Mycorrhiza

, Volume 22, Issue 5, pp 347–359 | Cite as

Water deficit improved the capacity of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of antioxidant compounds in lettuce leaves

Original Paper

Abstract

Lettuce, a major food crop within the European Union and the most used for the so-called ‘Fourth Range’ of vegetables, can associate with arbuscular mycorrhizal fungi (AMF). Mycorrhizal symbiosis can stimulate the synthesis of secondary metabolites, which may increase plant tolerance to stresses and enhance the accumulation of antioxidant compounds potentially beneficial to human health. Our objectives were to assess (1) if the application of a commercial formulation of AMF benefited growth of lettuce under different types and degrees of water deficits; (2) if water restrictions affected the nutritional quality of lettuce; and (3) if AMF improved the quality of lettuce when plants grew under reduced irrigation. Two cultivars of lettuce consumed as salads, Batavia Rubia Munguía and Maravilla de Verano, were used in the study. Four different water regimes were applied to both non-mycorrhizal and mycorrhizal plants: optimal irrigation (field capacity [FC]), a water regime equivalent to 2/3 of FC, a water regime equivalent to 1/2 of FC and a cyclic drought (CD). Results showed that mycorrhizal symbiosis improved the accumulation of antioxidant compounds, mainly carotenoids and anthocyanins, and to a lesser extent chlorophylls and phenolics, in leaves of lettuce. These enhancements were higher under water deficit than under optimal irrigation. Moreover, shoot biomass in mycorrhizal lettuces subjected to 2/3 of FC were similar to those of non-mycorrhizal plants cultivated under well-watered conditions. In addition, lettuces subjected to 2/3 FC had similar leaf RWC than their respective well-watered controls, regardless of mycorrhizal inoculation. Therefore, results suggest that mycorrhizal symbiosis can improve quality of lettuce and may allow restrict irrigation without reducing production.

Keywords

Anthocyanins Carotenoids Drought Lactuca sativa Mycorrhizal symbiosis Phenolic compounds 

Notes

Acknowledgements

Marouane Baslam is the recipient of a grant from Asociación de Amigos de la Universidad de Navarra (ADA). The authors are very grateful to Adriana Hernández, from Atens, Tarragona, Spain, for kindly providing the commercial inoculum.

