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Cover crop species affect mycorrhizae-mediated nutrient uptake and pest resistance in maize

  • Ebony G. Murrell (a1), Swayamjit Ray (a2), Mary E. Lemmon (a1), Dawn S. Luthe (a2) and Jason P. Kaye (a1)...


Arbuscular mycorrhizal fungi (AMF) can increase plant nutrient uptake and chemical defense production, both of which can improve plants’ ability to resist insect herbivory. Cover crops—non-commercial species planted in between cash crops in a crop rotation—can naturally alter both soil nutrients and AMF. We tested whether different cover crop species alter AMF colonization, plant nutrient status and plant–insect interactions in a subsequent maize crop. Cover crop species were either non-mycorrhizal, non-leguminous (canola, forage radish), mycorrhizal non-leguminous (cereal rye, oats), mycorrhizal leguminous (clover, pea) or absent (fallow). We measured the cascading consequences of cover crop treatment on maize root AMF colonization, maize growth and performance of an herbivorous insect (European corn borer) feeding on the maize. Maize AMF colonization was greater in plots previously planted with mycorrhizal (rye, oats) than non-mycorrhizal (canola, radish) cover crops or no cover crop (fallow). AMF colonization was linked to increased plant phosphorous and nitrogen, and maize growth increased with low plant N:P. Induced jasmonic acid pathway plant defenses increased with increasing maize growth and AMF colonization. European corn borer survivorship decreased with lower plant N:P, and insect development rate decreased with increased induced plant defenses. Our data describe a cascade in which cover crop species selection can increase or decrease mycorrhizal colonization of subsequent maize crop roots, which in turn impacts phosphorus uptake and may affect herbivory resistance in the maize. These results suggest that farmers could select cover crop species to manage nutrient uptake and pest resistance, in order to amend or limit fertilizer and pesticide use.


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Author for correspondence: Ebony G. Murrell, E-mail:


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Current address: The Land Institute, 2440 E Water Well Rd, Salina, KS 67401, USA.



