Mycorrhiza

, Volume 26, Issue 7, pp 685–697 | Cite as

Phosphorus supply, arbuscular mycorrhizal fungal species, and plant genotype impact on the protective efficacy of mycorrhizal inoculation against wheat powdery mildew

  • G Mustafa
  • B Randoux
  • B Tisserant
  • J Fontaine
  • M Magnin-Robert
  • A Lounès-Hadj Sahraoui
  • Ph Reignault
Original Article

Abstract

A potential alternative strategy to chemical control of plant diseases could be the stimulation of plant defense by arbuscular mycorrhizal fungi (AMF). In the present study, the influence of three parameters (phosphorus supply, mycorrhizal inoculation, and wheat cultivar) on AMF protective efficiency against Blumeria graminis f. sp. tritici, responsible for powdery mildew, was investigated under controlled conditions. A 5-fold reduction (P/5) in the level of phosphorus supply commonly recommended for wheat in France improved Funneliformis mosseae colonization and promoted protection against B. graminis f. sp. tritici in a more susceptible wheat cultivar. However, a further decrease in P affected plant growth, even under mycorrhizal conditions. Two commercially available AMF inocula (F. mosseae, Solrize®) and one laboratory inoculum (Rhizophagus irregularis) were tested for mycorrhizal development and protection against B. graminis f. sp. tritici of two moderately susceptible and resistant wheat cultivars at P/5. Mycorrhizal levels were the highest with F. mosseae (38 %), followed by R. irregularis (19 %) and Solrize® (SZE, 8 %). On the other hand, the highest protection level against B. graminis f. sp. tritici was obtained with F. mosseae (74 %), followed by SZE (58 %) and R. irregularis (34 %), suggesting that inoculum type rather than mycorrhizal levels determines the protection level of wheat against B. graminis f. sp. tritici. The mycorrhizal protective effect was associated with a reduction in the number of conidia with haustorium and with an accumulation of polyphenolic compounds at B. graminis f. sp. tritici infection sites. Both the moderately susceptible and the most resistant wheat cultivar were protected against B. graminis f. sp. tritici infection by F. mosseae inoculation at P/5, although the underlying mechanisms appear rather different between the two cultivars. This study emphasizes the importance of taking into account the considered parameters when considering the use of AMF as biocontrol agents.

Keywords

Arbuscular mycorrhizal fungi Powdery mildew Biocontrol Wheat genotype Phosphorus 

Notes

Acknowledgments

The Ministry of Higher Education in Syria mediated by Aleppo University supported this work.

