S, Bornaz S, Kachouri F (2003) La compétitivité du secteur de l’huile d’olive en Tunisie: prix, qualité et avantage concurrentiel national. Jel Classification F140:Q170
Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 55:2331–2341
Bücking H, Liepold E, Ambilwade P (2012) The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes, Chapter 4. Plant Science, pp 107–138. http://dx.doi.org/10.5772/52570
Calvo-Polanco M, Sánchez-Castro I, Cantos M, García JL, Azcón R, Ruiz-Lozano JM, Beuzón CR, Aroca R (2016) Effects of different arbuscular mycorrhizal fungal backgrounds and soils on olive plants growth and water relation properties under well-watered and drought conditions. Plant Cell Environ 39(11):2498–2514
Caravaca F, Diaz E, Barea JM, Azcon-Aguilar C, Roldàn A (2003) Photosynthesis and transpiration rates of Olea europaea subsp. sylvestris and Rhamnus lycioides as affected by water deficit and mycorrhiza. Biol Plant 46:637–639
Chapman HD, Pratt PF (1961) Methods of analysis for soils, plants and waters. University of California, Riverside, pp 161–174
Chartzoulakis KS (2005) Salinity and olive: growth, salt tolerance, photosynthesis and yield. Agric Water Manag 78:108–121
Davies FT Jr, Olalde-Portugal V, Aguilera-Gomez L, Alvarado MJ, Ferrera-Cerrato RC, Boutton TW (2002) Alleviation of drought stress of Chile ancho pepper (Capsicum annuum L. cv San luis) with arbuscular mycorrhiza indigenous to Mexico. Sci Hortic 92:347–359
Duan X, Neuman DS, Reiber JM, Green CD, Arnold M, Saxton AM, Auge RM (1996) Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought. J Exp Bot 47(303):1541–1550
Ennajeh M, Vadel AM, Khemira H (2009) Osmoregulation and osmoprotection in the leaf cells of two olive cultivars subjected to severe water deficit. Acta Physiol Plant 31:711–721
Garcia K, Zimmermann SD (2014) The role of mycorrhizal associations in plant potassium nutrition. Front Plant Sci 5:337
Gianinazzi S, Golotte A, Binet MN, Van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530
Gutjahr C, Paszkowski U (2013) Multiple control levels of root system remodeling in arbuscular mycorrhizal symbiosis. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00204
Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments. Plant Signal Behav 7:1456–1466
Institute SAS (1999) SAS/STAT User’s Guide. SAS Institute, Cary
Jackson D, Paglietti L, Ribeiro M, Karray B (2015) Tunisie: Analyse de la filière oléicole. Food and Agriculture Organization of United Nations, FAO Investment Center. Countries Highlights, p 186
Jaleel CA, Manivannan P, Wahid A, Farooq M, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 121:100–105
Khalvati M, Bartha B, Dupigny A, Schroder P (2010) Arbuscular mycorrhizal association is beneficial for growth and detoxification of xenobiotics of barley under drought stress. J Soils Sediments 10:54–64
Kjeldhal J (1883) Neue Methode zur Bestimmung des Stickstoffs in organischen Körpern. Z Anal Chem 22:366–382
Kramer PJ, Boyer JS (1997) Water relations of plants and soils. Academic Press, San Diego
Kramer PJ, Brix H (1965) Measurment of water deficit in plants. UNESCO Arid Zon Res 25:343–531
Krishnakumar S, Balakrishnan N, Muthukrishnan R, Kumar SR (2013) Myth and mystery of soil mycorrhiza: a review. Afr J Agric Res 8(38):4706–4717
Kubikova E, Moore JL, Ownlew BH, Mullen MD, Augé RM (2001) Mycorrhizal impact on osmotic adjustment in Ocimum basilicum during a lethal drying episode. J Plant Physiol 158:1227–1230
Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops—A meta-analysis. Soil Biol Biochem 81:147–158
Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscular mycorrhizal influence on zinc nutrition in crop plants—A meta-analysis. Soil Biol Biochem 69:123–131
Lone R, Shuab R, Wani KA, Ganaie MA, Tiwari AK, Koul KK (2015) Mycorrhizal influence on metabolites, indigestible oligosaccharides, mineral nutrition and phytochemical constituents in onion (Allium cepa L.) plant. Sci Hortic 193:55–61
Lo Gullo MA, Salleo S (1988) Different strategies of drought resistance in three Mediterranean scierophyllous trees growing in the same environmental conditions. New Phytol 108:267–276
Lovato PE, Gianinazzi-Pearson V, Trouvelot A, Gianinazzi S (1996) The state of art mycorrhizas and micropropagation. Adv Hort Sci 10:46–52
Manuela G, Luciano A (2002) Biotechnology of arbuscular mycorrhizas. Agriculture and food production. Appl Mycol Biotechnol 2:275–310
Meddad-Hamza A, Beddiar A, Gollotte A, Lemoine MC, Kuszala C, Gianinazzi S (2010) Arbuscular mycorrhizal fungi improve the growth of olive trees and their resistance to transplantation stress. Afr J Biotechnol 9(8):1159–1167
Mena-Violante HG, Ocampo-Jimenez O, Dendooven L, Martinez-Soto G, Gonzalez-Castafieda J, Davies FT Jr, Olalde-Portugal V (2006) Arbuscular mycorrhizal fungi enhance fruit growth and quality of chile ancho (Capsicum annuum L. cv San Luis) plants exposed to drought. Mycorrhiza 16:261–267
Nobel PS (1991) Physicochemical and environmental plant physiology. Academic Press, San Diego
Orfanoudakis M, Wheeler CT, Hooker JE (2010) Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza 20:117–126
