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Contributions of an arbuscular mycorrhizal fungus to growth and physiology of loquat (Eriobotrya japonica) plants subjected to drought stress

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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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Coyne PI, Aiken RM, Maas SJ, Lamm FR (2009) Evaluating yield tracker forecasts for maize in western Kansas. Agron J 101:671–680

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Janick J (2007) Genetic alteration associated with fruit domestication. Proc Second Int Symp Loquat Acta Hortic 750:27–35

    CAS  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Li HS (2000) Principles and techniques of plant physiological biochemical experiments. Higher Education Press, Beijing (in Chinese)

    Google Scholar 

  • Lin S (2007) World loquat production and research with special reference to China. Acta Horticult 750:37–44

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Luo HJ, Zheng ZB, Luo S, Pan YS (2007) Changes in leaf characters of loquat under repeated drought stresses. Acta Horticult 750:417–422

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mallick N, Mohn FH (2000) Reactive oxygen species: response of algal cells. J Plant Physiol 157:183–193

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410

    Article  CAS  PubMed  Google Scholar 

  • Muhammad W, Asghar A (2012) Mechanism of drought tolerance in plant and its management through different methods. Cont J Agric Sci 5:10–25

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202

    Article  CAS  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363

    Article  Google Scholar 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza 13:309–317

    Article  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410(6826):327–330

    Article  CAS  PubMed  Google Scholar 

  • Singh LP, Gill SG, Tuteja N (2011) Unravelling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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Acknowledgments

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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