References

  1. Abdel-Fattah GM, El-Haddad SA, Hafez EE, Rashad YM (2011) Induction of defense responses in common bean plants by arbuscular mycorrhizal fungi. Microbiol Res 166:268–281CrossRefPubMedGoogle Scholar
  2. Atkinson D (1973) Some general effects of phosphorus deficiency on growth and development. New Phytol 72:101–111CrossRefGoogle Scholar
  3. Azcón R, Ocampo JA (1981) Factors affecting the vesicular-arbuscular infection and mycorrhizal dependency of thirteen wheat cultivars. New Phytol 87:677–685CrossRefGoogle Scholar
  4. Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017CrossRefPubMedGoogle Scholar
  5. Buchenauer H, Hellwald KH (1985) Resistance of Erysiphe graminis on barley and wheat to sterol C-14-demethylation inhibitors. EPPO Bull 15:459–66CrossRefGoogle Scholar
  6. Cameron DD, Neal AL, van Wees SCM, Ton J (2014) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545CrossRefGoogle Scholar
  7. Campos-Soriano L, García-Martínez J, San Segundo B (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defense-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13:579–592CrossRefPubMedGoogle Scholar
  8. Caron M, Fortin JA, Richard C (1986) Effect of inoculation sequence on the interaction between Glomus intraradices and Fusarium oxysporum f. sp. radicis-lycopersici in tomatoes. Can J Plant Pathol 8:12–16CrossRefGoogle Scholar
  9. Carver TLW, Robbins MP, Zeyen RJ (1991) Effects of two PAL inhibitors on the susceptibility and localized auto-fluorescent host cell responses of oat leaves attacked by Erysiphe graminis DC. Physiol Mol Plant Pathol 39:269–287CrossRefGoogle Scholar
  10. Castellanos-Morales V, Cárdenas-Navarro R, García-Garrido JM, Illana A, Ocampo JA, Steinkellner S, Vierheilig H (2012) Bioprotection against Gaeumannomyces graminis in barley—a comparison between arbuscular mycorrhizal fungi. Plant Soil Environ 58:256–261Google Scholar
  11. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qui JL, Huckelhoven R, Stein M, Freialdenoven A, Somerville SC, Schulze-Lefert P (2003) Snare-protein-mediated disease resistance at the plant cell wall. Nature 425:973–1007CrossRefPubMedGoogle Scholar
  12. Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant-Microbe Interact 11:1017–1028CrossRefGoogle Scholar
  13. Cozzolino V, Pigna M, Di Meo V, Caporale AG, Violante A (2010) Effects of arbuscular mycorrhizal inoculation and phosphorus supply on the growth of Lactuca sativa L. and arsenic and phosphorus availability in an arsenic polluted soil under non-sterile conditions. Appl Soil Ecol 45:262–268CrossRefGoogle Scholar
  14. Fernández I, Merlos M, López-Ráez JA, Martínez-Medina A, Ferrol N, Azcón C, Bonfante P, Flors V, Pozo MJ (2014) Defense related phytohormones regulation in arbuscular mycorrhizal symbioses depends on the partner genotypes. J Chem Ecol 40:791–803CrossRefPubMedGoogle Scholar
  15. Fritz M, Jakobsen I, Lyngkjaer MF, Thordal-Christensen H, Pons-Kuehnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419CrossRefPubMedGoogle Scholar
  16. Gallou A, Mosquera HPL, Cranenbrouck S, Suárez JP, Declerck S (2011) Mycorrhiza induced resistance in potato plantlets challenged by Phytophthora infestans. Physiol Mol Plant Pathol 76:20–26CrossRefGoogle Scholar
  17. García-Garrido JM, Ocampo JA (1988) Interaction between Glomus mosseae and Erwinia carotovora and its effects on the growth of tomato plants. New Phytol 110:551–555CrossRefGoogle Scholar
  18. Gianinazzi S, Gollotte A, Binet MN, Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530CrossRefPubMedGoogle Scholar
  19. Gilbert N (2009) Environment: the disappearing nutrient. Nature 461:716–718CrossRefPubMedGoogle Scholar
  20. Görg R, Hollricher K, Schulze-Lefert P (1993) Functional analysis and RFLP-mediated mapping of the Mlg resistance locus in barley. Plant J3:857–866CrossRefGoogle Scholar
  21. Graham JH (2000) Assessing costs of arbuscular mycorrhizal symbiosis in agroecosystems. In: Podila GK, Douds DD (eds) Current advances in mycorrhizae research. APS, Minnesota, pp 127–140Google Scholar
  22. Grandison GS, Cooper KM (1986) Interaction of vesicular-arbuscular mycorrhizae and cultivars of alfalfa susceptible and resistant to Meloidogyne hapla. J Nematol 18:141–149PubMedPubMedCentralGoogle Scholar
  23. Grant C, Bittman S, Montrea M, Plenchette C, Morel C (2005) Soil and fertilizer phosphorus: effects on plant P supply and mycorrhizal development. Can J Plant Sci 85:3–14CrossRefGoogle Scholar
