Plant and Soil

, Volume 240, Issue 2, pp 343–352

Ecophysiological significance of chlorophyll loss and reduced photochemical efficiency under extreme aridity in Stipa tenacissima L.

  • L. Balaguer
  • F. I. Pugnaire
  • E. Martínez-Ferri
  • C. Armas
  • F. Valladares
  • E. Manrique


Stipa tenacissima L., a perennial tussock grass widely found in semi-arid environments of the Iberian Peninsula and North Africa, is subjected to multiple stresses during the extreme summer conditions of south-east Spain. We characterised the photoprotective mechanisms of S. tenacissima during the transition from spring to summer and autumn. S. tenacissima experienced a marked water deficit (Ψ{ pd} < -8.4 MPa) and the complete suppression of CO2 assimilation in August, associated with a 72% reduction of maximal photochemical efficiency of PSII (F{ v}/F{ m}). These reduced F{ v}/F{ m} values were related to the pre-dawn maintenance of high levels of epoxidized forms of xanthophyll-cycle pigments (DPS{ pd}, ca. 42% higher than spring values), and with a 60% reduction in the concentration of total chlorophyll (Chl a+b). These changes were associated with a low capacity of dissipation of the excitation energy non-radiatively (measured as NPQ). Leaves showed a complete recovery of F{ v}/F{ m} and xanthophyll and chlorophyll concentrations after the autumn rainfall, which reached levels similar to that of spring. This poikilohydric-type response of S. tenacissima to stress allows for a greater tolerance of water shortage, high temperature and high light intensity, which are typical in these semi-arid environments and accounts for its distinctive opportunistic growth.

arid environments drought photoprotective pigments poikilochlorophylly poikilohydry Stipa tenacissima 


