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Induction of DIMBOA accumulation and systemic defense responses as a mechanism of enhanced resistance of mycorrhizal corn (Zea mays L.) to sheath blight

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Abstract

Arbuscular mycorrhizas are the most important symbioses in terrestrial ecosystems and they enhance the plant defense against numerous soil-borne pathogenic fungi and nematodes. Two corn (Zea mays) varieties, Gaoyou-115 that is susceptible to sheath blight disease caused by Rhizoctonia solani and Yuenong-9 that is resistant, were used for mycorrhizal inoculation in this study. Pre-inoculation of susceptible Gaoyou-115 with arbuscular mycorrhizal fungus (AMF) Glomus mosseae significantly reduced the disease incidence and disease severity of sheath blight of corn. HPLC analysis showed that AMF inoculation led to significant increase in 2,4-dihydroxy-7-methoxy-2 H-1,4-benzoxazin-3(4 H)-one (DIMBOA) accumulation in the roots of both corn varieties and in leaves of resistant Yuenong-9. R. solani inoculation alone did not result in accumulation of DIMBOA in both roots and leaves of the two corn varieties. Our previous study showed that DIMBOA strongly inhibited mycelial growth of R. solani in vitro. Real-time PCR analysis showed that mycorrhizal inoculation itself did not affect the transcripts of most genes tested. However, pre-inoculation with G. mosseae induced strong responses of three defense-related genes PR2a, PAL, and AOS, as well as BX9, one of the key genes in DIMBOA biosynthesis pathway, in the leaves of corn plants of both Yuenong-9 and Gaoyou-115 after the pathogen attack. Induction of defense responses in pre-inoculated plants was much higher and quicker than that in non-inoculated plants upon R. solani infection. These results indicate that induction of accumulation of DIMBOA, an important phytoalexin in corn, and systemic defense responses by AMF, plays a vital role in enhanced disease resistance of mycorrhizal plants of corn against sheath blight. This study also suggests that priming is an important mechanism in mycorrhiza-induced resistance.

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Abbreviations

AMF:

Arbuscular mycorrhizal fungus

DIMBOA:

2,4-dihydroxy-7-methoxy-2 H-1,4- benzoxazin-3(4 H)-one

PAL:

Phenylalanine ammonia-lyase

AOS:

Allene oxide synthase

References

  • Akköprü A, Demir S (2005) Biological control of Fusarium wilt in tomato caused by Fusarium oxysporum f. sp. lycopersici by AMF Glomus intraradices and some Rhizobacter. J Phytopathol 153:544–550

    Article  Google Scholar 

  • Araim G, Saleem A, Arnason JT, Charest C (2009) Root colonization by an arbuscular mycorrhizal (AM) fungus increases growth and secondary metabolism of purple coneflower, Echinacea purpurea (L.) Moench. J Agr Food Chem 57:2255–2258

    Article  CAS  Google Scholar 

  • Azcón-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens—an overview of the mechanisms involved. Mycorrhiza 6:457–464

    Article  Google Scholar 

  • Bednarek P, Osbourn A (2009) Plant-microbe interactions: chemical diversity in plant defense. Science 324:746–748

    Article  CAS  PubMed  Google Scholar 

  • Bi HH, Song YY, Zeng RS (2007) Biochemical and molecular responses of host plants to mycorrhizal infection and their roles in plant defence. Allelopathy J 20:15–28

    Google Scholar 

  • Bohidar K, Wratten SD, Niemeyer HM (1986) Effects of hydroxamic acids on the resistance of wheat to the aphid Sitobion avenae. Ann Appl Biol 109:193–198

    Article  CAS  Google Scholar 

  • Bravo HR, Lazo W (1993) Antimicrobial activity of cereal hydroxamic acids and related compounds. Phytochemistry 33:569–571

    Article  CAS  Google Scholar 

  • Cambier V, Hance T, de Hoffmann E (1999) Non-injured maize contains several 1,4-benzoxazin-3-one related compounds but only as glucoconjugates. Phytochem Anal 10:119–126

    Article  CAS  Google Scholar 

  • Chellappan P, Christy SAA, Mahadevan A (2002) Multiplication of arbuscular mycorrhizal fungi on roots. In: Mukerji KG, Manoharachary C, Chamola BP (eds) Techniques in mycorrhizal studies. Kluwer Academic Publishers, The Netherlands, pp 285–297

