, 15:596

Mycorrhizal impact on drought stress tolerance of rose plants probed by chlorophyll a fluorescence, proline content and visual scoring

  • Alexandra Pinior
  • Gisela Grunewaldt-Stöcker
  • Henning von Alten
  • Reto J. Strasser
Original Paper


Micropropagated rose plants (Rosa hybrida L., cv. New Dawn) were inoculated with the arbuscular mycorrhizal (AM) fungus Glomus intraradices (Schenk and Smith) and subjected to different drought regimens. The dual objectives of these experiments were to investigate the mechanism and the extent to which AM can prevent drought damages and whether physiological analyses reveal enhanced drought tolerance of an economically important plant such as the rose. In a long-term drought experiment with four different water regimens, visual scoring of wilt symptoms affirmed that AM in a selected host–symbiont combination increased plant performance. This effect was mostly expressed if moderate drought stress was constantly applied over a long period. In a short-term experiment in which severe drought stress was implemented and plants were allowed to recover after 4 or 9 days, no visual differences between mycorrhizal and non-mycorrhizal roses were observed. Therefore, the early physiological steps conferring drought tolerance were prone to investigation. Proline content in leaves proved to be an unsuitable marker for AM-induced drought tolerance, whereas analysis of chlorophyll a fluorescence using the JIP test (collecting stress-induced changes of the polyphasic O-J-I-P fluorescence kinetics in a non-destructive tissue screening) was more explanatory. Parameters derived from this test could describe the extent of foliar stress response and help to differentiate physiological mechanisms of stress tolerance. AM led to a more intense electron flow and a higher productive photosynthetic activity at several sites of the photosynthetic electron transport chain. A K step, known as a stress indicator of general character, appeared in the fluorescence transient only in drought-stressed non-mycorrhizal plants; conversely, the data elucidate a stabilising effect of AM on the oxygen-evolving complex at the donor site of photosystem (PS) II and at the electron-transport chain between PS II and PS I. If drought stress intensity was reduced by a prolonged and milder drying phase, these significant tolerance features were less pronounced or missing, indicating a possible threshold level for mycorrhizal tolerance induction.


Arbuscular mycorrhiza Chlorophyll fluorescence Drought stress tolerance Glomus intraradices Rosa hybrida 





