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Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies

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Abstract

Water deficit is considered one of the most important abiotic factors limiting plant growth and yield in many areas on earth. Several eco-physiological studies have demonstrated that the arbuscular mycorrhizal (AM) symbiosis often results in altered rates of water movement into, through and out of the host plants, with consequent effects on tissue hydration and plant physiology. It is now accepted that the contribution of AM symbiosis to plant drought tolerance is the result of accumulative physical, nutritional, physiological and cellular effects. This review considers several aspects that should be investigated at a molecular level in order to gain a whole understanding of the different mechanisms by which the AM symbiosis protects the host plants against the detrimental effects of water deficit.

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References

  • Allen MF (1982) Influence of vesicular-arbuscular mycorrhizae on water movement through Bouteloua gracilis Lag ex Steud. New Phytol 91:191–196

    Google Scholar 

  • Allen MF (1991) The ecology of mycorrhizae. Cambridge University Press, Cambridge

  • Allen MF, Boosalis MG (1983) Effects of two species of VA mycorrhizal fungi on drought tolerance of winter wheat. New Phytol 93:67–76

    Google Scholar 

  • Augé RM (1989) Do VA mycorrhiza enhance transpiration by influencing host phosphorus status? J Plant Nutr 12:743–753

    Google Scholar 

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

    Article  Google Scholar 

  • Augé RM, Scheckel KA, Wample RL (1986) Greater leaf conductance of well-watered VA mycorrhizal rose plants is not related to phosphorus nutrition. New Phytol 103:107–116

    Google Scholar 

  • Augé RM, Scheckel KA, Wample RL (1987) Leaf water and carohydrate status of VA mycorrhizal rose exposed to water deficit stress. Plant Soil 99:291–302

    Google Scholar 

  • Augé RM, Stodola AJW, Brown MS, Bethlenfalvay GJ (1992a) Stomatal responses of mycorrhizal cowpea and soybean to short-term osmotic stress. New Phytol 120:117–125

    Google Scholar 

  • Augé RM, Foster JG, Loescher WH, Stodola AW (1992b) Symplastic sugar and free amino acid molality of Rosa roots with regard to mycorrhizal colonization and drought. Symbiosis 12:1-17

    Google Scholar 

  • Augé RM, Stodola AJW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97

    Article  Google Scholar 

  • Azcón R, Gómez M, Tobar RM (1996) Physiological and nutritional responses by Lactuca sativa to nitrogen sources and mycorrhizal fungi under drought. Biol Fertil Soils 22:156–161

    Article  Google Scholar 

  • Azcón-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens — an overview of the mechanisms involved. Mycorrhiza 6:457–464

    Article  Google Scholar 

  • Barea JM, Jeffries P (1995) Arbuscular mycorrhizas in sustainable soil-plant systems. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, Berlin Heidelberg New York, pp 521–561

    Google Scholar 

  • Barrieu F, Chaumont F, Chrispeels MJ (1998) High expression of the tonoplast aquaporin ZmTIP1 in epidermal and conducting tissues of maize. Plant Physiol 117:1153–1163

    Google Scholar 

  • Bartels D (2001) Targeting detoxification pathways: an efficient approach to obtain plants with multiple stress tolerance. Trends Plant Sci 6:284–286

    Article  CAS  PubMed  Google Scholar 

  • Bethlenfalvay GJ, Brown MS, Mihara KL, Stafford AE (1987) The Glycine-Glomus-Bradyrhizobium simbiosis. V. Effects of mycorrhizal on nodule activity and transpiration in soybean under drought stress. Plant Physiol 85:115–119

    Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    CAS  Google Scholar 

  • Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    CAS  Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Campbell WJ (1988) Nitrate reductase and its role in nitrate assimilation in plants. Physiol Plant 74:214–219

    CAS  Google Scholar 

  • Chrispeels MJ, Agre P (1994) Aquaporins: water channel proteins of plant and animal cells. Trends Biochem Sci 19:421–425

    Google Scholar 

  • Close T (1996) Dehydrins: Emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803.