  24. Habibzadeh Y (2015) The effect of arbuscular mycorrhizal fungi and phosphorus levels on dry matter production and root traits in cucumber (Cucumis sativus L.). Afr J Environ Sci Technol 9:65–70CrossRefGoogle Scholar
  25. Hao Z, Fayolle L, Van Tuinen D, Chatagnier O, Li X, Gianinazzi S, Gianinazzi-Pearson V (2012) Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defense gene responses in grapevine. J Exp Bot 63:3657–3672CrossRefPubMedPubMedCentralGoogle Scholar
  26. Heaney SP, Hall AA, Davies SA, Olaya G (2000) Resistance to fungicides in the QoI-STAR cross-resistance group: current perspectives. Proceedings of the British Crop Protection Conference—pests and diseases. Farnham, Surrey, pp 755–762Google Scholar
  27. Hetrick BAD, Wilson GWT, Gill BS, Cox TS (1995) Chromosome location of mycorrhizal responsive genes in wheat. Can J Bot 73:891–897CrossRefGoogle Scholar
  28. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Stn 347:1–32.Google Scholar
  29. Hückelhoven R, Fodor J, Preis C, Kogel K (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol 119:1251–1260CrossRefPubMedPubMedCentralGoogle Scholar
  30. Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–64CrossRefPubMedGoogle Scholar
  31. Kapoor R (2008) Induced resistance in mycorrhizal tomato is correlated to concentration of jasmonic acid. On Line J BiolSci 8:49–56CrossRefGoogle Scholar
  32. Khaosaad T, Vierheilig H, Nell M, Zitterl-Eglseer K, Novak J (2006) Arbuscular mycorrhiza alter the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 16:443–446CrossRefPubMedGoogle Scholar
  33. Koga H, Bushnell WR, Zeyen RJ (1990) Specificity of cell type and timing of events associated with papilla formation and the hypersensitive reaction in leaves of Hordeum vulgare attacked by Erysiphe graminis f. sp. hordei. Can J Bot 68:2344–2352CrossRefGoogle Scholar
  34. Kumar S, Sharma AK, Rawat SS, Jain DK, Ghosh S (2013) Use of pesticides in agriculture and livestock animals and its impact on environment of India. Asian J Environ Sci 8:51–57Google Scholar
  35. Le Souder C, Mazieres C, Rodes V (1998) La fertilisation minérale sur le blé : des pratiques régionales diversifiées. AGRESTE—LES CAHIERS 30:31–38Google Scholar
  36. Lee CS, Lee YJ, Jeun YC (2005) Observations of infection structures on the leaves of cucumber plants pre-treated with arbuscular mycorrhizal Glomus intraradices after challenge inoculation with Colletotrichum orbiculare. Plant Pathol J 21:237–243CrossRefGoogle Scholar
  37. Li T, Lin G, Zhang X, Chen YL, Zhang SB, Chen BD (2014) Relative importance of an arbuscular mycorrhizal fungus (Rhizophagus intraradices) and root hairs in plant drought tolerance. Mycorrhiza 24:592–602Google Scholar
  38. Li Y, Liu Z, Hou H, Lei H, Zhu X, Li X, He X, Tian C (2013) Arbuscular mycorrhizal fungi-enhanced resistance against Phytophthora sojae infection on soybean leaves is mediated by a network involving hydrogen peroxide, jasmonic acid, and the metabolism of carbon and nitrogen. Acta Physiol Plant 35:3465–3475CrossRefGoogle Scholar
  39. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544CrossRefPubMedGoogle Scholar
  40. Lynch JP, Lauchli A, Epstein E (1991) Vegetative growth of the common bean in response to phosphorus nutrition. Crop Sci 31:380–387CrossRefGoogle Scholar
  41. Mark GL, Cassells AC (1996) Genotype‐dependence in the interaction between Glomus fistulosum, Phytophthora fragariae and the wild strawberry (Fragaria vesca). Plant Soil 185:233–239Google Scholar
  42. Matsubara Y, Tamura H, Harada T (1995) Growth enhancement and Verticillium wilt control by vesicular-arbuscular mycorrhizal fungus inoculation in eggplant. J Japan Soc Hort Sci 64:555–561CrossRefGoogle Scholar
  43. Mcgonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501CrossRefGoogle Scholar
  44. Mollier A, Pellerin S (1999) Maize root system growth and development as influenced by phosphorus deficiency. J Exp Bot 50:487–497CrossRefGoogle Scholar
  45. Nair A, Kolet SP, Thulasiram HV, Bhargava S (2015) Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. Plant Biol 17:625–631CrossRefPubMedGoogle Scholar
  46. Oruc HH (2010) Fungicides and their effects on animals. In: Carisse O (ed) Fungicides. Intech Open Access, Rijeka, pp 349–362Google Scholar
