Abstract
Aims
Plant-beneficial fungi are non-pathogenic fungi that provide a variety of benefits to crops, including improved nutrition and increased resistance against biotic and abiotic stresses. However, to what extent these beneficial effects depend on fungal strain or host cultivar is not well known.
Methods
In this study, we investigated the effects of different species of plant-beneficial fungi on plant nutrient composition and resistance against zoophytophagous predators, and assessed whether effects are mediated by plant cultivar. We evaluated how seed inoculation of three tomato (Solanum lycopersicum L.) cultivars (Micro-Tom, Moneymaker and Pearson) with three fungi (Beauveria bassiana ARSEF 3097, Metarhizium brunneum ARSEF 1095 and Trichoderma harzianum T22) affected the leaf sap nutrient composition and feeding damage (number of necrotic rings) and mortality rate of Nesidiocoris tenuis.
Results
Plant nutrient composition was mainly determined by cultivar, but was also affected by fungal treatment. Significantly less necrotic rings were formed in fungus-inoculated plants compared to control plants. However, out of the nine cultivar-fungus combinations tested only the combination of Micro-Tom and B. bassiana showed less feeding damage by N. tenuis along with increased insect mortality.
Conclusions
We conclude that plant-beneficial fungi affect plant nutrient composition, but this has little effect on plant defense against N. tenuis, suggesting that differences in insect damage are most likely not mediated by changes in nutrient composition. Moreover, effects depended largely on the cultivar and fungal strain used, indicating that generalizations based on single strain or cultivar studies should be made with caution.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All relevant data are within the paper and its Supplementary Information.
Abbreviations
- PGPR:
-
Plant growth promoting rhizobacteria
- AMF:
-
Arbuscular mycorrhizal fungi
- PGPF:
-
Plant growth promoting fungi
- SDAY :
-
Sabouraud dextrose agar supplemented with yeast extract
- T:
-
Temperature
- RH:
-
Relative humidity
References
Akello J, Dubois T, Coyne D, Kyamanywa S (2008) Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage. Crop Protection 27(11):1437–1441. https://doi.org/10.1016/j.cropro.2008.07.003
Alam B, Lǐ J, Gě Q, Khan MA, Gōng J, Mehmood S, Yuán Y, Gǒng W (2021) Endophytic Fungi: From Symbiosis to Secondary Metabolite Communications or Vice Versa? Front Plant Sci 12(December):1–24. https://doi.org/10.3389/fpls.2021.791033
Alınç T, Cusumano A, Peri E, Torta L, Colazza S (2021) Trichoderma harzianum Strain T22 Modulates Direct Defense of Tomato Plants in Response to Nezara viridula Feeding Activity. J Chem Ecol 47:455–462. https://doi.org/10.1007/s10886-021-01260-3
Altomare C, Norvell WA, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth- promoting and biocontrol fungus Trichoderma harzianum Rifai 1295–22. Appl Environ Microbiol 65(7):2926–2933. https://doi.org/10.1128/aem.65.7.2926-2933.1999
Arnó J, Castañé C, Riudavets J, Gabarra R (2010) Risk of damage to tomato crops by the generalist zoophytophagous predator Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae). Bull Entomol Res 100(1):105–115. https://doi.org/10.1017/S0007485309006841
Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844. https://doi.org/10.1146/annurev.ento.47.091201.145300
Bamisile BS, Dash CK, Akutse KS, Keppanan R, Afolabi OG, Hussain M, Qasim M, Wang L (2018) Prospects of endophytic fungal entomopathogens as biocontrol and plant growth promoting agents: An insight on how artificial inoculation methods affect endophytic colonization of host plants. Microbiol Res 217:34–50. https://doi.org/10.1016/j.micres.2018.08.016
Bano A, Waqar A, Khan A, Tariq H (2022) Phytostimulants in sustainable agriculture. Front Sustain Food Syst. https://doi.org/10.3389/fsufs.2022.801788
Cardoso IM, Kuyper TW (2006) Mycorrhizas and tropical soil fertility. Agr Ecosyst Environ 116:72–84. https://doi.org/10.1016/j.agee.2006.03.011
