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Plant Responses to Drought Stress and Exogenous ABA Application are Modulated Differently by Mycorrhization in Tomato and an ABA-deficient Mutant (Sitiens)

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Abstract

The aims of the present study are to find out whether the effects of arbuscular mycorrhizal (AM) symbiosis on plant resistance to water deficit are mediated by the endogenous abscisic acid (ABA) content of the host plant and whether the exogenous ABA application modifies such effects. The ABA-deficient tomato mutant sitiens and its near-isogenic wild-type parental line were used. Plant development, physiology, and expression of plant genes expected to be modulated by AM symbiosis, drought, and ABA were studied. Results showed that only wild-type tomato plants responded positively to mycorrhizal inoculation, while AM symbiosis was not observed to have any effect on plant development in sitiens plants grown under well-watered conditions. The application of ABA to sitiens plants enhanced plant growth both under well-watered and drought stress conditions. In respect to sitiens plants subjected to drought stress, the addition of ABA had a cumulative effect in relation to that of inoculation with G. intraradices. Most of the genes analyzed in this study showed different regulation patterns in wild-type and sitiens plants, suggesting that their gene expression is modulated by the plant ABA phenotype. In the same way, the colonization of roots with the AM fungus G. intraradices differently regulated the expression of these genes in wild-type and in sitiens plants, which could explain the distinctive effect of the symbiosis on each plant ABA phenotype. This also suggests that the effects of the AM symbiosis on plant responses and resistance to water deficit are mediated by the plant ABA phenotype.

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References

  1. Allen MF, Moore TS, Christensen M (1982) Phytohormone changes Bouteloua gracilis infected by vesicular–arbuscular mycorrhizal fungi. II. Altered levels of gibberellin-like substances and abscisic acid in the host plant. Can J Bot 60:468–471

    CAS  Google Scholar 

  2. Araus JL, Bort J, Steduto P, Villegas D, Royo C (2003) Breeding cereals for Mediterranean conditions: ecophysilogy clues for biotechnology application. Ann Appl Biol 142:129–141

    Article  Google Scholar 

  3. Aroca R, Ferrante A, Vernieri P, Chrispeels MJ (2006) Drought, abscisic acid and transpiration rate effects on the regulation of PIP aquaporin gene expression and abundance in Phaseolus vulgaris plants. Ann Bot 98:1301–1310

    Article  PubMed  CAS  Google Scholar 

  4. Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporin in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816

    Article  PubMed  CAS  Google Scholar 

  5. Aroca R, Vernieri P, Irigoyen JJ, Sánchez-Díaz M, Tognoni F, Pardossi A (2003) Involvement of abscisic acid in leaf and root of maize (Zea mays L.) in avoiding chilling-induced water stress. Plant Sci 165:671–679

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  7. Balestrini R, Lanfranco L (2006) Fungal and plant gene expression in arbuscular mycorrhizal symbiosis. Mycorrhiza 16:509–524

    Article  PubMed  CAS  Google Scholar 

  8. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  9. Bernacchia G, Furini A (2004) Biochemical and molecular responses to water stress in resurrection plants. Physiol Plant 121:175–181

    Article  PubMed  CAS  Google Scholar 

  10. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    PubMed  CAS  Google Scholar 

  11. Blintsov AN, Gussakovskaya MA (2004) Immunochemical approach to the problem of differential determination of natural forms of abscisic acid. Biochem (Moscow) 69:1099–1108

    Article  CAS  Google Scholar 

  12. Bray EA (2002) Abscisic acid regulation of gene expression during water-deficit stress in the era of the Arabidopsis genome. Plant Cell Environ 25:153–161

    Article  PubMed  CAS  Google Scholar 

  13. Burbidge A, Grieva TM, Jackson AC, Thompson AJ, Taylor IB (1997) Structure and expression of a cDNA encoding a putative noexanthin cleavage enzyme (NCE), isolated from a wilt-related tomato (Lycopersicon esculentum Mil.) library. J Exp Bot 48:2111–2112

    Article  CAS  Google Scholar 

  14. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leun P, Nambara E, Asami T, Seo M (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signalling and abscisic acid biosynthesis and functions. Plant Cell 14:2723–2743