  47. 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
  48. Pineda A, Zheng SJ, Van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514CrossRefPubMedGoogle Scholar
  49. Pozo MJ, Jung SC, Martínez-Medina A, López-Ráez JA, Azcón-Aguilar C, Barea JM (2013) Root allies: arbuscular mycorrhizal fungi help plants to cope with biotic stresses. In: Aroca R (ed) Symbiotic endophytes, soil biology. Springer, Berlin, pp 289–307CrossRefGoogle Scholar
  50. Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defense responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534CrossRefPubMedGoogle Scholar
  51. Pozo MJ, Azcón-Aguilar C, Dumas-Gaudot E, Barea JM (1999) β-1, 3-glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Sci 141:149–157CrossRefGoogle Scholar
  52. Randoux B, Renard D, Nowak E, Sanssené J, Courtois J, Durand R, Reignault P (2006) Inhibition of Blumeria graminis f. sp. tritici germination and partial enhancement of wheat defenses by Milsana. Phytopathology 96:1278–1286CrossRefPubMedGoogle Scholar
  53. Ratnayake M, Leonard RT, Menge JA (1978) Root exudation in relation to supply of phosphorus and its possible relevance to mycorrhizal formation. New Phytol 81:543–552CrossRefGoogle Scholar
  54. Sanders FE, Tinker PB (1973) Phosphate flow into mycorrhizal roots. Pestic Sci 4:385–395CrossRefGoogle Scholar
  55. Seutin B, Bodson B (2012) Lutte intégrée contre les maladies. In : Gembloux Agro-Bio Tech ULG (ed) Livre blanc « Céréales », Gembloux, pp 21–25Google Scholar
  56. Shrinkhala M (2011) Study on the bioprotective effect of endomycorrhizae against M. graminicola in rice. Dissertation. Catholic University of Leuven, BelgiumGoogle Scholar
  57. Slezack S, Dumas-Gaudot E, Paynot M, Gianinazzi S (2000) Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches? Mol Plant-Microbe Interact 13:238–241CrossRefPubMedGoogle Scholar
  58. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  59. St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1997) Inhibition of Fusarium oxysporum f. sp. dianthi in the non-Vam species Dianthus caryophyllus by co-culture with Tagetes patula companion plants colonized by Glomus intraradices. Can J Bot 75:998–1005CrossRefGoogle Scholar
  60. Steinkellner S, Hage-Ahmed K, García-Garrido JM, Illana A, Ocampo JA, Vierheilig H (2011) A comparison of wild-type, old and modern tomato cultivars in the interaction with the arbuscular mycorrhizal fungus Glomus mosseae and the tomato pathogen Fusarium oxysporum f. sp. lycopersici. Mycorrhiza 22:189–94CrossRefPubMedGoogle Scholar
  61. Temperini O, Rouphael Y, Parrano L, Biagiola E, Colla G, Mariotti R, Rea E, Rivera CM (2009) Nursery inoculation of pepper with arbuscular mycorrhizal fungi: an effective tool to enhance transplant performance. Acta Hort (ISHS) 807:591–596CrossRefGoogle Scholar
  62. Vargas JM Jr (1973) A benzimidazole resistant strain of Erysiphe graminis. Phytopathology 63:1366–1368CrossRefGoogle Scholar
  63. Wanlei W, Yong L, Chen J, Xianglong J, Haibo Z, Guang W (2009) Impact of intercropping aphid resistant wheat cultivars with oilseed rape on wheat aphid (Sitobion avenae) and its natural enemies. Acta Ecol Sin 29:186–191CrossRefGoogle Scholar
  64. Yao MK, Tweddell RJ, Desilets H (2002) Effect of two vesicular-arbuscular mycorrhizal fungi on the growth of micropropagated potato plantlets and on the extent of disease caused by Rhizoctonia solani. Mycorrhiza 12:235–242CrossRefPubMedGoogle Scholar
  65. Yokoyamai K, Aist JR, Bayles CJ (1991) A papilla-regulating extract that induces resistance to barley powdery mildew. Physiol Mol Plant Pathol 39:71–78CrossRefGoogle Scholar
  66. Zafar ZU, Athar HR (2013) Influence of different phosphorus regimes on disease resistance in two cotton (Gossypium hirsutum L.) cultivars differing in resistance to cotton leaf curl virus (CLCUV). Pak J Bot 45:617–627Google Scholar
  67. Zhu HH, Yao Q (2004) Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibits Ralstonia solanacearum. J Phytopathol 152:537–542CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • G Mustafa
    • 1
  • B Randoux
    • 1
  • B Tisserant
    • 1
  • J Fontaine
    • 1
  • M Magnin-Robert
    • 1
  • A Lounès-Hadj Sahraoui
    • 1
  • Ph Reignault
    • 1
  1. 1.Unité de Chimie Environnementale et Interactions sur le Vivant (UCEIV)Université du Littoral Côte d’OpaleCalais CedexFrance

Personalised recommendations