Abstract
Loquat (Eriobotrya japonica) is an evergreen tree with a shallow root system subjected to drought stress. We have found that AM fungi can alleviate drought stress by improving loquat nutrient uptake. However, the physiological mechanisms of improving drought tolerance have not been described so far in loquat mycorrhiza symbiosis. Funneliformis mosseae was used as arbuscular mycorrhizal fungus and loquat was selected as a model for an evergreen, woody plant. Thus, a pot experiment with four treatments was conducted. Growth, leaf water status, solute accumulation, oxidative damage to lipids, antioxidant activities, and phytohormones were evaluated by non-mycorrhizal (NM) and arbuscular mycorrhizal (AM) loquat plants growing under well-watered or drought-stressed conditions. Results showed that AM plants had higher dry-biomass production and leaf water potential than NM plants under drought-stressed conditions. The drought-stressed AM roots accumulated more proline than in NM roots, while not in leaves. Lipid peroxides of leaves and roots in drought-stressed AM plants were 26 and 61 % lower than in NM plants. The AM symbiosis may enhance osmotic adjustment in roots, contributing to maintaining a water potential gradient and water absorption from soil into the roots. The cumulative effects increased the AM plant tolerance to drought stress. The results are compared to findings reported hitherto mainly from short-lived, herbaceous AM plants in the literature.
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References
Anjum SA, Xie XY, Wang LC, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res 6:2026–2032
Armada E, Azcón R, López-Castillo OM, Calvo-Polanco M, Ruiz-Lozano JM (2015) Autochthonous arbuscular mycorrhizal fungi and Bacillus thuringiensis from a degraded Mediterranean area can be used to improve physiological traits and performance of a plant of agronomic interest under drought conditions. Plant Physiol Biochem 90:64–74
Aroca R, Irigoyen JJ, Sanchez-Diaz M (2003) Drought enhances maize chilling tolerance. II. Photosynthetic traits and protective mechanisms against oxidative stress. Physiol Plant 117:540–549
Aroca R, Vernieri P, Ruiz-Lozano JM (2008) Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. J Exp Bot 59:2029–2041
Asrar AA, Abdel-Fattah GM, Elhindi KM (2012) Improving growth, flower yield, and water relations of snapdragon (Antirhinum majus L.) plants grown under well-watered and water-stress conditions using arbuscular mycorrhizal fungi. Photosynthetica 50(2):305–316
Audet P (2012) Arbuscular mycorrhizal symbiosis and other plant-soil interactions in relation to environmental stress. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, Berlin, pp 233–264
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42
Badenes ML, Janick J, Lin S, Zhang Z, Liang GL, Wang W (2013) Breeding loquat. In: Janick J (Ed) Plant Breeding Reviews 37:259–296
Badenes ML, Martínez-Calvo J, Llacer G (2000) Analysis of a germplasm collection of loquat (Eriobotrya japonica Lindl.). Euphytica 114(3):187–194
Bárzana G, Aroca R, Bienert GP, Chaumont F, Ruiz-Lozano JM (2014) New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant-Microbe Interact 27(4):349–363
Benhiba L, Fouad MO, Essahibi A, Ghoulam C, Qaddoury A (2015) Arbuscular mycorrhizal symbiosis enhanced growth and antioxidant metabolism in date palm subjected to long-term drought. Trees 1–9
Birhane E, Sterck FJ, Fetene M, Bongers F, Kuyper TW (2012) Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169:1–10
Coyne PI, Aiken RM, Maas SJ, Lamm FR (2009) Evaluating yield tracker forecasts for maize in western Kansas. Agron J 101:671–680
Daei G, Ardekani M, Rejali F, Teimuri S, Miransari M (2009) Alleviation of salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular mycorrhizal fungi under field conditions. J Plant Physiol 166:217–225
de Andrade SAL, Domingues AP, Mazzafera P (2015) Photosynthesis is induced in rice plants that associate with arbuscular mycorrhizal fungi and are grown under arsenate and arsenite stress. Chemosphere 134:141–149
Fan QJ, Liu JH (2011) Colonization with arbuscular mycorrhizal fungus affects growth, drought tolerance and expression of stress-responsive genes in Poncirus trifoliata. Acta Physiol Plant 33:1533–1542
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212
Feng JJ, Liu Q, Wang XD, Chen JW, Ye JD (2007) Characterization of a new loquat cultivar ‘Ninghaibai’. Proc Second Int Symp Loquat Acta Hortic 750:117–124
Ferreres F, Gomes D, Valentão P, Gonçalves R, Pio R, Chagas EA, Seabra RM, Andrade PB (2009) Improved loquat (Eriobotrya japonica Lindl.) cultivars: variation of phenolics and antioxidative potential. Food Chem 114(3):1019–1027
Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular infection in roots. New Phytol 84:489–500
Hamada A, Yoshioka S, Takuma D, Yokota J, Cui T, Kusunose M, Miyamura M, Kyotani S, Nishioka Y (2004) The effect of Eriobotrya japonica seed extract on oxidative stress in adriamycin-induced nephropathy in rats. Biol Pharm Bull 27(12):1961–1964
Hasanuzzaman M, Hossain MA, Silva JAT, Fujita M (2012) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Venkateswarlu B, Shanker AK, Shanker C, Maheswari M (eds) Crop stress and its management: perspectives and strategies. Springer, Berlin, pp 261–315
Hassine AB, Ghanem ME, Bouzid S, Lutts S (2008) An inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus L. differ in their ability to accumulate proline and glycinebetaine in response to salinity and water stress. J Exp Bot 59:1315–1326
He Q, Li XW, Liang GL, Ji K, Guo QG, Yuan WM, Zhou GZ, Chen KS, Weg WE, Gao ZS (2011) Genetic diversity and identity of Chinese loquat cultivars/accessions (Eriobotrya japonica) using apple SSR markers. Plant Mol Biol Report 29(1):197–208
Huang R, Xia R, Hu L, Lu Y, Wang M (2007) Antioxidant activity and oxygen-scavenging system in orange pulp during fruit ripening and maturation. Sci Hortic 11:166–172
Huang Z, Zou Z, He C, He Z, Zhang Z, Li J (2011) Physiological and photosynthetic responses of melon (Cucumis melo L.) seedlings to three Glomus species under water deficit. Plant Soil 339:391–399
Impa SM, Nadaradjan S, Jagadish SVK (2012) Drought stress induced reactive oxygen species and anti-oxidants in plants. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants. Springer, Berlin, pp 31–147
Irigoyen JJ, Einerich DW, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84(1):55–60
Janick J (2007) Genetic alteration associated with fruit domestication. Proc Second Int Symp Loquat Acta Hortic 750:27–35
Jimenez A, Hernandez JA, Del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114(1):275–284
Kim SH, Shin TY (2009) Anti-inflammatory effect of leaves of Eriobotrya japonica correlating with attenuation of p38 MAPK, ERK, and NF-κB activation in mast cells. Toxicol in Vitro 23(7):1215–1219
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
Li HS (2000) Principles and techniques of plant physiological biochemical experiments. Higher Education Press, Beijing (in Chinese)
Lin S (2007) World loquat production and research with special reference to China. Acta Horticult 750:37–44
Lin S, Huang X, Cueva J, Janick J (2007) Loquat: an ancient fruit crop with a promising future. Chronica Hort 47(2):12–15
Lin S, Sharpe SH, Janick J (1999) Loquat: botany and horticulture. Hortic Rev 23:233–276
Luo HJ, Zheng ZB, Luo S, Pan YS (2007) Changes in leaf characters of loquat under repeated drought stresses. Acta Horticult 750:417–422
Ma YH, Ma FW, Zhang JK, Li MJ, Wang YH, Liang D (2008) Effects of high temperature on activities and gene expression of enzymes involved in ascorbate–glutathione cycle in apple leaves. Plant Sci 175:761–766
Mallick N, Mohn FH (2000) Reactive oxygen species: response of algal cells. J Plant Physiol 157:183–193
Manoharan PT, Shanmugaiah V, Balasubramanian N, Gomathinayagam S, Sharma MP, Muthuchelian K (2010) Influence of AM fungi on the growth and physiological status of Erythrina variegata Linn. grown under different water stress conditions. Eur J Soil Biol 46:151–156
Martínez F, Palencia P, Weiland CM, Alonso D, Oliveira JA (2015) Influence of nitrification inhibitor DMPP on yield, fruit quality and SPAD values of strawberry plants. Sci Hortic 185:233–239
Marulanda A, Azcon R, Ruiz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119:526–533
Meyer AJ (2008) The integration of glutathione homeostasis and redox signaling. J Plant Physiol 165(13):1390–1403
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33(4):453–467
Miransari M, Bahrami HA, Rejali F, Malakouti MJ (2008) Using arbuscular mycorrhiza to reduce the stressful effects of soil compaction on wheat (Triticum aestivum L.) growth. Soil Biol Biochem 40:1197–1206
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410
Muhammad W, Asghar A (2012) Mechanism of drought tolerance in plant and its management through different methods. Cont J Agric Sci 5:10–25
Navarro A, Banón S, Morte A, Sánchez-Blanco MJ (2011) Effects of nursery preconditioning through mycorrhizal inoculation and drought in Arbutus unedo L. plants. Mycorrhiza 21:53–64
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279
Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa
Plenchette C, Fortin JA, Furlan V (1983) Growth response of several plant species to mycorrhiza in a soil of moderate P-fertility. Plant Soil 70(2):199–209
Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157(1):135–143
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
Qin Q, Kaas Q, Zhang L, Xu K, Li N, Zheng W, Lai Q (2013) Isolation and characterization of a cytosolic pyruvate kinase cDNA from loquat (Eriobotrya japonica Lindl.). Plant Mol Biol Report 31(1):109–119
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202
Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363
Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza 13:309–317
Ruiz-Lozano JM, Aroca R (2010) Host response to osmotic stresses: stomatal behaviour and water use efficiency of arbuscular mycorrhizal plants. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Netherlands, pp 239–256
Ruiz-Lozano JM, Porcel R, Azcón C, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63(11):4033–4044
Ruiz-Sánchez M, Aroca R, Muñoz Y, 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
Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410(6826):327–330
Singh LP, Gill SG, Tuteja N (2011) Unravelling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191
Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20
Sommer J, Pausch J, Brundrett MC, Dixon KW, Bidartondo MI, Gebauer G (2012) Limited carbon and mineral nutrient gain from mycorrhizal fungi by adult Australian orchids. Am J Bot 99(7):1133–1145
Subramanian K, Santhanakrishnan P, Balasubramanian P (2006) Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Sci Hortic 107:245–253
Sudhakar C, Lakshmi A, Giridarakumar S (2001) Changes in the antioxidant enzymes efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci 161:613–619
Teng N, Wang J, Chen T, Wu X, Wang Y, Lin J (2006) Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana. New Phytol 172:92–103
Thompson AJ, Andrews J, Mulholland BJ, McKee JM, Hilton HW, Horridge JS, Farquhar GD, Smeeton RC, Smillie IRA, Black CR, Taylor IB (2007) Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiol 143:1905–1917
Torelli A, Trotta A, Acerbi L, Arcidiacono G, Berta G, Branca C (2000) IAA and ZR content in leek (Allium porrum L.), as influenced by P nutrition and arbuscular mycorrhizae, in relation to plant development. Plant Soil 226:29–35
Torta L, Costantino D (1996) First record of the association within mycorrhizal fungi and roots of loquat, carob and prickly pear. Micol Ital 25(2):43–48
Vicente-Sánchez J, Nicolás E, Pedrero F, Alarcón JJ, Maestre-Valero JF, Fernández F (2014) Arbuscular mycorrhizal symbiosis alleviates detrimental effects of saline reclaimed water in lettuce plants. Mycorrhiza 24(5):339–348
Vilanova S, Badenes ML, Martínez-Calvo J, Llácer G (2001) Analysis of loquat germplasm (Eriobotrya japonica Lindl) by RAPD molecular markers. Euphytica 121(1):25–29
Wang XL, Yao Q, Feng QR, Huang JL, Hu YL (2007) Morphological characteristics of loquat mycorrhiza and inoculation effects of arbuscular mycorrhizal fungi on loquat. Acta Horticult 750:389–394
Wang Y, Wang D, Shi P, Omasa K (2014) Estimating rice chlorophyll content and leaf nitrogen concentration with a digital still color camera under natural light. Plant Methods 10(1):1–11
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
Zeng H, Tan F, Zhang Y, Feng Y, Shu Y, Wang J (2014) Effects of cultivation and return of Bacillus thuringiensis (Bt) maize on the diversity of the arbuscular mycorrhizal community in soils and roots of subsequently cultivated conventional maize. Soil Biol Biochem 75:254–263
Zhang W, Zhao X, Sun C, Li X, Chen K (2015) Phenolic composition from different loquat (Eriobotrya japonica Lindl.) cultivars grown in china and their antioxidant properties. Molecules 20(1):542–555
Zhang Y, Yao Q, Li J, Hu YL, Chen JZ (2014) Growth response and nutrient uptake of Eriobotrya japonica plants inoculated with three isolates of arbuscular mycorrhizal fungi under water stress condition. J Plant Nutr 37:690–703
Zheng M, Xia Q, Lu S (2015) Study on drying methods and their influences on effective components of loquat flower tea. LWT Food Sci Technol 63:14–20
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This work is financially supported by the National Natural Science Foundation of China (Grant Nos. 30471198 and 30871692), the Agriculture Fund of Guangdong Province (No. 2006B20301040), and the Natural Science Foundation of Guangdong Province (No. 07006666).
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Zhang, Y., Yao, Q., Li, J. et al. Contributions of an arbuscular mycorrhizal fungus to growth and physiology of loquat (Eriobotrya japonica) plants subjected to drought stress. Mycol Progress 14, 84 (2015). https://doi.org/10.1007/s11557-015-1108-1
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DOI: https://doi.org/10.1007/s11557-015-1108-1