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Identification of a Gene from the Arbuscular Mycorrhizal Fungus Glomus intraradices Encoding for a 14-3-3 Protein that is Up-Regulated by Drought Stress during the AM Symbiosis

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Abstract

In the present study, a 14-3-3 protein-encoding gene from Glomus intraradices has been identified after differential hybridization of a cDNA library constructed from the fungus growing in vitro and subjected to drought stress by addition of 25% PEG 6000. Subsequently, we have studied its expression pattern under drought stress in vitro and also when forming natural symbioses with different host plants. The results obtained suggest that Gi14-3-3 gene may be involved in the protection that the arbuscular mycorrhizal (AM) symbiosis confers to the host plant against drought stress. Our findings provide new evidences that the contribution of AM fungi to the enhanced drought tolerance of the host plant can be mediated by a group of proteins (the 14-3-3) that regulate both signaling pathways and also effector proteins involved in the final plant responses.

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References

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

    Article  Google Scholar 

  2. 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

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  5. Augé, RM, Sylvia, DM, Park, S, Buttery, BR, Saxton, AM, Moore, K, Cho, K (2004) Partitioning mycorrhizal influence on water relations of Phaseolus vulgaris into soil and plant components. Can J Bot 82: 503–514518

    Article  Google Scholar 

  6. Babakov, AV, Chelysheva, VV, Klychnikov, OI, Zorinyanz, SE, Trofimova, MS, de Boer, AH (2000) Involvement of 14-3-3 proteins in the osmotic regulation of H+-ATPase in plant plasma membranes. Planta 211: 446–448

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  8. Camoni, L, Harper, JF, Palmgren, MG (1998) 14-3-3 proteins activate a plant calcium-dependent protein kinase (CDPK). FEBS Lett 430: 381–384

    Article  PubMed  CAS  Google Scholar 

  9. Chelysheva, VV, Smolenskaya, IN, Trofimova, MC, Babakov, AV, Muromtsev, GS (1999) Role of the 14-3-3 proteins in the regulation of H+-ATPase activity in the plasma membrane of suspension-cultured sugar beet cells under cold stress. FEBS Lett 456: 22–26

    Article  PubMed  CAS  Google Scholar 

  10. Chung, HJ, Sehnke, PC, Ferl, RJ (1999) The 14-3-3 proteins: Cellular regulator of plant metabolism. Trends Plant Sci 4: 367–371

    Article  PubMed  Google Scholar 

  11. Comparot, S, Lingiah, G, Martin, T (2003) Function and specificity of 14-3-3 proteins in the regulation of carbohydrate and nitrogen metabolism. J Exp Bot 54: 59–604

    Article  CAS  Google Scholar 

  12. 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 

  13. Ferrol, N, Barea, JM, Azcon-Aguilar, C (2000) The plasma membrane H+-ATPase gene family in the arbuscular mycorrhizal fungus Glomus mosseae. Curr Genet 37: 112–118

    Article  PubMed  CAS  Google Scholar 

  14. Finnie, C, Andersen, CH, Borch, J, Gjetting, S, Christensen, AB, de Boer, AH, Thordal-Christensen, H, Collinge, DB (2002) Do 14-3-3 proteins and plasma membrane H+-ATPases interact in the barley epidermis in response to the barley powdery mildew fungus? Plant Mol Biol 49: 137–147

    Article  CAS  Google Scholar 

  15. Finnie, C, Borch, J, Collinge, DB (1999) 14-3-3 proteins: Eukaryotic regulatory proteins with many functions. Plant Mol Biol 40: 545–554

    Article  PubMed  CAS  Google Scholar 

  16. Gianinazzi-Pearson, V, Arnoud, C, Oufattole, M, Arango, M, Gianinazzi, S (2000) Differential activation of H+-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta 211: 609–613

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  18. 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 

  19. Gonzalez-Guerrero, M, Azcón-Aguilar, C, Mooney, M, Valderas, A, MacDiarmid, CW, Eide, DJ, Ferrol, N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Funct Genet Biol 42: 130–140

    Article  CAS  Google Scholar 

  20. 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 

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

    Article  Google Scholar 

  22. Herrin, DL, Schmidt, GW (1988) Rapid, reversible staining of northern blot prior to hybridization. BioTechniques 6: 196

    PubMed  CAS  Google Scholar 

  23. Janes, BE (1974) The effect of molecular size concentration in nutrient solution and exposure time on the amount and distribution of polyethylene glycol. Plant Physiol 54: 226–229

    PubMed  CAS  Google Scholar 

  24. Kerkeb, L, Vanema, K, Donaire, JP, Rodriguez-Rosales, MP (2002) Enhanced H+/ATP coupling ratio of H+-ATPase and increased 14-3-3 protein content in plasma membrane of tomato cells upon osmotic shock. Physiol Plant 116: 37– 41

    Article  PubMed  Google Scholar 

  25. Knight, H, Trewavas, AJ, Knight, MR (1997) Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J 12: 1067–1078

    Article  PubMed  CAS  Google Scholar 

  26. Kramer, PJ, Boyer, JS (1997) Water Relations of Plants and Soils. Academic Press. San Diego, USA

    Google Scholar 

  27. 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 

  28. Livak, KJ, Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \(2^{{ - \Delta \Delta {\text{Ct}}}} \) method. Methods 25: 402–408

    Article  PubMed  CAS  Google Scholar 

  29. Martin-Laurent, F, Franken, P, Gianinazzi, S (1995) Screening of cDNA fragments generated by differential RNA display. Anal Biochem 228: 182–184

    Article  PubMed  CAS  Google Scholar 

  30. Marulanda, A, Azcó n, R, Ruiz-Lozano, JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa L. plants under drought stress. Physiol Plant 119: 526–533

