Microbe-mediated organic fertilization increases insect predator attraction upon fruit damage in olive trees

Martin Aguirrebengoa , Beatriz Moreno , Nuria Guirado , Rafael Núñez , María L. Fernández-Sierra , Fernando Reyes , Jesús Martín , Emilio Benítez

Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (1) : 240281

PDF (1921KB)
Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (1) : 240281 DOI: 10.1007/s42832-024-0281-z
RESEARCH ARTICLE

Microbe-mediated organic fertilization increases insect predator attraction upon fruit damage in olive trees

Author information +
History +
PDF (1921KB)

Abstract

The objective of this study was to investigate the combined effect of soil amendments and pest attack on plant-induced defense and their impact on a biological control agent’s behavior. The effects of olive mill wastes revalorized through vermicomposting on the aboveground tri-trophic interactions among olive trees (Olea europaea), the olive seed-feeder, Prays oleae, and its natural predator, Chrysoperla carnea, were evaluated. The findings demonstrate that soil nitrogen and organic carbon levels, in conjunction with fungal diversity and functionality within olive roots, exert a significant influence on the volatile compounds emitted by the plant underattack that are most appealing to C. carnea. Moreover, the attractivenessof aerial volatiles was found to correlate with soil organic carbon content and the taxonomic and functional diversity of both bacteria and fungi in the olive root system. It is worthy of note that three particular volatile compounds, namely 5-hepten-2-one-6-methyl, acetic acid and nonanal, were consistently observed to attract C. carnea. These findings highlight the potential of soil amendments to enhance biological control strategies. Future research should prioritise the validation the greenhouse findings through large-scale field trials and the assessment of the practical applications of soil amendments in pest management programmes.

Graphical abstract

Keywords

Chrysoperla carnea / HIPVs / Olea europaea / Prays oleae / roots microbiome / soil amendments

Highlight

● Revalorized olive waste impacts root microbiome.

● Root microbiome modulates plant-induced defense.

● Insect’s exudate simulates the pest attack.

Cite this article

Download citation ▾
Martin Aguirrebengoa, Beatriz Moreno, Nuria Guirado, Rafael Núñez, María L. Fernández-Sierra, Fernando Reyes, Jesús Martín, Emilio Benítez. Microbe-mediated organic fertilization increases insect predator attraction upon fruit damage in olive trees. Soil Ecology Letters, 2025, 7(1): 240281 DOI:10.1007/s42832-024-0281-z

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Abarenkov, K., Zirk, A., Piirmann, T., Pöhönen, R., Ivanov, F., Nilsson, R.H., Kõljalg, U., 2024. UNITE mothur release for Fungi. UNITE Community. DOI:10.15156/BIO/2959342.

[2]

Aguirrebengoa, M., Moreno, B., Alcalá-Herrera, R., Núñez, R., Guirado, N., García, J.M., Pozo, M.J., Benítez, E., 2024. Modulation of volatile emissions in olive trees: sustained effect of Trichoderma afroharzianum T22 on induced plant defenses after simulated herbivory. Biology and Fertility of Soils60, 593–602.

[3]

Akanmu, A.O., Babalola, O.O., Venturi, V., Ayilara, M.S., Adeleke, B.S., Amoo, A.E., Sobowale, A.A., Fadiji, A.E., Glick, B.R., 2021. Plant disease management: leveraging on the plant-microbe-soil interface in the biorational use of organic amendments. Frontiers in Plant Science12, 700507.

[4]

Allen, C.D., Macalady, A.K., Chenchouni, H., Bachelet, D., McDowell, N., Vennetier, M., Kitzberger, T., Rigling, A., Breshears, D.D., Hogg, E.H., Gonzalez, P., Fensham, R., Zhang, Z., Castro, J., Demidova, N., Lim, J.H., Allard, G., Running, S.W., Semerci, A., Cobb, N., 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management259, 660–684.

[5]

Arimura, G.I., Matsui, K., Takabayashi, J., 2009. Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant and Cell Physiology50, 911–923.

[6]

Armstrong, G., Rahman, G., Martino, C., McDonald, D., Gonzalez, A., Mishne, G., Knight, R., 2022. Applications and comparison of dimensionality reduction methods for microbiome data. Frontiers in Bioinformatics2, 821861.

[7]

Badra, Z., Larsson Herrera, S., Cappellin, L., Biasioli, F., Dekker, T., Angeli, S., Tasin, M., 2021. Species-specific induction of plant volatiles by two aphid species in apple: real time measurement of plant emission and attraction of lacewings in the wind tunnel. Journal of Chemical Ecology47, 653–663.

