Abstract
We explored the activation of defense genes and the changes in volatile profiles in olive (Olea europaea var. Picual) plants subjected to mechanical wounding and prior soil inoculation with the fungus Trichoderma afroharzianum T22. Our findings indicate a sustained effect of the inoculant in olive plants, which shifted the constitutive volatile emission more significantly towards an aldehyde-dominated blend than the mechanical damage alone. Furthermore, we found that wounding alone did not alter the expression of hydroperoxide lyase genes associated with aldehyde biosynthesis. However, this expression was significantly enhanced when combined with prior T22 inoculation. Mechanical wounding amplified the plant’s immediate defensive response by enhancing the upregulation of the direct defense enzyme acetone cyanohydrin lyase. Trichoderma afroharzianum T22 also modulated direct defense, although to a lesser extent, and its effect persisted 9 months after inoculation. Metagenomic analyses revealed that aerial mechanical damage did influence specific root bacterial functions. Specifically, an upregulation of predicted bacterial functions related to various metabolic processes, including responses to biotic and abiotic stresses, was observed. On the contrary, T22’s impact on bacterial functional traits was minor and/or transient.
Data availability
All raw Illumina sequence data were deposited in the Sequence Read Archive (SRA) service of the NCBI database (https://www.ncbi.nlm.nih.gov/) (BioProject ID: PRJNA1076140).
References
Alagna F, Kallenbach M, Pompa A, De Marchis F, Rao R, Baldwin IT, Bonaventure G, Baldoni L (2015) Olive fruits infested with olive fly larvae respond with an ethylene burst and the emission of specific volatiles. J Integr Plant Biol 58:413–425. https://doi.org/10.1111/jipb.12343
Aranega-Bou P, de la Leyva O, Finiti M, García-Agustín I, González-Bosch P C (2014) Priming of plant resistance by natural compounds. Hexanoic acid as a model. Front Plant Sci 5:488. https://doi.org/10.3389/fpls.2014.00488
Aßhauer KP, Wemheuer B, Daniel R, Meinicke P (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31:2882–2884. https://doi.org/10.1093/bioinformatics/btv287
Benítez E, Paredes D, Rodríguez E, Aldana D, González M, Nogales R, Campos M, Moreno B (2017) Bottom-up effects on herbivore-induced plant defences: a case study based on compositional patterns of rhizosphere microbial communities. Sci Rep 7:6251. https://doi.org/10.1038/s41598-017-06714-x
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300. https://doi.org/10.1111/J.2517-6161.1995.TB02031.X
Cai F, Druzhinina IS (2021) In honor of John Bissett: authoritative guidelines on molecular identification of Trichoderma. Fungal Divers 107:1–69. https://doi.org/10.1007/s13225-020-00464-4
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Cardoni M, Gómez-Lama Cabanás C, Valverde-Corredor A, Villar R, Mercado-Blanco J (2022) Unveiling differences in root defense mechanisms between tolerant and susceptible olive cultivars to Verticillium Dahliae. Front Plant Sci 13:863055. https://doi.org/10.3389/fpls.2022.863055
Caselli A, Favaro R, Petacchi R, Angeli S (2021) Infestation of the gall midge Dasineura oleae provides first evidence of induced plant volatiles in olive leaves. Bull Entom Res 112:481–493. https://doi.org/10.1017/S0007485321001000
Cuddington K (2011) Legacy effects: the persistent impact of ecological interactions. Biol Theory 6:203–210. https://doi.org/10.1007/s13752-012-0027-5
Davidson-Lowe E, Ali JG (2021) Herbivore-induced plant volatiles mediate behavioral interactions between a leaf-chewing and a phloem-feeding herbivore. Basic Appl Ecol 53:39–48. https://doi.org/10.1016/j.baae.2021.03.005
Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J (2017) MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res 45:W180–W188. https://doi.org/10.1093/NAR/GKX295
Dicke M, van Loon J, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324. https://doi.org/10.1038/nchembio.169
Dini I, Marra R, Cavallo P, Pironti A, Sepe I, Troisi J, Scala G, Lombari P, Vinale F (2021) Trichoderma strains and metabolites selectively increase the production of volatile Organic compounds (VOCs) in Olive Trees. Metabolites 31(11):213. https://doi.org/10.3390/metabo11040213
Djonović S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM (2007) A proteinaceous elicitor Sm1 from the Beneficial Fungus Trichoderma virens is required for Induced systemic resistance in Maize. Plant Physiol 145:875–889. https://doi.org/10.1104/pp.107.103689
Fu J, Xiao Y, Wang Y, Liu ZH, Yang KJ (2019) Trichoderma affects the physiochemical characteristics and bacterial community composition of saline-alkaline maize rhizosphere soils in the cold-region of Heilongjiang Province. Plant Soil 436:211–227. https://doi.org/10.1007/s11104-018-03916-8
Gorman Z, Tolley JP, Koiwa H, Kolomiets MV (2021) The synthesis of pentyl leaf volatiles and their role in resistance to anthracnose leaf blight. Front Plant Sci 12. https://doi.org/10.3389/fpls.2021.719587
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species: opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56
Jangir M, Sharma S, Sharma S (2019) Non-target effects of Trichoderma on plants and soil microbial communities. In: Varma A, Tripathi S, Prasad R (eds) Plant Microbe Interface. Springer, Cham. Plant Microbe Interface, pp 239–251. https://doi.org/10.1007/978-3-030-19831-2_10
Jiang X, Walker BJ, He SY, Hu J (2023) The role of photorespiration in plant immunity. Front Plant Sci 14:1125945. https://doi.org/10.3389/fpls.2023.1125945
Kanehisa M, Furumichi M, Sato Y, Kawashima M, Ishiguro-Watanabe M (2023) KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res 51:D587–D592. https://doi.org/10.1093/nar/gkac963
Karmakar A, Mitra S, Barik A (2018) Systemically released volatiles from Solena Amplexicaulis plant leaves with color cues influencing attraction of a generalist insect herbivore. Inter J Pest Manag 64:210–220. https://doi.org/10.1080/09670874.2017.1383531)
Kassambara A (2023) Pipe-friendly framework for basic statistical tests. R Packag version 0.7.2, https://rpkgs.datanovia.com/rstatix/
Kassim MA, Rumbold K (2014) HCN production and hydroxynitrile lyase: a natural activity in plants and a renewed biotechnological interest. Biotechnol Lett 36:223–228. https://doi.org/10.1007/s10529-013-1353-9
Kaur S, Samota MK, Choudhary M, Pandey AK, Sharma A, Thakur J (2022) How do plants defend themselves against pathogens-biochemical mechanisms and genetic interventions. Physiol Mol Biol Plants 28:485–504. https://doi.org/10.1007/s12298-022-01146-y
Krzyżowski M, Francikowski J, Baran B, Babczyńska A (2020) The short-chain fatty acids as potential protective agents against Callosobruchus maculatus infestation. J Stored Prod Res 86:101570. https://doi.org/10.1016/j.jspr.2020.101570
Lau S-E, Teo WFA, Teoh EY, Tan BC (2022) Microbiome engineering and plant biostimulants for sustainable crop improvement and mitigation of biotic and abiotic stresses. Discov Food 2:9. https://doi.org/10.1007/s44187-022-00009-5
Liang X, Qian R, Wang D, Liu L, Sun C, Lin X (2022) Lipid-derived aldehydes: new key mediators of plant growth and stress responses. Biology (Basel) 11:1590. https://doi.org/10.3390/biology11111590
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 – ∆∆CT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