    Chapter  Google Scholar 

  • Cicek M, Esen A (1999) Expression of soluble and catalytically active plant (monocot) β -glucosidases in E. coli. Biotechnol Bioeng 63:392–400

    Article  CAS  PubMed  Google Scholar 

  • Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant–pathogen interactions. Trends Plant Sci 7:210–216

    Article  CAS  PubMed  Google Scholar 

  • Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071

    Article  CAS  PubMed  Google Scholar 

  • Corcuera LJ, Woodward MD, Helgeson JP, Kelman A, Upper C (1978) 2,4-Dihydroxy-7-methoxy-2 H-1,4-benzoxazin-3(4 H)-one, an inhibitor from Zea mays with differential activity against soft rotting Erwinia species. Plant Physiol 61:791–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cordero MJ, Raventos D, San Segundo B (1994) Differential expression and induction of chitinases and β-1,3-glucanases in response to fungal infection during germination of maize seeds. Mol Plant Microbe Interact 7:23–31

    Article  CAS  Google Scholar 

  • Cordier C, Gianinazzi S, Gianinazzi Pearson V (1996) Colonisation patterns of root tissues by Phytophthora nicotianae var. parasitica related to reduced disease in mycorrhizal tomato. Plant Soil 185:223–232

    Article  CAS  Google Scholar 

  • Cordier C, Pozo M, Barea J, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defence responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant Microbe Interact 11:1017–1028

    Article  CAS  Google Scholar 

  • Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847

    Article  CAS  PubMed  Google Scholar 

  • Douds DD, Millner P (1999) Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agric Ecosyst Environ 74:77–93

    Article  Google Scholar 

  • Elsen A, Gervacio D, Swennen R, De Waele D (2008) AMF-induced bioprotection against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18:251–256

    Article  CAS  PubMed  Google Scholar 

  • Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci U S A 101:1781–1785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Figueroa CC, Koenig C, Araya C, Santos MJ, Niemeyer HM (1999) Effect of DIMBOA, a hydroxamic acid from cereals, on peroxisomal and mitochondrial enzymes from aphids: evidence for the presence of peroxisomes in aphids. J Chem Ecol 25:2465–2475

    Article  CAS  Google Scholar 

  • Frey M, Chomet P, Glawischnig E, Stettner C, Grun S, Winkl-mair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277:696–699

    Article  CAS  PubMed  Google Scholar 

  • Fritz M, Jakobsen I, Lyngkjær MF, Thordal-Christensen H, Pons-Kühnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • García-Garrido JM, Ocampom JA (1989) Effect of VA mycorrhizal infection of tomato on damage caused by Pseudomonas syringae. Soil Biol Biochem 21:165–167

    Article  Google Scholar 

  • Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ 113:17–35

    Article  Google Scholar 

  • Grayer RJ, Kokubun T (2001) Plant-fungal interactions: the search for phytoalexins and other antifungal compounds from higher plants. Phytochemistry 56:253–263

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez C, Castanera P, Torres V (1988) Wound-induced changes in DIMBOA (2,4 dihydroxy-7-methoxy-2 H-1,4 benzoxzinone-3(4 H)-one) concentration in maize plants caused by Sesamia nonagrioides (Lepidoptera: Noctuidae). Ann Appl Biol 113:447–454

    Article  CAS  Google Scholar 

  • Hashimoto Y, Shudo K (1996) Chemistry of biologically active benzoxazinoids. Phytochemistry 43:551–559

    Article  CAS  PubMed  Google Scholar 

  • Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang JH, Zeng RS, Luo SM (2006) Studies on disease resistance of maize toward sheath blight induced by arbuscular mycorrhizal fungi. Chin J Appl Ecol Agric 14(3):167–169 (in Chinese)

    Google Scholar 

  • Huang JH, Zeng RS, Luo SM, Gu WX, Nie CR, Cao M, Li XH (2007) Antifungus activity of DIMBOA from maize seedlings compared with several phenolic acids. Nat Prod Res Dev 19:572–577

