Abstract
The interactions between arbuscular mycorrhizal fungi (AMF) and non-host species are poorly studied. Particularly scarce is information on members of the Amaranthaceae/Chenopodiaceae family. Sugar beet (Beta vulgaris) plants were co-cultivated with a host species (Hordeum vulgare) in the presence (+AMF) or absence of Rhizophagus intraradices to explore the hypothesis that the presence of an active, pre-established AMF mycelium induces defense responses in the non-host species. Biomass of sugar beet did not respond to the +AMF treatment, while its root exudation of organic acids and phenolic acids was drastically decreased upon co-cultivation with +AMF barley. The most conspicuous effect was observed on a wide range of potential defense parameters being differentially influenced by the +AMF treatment in this non-host species. Antioxidant defense enzymes were activated and the level of endogenous jasmonic acid was elevated accompanied by nitric oxide accumulation and lignin deposition in the roots after long-term +AMF treatment. In contrast, significant reductions in the levels of endogenous salicylic acid and tissue concentration and exudation of phenolic acids indicated that AM fungus hyphae in the substrate did not induce a hypersensitive-type response in the sugar beet roots and downregulated certain chemical defenses. Our results imply that the fitness of this non-host species is not reduced when grown in the presence of an AMF mycelium because of balanced defense costs. Further studies should address the question of whether or not such modulation of defense pattern influences the pest resistance of sugar beet plants under field conditions.
Similar content being viewed by others
Data availability
Not applicable.
References
Allen MF, Allen EB, Friese CF (1989) Responses of the non-mycotrophic plant Salsola kali to invasion by vesicular–arbuscular mycorrhizal fungi. New Phytol 111:45–49
Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390
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
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681
Bergmann W (1993) Ernährungsstörungen bei Kuturpflanzen. Ed 3. Gustav Fischer Verlag, Jena
Bhuiyan NH, Selvaraj G, Wei Y, King J (2009) Role of lignification in plant defense. Plant Signal Behav 4:158–159
Blilou I, Ocampo JA, García-Garrido JM (2000) Induction of Ltp (lipid transfer protein) and Pal (phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J Exp Bot 51:1969–1977
Bolton MD (2009) Primary metabolism and plant defense—fuel for the fire. Mol Plant-Microbe Interact 22:487–497
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77
Brundrett MC (2017) Global diversity and importance of mycorrhizal and nonmycorrhizal plants. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis, Ecological studies, analysis and synthesis, vol 230. Springer, Cham, pp 533–556
Casado-Vela J, Sellés S, Bru R (2005) Purification and kinetic characterization of polyphenol oxidase from tomato fruits (Lycopersicon esculentum cv. Muchamiel). J Food Biochem 29:381–401
Chen BJ, Hajiboland R, Bahrami-Rad S, Moradtalab N, Anten NP (2019) Presence of belowground neighbors activates defense pathways at the expense of growth in tobacco plants. Front Plant Sci 10:751
Chen YT, Wang Y, Yeh KC (2017) Role of root exudates in metal acquisition and tolerance. Curr Opin Plant Biol 39:66–72
Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60:391–408
Cosme M, Fernández I, Van der Heijden MGA, Pieterse CMJ (2018) Nonmycorrhizal plants: the exceptions that prove the rule. Trends Plant Sci 23:577–587
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47
de Pinto MC, Tommasi F, De Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells. Plant Physiol 130:698–708
Delaux PM, Varala K, Edger PP, Coruzzi GM, Pires JC, Ané JM (2014) Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genet 10:e1004487
Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. PNAS 98:13454–11349