López-Moral A, Llorens E, Scalschi L, García-Agustín P, Trapero A, Agustí-Brisach C (2022) Resistance induction in Olive Tree (Olea europaea) against Verticillium Wilt by two Beneficial Microorganisms and a copper Phosphite Fertilizer. Front Plant Sci 23:13:831794. https://doi.org/10.3389/fpls.2022.831794
Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL (2013) Practical innovations for high-throughput amplicon sequencing. Nat Methods 10:999–1002. https://doi.org/10.1038/nmeth.2634
Mallon CA, Le Roux X, van Doorn GS, Dini-Andreote F, Poly F, Salles JF (2018) The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader’s niche. ISME J 12:728–741. https://0.1038/s41396-017-0003-y
Marra R, Coppola M, Pironti A, Grasso F, Lombardi N, d’Errico G, Sicari A, Bolletti Censi S, Woo SL, Rao R et al (2020) The application of Trichoderma strains or metabolites alters the Olive Leaf Metabolome and the expression of Defense-related genes. J Fungi 6:369. https://doi.org/10.3390/jof6040369
Matsui K, Engelberth J (2022) Green Leaf volatiles—the forefront of plant responses against biotic attack. Plant Cell Physiol 63:1378–1390. https://doi.org/10.1093/pcp/pcac117
Meents AK, Mithöfer A (2020) Plant-plant communication: is there a role for volatile damage-associated molecular patterns? Front Plant Sci 11:583275. https://doi.org/10.3389/fpls.2020583275
Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylidès C, Haring MA, Schuurink RC (2008) The Arabidopsis her1 mutant implicates GABA in E-2-hexenal responsiveness. Plant J 53:197–213. https://doi.org/10.1111/j.1365-313X.2007.03323.x
Monte E (2023) The sophisticated evolution of Trichoderma to control insect pests. Proc Natl Acad Sci 120:e2301971120. https://doi.org/10.1073/pnas.2301971120
Moore JAM, Abraham PE, Michener JK, Muchero W, Cregger MA (2022) Ecosystem consequences of introducing plant growth promoting rhizobacteria to managed systems and potential legacy effects. New Phytol 234:1914–1918. https://doi.org/10.1111/nph.18010
Nawrocka J, Małolepsza U (2013) Diversity in plant systemic resistance induced by Trichoderma. Biol Control 67:149–156. https://doi.org/10.1016/j.biocontrol.2013.07.005
Nawrocka J, Szymczak K, Skwarek-Fadecka M, Małolepsza U (2023) Toward the analysis of volatile organic compounds from tomato plants (Solanum lycopersicum L.) treated with Trichoderma virens or/and Botrytis Cinerea. Cells 12:1271. https://doi.org/10.3390/cells12091271
Oksanen J (2017) Vegan: community ecology package-R package version 2.4-2. http://CRAN R-project org/package = vegan
Padilla MN, Hernández ML, Pérez AG, Sanz C, Martínez-Rivas JM (2010) Isolation, expression, and characterization of a 13-Hydroperoxide lyase gene from olive fruit related to the biosynthesis of the main virgin olive oil aroma compounds. J Agri Food Chem 58:5649–5657. https://doi.org/10.1021/jf9045396
Pennerman KK, Yin G, Bennett JW (2022) Eight-carbon volatiles: prominent fungal and plant interaction compounds. J Exp Bot 73:487–497. https://doi.org/10.1093/jxb/erab438
Qian L, Song F, Xia J, Wang R (2022) A glucuronic acid-producing endophyte Pseudomonas sp. MCS15 reduces cadmium uptake in rice by inhibition of ethylene biosynthesis. Front Plant Sci 13:876545
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
R Core Team (2022) R: a language and environment for statistical computing. R Found Stat Comput Vienna, Austria
Rauwerdink A, Lunzer M, Devamani T, Jones B, Mooney J, Zhang ZJ, Xu JH, Kazlauskas RJ, Dean AM (2016) Evolution of a catalytic mechanism. Mol Biol Evol 33:971–979. https://doi.org/10.1093/molbev/msv338
Rowen E, Kaplan I (2016) Induced plant volatiles: plant body odours structuring ecological networks. New Phytol 210:284–294