Chaverri P, Branco-Rocha F, Jaklitsch W, Gazis R, Degenkolb T, Samuels GJ (2015) Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia 107(3):558–590. https://doi.org/10.3852/14-147
Chen XL, Sun MC, Chong SL, Si JP, Wu LS (2022) Transcriptomic and Metabolomic Approaches Deepen Our Knowledge of Plant-Endophyte Interactions. Front Plant Sci 12(January):1–25. https://doi.org/10.3389/fpls.2021.700200
Cheplick GP, Clay K, Marks S (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111:89–97. https://doi.org/10.1111/j.1469-8137.1989.tb04222.x
Chung YR, Hoitink HAJ (1990) Interactions Between Thermophilic Fungi and Trichoderma harzianum in Suppression of Rhizoctionia Damping-Off in a Bark Compost-Amended Container Medium.pdf. Dis Control Pest Manag 80(1):73–77
Contreras-Cornej HA, Macias-Rodrigues L, Cortes-Penagos C, Lopze-Bucio J (2009) Trichoderma virens, a Plant Beneficial Fungus, Enhances Biomass Production and Promotes Lateral Root Growth through an Auxin-Dependent Mechanism in Arabidopsis. Plant Physiol 149:1579–1592. https://doi.org/10.1104/pp.108.130369
De la Cruz-Quiroz R, Roussos S, Rodríguez-Herrera R, Hernandez-Castillo D, Aguilar CN (2018) Growth inhibition of Colletotrichum gloeosporioides and Phytophthora capsici by native Mexican Trichoderma strains. Karbala Int J Modern Sci 4(2):237–243. https://doi.org/10.1016/j.kijoms.2018.03.002
De Puysseleyr V, De Man S, Höfte M, De Clercq P (2013) Plantless rearing of the zoophytophagous bug Nesidiocoris tenuis. Biocontrol 58(2):205–213. https://doi.org/10.1007/s10526-012-9486-7
Deng G, Liu LJ, Zhong XY, Lao CY, Wang HY, Wang B, Zhu C, Shah F, Peng DX (2014) Comparative proteome analysis of the response of ramie under N, P and K deficiency. Planta 239:1175–1186. https://doi.org/10.1007/s00425-014-2040-3
Esteves E, Locatelli G, Bou NA, Ferrarezi RS (2021) Sap analysis: A powerful tool for monitoring plant nutrition. Horticulturae 7(11):1–13. https://doi.org/10.3390/horticulturae7110426
Ferracini C, Bueno VHP, Dindo ML, Ingegno BL, Luna MG, Salas Gervassio NG, Sánchez NE, Siscaro G, van Lenteren JC, Zappalà L, Tavella L (2019) Natural enemies of Tuta absoluta in the Mediterranean basin, Europe and South America. Biocontrol Sci Tech 29(6):578–609. https://doi.org/10.1080/09583157.2019.1572711
Finkel OM, Castrillo G, Herrera Paredes S, Salas González I, Dangl JL (2017) Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol 38:155–163. https://doi.org/10.1016/j.pbi.2017.04.018
Francis F, Fingu-Mabola JC, Ben Fekih I (2022) Direct and Endophytic Effects of Fungal Entomopathogens for Sustainable Aphid Control: A Review. Agriculture (Switzerland) 12(12):2081. https://doi.org/10.3390/agriculture12122081
Gange AC, Koricheva J, Currie AF, Jaber LR, Vidal S (2019) Meta-analysis of the role of entomopathogenic and unspecialized fungal endophytes as plant bodyguards. New Phytol 223(4):2002–2010. https://doi.org/10.1111/nph.15859
Garantonakis N, Pappas ML, Varikou K, Skiada V, Broufas GD, Kavroulakis N, Papadopoulou KK (2018) Tomato inoculation with the endophytic strain Fusarium solani K results in reduced feeding damage by the zoophytophagous predator nesidiocoris tenuis. Front Ecol Evol 6:1–7. https://doi.org/10.3389/fevo.2018.00126
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. In Molecular ecology. (Vol. 2, Issue 2). Wiley-Blackwell. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Garrido-Jurado I, Resquín-Romero G, Amarilla SP, Ríos-Moreno A, Carrasco L, Quesada-Moraga E (2017) Transient endophytic colonization of melon plants by entomopathogenic fungi after foliar application for the control of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae). J Pest Sci 90(1):319–330. https://doi.org/10.1007/s10340-016-0767-2
Gupta S, Krasnoff SB, Underwood NL, Renwick JA, Roberts DW (1991) Isolation of beauvericin as an insect toxin from Fusarium semitectum and Fusarium moniliforme var. subglutinans. Mycopathologia 115(3):185–189. https://doi.org/10.1007/BF00462223