Derksen H, Rampitsch C, Daayf F (2013) Signaling cross-talk in plant disease resistance. Plant Sci 207:79–87
Dickerson DP, Pascholati SF, Hagerman AE, Butler LG, Nicholson RL (1984) Phenylalanine ammonia-lyase and hydroxycinnamate: CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum. Physiol Plant Pathol 25:111–123
Fernández I, Cosme M, Stringlis IA, Yu K, de Jonge R, van Wees SM, Pozo MJ, Pieterse CM, Van der Heijden MG (2019) Molecular dialogue between arbuscular mycorrhizal fungi and the nonhost plant Arabidopsis thaliana switches from initial detection to antagonism. New Phytol 223:867–881
Francis R, Read DJ (1995) Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Can J Bot 73:1301–1309
García-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386
Giovanetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular mycorrhizal infection in roots. New Phytol 84:489–500
Haase S, Neumann G, Kania A, Kuzyakov Y, Römheld V, Kandeler E (2007) Elevation of atmospheric CO2 and N-nutritional status modify nodulation, nodule-carbon supply, and root exudation of Phaseolus vulgaris L. Soil Biol Biochem 39:2208–2221
Hajiboland R (2013) Role of arbuscular mycorrhiza in amelioration of salinity. In: Ahmad P, Azooz MM, Prasad MNV (eds) Salt stress in plants. Springer, New York, pp 301–354
Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327
Hajiboland R, Bastani S, Bahrami-Rad S, Poschenrieder C (2015) Interactions between aluminum and boron in tea (Camellia sinensis) plants. Acta Physiol Plant 37:54
Hajiboland R, Moradtalab N, Aliasgharzad N, Eshaghi Z, Feizy J (2018) Silicon influences growth and mycorrhizal responsiveness in strawberry plants. Physiol Mol Biol Plants 24:1103–1115
Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42
Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110
Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468
Jaiswal PC (2004) Soil, plant and water analysis. Kalyani Publishers, New Delhi
Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91
Jaworski EG (1971) Nitrate reductase assay in intact plant tissues. Biochem Biophys Res Commun 43:1274–1279
Johnson CM, Stout PR, Broyer TC, Carlton AB (1957) Comparative chloride requirements of different plant species. Plant Soil 8:337–353
Johnson NC (1998) Responses of Salsola kali and Panicum virgatum to mycorrhizal fungi, phosphorus and soil organic matter: implications for reclamation. J Appl Ecol 35:86–94
Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reaction in plant defense and growth induction. Plant Cell Rep 21:829–837
Khaosaad T, Krenn L, Medjakovic S, Ranner A, Lössl A, Nell M, Jungbauer A, Vierheilig H (2008) Effect of mycorrhization on the isoflavone content and the phytoestrogen activity of red clover. J Plant Physiol 165:1161–1167
Khorassani R, Hettwer U, Ratzinger A, Steingrobe B, Karlovsky P, Claassen N (2011) Citramalic acid and salicylic acid in sugar beet root exudates solubilize soil phosphorus. BMC Plant Biol 11:121
Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y (2000) Nitric oxide and salicylic acid signaling in plant defense. PNAS 97:8849–8855
Lambers H, Teste FP (2013) Interactions between arbuscular mycorrhizal and non-mycorrhizal plants: do non-mycorrhizal species at both extremes of nutrient availability play the same game? Plant Cell Environ 36:1911–1915
Larose G, Chênevert R, Moutoglis P, Gagné S, Piché Y, Vierheilig H (2002) Flavonoid levels in roots of Medicago sativa are modulated by the developmental stage of the symbiosis and the root colonizing arbuscular mycorrhizal fungus. J Plant Physiol 159:1329–1339
Latef AA, Hashem A, Rasool S, Abd-Allah EF, Alqarawi AA, Egamberdieva D, Jan S, Anjum NA, Ahmad P (2016) Arbuscular mycorrhizal symbiosis and abiotic stress in plants: a review. J Plant Biol 59:407–426
Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82:1016–1045
Lehmann S, Serrano M, L’Haridon F, Tjamos SE, Metraux JP (2015) Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry 112:54–62