    Article  CAS  Google Scholar 

  • Csonka LN, Hanson AD (1991) Prokaryotic osmoregulation: genetics and physiology. Annu Rev Microbiol 45:569–606

    Article  CAS  PubMed  Google Scholar 

  • Duan X, Newman DS, Reiber JM, Green CD, Saxton AM, Augé RM (1996) Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought. J Exp Bot 47:1541–1550

    CAS  Google Scholar 

  • Dure L (1993) Structural motifs in LEA proteins of higher plants. In: Close TJ, Bray EA (eds) Response of plants to cellular dehydration during environmental stress. American Society of Plant Physiologists, Rockville, Md., pp 91–103

  • Faber BA, Zasoski RJ, Munns DN (1991) A method for measuring hyphal nutrient and water uptake in mycorrhizal plants. Can J Bot 69:87–94

    Google Scholar 

  • Fitter AH (1985) Functioning of vesicular-arbuscular mycorrhizas under field conditions. New Phytol 99:257–265

    Google Scholar 

  • Gamble PE, Burke JJ (1984) Effect of water deficit on the chloroplast antioxidant system. I. Alterations in glutathione reductase activity. Plant Physiol 76:615–621

    CAS  Google Scholar 

  • George E, Häuser KU, Vetterlein D, Gorgus E, Marschner H (1992) Water and nutrient translocation by hyphae of Glomus mosseae. Can J Bot 70:2130–2137

    Google Scholar 

  • Goicoechea N, Antolin MC, Sánchez-Díaz M (1997) Gas exchange is related to the hormone balance in mycorrhizal or nitrogen-fixing alfalfa subjected to drought. Physiol Plant 100:989–997

    Article  CAS  Google Scholar 

  • Goicoechea N, Szalai G, Antolín MC, Sánchez-Díaz M, Paldi E (1998) Influence of arbuscular mycorrhizae and Rhizobium on free polyamines and proline levels in water-stressed alfalfa. J Plant Physiol 153:706–711

    CAS  Google Scholar 

  • Green CD, Stodola A, Augé RM (1998) Transpiration of detached leaves from mycorrhizal and nonmycorrhizal cowpea and rose plants given varying abscisic acid, pH, calcium and phosphorus. Mycorrhiza 8:93–99

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine. Clarendom Press, Oxford

  • Hamblin AP (1985) The influence of soil structure on water movement, crop root growth, and water uptake. Adv Agron 38:95–158

    Google Scholar 

  • Hardie K (1985) The effect of removal of extraradical hyphae on water uptake by vesicular-arbuscular mycorrhizal plants. New Phytol 101:677–684

    Google Scholar 

  • Ho I, Trappe JM (1975) Nitrate reducing capacity of two vesicular-arbuscular mycorrhizal fungi. Mycologia 67: 886–888

    CAS  PubMed  Google Scholar 

  • Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438

    CAS  PubMed  Google Scholar 

  • Hoff T, Stummann BM, Henningsen KW (1992) Structure, function and regulation of nitrate reductase in higher plants. Physiol Plant 84: 616–624

    Article  CAS  Google Scholar 

  • Hu CA, Delaunew AJ, Verma DPS (1992) A bifunctional enzyme (Δ1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci USA 89:9354–9358

    CAS  PubMed  Google Scholar 

  • Imai R (1996) A lea-class gene of tomato confers salt and freezing tolerance when overexpressed in Saccharomyces cerevisisae. Gene 170:243–248

    Article  CAS  PubMed  Google Scholar 

  • Iturbe-Ormaetxe I, Escuredo PR, Arrese-Igor C, Becana M (1998) Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol 116:173–181

