Endophytic effects of Aspergillus oryzae on radish (Raphanus sativus) and its herbivore, Plutella xylostella
We provide evidence that Aspergillus oryzae not only acts as an endophyte in Raphanus sativus, but also works as a plant growth promoter and provides some protection against its herbivore, Plutella xylostella affecting its feeding rate, mortality and fitness parameters, thereby contributing to the pest population suppression.
Seed inoculation of radish seeds with the fungus Aspergillus oryzae allowed its establishment as an endophyte promoting plant growth and negatively affecting fitness parameters of its major herbivore, diamondback moth, Plutella xylostella. Endophytic fungi may contribute to the growth of their host plants and enhance resistance to herbivores and diseases. We evaluated the effect of A. oryzae (Ahlburg) E. Cohn as an endophyte in radish (Raphanus sativus L.) on growth and development of the plants themselves and their major herbivore, the diamondback moth P. xylostella (L). A. oryzae colonization rates in leaves were significantly higher than in roots and stems, with a rate of 80% in leaves, 40% in stems and 20% in roots 1 week after seed inoculation. Colonization gradually decreased in the various plant tissues, and disappeared completely in roots, stems and leaves within 2, 5 and 7 weeks, respectively. A. oryzae did not affect seed germination; however, it promoted radish growth with endophytic plants attaining average heights of 116 mm compared to 99.6 mm in the controls at the third week post-inoculation. The P. xylostella fitness parameters, consumption, larval and pupal weights, and feeding on the endophytic plants were significantly lower than the controls, while larval mortality was significantly higher. Larvae fed on endophytic plants consumed 0.46 mg less leaf matter in the first week post seed inoculation and weighed 0.83 mg less as mature 4th instars than controls. We have demonstrated that A. oryzae can establish as an endophyte in R. sativus through seed inoculation providing some plant growth promotion and protection against its herbivore by increasing its mortality and negatively affecting its fitness parameters, suggesting that adopting seed treatments with A. oryzae may be beneficial in the commercial cultivation of radish.
KeywordsDiamondback moth Seed treatment Alternaria alternata Plant growth promotion Endophytic properties
Aspergillus seed treatment
Control seed treatment
Potato dextrose agar
This work was supported by the National Natural Science Foundation of China to Profs. You (Nos. 31320103922 and 31230061) and Xia (No. 31501639). Dr. Goettel is supported by a Jinshan Scholar Fellowship. We are grateful for the project of Distinguished Young Scholars at Fujian Agriculture and Forestry University (XJQ201624).
Compliance with ethical standards
Conflict of interest
The authors declare that there is no conflict of interest.
- Akutse KS, Maniania NK, Fiaboe KKM, Berg JVD, Ekesi S (2013) Endophytic colonization of Vicia faba and Phaseolus vulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyza huidobrensis (Diptera: Agromyzidae). Fungal Ecol 6:293–301. https://doi.org/10.1016/j.funeco.2013.01.003 CrossRefGoogle Scholar
- Baxter SW, Chen M, Dawson A, Zhao JZ, Vogel H, Shelton AM, Heckel DG, Jiggins CD (2010) Mis-spliced transcripts of nicotinic acetylcholine receptor α6 are associated with field evolved spinosad resistance in Plutella xylostella (L.). PLoS Genet 6:e1000802. https://doi.org/10.1371/journal.pgen.1000802 CrossRefPubMedPubMedCentralGoogle Scholar
- Fisher PJ, Petrini O (1992) Fungal saprobes and pathogens as endophytes of rice (Oryza sativa L.). New Phytol 120:137–143. https://doi.org/10.1111/j.1469-8137.1992.tb01066.x CrossRefGoogle Scholar