    Article  CAS  Google Scholar 

  31. Murphy, PJ, Langridge, P, Smith, SE (1997) Cloning plant genes differentially expressed during colonization of roots of Hordeum vulgare by the vesicular–arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 135: 291–301

    Article  CAS  Google Scholar 

  32. Muslin, AJ, Xing, H (2000) 14-3-3 proteins: Regulation of subcellular localization by molecular interference. Cell Signal 12: 703–709

    Article  PubMed  CAS  Google Scholar 

  33. Palmgren, MG (1998) Proton gradients and plant growth: role of the plasma membrane H+-ATPase. Adv Bot Res 28: 1–70

    Article  CAS  Google Scholar 

  34. Palmgren, MG, Fuglsang, AT, Jahn, T (1998) Deciphering the role of 14-3-3 proteins. Exp Biol Online 3: 1–17

    Google Scholar 

  35. Phillips, JM, Hayman, DS (1970) Improved procedure of clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55: 159–161

    Article  Google Scholar 

  36. Porcel, R, Azcón, R, Ruiz-Lozano, JM (2005) Evaluation of the role of genes encoding for dehydrin proteins (LEA D-11) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca sativa plants. J Exp Bot 56: 1933–1942

    Article  PubMed  CAS  Google Scholar 

  37. 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 

  38. Porcel, R, Gómez, M, Kaldenhoff, R, Ruiz-Lozano, JM (2005) Impairment of NtAQP1 gene expression in tobacco plants does not affect root colonization pattern by arbuscular mycorrhizal fungi but decreases their symbiotic efficiency under drought. Mycorrhiza 15: 417–423

    Article  PubMed  CAS  Google Scholar 

  39. 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  PubMed  CAS  Google Scholar 

  40. Reid, CP, Bowen, GD, McCleod, S (1978) Phosphorus contamination in polyethylene glycol. Plant Physiol 61: 708–709

    PubMed  CAS  Google Scholar 

  41. Roberts, MR (2003) 14-3-3 proteins find new partners in plant cell signalling. Trends Plant Sci 8: 218–223

    Article  PubMed  CAS  Google Scholar 

  42. Roberts, MR, de Bruxelles, GL (2002) Plant 14-3-3 protein families: evidence for isoform-specific functions? Biochem Soc Trans 30: 373–378

    Article  PubMed  CAS  Google Scholar 

  43. Roberts, MR, Salinas, J, Collinge, DB (2002) 14-3-3 proteins and the response to abiotic and biotic stress. Plant Mol Biol 1031: 1031–1039

    Article  Google Scholar 

  44. 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 

  45. 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

    Article  CAS  Google Scholar 

  46. 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

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  50. Ruiz-Lozano, JM, Collados, C, Porcel, R, Azcón, R, Barea, JM (2002) Identification of a cDNA from the arbuscular mycorrhizal fungus Glomus intraradices which is expressed during symbiosis and up-regulated by N fertilization. Mol Plant–Microb Interact 15: 360–367

    CAS  Google Scholar 

  51. Sambrook, J, Fritsch, EF, Maniatis, TA (1989) Molecular Cloning: A Laboratory Manual 2nd ed. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY

    Google Scholar 

  52. Sambrook, J, Fritsch, EF, Maniatis, TA (1989) Molecular Cloning: A Laboratory Manual 2nd ed. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY

    Article  PubMed  CAS  Google Scholar 

  53. Sanger, F, Nicklen, S, Coulsen, AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci U S A 74: 5463–5467

    Article  CAS  Google Scholar 

  54. Siefritz, F, Tyree, MT, Lovisolo, C, Schubert, A, Kaldenhoff, R (2002) PIP1 plasma membrane aquaporins in tobacco: From cellular effects to function in plants. Plant Cell 14: 869–876

    Article  PubMed  CAS  Google Scholar 

  55. St-Arnaud, M, Hamel, C, Vimard, B, Caron, M, Fortin, JA (1996) Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycol Res 100: 328–332

    Article  Google Scholar 

  56. Verslues, PE, Ober, ES, Sharp, RE (1998) Root growth and oxygen relations at low water potentials. Impact of oxygen availability in polyethylene glycol solutions. Plant Physiol 116: 1403–1412

    Article  PubMed  CAS  Google Scholar 

  57. Wang, WX, Vinocur, B, Altman, A (2003) Plant response to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218: 1–14

    Article  PubMed  CAS  Google Scholar 

  58. Wang, WX, Vinocur, B, Shoseyov, O, Altman, A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9: 244–252

    Article  PubMed  CAS  Google Scholar 

  59. Zhou, GL, Yamamoto, T, Ozoe, F, Yano, D, Tanaka, K, Matsuda, M, Kawamukai, M (2000) Identification of a 14-3-3 protein from Lentinus edodes that interacts with CAP (adenylyl cyclase-associated protein), and conservation of this interaction in fission yeast. Biosci Biotechnol Biochem 64: 149–159

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

This work and R. Porcel were financed by CICYT-FEDER (Project AGL2002-03952).

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  1. Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín (CSIC), Prof. Albareda, 1, 18008, Granada, Spain

    Rosa Porcel, Ricardo Aroca, Custodia Cano, Alberto Bago & Juan Manuel Ruiz-Lozano

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  1. Rosa Porcel
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  2. Ricardo Aroca
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Correspondence to Juan Manuel Ruiz-Lozano.

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Porcel, R., Aroca, R., Cano, C. et al. Identification of a Gene from the Arbuscular Mycorrhizal Fungus Glomus intraradices Encoding for a 14-3-3 Protein that is Up-Regulated by Drought Stress during the AM Symbiosis. Microb Ecol 52, 575–582 (2006). https://doi.org/10.1007/s00248-006-9015-2

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