Passioura JB (1996) Drought and drought tolerance. Plant Growth Regul 20:79–83
Philips JM, Hayman DS (1970) Improved procedure for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161
Pinior A, Grunewaldt-Stöcker G, Von Alten H, Strasser RJ (2005) Mycorrhizal impact on drought stress tolerance of rose plants probed by chlorophyll a fluorescence, proline content and visual scoring. Mycorrhiza 15(8):596–605
Plenchette C, Fortin JA, Furlan V (1983) Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. Mycorrhizal dependency under field conditions. Plant Soil 70:199–309
Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750
Porras-Soriano A, Soriano-Martin ML, Porras-Piedra A, Azcon R (2009) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166:1350–1359
Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistence. Curr Opin Plant Biol 10:393–398
Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defense mechanisms, chapter 9. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function, pp 193–207. https://doi.org/10.1007/978-90-481-9489-6_9
Rapparini F, Peñuelas J (2014) Mycorrhizal fungi to alleviate drought stress on plant growth, Chapter 2. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses, vol 1. https://doi.org/10.1007/978-1-4614-9466-9_2
Rejsková A, Patková L, Stodůlková E, Lipavska H (2007) The effect of abiotic stresses on carbohydrate status of olive shoots (Olea europaea L.) under in vitro conditions. J Plant Physiol 164(2):174–184
Robyt JF, White BJ (1987) Biochemical techniques—theory and practice. Books/Cole Publishing Company, Monterey, pp 267–275
Rossi L, Sebastiani L, Tognetti R, D’andria R, Morelli G, Cherubini P (2013) Tree-ring wood anatomy and stable isotopes show structural and functional adjustments in olive trees under different water availability. Plant Soil 372:567–579
Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317
Ruiz-Lozano JM, Azcón R (1996) Mycorrhizal colonization and drought stress as factors affecting nitrate reductase activity in lettuce plants. Agric Ecosyst Environ 60:175–181
Ruiz-Lozano JM, Azcón R, Gómez M (1995) Effects of arbuscular mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Appl Environ Microbiol 61:456–460
Ruiz-Lozano JM, Aroca R, Zamarreño AM, Molina M, Andreo-Jiménez B, Porcel R, García-Mina JM, Ruyter-Spira C, López-Ráez JA (2016) Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ 39(2):441–452
Ruiz-Sánchez M, Aroca R, Muñoz Y, Armada E, Polón R, Ruiz-Lozano JM (2010) The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869
Scholander PF, Hammel HT, Bradstreet ED, Henningsen EA (1965) Sap pressure in vascular plants. Science 148:339–346
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250
Srivastava AK, Singh S, Marathe RA (2002) Organic citrus: soil fertility and plant nutrition. J Sustain Agric 19:5–29
Subramanian KS, Charest C (1995) Influence of arbuscular mycorrhizae on the metabolism of maize under drought stress. Mycorrhiza 5:273–278
Subramanian KS, Charest C (1999) Acquisition of N by external hyphae of an arbuscular mycorrhizal fungus and its impact on physiological responses in maize under drought-stressed and well-watered conditions. Mycorrhiza 9:69–75
Taylor A, Pereira N, Thomas B, Pink DAC, Jones JE, Bending GD (2015) Growth and nutritional responses to arbuscular mycorrhizal fungi are dependent on onion genotype and fungal species. Biol Fertil Soils. https://doi.org/10.1007/s00374-015-1027-y
Troll W, Lindsley JA (1955) Photometric method for the determination of proline. J Biol Chem 215:655–660
Trouvelot A, Kough JL, Gianinazzi V (1986) Mesure de taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In physiological and genetic aspects of mycorhizical, V. Gianinazzi-Pearson et S. Gianinazzi. (éd.). INRA, Paris, pp 217–221
Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425
Wu QS, Zou YN, He XH (2011) Differences of hyphal and soil phosphatase activities in drought-stressed mycorrhizal trifoliate orange (Poncirus trifoliata) seedlings. Sci Hortic 129:294–298
Wu QS, Srivastava AK, Zoua YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87
Yooyongwech S, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-um S (2016) Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Sci Hortic 198:107–117
Zhang L, Jiang C, Zhou J, Declerck S, Tian C, Feng G (2016) Increasing phosphorus concentration in the extraradical hyphae of Rhizophagus irregularis DAOM 197198 leads to a concomitant increase in metal minerals. Mycorrhiza 26(8):909–918
Zou YN, Srivastava AK, Ni QD, Wu QS (2015) Disruption of mycorrhizal extraradical mycelium and changes in leaf water status and soil aggregate stability in rootbox-grown trifoliate orange. Front Microbiol 6:203
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Ouledali, S., Ennajeh, M., Zrig, A. et al. Estimating the contribution of arbuscular mycorrhizal fungi to drought tolerance of potted olive trees (Olea europaea). Acta Physiol Plant 40, 81 (2018). https://doi.org/10.1007/s11738-018-2656-1
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DOI: https://doi.org/10.1007/s11738-018-2656-1