Hariyadi BW, Nizak F, Nurmalasari IR, Kogoya Y (2019) Effect of Dose And Time of Npk Fertilizer Application on The Growth And Yield of Tomato Plants (Lycopersicum Esculentum Mill). J Agric Sci 2(2):101–111
Harman GE, Petzoldt R, Comis A, Chen J (2004) Interactions Between Trichoderma harzianum Strain T22 and Maize Inbred Line Mo17 and Effects of These Interactions on Diseases Caused by Pythium ultimum and Colletotrichum graminicola. Biol Control 94(2):147–153
Hyakumachi M (1994) Plant-growth-promoting fungi from turfgrass rhizosphere with potential for disease suppression. Soil Microorg. 44:53–68 (http://ci.nii.ac.jp/naid/110009467810/en/)
Ingels R, Bosmans L, Pekas A, Huysmans M, Moerkens R (2022) Preference and plant damage caused by Nesidiocoris tenuis on twenty‑one commercial tomato cultivars. J Pest Sci 0123456789. https://doi.org/10.1007/s10340-022-01530-3
Jaber LR, Alananbeh KM (2018) Fungal entomopathogens as endophytes reduce several species of Fusarium causing crown and root rot in sweet pepper (Capsicum annuum L.). Biol Control 126:117–126. https://doi.org/10.1016/j.biocontrol.2018.08.007
Jaber LR, Araj SE (2018) Interactions among endophytic fungal entomopathogens (Ascomycota: Hypocreales), the green peach aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the aphid endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Biol Control 116:53–61. https://doi.org/10.1016/j.biocontrol.2017.04.005
Jaber LR, Ownley BH (2018) Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116:36–45. https://doi.org/10.1016/j.biocontrol.2017.01.018
Klieber J, Reineke A (2016) The entomopathogen Beauveria bassiana has epiphytic and endophytic activity against the tomato leaf miner Tuta absoluta. J Appl Entomol 140(8):580–589. https://doi.org/10.1111/jen.12287
Krell V, Unger S, Jakobs-Schoenwandt D, Patel AV (2018) Endophytic Metarhizium brunneum mitigates nutrient deficits in potato and improves plant productivity and vitality. Fungal Ecol 34:43–49. https://doi.org/10.1016/j.funeco.2018.04.002
Kubheka BP, Ziena LW (2022) Trichoderma: A Biofertilizer and a Bio-Fungicide for Sustainable Crop Production. In IntechOpen: Vol. Trichoderm (pp. 1–16). https://doi.org/10.5772/intechopen.102405
Lievens B, Brouwer M, Vanachter ACRC, Lévesque CA, Cammue BPA, Thomma BPHJ (2003) Design and development of a DNA array for rapid detection and identification of multiple tomato vascular wilt pathogens. FEMS Microbiol Lett 223(1):113–122. https://doi.org/10.1016/S0378-1097(03)00352-5
Mallebrera B, Prosperini A, Font G, Ruiz MJ (2018) In vitro mechanisms of Beauvericin toxicity: A review. Food Chem Toxicol 111:537–545. https://doi.org/10.1016/j.fct.2017.11.019
Mattoo AJ, Nonzom S (2021) Endophytic fungi: understanding complex cross-talks. Symbiosis 83(3):237–264. https://doi.org/10.1007/s13199-020-00744-2
Meena VS, Meena SK, Verma JP, Kumar A, Aeron A, Mishra PK, Bisht JK, Pattanayak A, Naveed M, Dotaniya ML (2017) Plant beneficial rhizospheric microorganism (PBRM) strategies to improve nutrients use efficiency: A review. Ecol Eng 107:8–32. https://doi.org/10.1016/j.ecoleng.2017.06.058
Meincke R, Weinert N, Radl V, Schloter M, Smalla K, Berg G (2010) Development of a molecular approach to describe the composition of Trichoderma communities. J Microbiol Methods 80(1):63–69. https://doi.org/10.1016/j.mimet.2009.11.001
Moerkens R, Pekas A, Bellinkx S, Hanssen I, Huysmans M, Bosmans L, Wäckers F (2020) Nesidiocoris tenuis as a pest in Northwest Europe: Intervention threshold and influence of Pepino mosaic virus. J Appl Entomol 144(7):566–577. https://doi.org/10.1111/jen.12789
Naselli M, Zappalà L, Gugliuzzo A, Tropea Garzia G, Biondi A, Rapisarda C, Cincotta F, Condurso C, Verzera A, Siscaro G (2017) Olfactory response of the zoophytophagous mirid Nesidiocoris tenuis to tomato and alternative host plants. Arthropod-Plant Interactions 11(2):121–131. https://doi.org/10.1007/s11829-016-9481-5