    Article  CAS  Google Scholar 

  • Iturbe-Ormaetxe I, Matamoros MA, Rubio MC, Dalton DA, Becana M (2001) The antioxidants of legume nodule mitochondria. Mol Plant-Microbe Interact 14:1189–1196

    CAS  Google Scholar 

  • Jastrow JD, Miller RM (1991) Methods for assessing the effects of biota on soil structure. Agric Ecosyst Environ 34:279–303

    Google Scholar 

  • Jiménez A, Hernández JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    PubMed  Google Scholar 

  • Johnson KD, Höfte H, Chrispeels MJ (1990) An intrinsic tonoplast protein of proteins storage vacuoles in seeds is structurally related to a bacterial solute transporter (GlpF). Plant Cell 2:525–532

    Google Scholar 

  • Kaldorf M, Zimmer W, Bothe H (1994) Genetic evidence for the occurrence of assimilatory nitrate reductase in arbuscular mycorrhizal fungi. Mycorrhiza 5:23–28

    Article  CAS  Google Scholar 

  • Kaldorf M, Schemelzer E, Bothe H (1998) Expression of maize and fungal nitrate reductase in arbuscular mycorhiza. Mol Plant-Microbe Interact 11:439–448

    CAS  Google Scholar 

  • Kameli A, Losel DM (1993) Carbohydrates and water status in wheat plants under water stress. New Phytol 125:609–614

    CAS  Google Scholar 

  • Kammerloher W, Fischer U, Pienchottka GP, Schäffner AR (1994) Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant J 6:187–199

    Article  CAS  PubMed  Google Scholar 

  • Kishor PB, Hong Z, Miao GH, Hu CA, Verma DPS (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394

    Google Scholar 

  • Kjellbom P, Larsson C, Johansson I, Karlsson M, Johanson U (1999) Aquaporins and water homeostasis in plants. Trends Plant Sci 4:308–314

    PubMed  Google Scholar 

  • Koide R (1993) Physiology of the mycorrhizal plant. Adv Plant Pathol 9:33–54

    Google Scholar 

  • Krajinski F, Biela A, Schubert D, Gianinazzi-Pearson V, Kaldenhoff R, Franken P (2000) Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago truncatula. Planta 211:85–90

    CAS  PubMed  Google Scholar 

  • Kramer PJ, Boyer JS (1997) Water relations of plants and soils. Academic Press, San Diego, Calif.

  • 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

    CAS  Google Scholar 

  • Marschner H (1986) Mineral nutrition of higher plants. Academic Press, London

  • Moran JF, Becana M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparicio-Tejo P (1994) Drought induces oxidative stress in pea plants. Planta 194:346–352

    CAS  Google Scholar 

  • Morgan JM (1984) Osmoregulation and water stress in higher plants. Annu Rev Plant Physiol 33:299–319

    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

    CAS  Google Scholar 

  • Oades JM, Waters AG (1991) Aggregate hierarchy in soils. Aust J Soil Res 29:815–828

    Google Scholar 

  • Palma JM, Longa MA, del Rio LA, Arines J (1993) Superoxide dismutase in vesicular-arbuscular red clover plants. Physiol Plant 87:77–83

    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 157:135–143

    Article  CAS  Google Scholar 

  • Rhodes D, Handa S, Bressan RA (1986) Metabolic changes associated with adaptation of plant cells to water stress. Plant Physiol 82:890–903

    CAS  Google Scholar 

  • Roussel H, Bruns S, Gianinazzi-Pearson V, Hahlbrock K, Franken P (1997) Induction of a membrane intrinsic protein-encoding mRNA in arbuscular mycorrhiza and elicitor-stimulated cell suspension cultures of parsley. Plant Sci 126:203–210

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Azcón R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plant 95:472–478

    CAS  Google Scholar 

  • Ruiz-Lozano JM, Azcón R (1996) Mycorrhizal colonization and drought stress exposition as factors affecting nitrate reductase activity in lettuce plants. Agric Ecosyst Environ 60:175–181