arbuscular mycorrhiza


arbuscular mycorrhizal fungi

Chl a

chlorophyll a




energy flux for electron transport

Fo, Fm

initial and maximum Chl a fluorescence


maximum quantum efficiency of primary photochemistry of photosystem II

O, K, J, I, P

intermediate steps of Chl a fluorescence rise between Fo and Fm


oxygen-evolving complex


performance index

PS I and PS II

photosystems I and II




reaction centre


normalized area above the Chl a fluorescence transient


energy flux for trapping


  1. Augé RM (2001) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  2. Augé RM, Duan X (1991) Mycorrhizal symbiosis and nonhydraulic root signals of drying soil. Plant Physiol 97:821–824PubMedCrossRefGoogle Scholar
  3. Augé RM, Foster JG, Loescher WH, Stodola AJW (1992) Symplastic molality of free amino acids and sugars in Rosa roots with regard to VA mycorrhizae and drought. Symbiosis 12:1–17Google Scholar
  4. Augé RM, Stodola AJW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97CrossRefGoogle Scholar
  5. Backhaus GF (1984) Untersuchungen zur Nutzung der endotrophen (VA) Mykorrhiza in der gärtnerischen Pflanzenproduktion. PhD thesis, Hannover University, GermanyGoogle Scholar
  6. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  7. Bethlenfalvay GJ, Brown MS, Ames RN, Thomas RS (1988) Effect of drought on host and endophyte development in mycorrhizal soybeans in relation to water use and phosphate uptake. Physiol Plant 72:565–571CrossRefGoogle Scholar
  8. Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osório ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot 89:907–916CrossRefPubMedGoogle Scholar
  9. D'Arcy CJ, Eastburn DM, Schumann GL (2000) Illustrated glossary of plant pathology. American Phytopathological Society, St. Paul. DOI 10.1094/PHI-I-2001-0219-01
  10. Davies WJ, Santamaria JM (2000) Physiological markers for microplant shoot and root quality. Acta Hortic 530:363–376Google Scholar
  11. Davies FTJ, Svenson SE, Cole JC, Havaphutanon L, Duray SA, Olalde-Portugal V, Meier CE, Bo SH (1996) Non-nutritional stress acclimation of mycorrhizal woody plants exposed to drought. Tree Physiol 16:985–993PubMedGoogle Scholar
  12. Dehne HW, Backhaus GF (1986) The use of vesicular arbuscular mycorrhizal fungi in plant production. I. Inoculum production. J Plant Dis Protect 93:415–424Google Scholar
  13. Duan X, Neuman 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 47:1541–1550CrossRefGoogle Scholar
  14. Goicoechea N, Szalai G, Antolin MC, Sanchez-Diaz M, Paldi E (1998) Influence of arbuscular mycorrhizae and rhizobium on free polyamines and proline levels in water-stressed alfalfa. J Plant Physiol 153:706–711Google Scholar
  15. Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160CrossRefGoogle Scholar
  16. Guissé B, Srivastava A, Strasser RJ (1995) Effects of high temperature and water stress on the polyphasic chlorophyll a fluorescence transient of potato leaves. In: Mathis P (ed) Photosynthesis. Kluwer, Dordrecht, pp 913–916Google Scholar
  17. Jones HG (1998) Stomatal control of photosynthesis and transpiration. J Exp Bot 49:387–398CrossRefGoogle Scholar
  18. Larcher W (1994) Ökophysiologie der Pflanzen, 5. Auflage, Ulmer, Stuttgart, pp 299–312Google Scholar
  19. Mohamed MAH, Harris PJC, Henderson J (2000) In vitro selection and characterisation of a drought tolerant clone of Tagetes minuta. Plant Sci 159:213–222CrossRefPubMedGoogle Scholar
  20. Morte A, Lovisolo C, Schubert A (2000) Effect of drought stress on growth and water relations of the mycorrhizal association Helianthemum almerienseTerfezia claveryi. Mycorrhiza 10:115–119CrossRefGoogle Scholar
  21. Ott T, Clarke J, Birks K, Johnson G (1999) Regulation of the photosynthetic electron transport chain. Planta 209:250–258CrossRefPubMedGoogle Scholar
  22. 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 55:1743–1750PubMedCrossRefGoogle Scholar
  23. Reichenbach Graf von H, Schönbeck F (1995) Influence of VA-mycorrhiza on drought tolerance of flax (Linum usitatissimum L.). I. Influence of VAM on growth and morphology of flax and on physical parameters of the soil. Angew Bot 69:49–54Google Scholar
  24. Rhodes D, Verslues PE, Sharp RE (1998) Role of amino acids in abiotic stress resistance. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. Marcel Dekker, New York, pp 319–356Google Scholar
  25. Rivera-Becerril F, Calantzis C, Turnau K, Caussanel JP, Belimov AA, Gianinazzi S, Strasser RJ, Gianinazzi-Pearson V (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot 53:1177–1185CrossRefPubMedGoogle Scholar
  26. Schönbeck F, Grunewaldt-Stöcker G, von Alten H (1994) Mycorrhizae. In: Campbell CL, Benson DM (eds) Epidemiology and management of root diseases. Springer, Berlin Heidelberg New York, pp 65–81Google Scholar
  27. Srivastava A, Guissé B, Greppin H, Strasser RJ (1997) Regulation of antenna structure and electron transport in photosystem II of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. Biochim Biophys Acta 1320:95–106CrossRefGoogle Scholar
  28. Strasser B (1997) Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynthesis Res 52:147–155CrossRefGoogle Scholar
  29. Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42CrossRefGoogle Scholar
  30. Strasser RJ, Srivastava A, Tsimilli-Michael M (1999) Screening the vitality and photosynthetic activity of plants by fluorescence transient. In: Behl RK, Punia MS, Lather BPS (eds) Crop improvement for food security. SSARM, Hisar, pp 72–115Google Scholar
  31. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M (ed) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor & Francis, London, pp 445–483Google Scholar
  32. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Advances in photosynthesis and respiration vol 19. Chlorophyll fluorescence: a signature of photosynthesis chapter 12. Kluwer, Dordrecht, pp 321–362Google Scholar
  33. Tsimilli-Michael M, Strasser RJ (2002) Mycorrhization as a stress adaptation procedure. In: Gianinazzi S, Haselwandter K, Schüepp H, Barea JM (eds) Mycorrhiza technology in agriculture. Birkhäuser, Basel, pp 199–210Google Scholar
  34. Tsimilli-Michael M, Eggenberg P, Biro B, Koves-Pechy K, Voros I, Strasser RJ (2000) Synergistic and antagonistic effects of arbuscular mycorrhizal fungi and Azospirillum and Rhizobium nitrogen fixers on the photosynthetic activity of alfalfa, probed by the polyphasic chlorophyll a fluorescence transient O-J-I-P. Appl Soil Ecol 15:169–182CrossRefGoogle Scholar
  35. Vierheilig H, Coughlan A-P, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular mycorrhizal fungi. Microbiology 64:5004–5007Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Alexandra Pinior
    • 1
  • Gisela Grunewaldt-Stöcker
    • 1
  • Henning von Alten
    • 1
  • Reto J. Strasser
    • 2
  1. 1.Institute of Plant Diseases and Plant ProtectionUniversity of HannoverHannoverGermany
  2. 2.Bioenergetics LaboratoryUniversity of GenevaGenevaSwitzerland

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