Lekberg Y, Rosendahl S, Olsson PA (2015) The fungal perspective of arbuscular mycorrhizal colonization in ‘nonmycorrhizal’ plants. New Phytol 205:1399–1403
Lenoir I, Fontaine J, Sahraoui AL (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15
Li L, Tilman D, Lambers H, Zhang FS (2014) Biodiversity and overyielding: insights from below-ground facilitation of intercropping in agriculture. New Phytol 203:63–69
Lucena C, Porras R, Romera FJ, Alcántara E, García MJ, Pérez-Vicente R (2018) Similarities and differences in the acquisition of Fe and P by dicot plants. Agronomy 8:148
Lucini L, Colla G, Moreno MB, Bernardo L, Cardarelli M, Terzi V, Bonini P, Rouphael Y (2019) Inoculation of Rhizoglomus irregulare or Trichoderma atroviride differentially modulates metabolite profiling of wheat root exudates. Phytochemistry 157:158–167
Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal Behav 5:359–368
Markham JH, Zekveld C (2007) Nitrogen fixation makes biomass allocation to roots independent of soil nitrogen supply. Can J Bot 85:787–793
Matsumura A, Horii S, Ishii T (2007) Effects of arbuscular mycorrhizal fungi and intercropping with bahiagrass on growth and anti-oxidative enzyme activity of radish. J Japan Soc Hort Sci 76:224–229
Mika A, Minibayeva F, Beckett R, Lüthje S (2004) Possible functions of extracellular peroxidases in stress-induced generation and detoxification of active oxygen species. Phytochem Rev 3:173–193
Mnasri M, Janoušková M, Rydlová J, Abdelly C, Ghnaya T (2017) Comparison of arbuscular mycorrhizal fungal effects on the heavy metal uptake of a host and a non-host plant species in contact with extraradical mycelial network. Chemosphere 171:476–484
Moradtalab N, Weinmann M, Walker F, Höglinger B, Ludewig U, Neumann G (2018) Silicon improves chilling tolerance during early growth of maize by effects on micronutrient homeostasis and hormonal balances. Front Plant Sci 9:420
Morrison IM (1972) A semi-micro method for the determination of lignin and its use in predicting the digestibility of forage crops. J Sci Food Agric 23:455–463
Mur LA, Prats E, Pierre S, Hall MA, Hebelstrup KH (2013) Integrating nitric oxide into salicylic acid and jasmonic acid/ethylene plant defense pathways. Front Plant Sci 4:215
Naoumkina MA, Zhao Q, Gallego-Giraldo LI, Dai X, Zhao PX, Dixon RA (2010) Genome-wide analysis of phenylpropanoid defence pathways. Mol Plant Pathol 11:829–846
Neilson EH, Goodger JQ, Woodrow IE, Møller BL (2013) Plant chemical defense: at what cost? Trends Plant Sci 18:250–258
Palmer IA, Shang Z, Fu ZQ (2017) Salicylic acid-mediated plant defense: recent developments, missing links, and future outlook. Front Biol 12:258–270
Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265
Pongrac P, Vogel-Mikuš K, Regvar M, Tolrà R, Poschenrieder C, Barceló J (2008) Glucosinolate profiles change during the life cycle and mycorrhizal colonization in a Cd/Zn hyperaccumulator Thlaspi praecox (Brassicaceae). J Chem Ecol 34:1038–1044
Poveda J, Hermosa R, Monte E, Nicolás C (2019) Trichoderma harzianum favours the access of arbuscular mycorrhizal fungi to non-host Brassicaceae roots and increases plant productivity. Sci Rep 9:11650
Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398
Pozo MJ, Verhage A, García-Andrade J, García JM, Azcón-Aguilar C (2009) Priming plant defence against pathogens by arbuscular mycorrhizal fungi. In: Azcón-Aguilar C, Barea J, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas-functional processes and ecological impact. Springer, Berlin, pp 123–135
Regvar M, Vogel K, Irgel N, Wraber T, Hildebrandt U, Wilde P, Bothe H (2003) Colonization of pennycresses (Thlaspi spp.) of the Brassicaceae by arbuscular mycorrhizal fungi. J Plant Physiol 160:615–626
Rinaudo V, Bàrberi P, Giovannetti M, van der Heijden MG (2010) Mycorrhizal fungi suppress aggressive agricultural weeds. Plant Soil 333:7–20
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, Ed 3. Academic Press, New York