    Article  PubMed  CAS  Google Scholar 

  15. Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803

    Article  CAS  Google Scholar 

  16. Cohen A, Moses MS, Plants AL, Bray EA (1999) Multiple mechanisms control the expression of abscisic acid (ABA)-requiring genes in tomato plants exposed to soil water deficit. Plant Cell Environ 22:989–998

    Article  CAS  Google Scholar 

  17. Danneberg G, Latus C, Zimmer W, Hundeshagen B, Schneider-Poetsch HJ, Bothe H (1992) Influence of vesicular-arbuscular mycorrhiza on phytohormone balance in maize (Zea mays L.). J Plant Physiol 141:33–39

    Google Scholar 

  18. Denby K, Gehring C (2005) Engineering drought and salinity tolerance in plants: lessons from genome-wide expression profiling in Arabidopsis. Trends Biotechnol 23:547–552

    Article  PubMed  CAS  Google Scholar 

  19. Duncan DB (1955) Multiple range and multiple F-tests. Biometrics 11:1–42

    Article  Google Scholar 

  20. Esch H, Hundeshagen B, Schneider-Poetsch HJ, Bothe H (1994) Demonstration of abscisic acid in spores and hyphae of the arbuscular-mycorrhizal fungus Glomus and in the N2-fixing cyanobacterium Anabaena variabilis. Plant Sci 99:9–16

    Article  CAS  Google Scholar 

  21. Estrada-Luna AA, Davies FT (2003) Arbuscular mycorrhizal fungi influence water relations, gas exchange, abscisic acid and growth of micropropagated chile ancho pepper (Capsicum annuum) plantlets during acclimatization and post-acclimatization. J Plant Physiol 160:1073–1083

    Article  PubMed  CAS  Google Scholar 

  22. Gianinazzi-Pearson V, Brechenmacher L (2004) Functional genomics of arbuscular mycorrhiza: decoding the symbiotic cell programme. Can J Bot 82:1228–1234

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  24. 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 

  25. Hartung W, Schraut D, Jiang F (2005) Physiology of abscisic acid (ABA) in roots under stress—a review of the relationship between root ABA and radial water and ABA flows. Aust J Agric Res 56:1253–1259

    Article  CAS  Google Scholar 

  26. Herde O, Peña-Cortés H, Wasternack C, Willmitzer L, Fisahn J (1999) Electric signaling and Pin2 gene expression on different abiotic stimuli depend on a distinct threshold of endogenous abscisic acid in several abscisic acid-deficient tomato mutants. Plant Physiol 119:213–218

    Article  PubMed  CAS  Google Scholar 

  27. Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo JA, García-Garrido JM (2007) Abscisic acid determines arbuscule development and functionality in tomato arbuscular mycorrhiza. New Phytol 175:554–564

    Article  PubMed  CAS  Google Scholar 

  28. Holbrook NM, Shashidnar VR, James RA, Munss R (2002) Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. J Exp Bot 53:1503–1514

    Article  PubMed  CAS  Google Scholar 

  29. Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153

    Article  PubMed  CAS  Google Scholar 

  30. Iuchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2000) A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol 123:553–562

    Article  PubMed  CAS  Google Scholar 

  31. Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microbial Ecol 55:45–53

    Article  Google Scholar 

  32. Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54:713–725

    Article  PubMed  CAS  Google Scholar 

  33. Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Güclü J, Vinh J, Heyes J, Franck KI, Schäffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509–522

    Article  PubMed  CAS  Google Scholar 

  34. Javot H, Maurel C (2002) The role of aquaporins in root water uptake. Ann Bot 90:301–313

    Article  PubMed  CAS  Google Scholar 

  35. Johansson I, Karlsson M, Johansson U, Larsson C, Kjellbom P (2000) The role of aquaporins in cellular and whole plant water balance. Biochim Biophys Acta 1465:324342

    Google Scholar 

  36. Kulkarni MJ, Prasad TG, Sashidhar VR (2000) Genotypic variation in ‘early warning signals’ from roots in drying soil: intrinsic differences in ABA synthesising capacity rather than root density determines total ABA ‘message’ in cowpea (Vigna unguiculata L.). Ann Appl Biol 136:267–272