References

  1. Agüero MV, Barg MV, Yommi A, Camelo A, Roura SI (2008) Postharvest changes in water status and chlorophyll content of lettuce (Lactuca sativa L.) and their relationship with overall visual quality. J Food Sci 73:47–55CrossRefGoogle Scholar
  2. Agüero MV, Ponce AG, Moreira MR, Roura SI (2011) Lettuce quality loss under conditions that favor the wilting phenomenon. Postharv Biol Technol 59:124–131CrossRefGoogle Scholar
  3. Augé RM (2001) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  4. Azcón-Aguilar C, Barea JM (1997) Applying mycorrhiza biotechnology to horticulture: significance and potentials. Sci Hortic 68:1–24CrossRefGoogle Scholar
  5. Azcón-Aguilar C, Jaizme-Vega MC, Calvet C (2002) The contribution of arbuscular mycorrhizal fungi for bioremediation. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture. From Genes to Bioproducts. Birkhäuser Verlag, Berlin, pp 187–197CrossRefGoogle Scholar
  6. Bagyaraj DJ (1994) Vesicular–arbuscular mycorrhiza: application in agriculture. In: Norris JR, Read DJ, Varma AK (eds) Techniques for the study of mycorrhiza. Academic, London, pp 819–833Google Scholar
  7. Balestrini R, Lanfranco L (2006) Fungal and plant gene expression in arbuscular mycorrhizal symbiosis. Mycorrhiza 16:509–524PubMedCrossRefGoogle Scholar
  8. Barg M, Agüero MV, Yommi A, Roura SI (2009) Evolution of plant water status indices during butterhead lettuce growth and its impact on post-storage quality. J Sci Food Agric 89:422–429CrossRefGoogle Scholar
  9. Baslam M, Garmendia I, Goicoechea N (2011) Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse-grown lettuce. J Agric Food Chem 59:5504–5515PubMedCrossRefGoogle Scholar
  10. Bolgiano NC, Safir GR, Warnacke DD (1983) Mycorrhizal infection and growth of onion in the field in relation to phosphorus and water availability. J Am Soc Hortic Sci 108:819–825Google Scholar
  11. Bonfante-Fasolo P (1984) Anatomy and morphology of VA mycorrhizae. In: Powell CL, Bagyaraj DJ (eds) VA mycorrhiza. CRC, Boca Raton, pp 35–46Google Scholar
  12. Borghi S (2003) Special: IV range (vegetables). Colture Protette 32:21–43Google Scholar
  13. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  14. Bunning ML, Kendall PA, Stone MB, Stonaker FH, Stushnoff C (2010) Effects of seasonal variation on sensory properties and total phenolic content of 5 lettuce cultivars. J Food Sci 75:156–161CrossRefGoogle Scholar
  15. Calvo MM (2005) Lutein: a valuable ingredient of fruit and vegetables. Crit Rev Food Sci 45:671–696CrossRefGoogle Scholar
  16. Cevahir G, Yentür S, Yazgan M, Ünal M, Yilmazer N (2004) Peroxidase activity in relation to anthocyanin and chlorophyll content in juvenile and adult leaves of “mini-star” Gazania splendens. Pak J Bot 36:603–609Google Scholar
  17. Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9CrossRefGoogle Scholar
  18. Chapuis-Lardy L, Contour-Ansel D, Bernhard-Reversat F (2002) High performance liquid chromatography of water-soluble phenolics in leaf litter of three Eucalyptus hybrids (Congo). Plant Sci 163:217–222CrossRefGoogle Scholar
  19. Fernandes TM, Gomes BB, Lanfer-Marquez UM (2007) Apparent absorption of chlorophyll from spinach in an assay with dogs. Innov Food Sci Emerg 8:426–432CrossRefGoogle Scholar
  20. Gallardo M, Jackson LE, Schullback K, Snyder R, Thompson R, Wyland L (1996) Production and water use in lettuces under variable water supply. Irrig Sci 16:125–137CrossRefGoogle Scholar
  21. Garmendia I, Goicoechea N, Aguirreolea J (2004) Antioxidant metabolism in asymptomatic leaves of Verticillium-infected pepper associated with an arbuscular mycorrhizal fungus. J Phytopathol 152:593–599CrossRefGoogle Scholar
  22. Gianinazzi S, Gollotte A, Binet M-N, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530PubMedCrossRefGoogle Scholar
  23. Goicoechea N, Merino S, Sánchez-Díaz M (2004) Contribution of arbuscular mycorrhizal fungi (AMF) to the adaptations exhibited by the deciduous shrub Anthyllis cytisoides under water deficit. Physiol Plant 122:453–464CrossRefGoogle Scholar
  24. Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  25. Hayman DS, Barea JM, Azcón R (1976) Vesicular–arbuscular mycorrhiza in southern Spain: its distribution in crops growing in soil of different fertility. Phytopathol Mediterr 15:1–6Google Scholar
  26. Herrmann K (1976) Flavanols and flavones in food plants: a review. Int J Food Sci Technol 11:433–448CrossRefGoogle Scholar
  27. Hewitt EJ (1952) Sand and water culture methods used in the study of plant nutrition. Tech Commun no. 22, Famham Royal. Commonwealth Agriculture Bureau, Bucks, UKGoogle Scholar
  28. Jarvis CE, Walker JRL (1993) Simultaneous, rapid, spectrophotometric determination of total starch, amylose and amylopectin. J Sci Food Agric 63:53–57CrossRefGoogle Scholar
  29. Kang H-M, Saltveit KE (2002) Antioxidant capacity of lettuce leaf tissues increases after wounding. J Agric Food Chem 50:7536–7541PubMedCrossRefGoogle Scholar
  30. Ke D, Salveit ME Jr (1988) Plant hormone interaction and phenolic metabolism in the regulation of russet spotting in iceberg lettuce. Plant Physiol 88:1136–1140PubMedCrossRefGoogle Scholar