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Baulcombe, D, Crute, I, Davie, B, Dunwell, J, Gale, M, Jones, J, Pretty, J, Sutherland, W and Toulmin, C (2009) Reaping the Benefits: Science and The Sustainable Intensification of Global Agriculture. London: The Royal Society.
Berendsen, RL, Pieterse, CMJ and Bakker, PA (2012) The rhizosphere microbiome and plant health. Trends in Plant Science 17, 478486.
Bittman, S, Hunt, D, Kowalenko, CG, Wu, X and Forge, T (2004) Early phosphorus nutrition in corn and the role of mycorrhizae. In Bittman, S and Kowalenko, CG (eds), Advanced Silage Corn Management: A Production Guide for Coastal British Columbia and the Pacific Northwest. Agassiz, BC, Canada: Pacific Field Corn Association, pp. 4248.
Buysens, C, César, V, Ferrais, F, Dupré de Boulois, H and Declerck, S (2016) Inoculation of Medicago sativa cover crop with Rhizophagus irregularis and Trichoderma harzianum increases the yield of subsequently-grown potato under low nutrient conditions. Applied Soil Ecology 105, 137143.
Cameron, DD, Neal, AL, van Wees, SCM and Ton, J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends in Plant Science 18, 539545.
Chen, Y, Olson, DM and Ruberson, JR (2010) Effects of nitrogen fertilization on tritrophic interactions. Arthropod-Plant Interactions 4, 8194.
Chuang, WP, Herde, M, Ray, S, Castano-Duque, L, Howe, GA and Luthe, DS (2014) Caterpillar attack triggers accumulation of the toxic maize protein RIP2. New Phytologist 201, 928939.
Clark, AJ, Decker, AM, Meisinger, JJ and McIntosh, MS (1997) Kill date of vetch, rye, and a vetch-rye mixture: II. Soil moisture and corn yield. Agronomy Journal 89, 434441.
Coll, M and Bottrell, DG (1992) Mortality of European corn borer larvae by natural enemies in different corn microhabitats. Biological Control 2, 95103.
Collins, HP, Alva, A, Boydston, RA, Cochran, RL, Hamm, PB, McGuire, A and Riga, E (2006) Soil microbial, fungal, and nematode responses to soil fumigation and cover crops under potato production. Biology and Fertility of Soils 42, 247257.
Cook, K, Ratcliffe, S, Gray, M and Steffey, K (2003) European Corn Borer—Ostrinia Nubilalis (Hubner). Insect Fact Sheet. Urbana, IL, USA: University of Illinois, Department of Crop Sciences.
CTIC, SARE, and ASTA (2016) Annual Report 2015–2016 Cover Crop Survey.
Deepika, S and Kothamasi, D (2014) Soil moisture—a regulator of arbuscular mycorrhizal fungal community assembly and symbiotic phosphorus uptake. Mycorrhiza 25, 6775.
Finney, DM and Kaye, JP (2016) Functional diversity in cover crop polycultures increases multifunctionality of an agricultural system. Journal of Applied Ecology 54, 509517.
Finney, DM, White, CM and Kaye, JP (2016) Biomass production and carbon/nitrogen ratio influence ecosystem services from cover crop mixtures. Agronomy Journal 108, 3952.
Garnett, T, Appleby, MC, Balmford, A, Bateman, IJ, Benton, TG, Bloomer, P, Burlingame, B, Dawkins, M, Dolan, L, Fraser, D, Herrero, M, Hoffmann, I, Smith, P, Thornton, PK, Toulmin, C, Vermeulen, SJ and Godfray, HCJ (2013) Sustainable intensification in agriculture: premises and policies. Science Magazine 341, 3334.
Hunter, MC, Smith, RG, Schipanski, ME, Atwood, LW and Mortensen, DA (2017) Agriculture in 2050: recalibrating targets for sustainable intensification. BioScience 67, 386391.
Huot, B, Yao, J, Montgomery, BL and He, SY (2014) Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Molecular Plant 7, 12671287.
Javaid, A (2009) Arbuscular mycorrhizal mediated nutrition in plants. Journal of Plant Nutrition 32, 15951618.
Jeffries, P, Gianinazzi, S, Perotto, S, Turnau, K and Barea, JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biology and Fertility of Soils 37, 116.
Kabir, Z (2005) Tillage or no-tillage: impacts on mycorrhizae. Canadian Journal of Plant Science 85, 2329.
Kabir, Z and Koide, RT (2000) The effects of dandelion or a cover crop on mycorrhizal inoculum potential, soil aggregation and yield of maize. Agriculture, Ecosystem and Environment 78, 167174.
Kabir, Z and Koide, RT (2002) Effect of autumn and winter mycorrhizal cover crops on soil properties, nutrient uptake and yield of sweet corn in Pennsylvania, USA. Plant and Soil 238, 205215.
Karban, R and Myers, JJH (1989) Induced plant responses to herbivory. Annual Review of Ecology and Systematics 20, 331348.