    CAS  Google Scholar 

  • Jonczyk R, Schmidt H, Osterrieder A, Fiesselmann A, Schullehner K, Haslbeck M, Sicker D, Hofmann D, Yalpani N, Simmons C, Frey M, Gierl A (2008) Elucidation of the final reactions of DIMBOA-glucoside biosynthesis in maize: characterization of Bx6 and Bx7. Plant Physiol 146:1053–1063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khaosaad T, Garcia-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol Biochem 39:727–734

    Article  CAS  Google Scholar 

  • Kiefer E, Heller W, Ernst D (2000) A simple and efficient protocol for isolation of functional RNA from plant tissues rich in secondary metabolites. Plant Mol Biol Rep 18:33–39

    Article  CAS  Google Scholar 

  • Li HR, Wu BC, Yan SQ (1998) Aetiology of Rhizoctonia in sheath blight of maize in Sichuan. Plant Pathol 47(1):16–21

    Article  Google Scholar 

  • Liu RJ (1995) Effect of vesicular-arbuscular mycorrhizal fungi on verticillium wilt of cotton. Mycorrhiza 5:293–297

    Article  Google Scholar 

  • Liu JH, Wang XM, Fang ZW, Li YL (1999) Breeding and cultivated technology of high quality and high yield new corn variety Yuenong-9. Guangdong Agricultural Sciences 4:13–14, in Chinese

    Google Scholar 

  • Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Maldonado-Bonilla LD, Betancourt-Jiménez M, Lozoya-Gloria E (2008) Local and systemic gene expression of sesquiterpene phytoalexin biosynthetic enzymes in plant leaves. Eur J Plant Pathol 121:439–449

    Article  CAS  Google Scholar 

  • Mauch-mani B, Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8:203–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morant AV, Jorgensen K, Jorgensen C, Paquette SM, Sánchez-Pérez R, Møller L, Bak S (2008) β-Glucosidases as detonators of plant chemical defense. Phytochemistry 69:1795–1813

    Article  CAS  PubMed  Google Scholar 

  • Morse S, Wratten SD, Edwards PJ, Niemeyer HM (1991) Changes in the hydroxamic acid content of maize leaves with time and after artificial damage: implications for insect attack. Ann Appl Biol 119:239–249

    Article  CAS  Google Scholar 

  • Mukerji KG, Manoharachary C, Chamola BP (2002) Techniques in mycorrhizal studies. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • Niemeyer HM (1988) Hydroxamic acids (4-hydroxy-1,4-benzoxazin-3-ones), defence chemicals in the Gramineae. Phytochemistry 27:3349–3358

    Article  CAS  Google Scholar 

  • Niemeyer HM, Perez FJ (1995) Potential of hydroxamic acids in the control of cereal pests, diseases and weeds. In: Inderjit KM, Dakshini M, Einhellig FA (eds) Allelopathy organisms, processes, and applications. American Chemical Society, Washington DC, pp 260–270

    Google Scholar 

  • Niemeyer HM, Pesel E, Copaja SV, Bravo HR, Franke S, Francke W (1989) Changes in hydroxamic acid levels of wheat plants induced by aphid feeding. Phytochemistry 28:447–449

    Article  CAS  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  CAS  PubMed  Google Scholar 

  • Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcon-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophtora infection in tomato plants. J Exp Bot 53:525–534

    Article  CAS  PubMed  Google Scholar 

  • Rostás M (2007) The effects of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one on two species of Spodoptera and the growth of Setosphaeria turcica in vitro. J Pest Sci 80:35–40

    Article  Google Scholar 

  • Ruiz-Lozano JM, Azcón R, Palma JM (1996) Superoxide dismutase activity in arbuscular mycorrhizal Lactuca sativa plants subjected to drought stress. New Phytol 134:327–333

    Article  CAS  Google Scholar 

  • Safir G (1968) The influence of vesicular mycorrhiza on the resistance of onion to Pyrenochaeta terrestris. MS. Thesis, University of Illinois, Urbana, USA

  • Saunders M, Kohn LM (2008) Host-synthesized secondary compounds influence the in vitro interactions between fungal endophytes of maize. Appl Environ Microb 74:136–142

    Article  CAS  Google Scholar 

  • Schaller F, Schaller A, Stintz A (2005) Biosynthesis and metabolism of jasmonates. J Plant Growth Regul 23:179–199