    Article  CAS  Google Scholar 

  37. Lian HL, Yu X, Lane D, Sun WN, Tang ZC, Su WA (2006) Upland rice and lowland rice exhibit different PIP expression under water deficit and ABA treatment. Cell Res 16:651–660

    Article  PubMed  CAS  Google Scholar 

  38. Linforth RST, Bowman WR, Griffin DA, Marples BA, Taylor IB (1987) 2-trans-ABA alcohol accumulation in the wilty tomato mutants flacca and sitiens. Plant Cell Environ 10:599–606

    CAS  Google Scholar 

  39. Ludwig-Müller J (2000) Hormonal balance in plants during colonization by mycorrhizal fungi. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, The Netherlands, pp 263–285

    Google Scholar 

  40. Luu D-T, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96

    Article  CAS  Google Scholar 

  41. Mäkelä P, Munns R, Colmer TD, Peltonen-Sainio P (2003) Growth of tomato and an ABA-deficient mutant (sitiens) under saline conditions. Physiol Plant 117:58–63

    Article  Google Scholar 

  42. Maurel C, Tacnet F, Güclü J, Guern J, Ripoche P (1997) Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc Natl Acad Sci USA 94:7103–7108

    Article  PubMed  CAS  Google Scholar 

  43. Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222:709–715

    Article  PubMed  CAS  Google Scholar 

  44. Murakami-Mizukami Y, Yamamoto Y, Yamaki S (1991) Analyses of indole acetic acid and abscisic acid contents in nodules of soybean plants bearing VA mycorrhizas. Soil Sci Plant Nutr 37:291–298

    CAS  Google Scholar 

  45. Nagel OW, Konings H, Lambers H (1994) Growth rate, plant development and water relations of the ABA-deficient tomato mutant sitiens. Physiol Plant 92:102–108

    Article  CAS  Google Scholar 

  46. Ouziad F, Wilde P, Schmelzer E, Hildebrandt U, Bothe H (2006) Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ Exp Bot 57:177–186

    Article  CAS  Google Scholar 

  47. 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 

  48. Porcel R, Aroca R, Azcón R, Ruiz-Lozano JM (2006) PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Mol Biol 60:389–404

    Article  PubMed  CAS  Google Scholar 

  49. Porcel R, Azcón R, Ruiz-Lozano JM (2004) Evaluation of the role of genes encoding for D1-pyrroline-5-carboxylate synthetase (P5CS) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca sativa plants. Physiol Mol Plant Pathol 65:211–221

    Article  CAS  Google Scholar 

  50. 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 

  51. Quarrie SA (1991) Implications of genetic differences in ABA accumulation for crop production. In: Davies WJ, Jones HG (eds) Abscisic acid: physiology and biochemistry. BIOS, Oxford, pp 227–243

    Google Scholar 

  52. Rincon A, Priha O, Lelu-Walter MA, Bonnet M, Sotta B, Le Tacon F (2005) Shoot water status and ABA responses of transgenic hybrid larch Larix kaempferi X L. decidua to ectomycorrhizal fungi and osmotic stress. Tree Physiol 25:1101–1108

    PubMed  Google Scholar 

  53. Rock CD (2000) Pathways to abscisic acid-regulated gene expression. New Phytol 148:357–396

    Article  CAS  Google Scholar 

  54. Rodrigo MJ, Alquezar B, Zacarías L (2006) Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L. Osbeck). J Exp Bot 57:633–643

    Article  PubMed  CAS  Google Scholar 

  55. 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 

  56. Ruiz-Lozano JM, Azcón R (1997) Effect of calcium application on the tolerance of mycorrhizal lettuce plants to polyethylene glycol-induced water stress. Symbiosis 23:9–22

    Google Scholar 

  57. Ruiz-Lozano JM, Porcel R, Aroca R (2006) Does the enhanced tolerance of arbuscular mycorrhizal plants to water deficit involve modulation of drought-induced plant genes? New Phytol 171:693–698

    Article  PubMed  CAS  Google Scholar 

  58. Sambrook J, Fritsch EF, Maniatis TA (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  59. Savoure A, Hua XJ, Bertauche N, Van Montagu M, Verbruggen N (1997) Abscisic acid-independent and abscisic acid-dependent regulation of proline biosynthesis following cold and osmotic stresses in Arabidopsis thalina. Mol Gen Genet 254:104–109