Song YY, Ye M, Li CY, Wang RL, Wei XC, Luo SM, Zeng RS (2013) Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. J Chem Ecol 39:1036–1044
Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306
Sun J, Zhang X, Broderick M, Fein H (2003) Measurement of nitric oxide production in biological systems by using Griess reaction assay. Sensors 3:276–284
Swain T, Hillis EE (1959) The phenolic constituents of Prunus domestica I. The quantitative analysis of phenolic constituents. J Sci Food Agric 10:63–68
Tertivanidis K, Goudoula C, Vasilikiotis C, Hassiotou E, Perl-Treves R, Tsaftaris A (2004) Superoxide dismutase transgenes in sugar beets confer resistance to oxidative agents and the fungus C. beticola. Transgenic Res 13:225–233
Tong Y, Gabriel-Neumann E, Krumbein A, Ngwene B, George E, Schreiner M (2015) Interactive effects of arbuscular mycorrhizal fungi and intercropping with sesame (Sesamum indicum) on the glucosinolate profile in broccoli (Brassica oleracea var. Italica). Environ Exp Bot 109:288–295
Torres MA (2010) ROS in biotic interactions. Physiol Plant 138:414–429
van Dam NM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21:256–265
Veiga RS, Faccio A, Genre A, Pieterse CM, Bonfante P, van der Heijden MG (2013) Arbuscular mycorrhizal fungi reduce growth and infect roots of the non-host plant Arabidopsis thaliana. Plant Cell Environ 36:1926–1937
Veiga RS, Howard K, van der Heijden MG (2012) No evidence for allelopathic effects of arbuscular mycorrhizal fungi on the non-host plant Stellaria media. Plant Soil 360:319–331
Vierheilig H, Bennett R, Kiddle G, Kaldorf M, Ludwig-Müller J (2000) Differences in glucosinolate patterns and arbuscular mycorrhizal status of glucosinolate-containing plant species. New Phytol 146:343–352
Wang Y, Loake GJ, Chu C (2013) Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. Front Plant Sci 4:314
Wehner J, Antunes PM, Powell JR, Mazukatow J, Rillig MC (2010) Plant pathogen protection by arbuscular mycorrhizas: a role for fungal diversity? Pedobiologia 53:197–201
Yang L (2016) Root exudation pattern of sugar beet (Beta vulgaris L.) as influenced by light intensity and P deficiency. In: Dissertation. University of Göttingen, Germany
Zhang H, Qin Z, Chu Y, Li X, Christie P, Zhang J, Gai J (2019) Interactions between arbuscular mycorrhizal fungi and non-host Carex capillacea. Mycorrhiza 29:149–157
Zhang RQ, Zhu HH, Zhao HQ, Yao Q (2013) Arbuscular mycorrhizal fungal inoculation increases phenolic synthesis in clover roots via hydrogen peroxide, salicylic acid and nitric oxide signaling pathways. J Plant Physiol 170:74–79
Acknowledgments
The authors are grateful to Dr. Günter Neumann (Institute of Crop Science, University of Hohenheim, Germany) for providing analytical facilities for organic and phenolic acids and Dr. Frank Walker (Institute of Phytomedicine, University of Hohenheim, Germany) for SA and JA analysis facilities.
Code availability
Not applicable.
Funding
This work was financially supported by the University of Tabriz. CP is supported by the Spanish MICINN project PID2019-104000RB-100.
Author information
Authors and Affiliations
Contributions
RH conceived and designed the experiments, analyzed and interpreted the data, and wrote the manuscript in consultation with NA and CP; NS cultivated plants and performed physiological plant analyses; NM analyzed organic acids, phenolics, SA, and JA; KS performed statistical analyses; CP and NA critically revised the manuscript. All authors discussed the results and contributed to the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hajiboland, R., Sadeghzadeh, N., Moradtalab, N. et al. The arbuscular mycorrhizal mycelium from barley differentially influences various defense parameters in the non-host sugar beet under co-cultivation. Mycorrhiza 30, 647–661 (2020). https://doi.org/10.1007/s00572-020-00978-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-020-00978-4