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  1. Abernethy G A, Fountain D W and McManus M T 1998 Observations on the leaf anatomy of Festuca novae-zelandiae and biochemical responses to a water deficit. New Zealand Journal of Botany 36, 113-123.Google Scholar
  2. Adams III W W, Demmig-Adams B, Verhoeven A S and Barker D H 1995 'Photoinhibition' during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust. J. Plant Physiol. 22, 261-76.Google Scholar
  3. Aguiar M R and Sala O E 1999 Patch structure, dynamics and implications for the functioning of arid ecosystems. Trends Ecol. Evol. 14, 273-277.PubMedGoogle Scholar
  4. Barrs H D and Weatherley P E 1962 A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust. J. Biol. Sci. 15, 413-428.Google Scholar
  5. Bewley J D 1979 Physiological aspects of desiccation tolerance. Annu. Rev. Plant Physiol. 30, 195-238.Google Scholar
  6. Bilger W and Björkman O 1990 Role of the xanthophyll cycle and energy dissipation in differently oriented faces of the cactus Opuntia macrorhiza. Oecologia 109, 353-361.Google Scholar
  7. Carrera A L, Sain C L and Bertiller M B 2000 Patterns of nitrogen conservation in shrubs and grasses in the Patagonian Monte, Argentina. Plant Soil 224, 185-193.Google Scholar
  8. Casper C, Eickmeier W G and Osmond C B 1993 Changes of fluorescence and xanthophyll pigments during dehydration in the resurrection plant Selaginella lepidophylla in low and medium light intensities. Oecologia 94, 528-533.Google Scholar
  9. Csintalan Z, Tuba Z and Lichtenthaler H K 1998 Changes in laserinduced chlorophyll fluorescence ratio F690/F735 in the poikilochlorophyllous desiccation tolerant plant Xerophyta scabrida during desiccation. J. Plant Physiol. 152, 540-544.Google Scholar
  10. DiBlasi S, Puliga S, Losi L and Vazzana C 1998 S. stapfianus and E. curvula cv. Consol in vivo photosynthesis, PSII activity and ABA content during dehydration. Plant Growth Regul. 25, 97-104.Google Scholar
  11. Drazic G, Mihailovic N and Stevanovic B 1999 Chlorophyll metabolism in leaves of higher poikilohydric plants Ramonda serbica Panc. and Ramonda nathaliae Pan. et Petrov. during dehydration and rehydration. J. Plant Physiol. 154, 379-384.Google Scholar
  12. Elvira S, Alonso R, Castillo F J and Gimeno B S 1998 On the response of pigments and antioxidants of Pinus halepensis seedlings to Mediterranean climatic factors and long-term ozone exposure. New Phytol. 138, 419-432.Google Scholar
  13. Epron D, Dreyer E and Bréda N 1993 Photosynthesis of oak tress [Quercus petraea (Matt.) Liebl.] during drought under field conditions: diurnal course of net CO2 assimilation and photochemical efficiency of photosystem II. Plant Cell Environ. 15, 809-820.Google Scholar
  14. Farrant J M, Cooper K, Kruger L A and Sherwin H W 1999 The effect of drying rate on the survival of three desiccation-tolerant angiosperm species. Ann. Bot. 84, 371-379.Google Scholar
  15. Figueroa M E, Fernandez-Baco L, Luque T and Davy A J 1997 Chlorophyll fluorescence, stress and survival in populations of Mediterranean grassland species. J. Veg. Sci. 8, 881-888.Google Scholar
  16. FAO 1998 World reference base for soil resources. ISSS-ISRICFAO, Rome.Google Scholar
  17. Gaff D F 1989 Responses of desiccation tolerant 'resurrection' plants to water stress. In Structural and Functional Responses to Environmental Stresses. Eds. K H Kreeb, H Richter and T M Hinckley. pp 255-268. SPB Academic Publishing, The Hague.Google Scholar
  18. Gamarra R and Montouto O 1999 Distribution of steppic plants in western Mediterranean and adjacent regions. Acta Botanica Fennica 162, 125-128.Google Scholar
  19. Garcia-Plazaola J I, Artetxe U and Becerril J M 1999 Diurnal changes in antioxidant and carotenoid composition in the Mediterranean sclerophyll tree Quercus ilex (L.) during winter. Plant Sci. 143, 125-133.Google Scholar
  20. Genty B, Briantais J M and Baker N R 1989 The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 99, 87-92.Google Scholar
  21. Ghasempour H R, Gaff D F, Williams R P W and Gianello R D 1998 Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Regul. 24, 185-191.Google Scholar
  22. Haase P, Pugnaire F I, Clark S C and Incoll L D 1999 Environmental control of canopy dynamics and photosynthetic rate in the evergreen tussock grass Stipa tenacissima. Plant Ecol. 145, 327-339.Google Scholar
  23. Hetherington S E and Smillie R M 1982 Humidity-sensitive degreening and regreening of leaves of Borya nitida Labill. as followed by changes in chlorophyll fluorescence. Aust. J. Plant Physiol. 9, 587-599.Google Scholar
  24. Horton P and Ruban A 1994 The role of light-harvesting complexes II in energy quenching. In Photoinhibition of Photosynthesis. From Molecular Mechanisms to the Field. Eds. N R Baker and J R Bowyer. pp 111-128. Bios Scientific Publishers, Oxford.Google Scholar
  25. Kappen L and Valladares F 1999 Opportunistic growth and dessication tolerance: the ecological success of poikilohydrous autotrophs. In Handbook of Functional Plant Ecology. Eds. F P Pugnaire and F Valladares. pp 9-80. Marcel Dekker, New York.Google Scholar
  26. Karavatas S and Manetas Y 1999 Seasonal patterns of photosystem II photochemical efficiency in evergreen sclerophylls and drought semi-deciduous shrubs under Mediterranean field conditions. Photosynthetica 36, 41-49.Google Scholar
  27. Kyparissis A, Drilias P and Manetas Y 2000 Seasonal fluctuations in photoprotective (xanthophyll cycle) and photoselective (chlorophylls) capacity in eight Mediterranean plant species belonging to two different growth forms. Aust. J. Plant Physiol. 27, 265-272.Google Scholar
  28. Kyparissis A, Petropoulou Y and Manetas Y 1995 Summer survival of leaves in a soft-leaved shrub (Phlomis fruticosa L. Labiatae) under Mediterranean field conditions: avoidance of photoinhibitory damage through decreased chlorophyll contents. J. Exp. Bot. 46, 1825-1831.Google Scholar