    Article  PubMed  CAS  Google Scholar 

  60. Schwartz SH, Qin X, Zeevaart JAD (2003) Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes, and enzymes. Plant Physiol 131:1591–1601

    Article  PubMed  CAS  Google Scholar 

  61. Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Cur Opin Biotechnol 14:194–199

    Article  CAS  Google Scholar 

  62. Sharp RE, LeNoble ME, Else M, Thorne ET, Gherandi F (2000) Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for and interaction with ethylene. J Exp Bot 51:1575–1584

    Article  PubMed  CAS  Google Scholar 

  63. Shiota H, Sudoh T, Tanaka I (2006) Expression analysis of genes encoding plasma membrane aquaporins during seed and fruit development in tomato. Plant Sci 171:277–285

    Article  CAS  Google Scholar 

  64. Smart LB, Moskal WA, Cameron KD, Bennett AB (2001) Mip genes are down-regulated under drought stress in Nicotiana glauca. Plant Cell Physiol 42:686–693

    Article  PubMed  CAS  Google Scholar 

  65. Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis-epoxycarotenoid dioxygenase gene family. Plant J 35:44–56

    Article  PubMed  CAS  Google Scholar 

  66. Taylor I, Linforth R, Al-Naieb R, Bowman W, Marples B (1988) The wilty tomato mutants flacca and sitiens are impaired in the oxidation of ABA-aldehyde to ABA. Plant Cell Environ 11:739–745

    Article  CAS  Google Scholar 

  67. Vernieri P, Perata P, Armellini D, Bugnoli M, Presentini R, Lorenzi R, Ceccarelli N, Alpi A, Tognoni F (1989) Solid phase radioimmunoassay for the quantitation of abscisic acid in plant crude extracts using a new monoclonal antibody. J Plant Physiol 134:441–446

    CAS  Google Scholar 

  68. Walker-Simmons M (1987) ABA levels and sensitivity in developing wheat embryos of sprouting resistant and susceptible cultivars. Plant Physiol 84:61–66

    PubMed  CAS  Google Scholar 

  69. Wan X, Li L (2006) Regulation of ABA level and water-stress tolerance of Arabidopsis by ectopic expression of a peanut 9-cis-epoxycarotenoid dioxygenase gene. Biochem Biophys Res Commun 347:1030–1038

    Article  PubMed  CAS  Google Scholar 

  70. Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210

    Article  PubMed  CAS  Google Scholar 

  71. Xiong L, Zhu JK (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36

    Article  PubMed  CAS  Google Scholar 

  72. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    Article  PubMed  CAS  Google Scholar 

  73. Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119

    Article  Google Scholar 

  74. Zhang J, Zhang X, Liang J (1995) Exudation rate and hydraulic conductivity of maize roots are enhanced by soil drying and abscisic acid treatment. New Phytol 131:329–336

    Article  CAS  Google Scholar 

  75. Zeewaart JAD (1999) Abscisic acid metabolism and its regulation. In: Hooykaas MA, Hall MA, Libbenga KR (eds) Biochemistry and molecular biology of plant hormones. Elsevier, New York, pp 189–207

    Chapter  Google Scholar 

  76. Zhu C, Schraut D, Hartung W, Schäffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. J Exp Bot 56:2971–2981

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was financed by CICYT-FEDER (Project AGL2005-01237). R. Aroca was financed by the Spanish Ministry of Education and Science throughout the Juan de la Cierva program. We thank Dr. I. Taylor (University of Nottingham, UK), Dr. A. Downie (University of Kentucky Lexington, USA), and Dr. H. Shiota (Yokohama City University, Japan) for providing us with the probes for NCED, dehydrin, and PIP aquaporin genes, respectively. We thank Michael O’Shea for correcting the English text.

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Aroca, R., del Mar Alguacil, M., Vernieri, P. et al. Plant Responses to Drought Stress and Exogenous ABA Application are Modulated Differently by Mycorrhization in Tomato and an ABA-deficient Mutant (Sitiens). Microb Ecol 56, 704–719 (2008). https://doi.org/10.1007/s00248-008-9390-y

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