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.
Similar content being viewed by others
References
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 166:268–281
Atkinson D (1973) Some general effects of phosphorus deficiency on growth and development. New Phytol 72:101–111
Azcón R, Ocampo JA (1981) Factors affecting the vesicular-arbuscular infection and mycorrhizal dependency of thirteen wheat cultivars. New Phytol 87:677–685
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 64:1002–1017
Buchenauer H, Hellwald KH (1985) Resistance of Erysiphe graminis on barley and wheat to sterol C-14-demethylation inhibitors. EPPO Bull 15:459–66
Cameron DD, Neal AL, van Wees SCM, Ton J (2014) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545
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 13:579–592
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 8:12–16
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 39:269–287
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 58:256–261
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 425:973–1007
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 11:1017–1028
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 45:262–268
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 40:791–803
Fritz M, Jakobsen I, Lyngkjaer MF, Thordal-Christensen H, Pons-Kuehnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419
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 76:20–26
García-Garrido JM, Ocampo JA (1988) Interaction between Glomus mosseae and Erwinia carotovora and its effects on the growth of tomato plants. New Phytol 110:551–555
Gianinazzi S, Gollotte A, Binet MN, Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530
Gilbert N (2009) Environment: the disappearing nutrient. Nature 461:716–718
Görg R, Hollricher K, Schulze-Lefert P (1993) Functional analysis and RFLP-mediated mapping of the Mlg resistance locus in barley. Plant J3:857–866
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 127–140
Grandison GS, Cooper KM (1986) Interaction of vesicular-arbuscular mycorrhizae and cultivars of alfalfa susceptible and resistant to Meloidogyne hapla. J Nematol 18:141–149
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 85:3–14
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 9:65–70
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 63:3657–3672
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 755–762
Hetrick BAD, Wilson GWT, Gill BS, Cox TS (1995) Chromosome location of mycorrhizal responsive genes in wheat. Can J Bot 73:891–897
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Stn 347:1–32.
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 119:1251–1260
Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–64
Kapoor R (2008) Induced resistance in mycorrhizal tomato is correlated to concentration of jasmonic acid. On Line J BiolSci 8:49–56
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 16:443–446
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 68:2344–2352
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 8:51–57
Le Souder C, Mazieres C, Rodes V (1998) La fertilisation minérale sur le blé : des pratiques régionales diversifiées. AGRESTE—LES CAHIERS 30:31–38
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 21:237–243
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 24:592–602
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 35:3465–3475
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 50:529–544
Lynch JP, Lauchli A, Epstein E (1991) Vegetative growth of the common bean in response to phosphorus nutrition. Crop Sci 31:380–387
Mark GL, Cassells AC (1996) Genotype‐dependence in the interaction between Glomus fistulosum, Phytophthora fragariae and the wild strawberry (Fragaria vesca). Plant Soil 185:233–239
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 64:555–561
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 115:495–501
Mollier A, Pellerin S (1999) Maize root system growth and development as influenced by phosphorus deficiency. J Exp Bot 50:487–497
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 17:625–631
Oruc HH (2010) Fungicides and their effects on animals. In: Carisse O (ed) Fungicides. Intech Open Access, Rijeka, pp 349–362
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 55:158–161
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 15:507–514
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 289–307
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 53:525–534
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 141:149–157
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 96:1278–1286
Ratnayake M, Leonard RT, Menge JA (1978) Root exudation in relation to supply of phosphorus and its possible relevance to mycorrhizal formation. New Phytol 81:543–552
Sanders FE, Tinker PB (1973) Phosphate flow into mycorrhizal roots. Pestic Sci 4:385–395
Seutin B, Bodson B (2012) Lutte intégrée contre les maladies. In : Gembloux Agro-Bio Tech ULG (ed) Livre blanc « Céréales », Gembloux, pp 21–25
Shrinkhala M (2011) Study on the bioprotective effect of endomycorrhizae against M. graminicola in rice. Dissertation. Catholic University of Leuven, Belgium
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 13:238–241
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
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 75:998–1005
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 22:189–94
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) 807:591–596
Vargas JM Jr (1973) A benzimidazole resistant strain of Erysiphe graminis. Phytopathology 63:1366–1368
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 29:186–191
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 12:235–242
Yokoyamai K, Aist JR, Bayles CJ (1991) A papilla-regulating extract that induces resistance to barley powdery mildew. Physiol Mol Plant Pathol 39:71–78
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 45:617–627
Zhu HH, Yao Q (2004) Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibits Ralstonia solanacearum. J Phytopathol 152:537–542
Acknowledgments
The Ministry of Higher Education in Syria mediated by Aleppo University supported this work.
Author information
Authors and Affiliations
Corresponding author
Additional information
A. Lounès-Hadj Sahraoui and Ph. Reignault are co-last authors.
Rights and permissions
About this article
Cite this article
Mustafa, G., Randoux, B., Tisserant, B. et al. Phosphorus supply, arbuscular mycorrhizal fungal species, and plant genotype impact on the protective efficacy of mycorrhizal inoculation against wheat powdery mildew. Mycorrhiza 26, 685–697 (2016). https://doi.org/10.1007/s00572-016-0698-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-016-0698-z