Naznin HA, Kiyohara D, Kimura M, Miyazawa M, Shimizu M, Hyakumachi M (2014) Systemic resistance induced by volatile organic compounds emitted by plant growth-promoting fungi in Arabidopsis thaliana. PLoS ONE 9(1):e86882. https://doi.org/10.1371/journal.pone.0086882
Newton AC, Fitt BDL, Atkins SD, Walters DR, Daniell TJ (2010) Pathogenesis, parasitism and mutualism in the trophic space of microbe-plant interactions. Trends Microbiol 18(8):365–373. https://doi.org/10.1016/j.tim.2010.06.002
Öǧüt M, Akdaǧ C, Düzdemir O, Sakin MA (2005) Single and double inoculation with Azospirillum/Trichoderma: The effects on dry bean and wheat. Biol Fertil Soils 41(4):262–272. https://doi.org/10.1007/s00374-004-0818-3
Olsen JK, Lyons DJ (1994) Petiole sap nitrate is better than total nitrogen in dried leaf for indicating nitrogen status and yield responsiveness of Capsicum in subtropical Australia. Aust J Exp Agric 34(6):835–843. https://doi.org/10.1071/EA9940835
Peña-Fleitas MT, Gallardo M, Thompson RB, Farneselli M, Padilla FM (2015) Assessing crop N status of fertigated vegetable crops using plant and soil monitoring techniques. Ann Appl Biol 167:387–405. https://doi.org/10.1111/aab.12235
Pérez-Hedo M, Riahi C, Urbaneja A (2021) Use of zoophytophagous mirid bugs in horticultural crops: Current challenges and future perspectives. Pest Manag Sci 77:33–42. https://doi.org/10.1002/ps.6043
Pérez-Hedo M, Urbaneja A (2016). The Zoophytophagous Predator Nesidiocoris tenuis: A Successful But Controversial Biocontrol Agent in Tomato Crops. In Advances in insect control and resistance management (121–138). Springer International Publishing AG. https://doi.org/10.1007/978-3-319-31800-4_7
Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. https://doi.org/10.1146/annurev-phyto-082712-102340
Posadas JB, Comerio RM, Mini JI, Nussenbaum AL, Lecuona RE, Posadas JB, Comerio RM, Mini JI, Nussenbaum AL, Lecuona RE (2017) A novel dodine-free selective medium based on the use of cetyl trimethyl ammonium bromide (CTAB) to isolate Beauveria bassiana, Metarhizium anisopliae sensu lato and Paecilomyces lilacinus from soil. Mycologia 104(4):974–980. https://doi.org/10.3852/11-234
Powell WA, Klingeman WE, Ownley BH, Gwinn KD, Dee M, Flanagan PC (2007) Endophytic Beauveria bassiana in tomatoes yields mycosis in tomato fruitworm larvae. HortScience. 42(4):933 (issn 0018-5345)
Prieto KR, Echaide-Aquino F, Huerta-Robles A, Valério HP, Macedo-Raygoza GM, Prado F, Medeiros MHG, Brito HF, da Silva IGN, Felinto MCFC, White JF, Mascio P, Di, Beltran-García MJ (2017) Endopytic bacteria and rare elements; Promising candidates for nutrient use efficiency in plants. In Plant Macronutrient Use Efficiency (pp. 285–306). https://doi.org/10.1016/B978-0-12-811308-0/00016-8
Prudic KL, Oliver JC, Bowers MD (2005) Soil nutrient effects on oviposition preference, larval performance, and chemical defense of a specialist insect herbivore. Oecologia 143:578–587. https://doi.org/10.1007/s00442-005-0008-5
Rondot Y, Reineke A (2018) Endophytic Beauveria bassiana in grapevine Vitis vinifera (L.) reduces infestation with piercing-sucking insects. Biol Control 116:82–89. https://doi.org/10.1016/j.biocontrol.2016.10.006
Sanchez JA (2008) Zoophytophagy in the plantbug Nesidiocoris tenuis. Agric for Entomol 10(2):75–80. https://doi.org/10.1111/j.1461-9563.2007.00357.x
Sani MNH, Hasan M, Uddain J, Subramaniam S (2020) Impact of application of Trichoderma and biochar on growth, productivity and nutritional quality of tomato under reduced N-P-K fertilization. Annals of Agricultural Sciences 65(1):107–115. https://doi.org/10.1016/j.aoas.2020.06.003
Schneider S, Widmer F, Jacot K, Kölliker R, Enkerli J (2012) Spatial distribution of Metarhizium clade 1 in agricultural landscapes with arable land and different semi-natural habitats. Appl Soil Ecol 52:20–28. https://doi.org/10.1016/j.apsoil.2011.10.007
Singh DP, Singh HB, Prabha R (2017) Plant-Microbe Interactions in Agro-Ecological Perspectives. In Plant-Microbe Interactions in Agro-Ecological Perspectives (Vol. 2). https://doi.org/10.1007/978-981-10-6593-4