Koch, FC and McMeekin, TL (1924) A new direct nesslerization micro-Kjeldahl method and a modification of the Nessler-Folin reagent for ammonia. Journal of the American Chemical Society 46, 20662069.
Koricheva, J, Gange, AC and Jones, T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90, 20882097.
Labatte, JM, Meusnier, S, Migeon, A, Chaufaux, J, Couteaudier, Y, Got, B and Riba, G (1991) Modelling damage on corn by the European corn borer, Ostrinia nubilalis: evolution of the number of cavities, their length and their within-plant distribution. Annals of Applied Biology 119, 401413.
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods (San Diego, Calif.) 25, 402408.
Louis, J, Peiffer, M, Ray, S, Luthe, DS and Felton, GW (2013) Host-specific salivary elicitor(s) of European corn borer induce defenses in tomato and maize. New Phytologist 199, 6673.
McGonigle, TP, Miller, MH, Evans, DG, Fairchild, GL and Swan, JA (1990) A New method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115, 495501.
Murrell, EG and Cullen, EM (2014) Conventional and organic soil fertility management practices affect corn plant nutrition and Ostrinia nubilalis (Lepidoptera: Crambidae) larval performance. Environmental Entomology 43, 12641274.
Murrell, EG, Schipanski, ME, Finney, DM, Hunter, MC, Baraibar, B, White, CM, Mortensen, DA and Kaye, JP (2017) Achieving diverse cover crop mixtures: effects of planting date and seeding rate. Agronomy 109, 259271.
NOAA NCDC (2018) No Title. Climate Data Online (CDO) [Internet]. Available at
Pozo, MJ and Azcón-Aguilar, C (2007) Unraveling mycorrhiza-induced resistance. Current Opinion in Plant Biology 10, 393398.
Ranells, NN and Wagger, MG (1992) Nitrogen release from crimson clover in relation to plant growth stage and composition. Agronomy Journal 84, 424430.
Ranells, NN and Wagger, MG (1996) Nitrogen release from grass and legume cover crop monocultures and bicultures. Agronomy Journal 88, 777782.
Raven, JA (2013) RNA function and phosphorus use by photosynthetic organisms. Frontiers in Plant Science 4, 113.
SAS (2009) Jones, E and Huddleston, A (eds), SAS/STAT 9.2 User's Guide, 2nd Edn. Cary, NC, USA: SAS Institute Inc. pp. 38924092.
Shivaji, R, Camas, A, Ankala, A, Engelberth, J, Tumlinson, JH, Williams, WP, Wilkinson, JR and Luthe, DS (2010) Plants on constant alert: elevated levels of jasmonic acid and jasmonate-induced transcripts in caterpillar-resistant maize. Journal of Chemical Ecology 36, 179191.
Song, YY, Cao, M, Xie, LJ, Liang, XT, Zeng, RS, Su, YJ, Huang, JH, Wang, RL and Luo, SM (2011) 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, 721731.
Teasdale, JR and Abdul-Baki, AA (1998) Comparison of mixtures vs. monocultures of cover crops for fresh-market tomato production with and without herbicide. HortScience 33, 11631166.
Vierheilig, H, Coughlan, AP, Wyss, URS and De Recherche, C (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64, 50045007.
Viola, DV, Mordecai, EA, Jaramillo, AG, Sistla, SA, Albertson, LK, Gosnell, JS, Cardinale, BJ and Levine, JM (2010) Competition-defense tradeoffs and the maintenance of plant diversity. Proceedings of the National Academy of Sciences 107, 1721717222.
Watanabe, F and Olsen, SR (1965) Test of an ascorbic acid method for determining P in water and NaHCO3 extracts from soil. Soil Science Society of America Proceedings 29, 677678.
White, CM and Weil, RR (2010) Forage radish and cereal rye cover crop effects on mycorrhizal fungus colonization of maize roots. Plant and Soil 328, 507521.
White, CM, DuPont, ST, Hautau, M, Hartman, D, Finney, DM, Bradley, B, LaChance, JC and Kaye, JP (2017) Managing the trade off between nitrogen supply and retention with cover crop mixtures. Agriculture, Ecosystems and Environment 237, 121133.
Willis, A, Rodrigues, BF and Harris, PJC (2013) The ecology of arbuscular mycorrhizal fungi. Critical Reviews in Plant Sciences 32, 120.
Wittstock, U and Gershenzon, J (2002) Constitutive plant toxins and their role in defense against herbivores and pathogens. Current Opinion in Plant Biology 5, 300307.
Wolf, A and Beegle, D (2011) Recommended soil tests for micronutrients. In Sims, DB, Thomas, J and Beegle, (eds), Recommended Soil Testing Procedures for the Northeastern United States. Northeast Regional Bulletin #493, 3rd Edn. Newark, DE, USA: Agricultural Experiment Station, University of Delaware, pp. 4045.
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