    Article  Google Scholar 

  • Sicker D, Frey M, Schulz M, Gierl A (2000) Role of natural benzoxazinones in the survival strategy of plants. Int Rev Cytol 198:319–346

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, Cambridge

    Google Scholar 

  • Søltoft M, Jørgensen LN, Svensmark B, Fomsgaard IS (2008) Benzoxazinoid concentrations show correlation with Fusarium Head Blight resistance in Danish wheat varieties. Biochem Syst Ecol 36:245–259

    Article  Google Scholar 

  • Sriram S, Raguchander T, Vidhyasekaran P, Muthukrishnan S, Samiyappan R (1997) Genetic relatedness with special reference to virulence among the isolates of Rhizoctonia solani causing sheath blight in rice. J Plant Dis Prot 104:260–271

    Google Scholar 

  • St-Arnaud M, Vujanovic V (2007) Effect of the arbuscular mycorrhizal symbiosis on plant diseases and pests. In: Hamel C, Plenchette C (eds) Mycorrhizae in crop production: applying knowledge. Haworth, Binghampton, pp 67–122

    Google Scholar 

  • Ton J, D'Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TC (2006) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26

    Article  PubMed  Google Scholar 

  • Toussaint JP, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17:291–297

    Article  CAS  PubMed  Google Scholar 

  • van Hulten M, Pelser M, Van Loon LC, Pieterse CMJ, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci USA 103:5602–5607

    Article  PubMed  PubMed Central  Google Scholar 

  • van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  Google Scholar 

  • Varma A, Hock B (1995) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, Berlin

    Book  Google Scholar 

  • Weibull J, Niemeyer HM (1995) Changes in dihydroxymethoxybenzoxazinone glycoside content in wheat plants infected by three plant pathogenic fungi. Physiol Mol Plant Pathol 47:201–212

    Article  CAS  Google Scholar 

  • Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227

    Article  Google Scholar 

  • Wilkes MA, Marshall DR, Copeland L (1999) Hydroxamic acids in cereal roots inhibit the growth of take-all. Soil Biol Biochem 31:1831–1836

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zubek S, Stojakowska A, Anielska T, Turnau K (2010) Arbuscular mycorrhizal fungi alter thymol derivative contents of Inula ensifolia L. Mycorrhiza 20:497–504

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was financially supported by the National 973 project of China (2011CB100400), Natural Science Foundation of China (31070388, 30870390), Guangdong Province Universities and Colleges Pearl River Scholar Funded Scheme (2010), Guangdong Natural Science Foundation of China (8451064201001012), Guangdong Science and Technology Plan Project (2008A030101008, 2008B021500001). We thank Dr. Yinglong Chen at the University of Western Australia for helpful comments on manuscript reversion.

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  1. Key Laboratory of Ecological Agriculture, Ministry of Agriculture, South China Agricultural University, Wushan, Guangzhou, 510642, People’s Republic of China

    Yuan Yuan Song, Man Cao, Li Jun Xie, Xiao Ting Liang, Ren Sen Zeng, Yi Juan Su, Rui Long Wang & Shi Ming Luo

  2. Key Laboratory of Agroecology and Rural Environment of Guangdong Regular Higher Education Institutions, South China Agricultural University, Wushan, Guangzhou, 510642, People’s Republic of China

    Yuan Yuan Song, Man Cao, Li Jun Xie, Xiao Ting Liang, Ren Sen Zeng, Yi Juan Su, Rui Long Wang & Shi Ming Luo

  3. Institute of Tropical and Subtropical Ecology, South China Agricultural University, Wushan, Guangzhou, 510642, People’s Republic of China

    Yuan Yuan Song, Man Cao, Li Jun Xie, Xiao Ting Liang, Ren Sen Zeng, Yi Juan Su, Jing Hua Huang, Rui Long Wang & Shi Ming Luo

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  1. Yuan Yuan Song
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Song, Y.Y., Cao, M., Xie, L.J. et al. Induction of DIMBOA accumulation and systemic defense responses as a mechanism of enhanced resistance of mycorrhizal corn (Zea mays L.) to sheath blight. Mycorrhiza 21, 721–731 (2011). https://doi.org/10.1007/s00572-011-0380-4

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