    Article  Google Scholar 

  • Ruiz-Lozano JM, Azcón R, Gómez M (1995a) Effects of arbuscular mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Appl Environ Microbiol 61:456–460

    CAS  Google Scholar 

  • Ruiz-Lozano JM, Gómez M, Azcón R (1995b) Influence of different Glomus species on the time-course of physiological plant responses of lettuce to progressive drought stress periods. Plant Sci 110: 37–44

    Article  CAS  Google Scholar 

  • Ruiz-Lozano J, Azcón R, Palma JM (1996) Superoxide dismutase activity in arbuscular-mycorrhizal Lactuca sativa L. plants subjected to drought stress. New Phytol 134:327–333

    CAS  Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM, Azcón R (2001a) Clonig of cDNAs encoding SODs from lettuce plants which show differential regulation by arbuscular mycorhizal symbiosis and by drought stress. J Exp Bot 52:2241–2242

    CAS  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM, Azcón R (2001b) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol 151:493–502

    Article  CAS  Google Scholar 

  • Safir GR, Boyer JS, Gerdemann JW (1971) Mycorrhizal enhancement of water transport in soybean. Science 172:581–583

    Google Scholar 

  • Safir GR, Boyer JS, Gerdemann JW (1972) Nutrient status and mycorrhizal enhancement of water transport in soybean. Plant Physiol 49:700–703

    Google Scholar 

  • Sánchez-Díaz M, Aguirreolea J (1993) Efectos fisiológicos que causa la falta persistente de agua en los cultivos. Phytoma 51:26–36

    Google Scholar 

  • Sánchez-Díaz M, Honrubia M (1994) Water relations and alleviation of drought stress in mycorrhizal plants. In: Gianinazzi S, Schüepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkäuser, Basel, pp 167–178

  • Schmidt E (1982) Nitrification in soil. In: Stevenson FJ (ed) Nitrogen in agricultural soils. American Society of Agronomy, Madison, Wis., pp 253–287

  • Sgherri CLM, Navari-Izzo F (1995) Sunflower seedlings subjected to increasing water deficit stress: oxidative stress and defence mechanisms. Physiol Plant 93:25–30

    Article  CAS  Google Scholar 

  • Singh DK, Sale PWG, Pallaghy CK, Singh V (2000) Role of proline and leaf expansion rate in the recovery of stressed white clover leaves with increased phosphorus concentration. New Phytol 146:261–269

    Article  CAS  Google Scholar 

  • Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58

    CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, San Diego, Calif.

  • Tazawa M, Asai K, Wasaki N (1996) Characteristics of Hg- and Zn-sensitive water channels in the plasma membrane of chara cells. Bot Acta 109:388–396

    CAS  Google Scholar 

  • Tobar RM, Azcón R, Barea JM (1994) Improved nitrogen uptake and transport from 15N-labeled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. New Phytol 126:119–122

    Google Scholar 

  • Varma A, Hock B (eds) (1998) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Xu DP, Duan X, Wang B, Hong B, Ho TD, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257

    CAS  Google Scholar 

  • Yoshiba Y, Kiyosue T, Katagiri T, Ueda H, Mizoguchi T, Yamaguchi-Shinozaki K, Wada K, Harada Y, Shinozaki K (1995) Correlation between the induction of a gene for Δ1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thalina under osmotic stress. Plant J 7:751–760

    Google Scholar 

  • Zhu JK, Hasegawa PM, Bressan R (1997) Molecular aspects of osmotic stress in plants. Crit Rev Plant Sci 16:253–277

    CAS  Google Scholar 

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Acknowledgements

I would like to thank Dr R. Azcón for encouragement to write this review and for critical reading of the first draft. This work is part of a CICYT-FEDER project (Project AGL2002–03952).

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Ruiz-Lozano, J.M. Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13, 309–317 (2003). https://doi.org/10.1007/s00572-003-0237-6

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