  29. Long S P, Humphries S and Falkowski P G 1994 Photoinhibition of photosynthesis in nature. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 633-662.CrossRefGoogle Scholar
  30. Markovska Y K, Tsonev T D, Kimenov G P and Tutekova A 1994 Physiological changes in higher poikilohydric plants-Haberlea rhodopensis Friv. and Ramonda serbica Pan.-during drought and re-watering at different light regimes. J. Plant Physiol. 144, 100-108.Google Scholar
  31. Martínez-Ferri E 1999 Definición de tipos funcionales en especies mediterráneas arbóreas sobre la base de su eficiencia en el uso de la luz. PhD thesis, Universidad Complutense de Madrid, Spain.Google Scholar
  32. Martínez-Ferri E, Balaguer L, Valladares F, Chico J M and Manrique E 2000 Energy dissipation in drought-avoiding and drought-tolerant tree species at mid-day during the Mediterranean summer. Tree Physiol. 20, 131-138.PubMedGoogle Scholar
  33. Madon O and Medail F 1997 The ecological significance of annuals on a Mediterranean grassland (Mt. Ventoux, France). Plant Ecol. 129, 189-199.Google Scholar
  34. Maroco J P, Pereira J S and Chaves M M 1997 Stomatal responses to leaf-to-air vapour pressure deficit in sahelian species. Aust. J. Plant Physiol. 24, 381-387.Google Scholar
  35. Maxwell K and Johnson G N 2000 Chlorophyll fluorescence-a practical guide. J. Exp. Bot. 51, 659-668.PubMedGoogle Scholar
  36. Munné-Bosh S and Alegre L 2000b Changes in the carotenoids, tocopherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus officinalis plants. Planta 210, 925-931.PubMedGoogle Scholar
  37. Ottander C, Campbell D and Öquist G 1995 Seasonal changes in photosystem II organisation and pigment composition in Pinus sylvestris. Planta 197, 176-183.Google Scholar
  38. Pugnaire F I and Haase P 1996 Comparative physiology and plant growth of two perennial tussock grass species in a semi-arid environment. Ann. Bot. 77, 81-86.Google Scholar
  39. Pugnaire F I, Haase P, Incoll L D and Clark S C 1996 Response of the tussock grass Stipa tenacissima to watering in a semi-arid environment. Func. Ecol. 10, 265-274.Google Scholar
  40. Qian Y L, Fry J D and Upham W S 1997 Rooting and drought avoidance of warm-season turfgrasses and tall fescue in Kansas. Crop Sci. 37, 905-910.Google Scholar
  41. Quartacci M F, Forli M, Rascio N, Vecchia D, Bochicchio A and Navari-Izzo F 1997 Dessication-tolerant Sporobolus stapfianus, lipid composition and cellular ultrastructure during dehydration and rehydration. J. Exp. Bot. 48, 1269-1279.Google Scholar
  42. Richter M, Goss R, Wagner B and Holzwarth A R 1999 Characterization of the fast and slow reversible components of non-photochemical quenching in isolated pea thylakoids by picosecond time-resolved chlorophyll fluorescence analysis? Biochemistry 38, 12718-12726.PubMedGoogle Scholar
  43. Ruban A and Horton P 1999 The xanthophyll cycle modulates the kinetics of nonphotochemical energy disipation in isolated light harvesting complexes, intact chloroplasts, and leaves of spinach. Plant Physiol. 119, 531-542.PubMedGoogle Scholar
  44. Scholander P F, Hammel H T, Bradstreet E D and Hemmingsen E A 1965 Sap pressure in vascular plants. Science 148, 339-346.Google Scholar
  45. Schreiber U, Bilger W and Neubauer C 1994 Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. In Ecophysiology of Photosynthesis. Eds. E D Schulze and M Caldwell. pp 49-70. Springer-Verlag, Berlin.Google Scholar
  46. Scott P 2000 Resurrection plants and the secrets of eternal leaf. Ann. Bot. 85, 159-166.Google Scholar
  47. Smirnoff N 1993 The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 72, 525-533.Google Scholar
  48. Tuba Z, Csintalan Z, Szente K, Nagy Z and Grace J 1998 Carbon gains by desiccation-tolerant plants at elevated CO2. Func. Ecol. 12, 39-44.Google Scholar
  49. Tuba Z, Lichtenthaler H K, Csintalan Z, Nagy Z and Szente K 1996 Loss of chlorophylls, cessation of photosynthetic CO2 assimilation and respiration in the poikilochlorophyllous plant Xerophyta scabrida during desiccation. Physiol. Plant. 96, 383-388.Google Scholar
  50. Tuba Z, Smirnoff N, Csintalan Z, Szente K and Nagy Z 1997 Respiration during slow desiccation of the poikilochlorophyllous desiccation tolerant plant Xerophyta scabrida at present-day CO2 concentration. Plant Physiol. Biochem. 35, 381-386.Google Scholar
  51. Val J, Monge E and Baker N R 1994 An improved HPLCmethod for rapid analysis of the xanthophyll cycle pigments. J. Chromatogr. Sci. 32, 286-289.Google Scholar
  52. Valladares F and Pugnaire F I 1999 Tradeoffs between irradiance capture and avoidance in semi-arid environments assessed with a crown architecture model. Ann. Bot. 83, 459-469.Google Scholar
  53. Volaire F, Thomas H and Lelievre F 1998 Survival and recovery of perennial forage grasses under prolonged Mediterranean drought. I. Growth, death, water relations and solute content in herbage and stubble. New Phytol. 140, 439-449.Google Scholar
  54. von Caemmerer S and Farquhar G D 1981 Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376-387.Google Scholar
  55. Werner C, Correia O and Beyschlag W 1999 Two different strategies of Mediterranean macchia plants to avoid photoinhibitory damage by excessive radiation levels during summer drought. Acta Oecol. 20, 15-23.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • L. Balaguer
    • 1
  • F. I. Pugnaire
    • 2
  • E. Martínez-Ferri
    • 1
    • 3
    • 4
  • C. Armas
    • 2
  • F. Valladares
    • 5
  • E. Manrique
    • 3
  1. 1.Departamento de Biología Vegetal I, Facultad de BiologíaUniversidad ComplutenseMadridSpain
  2. 2.Estación Experimental de Zonas Áridas. Consejo Superior de Investigaciones CientíficasAlmeríaSpain
  3. 3.Departamento de Biología Vegetal II, Facultad de FarmaciaUniversidad ComplutenseMadridSpain
  4. 4.Plant Sciences, Faculty of AgricultureThe University of Western AustraliaCrawleyAustralia
  5. 5.Centro de Ciencias Medioambientales. Consejo Superior de Investigaciones CientíficasMadridSpain

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