Schilirò E, Ferrara M, Nigro F, Mercado-Blanco J (2012) Genetic responses induced in olive roots upon colonization by the biocontrol endophytic bacterium Pseudomonas fluorescens PICF7. PLoS ONE 7:e48646. https://doi.org/10.1371/journal.pone.0048646
Shahriar SA, Islam MN, Chun CN, Kaur P, Rahim MA, Islam MM, Uddain J, Siddiquee S (2022) Microbial metabolomics interaction and ecological challenges of Trichoderma species as biocontrol inoculant in crop rhizosphere. Agronomy 12:900. https://doi.org/10.3390/agronomy12040900
Siegień I, Bogatek R (2006) Cyanide action in plants — from toxic to regulatory. Acta Physiol Plant 28:483–497. https://doi.org/10.1007/BF02706632
Smulders L, Benítez E, Moreno B, López-García Á, Pozo MJ, Ferrero V, de la Peña E, Alcalá, Herrera R (2021) Tomato Domestication Affects Potential Functional Molecular Pathways of Root-Associated Soil Bacteria. Plants (Basel) 17;10(9):1942. https://doi.org/10.3390/plants10091942
Takabayashi J (2022) Herbivory-induced plant volatiles mediate multitrophic relationships in ecosystems. Plant Cell Physiol 63:1344–1355. https://doi.org/10.1093/pcp/pcac107
Takabayashi J, Shiojiri K (2019) Multifunctionality of herbivory-induced plant volatiles in chemical communication in tritrophic interactions. Curr Opin Insect Sci 32:110–117. https://doi.org/10.1016/j.cois.2019.01.003
Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M (2014) Development of a prokaryotic universal primer for simultaneous analysis of bacteria and archaea using next-generation sequencing. PLoS ONE 9:e105592. https://doi.org/10.1371/journal.pone.010559
Thaler DS (2021) Is global microbial biodiversity increasing, decreasing, or staying the same? Front Ecol Evol 9:565649. https://doi.org/10.3389/fevo.2021.565649
Vetter J (2000) Plant cyanogenic glycosides. Toxicon 38:11–36. https://doi.org/10.1016/S0041-0101(99)00128-2
Vincenti S, Mariani M, Alberti JC, Jacopini S, Brunini-Bronzini de Caraffa V, Berti L, Maury J (2019) Biocatalytic synthesis of natural green leaf volatiles using the lipoxygenase metabolic pathway. Catalysts 9:873. https://doi.org/10.3390/catal9100873
Viterbo A, Wiest A, Brotman Y, Che, I, Kenerley C (2007) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746
Wang X, Chapman KD (2013) Lipid signaling in plants. Front Plant Sci 4:216. https://doi.org/10.3389/fpls.2013.00216
Waterman JM, Cazzonelli CI, Hartley SE, Johnson SN (2019) Simulated herbivory: the key to disentangling plant defence responses. Trends Ecol Evol 34:447–458. https://doi.org/10.1016/J.TREE.2019.01.008
Woo SL, Hermosa R, Lorito M, Monte E (2023) Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture. Nat Rev Microbiol 21:312–326. https://doi.org/10.1038/s41579-022-00819-5
Xiao L, Carrillo J, Siemann E, Ding J (2019) Herbivore-specific induction of indirect and direct defensive responses in leaves and roots. AoB Plants 11:plz003. https://doi.org/10.1038/s41579-022-00819-5
Acknowledgements
This study was supported by grant P20-00139 and the postdoctoral contract grant P12-AGR-1419 funded by Consejería de Transformación Económica, Industria, Conocimiento y Universidades, Junta de Andalucía, and by “ERDF A way of making Europe. We would like to thank Estefania Berrio from the Department of Soil Microbiology and Symbiotic Systems, EEZ-CSIC, for her invaluable assistance with the qPCR analyses.
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Aguirrebengoa, M., Moreno, B., Alcalá-Herrera, R. et al. Modulation of volatile emissions in olive trees: sustained effect of Trichoderma afroharzianum T22 on induced plant defenses after simulated herbivory. Biol Fertil Soils (2024). https://doi.org/10.1007/s00374-024-01830-z
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DOI: https://doi.org/10.1007/s00374-024-01830-z