Siscaro G, Lo Pumo C, Tropea Garzia G, Tortorici S, Gugliuzzo A, Ricupero M, Biondi A, Zappalà L (2019) Temperature and tomato variety influence the development and the plant damage induced by the zoophytophagous mirid bug Nesidiocoris tenuis. J Pest Sci 92(3):1049–1056. https://doi.org/10.1007/s10340-019-01096-7
Soad AA, Guan-lin X, Coosemans J (2005) Delivery Methods for Introducing Endophytic Bacillus into Tomato and Their Effect on Growth Promotion and Suppression of Tomato Wilt. Plant Pathol J 4(1):69–74. https://doi.org/10.3923/ppj.2005.69.74
Soto-Barajas MC, Zabalgogeazcoa I, Gómez-Fuertes J, González-Blanco V, Vázquez-de-Aldana BR (2016) Epichloë endophytes affect the nutrient and fiber content of Lolium perenne regardless of plant genotype. Plant Soil 405(1–2):265–277. https://doi.org/10.1007/s11104-015-2617-z
Sung J, Sonn Y, Lee Y, Kang S, Ha S, Krishnan HB, Oh T (2015) Compositional changes of selected amino acids, organic acids, and soluble sugars in the xylem sap of N, P, or K-deficient tomato plants. Plant Soil 178:792–797. https://doi.org/10.1002/jpln.201500071
Tian L, Lin X, Tian J, Ji L, Chen Y, Tran LSP, Tian C (2020) Research advances of beneficial microbiota associated with crop plants. Int J Mol Sci 21(5):1–18. https://doi.org/10.3390/ijms21051792
Urbaneja A, González-Cabrera J, Arnó J, Gabarra R (2012) Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Manag Sci 68(9):1215–1222. https://doi.org/10.1002/ps.3344
Vega FE (2018) The use of fungal entomopathogens as endophytes in biological control: a review. Mycologia 110(1):4–30. https://doi.org/10.1080/00275514.2017.1418578
Vidal S, Jaber LR (2015) Entomopathogenic fungi as endophytes: Plant-endophyte-herbivore interactions and prospects for use in biological control. Current Science 109(1):46–54 (https://www.jstor.org/stable/24905690)
Wilberts L, Vuts J, Caulfield JC, Thomas G, Birkett MA, Herrera-Malaver B, Verstrepen KJ, Sobhy IS, Jacquemyn H, Lievens B (2022) Impact of endophytic colonization by entomopathogenic fungi on the behavior and life history of the tobacco peach aphid Myzus persicae var. nicotianae. PLoS One 17(9 September):1–17. https://doi.org/10.1371/journal.pone.0273791
Wilberts L, Rojas-preciado N, Jacquemyn H, Lievens B (2023) Fungal strain and crop cultivar affect growth of sweet pepper plants after root inoculation with entomopathogenic fungi. Front Plant Sci 1–10. https://doi.org/10.3389/fpls.2023.1196765
Woo SL, Hermosa R, Lorito M, Monte E (2022) Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture. Nat Rev Microbiol. https://doi.org/10.1038/s41579-022-00819-5
Zappalà L, Biondi A, Alma A, Al-Jboory IJ, Arnò J, Bayram A, Chailleux A, El-Arnaouty A, Gerling D, Guenaoui Y, Shaltiel-Harpaz L, Siscaro G, Stavrinides M, Tavella L, Vercher Aznar R, Urbaneja A, Desneux N (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. J Pest Sci 86(4):635–647. https://doi.org/10.1007/s10340-013-0531-9
Acknowledgements
We are grateful to VLAIO (Flanders Innovation and Entrepreneurship) for financial support of this research [project HBC.2018.2199]. Further, we would like to thank Biobest for providing us with N. tenuis and Ephestia eggs to maintain our N. tenuis lab culture.
Author information
Authors and Affiliations
Contributions
CM, HJ and BL contributed to the study conception and design. Material preparation, data collection and analysis were performed by CM, LC and RI. The first draft of the manuscript was written by CM and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
The datasets generated during and/or analyzed during the current study are available from the corresponding author on request.
Additional information
Responsible Editor: Beatriz Vazquez-de-Aldana.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Meesters, C., Cialdella, L., Ingels, R. et al. Cultivar-dependent effects of plant-beneficial fungi on plant nutrient composition and feeding damage by Nesidiocoris tenuis. Plant Soil 492, 177–190 (2023). https://doi.org/10.1007/s11104-023-06165-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06165-6