  31. Kohler J, Hernández JA, Caravaca F, Roldán A (2008) Plant-growth promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Funct Plant Biol 35:141–151CrossRefGoogle Scholar
  32. Krishna H, Singh SK, Sharma RR, Khawale RN, Grover M, Patel VB (2005) Biochemical changes in micropropagated grape (Vitis vinifera L.) plantlets due to arbuscular–mycorrhizal fungi (AMF) inoculation during ex vitro acclimatization. Sci Hortic 106:554–567CrossRefGoogle Scholar
  33. Lee J, Scagel CF (2009) Chicoric acid found in basil (Ocinum basilicum L.) leaves. Food Chem 115:650–656CrossRefGoogle Scholar
  34. Leipner J, Fracheboud Y, Stamp P (1997) Acclimation by suboptimal temperature diminishes photooxidative damage in maize leaves. Plant Cell Environ 20:366–372CrossRefGoogle Scholar
  35. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Colowick SP, Kaplan NO (eds) Methods in enzymology. Academic, San Diego, pp 350–382Google Scholar
  36. Llorach R, Martínez-Sánchez A, Tomás-Barberán FA, Gil MI, Ferreres F (2008) Characterisation of polyphenols and antioxidant properties of five lettuce varieties and escarole. Food Chem 108:1028–1038CrossRefGoogle Scholar
  37. López-Galvez G, Saltveit ME, Cantwell MI (1996) Wound-induced phenylalanine ammonia lyase activity: factors affecting its induction and correlation with the quality of minimally processed lettuce. Postharv Biol Technol 9:223–233CrossRefGoogle Scholar
  38. Mancinelli AL (1984) Photoregulation of anthocyanin synthesis: VIII. Effect of light pretreatments. Plant Physiol 75:447–453PubMedCrossRefGoogle Scholar
  39. Marulanda A, Azcón R, Ruiz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119:523–533CrossRefGoogle Scholar
  40. Mulabagal V, Ngouajio M, Nair A, Zhang Y, Gottumukkala AL, Nair MG (2010) In vitro evaluation of red and green lettuce (Lactuca sativa) for functional food properties. Food Chem 118:300–306CrossRefGoogle Scholar
  41. Oh M-M, Trick HN, Rajashekar CB (2009) Secondary metabolism and antioxidants are involved in environmental adaptation and stress tolerance in lettuce. J Plant Physiol 166:180–191PubMedCrossRefGoogle Scholar
  42. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  43. Pietrini F, Massacci A (1998) Leaf anthocyanin content changes in Zea mays L. grown at low temperature: significance for the relationship between the quantum yield of PS II and the apparent quantum yield of CO2 assimilation. Photosynth Res 58:213–219CrossRefGoogle Scholar
  44. Potters G, Horemans N, Jansen MAK (2010) The cellular redox state in plant stress biology – a charging concept. Plant Physiol Biochem 48:292–300PubMedCrossRefGoogle Scholar
  45. Rao AV, Rao LG (2007) Carotenoids and human health. Pharmacol Res 55:207–216PubMedCrossRefGoogle Scholar
  46. 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 95:472–478CrossRefGoogle Scholar
  47. Ruiz-Lozano JM, Gómez M, Azcón R (1995) Influence of different Glomus species on the time-course of physiological plant responses of lettuce to progressive drought stress periods. Plant Sci 110:37–44CrossRefGoogle Scholar
  48. Sánchez-Díaz M, Pardo M, Antolín MC, Peña J, Aguirreolea J (1990) Effect of water stress on photosynthetic activity in the MedicagoRhizobiumGlomus symbiosis. Plant Sci 71:215–221CrossRefGoogle Scholar
  49. Seeram NP (2008) Berry fruits: compositional elements, biochemical activities, and the impact of their intake on human health, performance, and disease. J Agric Food Chem 56:627–629PubMedCrossRefGoogle Scholar
  50. Séstak Z, Càtsky J, Jarvis P (1971) Plant photosynthetic production. Manual of methods. Dr Junk, The HagueGoogle Scholar
  51. Stintzing FC, Carle R (2004) Functional properties of anthocyanins and betalains in plants, food, and in human nutrition. Trends Food Sci Technol 15:19–38CrossRefGoogle Scholar
  52. Strack D, Fester T (2006) Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol 172:22–34PubMedCrossRefGoogle Scholar
  53. Tomás-Barberán FA, Loaiza-Velarde J, Bonfanti A, Saltveit ME (1997) Early wound- and ethylene-induced changes in phenylpropanoid metabolism in harvested lettuce. J Am Soc Hortic Sci 122:399–404Google Scholar
  54. Tsabedze MW, Wahome PK (2010) Influence of different irrigation regimes on production of lettuce (Lactuca sativa L.). Am–Euras J Agric Environ Sci 8:233–238Google Scholar
  55. Waterman PT, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific, LondonGoogle Scholar
  56. Weatherley PE (1950) Studies in the water relations of the cotton plant. I. The field measurements of water deficits in leaves. New Phytol 49:81–87CrossRefGoogle Scholar
  57. Yemm E, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514PubMedGoogle Scholar
  58. You Q, Wang B, Chen F, Huang Z, Wang X, Luo PG (2011) Comparison of anthocyanins and phenolics in organically and conventionally grown blueberries in selected cultivars. Food Chem 125:201–208CrossRefGoogle Scholar
  59. Zuccarini P (2007) Mycorrhizal infection ameliorates chlorophyll content and nutrient uptake of lettuce exposed to saline irrigation. Plant Soil Environ 53:283–289Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Dpto. Biología Vegetal, Sección Biología Vegetal (Unidad Asociada al CSIC, EEAD, Zaragoza e ICVV, Logroño), Facultades de Ciencias y FarmaciaUniversidad de NavarraPamplonaSpain

Personalised recommendations