- Greenfield M, Gomez-Jimenez MI, Ortiz V, Vega FE, Kramer M, Parsa S (2016) Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biol Control 95:40–48. https://doi.org/10.1016/j.biocontrol.2016.01.002 CrossRefPubMedPubMedCentralGoogle Scholar
- Inglis GD, Enkerli J, Goettel MS (2012) Laboratory techniques used for entomopathogenic fungi: hypocreales. In: Lacey LA (ed) Manual of techniques in invertebrate pathology. Academic Press, London, pp 189–253. https://doi.org/10.1016/b978-0-12-386899-2.00007-5 CrossRefGoogle Scholar
- Kepler RM, Sung GH, Harada Y, Tanaka K, Tanaka E, Hosoya T, Bischoff JF, Spatafora JW (2012) Host jumping onto close relatives and across kingdoms by Tyrannicordyceps (Clavicipitaceae) gen. nov. and Ustilaginoidea_ (Clavicipitaceae). Am J Bot 99:552–561. https://doi.org/10.3732/ajb.1100124 CrossRefPubMedGoogle Scholar
- Larran S, Rollán C, Ángeles HB, Alippi HE, Urrutia MI (2002b) Endophytic fungi in healthy soybean leaves. Prod Prot Veg 17:173–178Google Scholar
- Li Z, Feng X, Liu SS, You M, Furlong MJ (2016) Biology, ecology, and management of the diamondback moth in China. Annu Rev Entomol 61:277–296. https://doi.org/10.1146/annurev.en.38.010193.001423 CrossRefPubMedGoogle Scholar
- Lopez DC, Sword GA (2015) The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biol Control 89:53–60. https://doi.org/10.1016/j.biocontrol.2015.03.010 CrossRefGoogle Scholar
- Malinowski DP, Brauer DK, Belesky DP (1999) The endophyte Neotyphodium coenophialum affects root morphology of tall fescue grown under phosphorus eficiency. J Agron Crop Sci 183:56–60Google Scholar
- Nihorimbere V, Ongena M, Smargiassi M, Thonart P (2011) Beneficial effect of the rhizosphere microbial community for plant growth and health. Biotechnol Agron Soc Environ 15:327–337Google Scholar
- Russo ML, Pelizza SA, Cabello MN, Stenglein SA, Vianna MF, Scorsetti AC (2016) Endophytic fungi from selected varieties of soybean (Glycine max L. Merr.) and corn (Zea mays L.) grown in an agricultural area of Argentina. Rev Argent Microbiol 48:154–160. https://doi.org/10.1016/j.ram.2015.11.006 PubMedGoogle Scholar
- Schulz B, Guske S, Dammann U, Boyle C (1998) Endophyte-host interactions. II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213–227. http://www.org/serials/c_54cc45ac
- Shelton AM, Wyman JA (1992) Insecticide resistance of diamondback moth in North America. In: Diamondback moth and other crucifer pests: proceedings second international workshop, Tainan (Taiwán), 10–14 December 1990. Asian Vegetable Research and Development Center, Shanhua, Taiwan, pp 447–454Google Scholar
- Shikano I, Rosa C, Tan CW, Felton GW (2017) Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annu Rev Phytopathol 55:313–331. https://doi.org/10.1146/annurev-phyto-080516-035319 CrossRefPubMedGoogle Scholar
- Talekar NS (1993) Biology, ecology, and management of the diamondback moth. Annu Rev Entomol 38:275–301. https://doi.org/10.1146/annurev.en.38.010193.001423 CrossRefGoogle Scholar
- United States Environmental Protection Agency (1997) Biotechnology program under toxic substances control act Aspergillus oryzae final risk assessment. US EPA, Washington, DC. http://www.epa.gov/oppt/biotech/pubs/fra/fra007.htm
- Usman F, Abid M, Hussain F, Khan SA, Sultana J (2014) Soil borne fungi associated with different vegetable crops in Sindh, Pakistan. Pak J Sci Ind Res 57:140–147. https://www.researchgate.net/publication/270686022
- Vogl AE (1898) Mehl und die anderen mehlprodukte der cerealien und leguminosen. Z Nahr Unters Hyg Warenkd 12:25–29Google Scholar
- Zhao LF, Xu YJ (2006) Research progress on the application of Aspergillus oryzae. China Brewing 156:8–10Google Scholar