Cereal crops including maize (Zea mays L.) are inhabited by non-disease causing microbes known as endophytes that can promote plant growth, aid in host nutrient acquisition and promote host pathogen resistance. Screening endophytes for beneficial traits in planta using large, slow-growing cereals is challenging, thus a rapid but relevant in planta system is needed. Here, we propose that turfgrasses can be used as high-throughput assay systems for screening cereal microbes for beneficial nutrient traits. Turfgrasses are genetic relatives of cereals, but small with fast growth rates; they can be grown in test tubes under sterile conditions on defined media. Five turfgrass genotypes were evaluated for traits ideal for assaying endophytes with nutrient acquisition traits. Based on these criteria, annual ryegrass (Lolium multiflorum) was selected as a high-throughput assay system. Annual ryegrass was then used to test a collection of maize endophytes for their ability to promote plant biomass in the absence of nitrogen. Out of 75 bacterial endophytes tested, one strain (an Enterobacter sp) consistently promoted root and shoot biomass. We discuss the potential of annual ryegrass as a model assay system to test cereal endophytes for acquisition of various nutrients, changes in root/shoot architecture as well as anti-pathogen traits.
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Arcand MM, Schneider KD (2006) Plant- and microbial-based mechanisms to improve the agronomic effectiveness of phosphate rock: a review. An Acad Bras Cienc 78:791–807
Budak H, Shearman RC, Gaussoin RE, Dweikat I (2004) Application of sequence-related amplified polymorphism markers for characterization of turfgrass species. Hortscience 39:955–958
de Souza R, Ambrosini A, Passaglia LMP (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419. https://doi.org/10.1590/s1415-475738420150053
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:15. https://doi.org/10.6064/2012/963401
Johnston-Monje D, Raizada MN (2011a) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6:e20396. https://doi.org/10.1371/journal.pone.0020396
Johnston-Monje D, Raizada MN (2011b) Integration of biotechnologies - plant and endophyte relationships: nutrient management. In: moo-young M (ed) comprehensive biotechnology, second edition, vol 4. Elsevier, pp 713-727
Kim S, Lowman S, Hou G, Nowak J, Flinn B, Mei C (2012) Growth promotion and colonization of switchgrass (Panicum virgatum) cv. Alamo by bacterial endophyte Burkholderia phytofirmans strain PsJN. Biotechnol Biofuels 5:37. https://doi.org/10.1186/1754-6834-5-37
Kurepin LV, Zaman M, Pharis RP (2014) Phytohormonal basis for the plant growth promoting action of naturally occurring biostimulators. J Sci Food Agric 94:1715–1722
Li M, G-p S, Wu Y-j, Yu Z-l, Bañuelos G, Yu H-q (2014) Enhancement of nitrogen and phosphorus removal from eutrophic water by economic plant annual ryegrass (Lolium multiflorum) with ion implantation. Environ Sci Pollut Res 21:9617–9625. https://doi.org/10.1007/s11356-014-2987-4
Ludwig-Müller J (2015) Bacteria and fungi controlling plant growth by manipulating auxin: balance between development and defense. J Plant Physiol 172:4–12
Pechanova O, Takáč T, Šamaj J, Pechan T (2013) Maize proteomics: an insight into the biology of an important cereal crop. Proteomics 13:637–662
Pérez-Montaño F et al (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336. https://doi.org/10.1016/j.micres.2013.09.011
Pliego C, Ramos C, Vicente A, Cazorla F (2011) Screening for candidate bacterial biocontrol agents against soilborne fungal plant pathogens. Plant Soil 340:505–520. https://doi.org/10.1007/s11104-010-0615-8
Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443. https://doi.org/10.1016/j.pbi.2011.04.004
Rey T, Schornack S (2013) Interactions of beneficial and detrimental root-colonizing filamentous microbes with plant hosts. Genome Biol 14:121–121. https://doi.org/10.1186/gb-2013-14-6-121
Richardson A, Barea J-M, McNeill A, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339. https://doi.org/10.1007/s11104-009-9895-2
Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767. https://doi.org/10.1093/aob/mct048
Sharma NC, Sahi SV (2005) Characterization of phosphate accumulation in Lolium multiflorum for remediation of phosphorus-enriched soils. Environ Sci Technol 39:5475–5480. https://doi.org/10.1021/es050198t
Sharma NC, Sahi SV, Jain JC, Raghothama KG (2004) Enhanced accumulation of phosphate by Lolium multiflorum cultivars grown in phosphate-enriched medium. Environ Sci Technol 38:2443–2448. https://doi.org/10.1021/es030466s
Sharma S, Sayyed R, Trivedi M, Gobi T (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2:587
Shehata HR, Lyons EM, Jordan KS, Raizada MN (2016a) Bacterial endophytes from wild and ancient maize are able to suppress the fungal pathogen Sclerotinia homoeocarpa. J Appl Microbiol 120:756–769. https://doi.org/10.1111/jam.13050
Shehata HR, Lyons EM, Jordan KS, Raizada MN (2016b) Relevance of in vitro agar based screens to characterize the anti-fungal activities of bacterial endophyte communities. BMC Microbiol 16:1–7. https://doi.org/10.1186/s12866-016-0623-9
Shehata HR, Raizada MN (2017) A Burkholderia endophyte of the ancient maize landrace Chapalote utilizes c-di-GMP-dependent and independent signaling to suppress diverse plant fungal pathogen targets. FEMS Microbiol Lett 364:fnx138
Tkacz A, Poole P (2015) Role of root microbiota in plant productivity. J Exp Bot 66:2167–2175. https://doi.org/10.1093/jxb/erv157
Venuto BC, Ward JD, Twidwell EK (2002) Effects of soil type and soil chemical composition on nutrient content of annual ryegrass for beef and dairy cow nutrition. J Plant Nutr 26:1789–1799. https://doi.org/10.1081/pln-120023283
Wani Z, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biot 99:2955–2965. https://doi.org/10.1007/s00253-015-6487-3
This research was supported by grants to MNR from the Ontario Turfgrass Research Foundation and Growing Forward 2 funds to the Agricultural Adaptation Council (052188 and 052189). HRS was supported by a generous scholarship from the Egyptian Government.
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The authors declare no conflict of interest.
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Shehata, H.R., Lyons, E.M. & Raizada, M.N. Turfgrasses as model assay systems for high-throughput in planta screening of beneficial endophytes isolated from cereal crops. Symbiosis 76, 71–76 (2018). https://doi.org/10.1007/s13199-017-0511-6
- Model assay system
- Cereal crops