[8]

Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software67, 1–48.

[9]

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. Scientific Reports7, 6251.

[10]

Botta-Dukát, Z., 2005. Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. Journal of Vegetation Science16, 533–540.

[11]

Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., Holmes, S.P., 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods13, 581–583.

[12]

Chauhan, P., Sharma, N., Tapwal, A., Kumar, A., Verma, G.S., Meena, M., Seth, C.S., Swapnil, P., 2023. Soil microbiome: diversity, benefits and interactions with plants. Sustainability15, 14643.

[13]

Chen, D.Q., Shao, M., Sun, S.Z., Liu, T.T., Zhang, H., Qin, N.N., Zeng, R.S., Song, Y.Y., 2019. Enhancement of jasmonate-mediated antiherbivore defense responses in tomato by acetic acid, a potent inducer for plant protection. Frontiers in Plant Science10, 764.

[14]

Chong, J., Liu, P., Zhou, G.Y., Xia, J.G., 2020. Using microbiomeanalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nature Protocols15, 799–821.

[15]

Cui, Y., Ouyang, S.N., Zhao, Y.J., Tie, L., Shao, C.C., Duan, H.L., 2022. Plant responses to high temperature and drought: a bibliometrics analysis. Frontiers in Plant Science13, 1052660.

[16]

Dhariwal, A., Chong, J., Habib, S., King, I.L., Agellon, L.B., Xia, J.G., 2017. MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Research45, W180–W188.

[17]

Dicke, M., Baldwin, I.T., 2010. The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science15, 167–175.

[18]

Escobar-Bravo, R., Lin, P.A., Waterman, J.M., Erb, M., 2023. Dynamic environmental interactions shaped by vegetative plant volatiles. Natural Product Reports40, 840–865.

[19]

Espinoza Vidaurre, S.M., Velásquez Rodríguez, N.C., Gambetta Quelopana, R.L., Martinez Valdivia, A.N., Leo Rossi, E.A., Laura De La Cruz, K.M., 2023. Understanding factors that influence pest risk in olive production. Sustainability15, 16445.

[20]

FAOSTAT, 2019. Food and Agriculture Organization of the United Nations. Production: Crops [Online]. Available at the website of FAO.

[21]

Farooqi, Z.U.R., Qadir, A.A., Alserae, H., Raza, A., Mohy-Ud-Din, W., 2023. Organic amendment–mediated reclamation and build-up of soil microbial diversity in salt-affected soils: fostering soil biota for shaping rhizosphere to enhance soil health and crop productivity. Environmental Science and Pollution Research30, 109889–109920.

[22]

Fernández-González, A.J., Cardoni, M., Gómez-Lama Cabanás, C., Valverde-Corredor, A., Villadas, P.J., Fernández-López, M., Mercado-Blanco, J., 2020. Linking belowground microbial network changes to different tolerance level towards Verticillium wilt of olive. Microbiome8, 11.

[23]

Food and Agriculture Organization of the United Nations, 2019. RECSOIL: Recarbonization of Global Agricultural Soils [Online]. Available at the website of FAO.

[24]

Hjältén, J., 2008. Simulating herbivory: problems and possibilities. In: Weisser, W.W., Siemann, E., eds. Insects and Ecosystem Function. Berlin: Springer243–255.

[25]

Ihrmark, K., Bödeker, I.T.M., Cruz-Martinez, K., Friberg, H., Kubartova, A., Schenck, J., Strid, Y., Stenlid, J., Brandström-Durling, M., Clemmensen, K.E., Lindahl, B.D., 2012. New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiology Ecology82, 666–677.

[26]

Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics24, 1403–1405.

[27]

Jombart, T., Ahmed, I., 2011. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics27, 3070–3071.

[28]

Jones, A.C., Felton, G.W., Tumlinson, J.H., 2022. The dual function of elicitors and effectors from insects: reviewing the ‘arms race’ against plant defenses. Plant Molecular Biology109, 427–445.

[29]

Laliberté, E., Legendre, P., 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology91, 299–305.

[30]

Laliberté, E., Legendre, P., Shipley, B., 2014. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R Package Version 1.0-12.

[31]

Lidoy, J., Lópéz-García, Á., Amate, C., García, J.M., Flors, V., García-Garrido, J.M., Azcón-Aguilar, C., López-Ráez, J.A., Pozo, M.J., 2023. Regulation of mycorrhizal colonization under stress in tomato depends on symbiotic efficiency. Environmental and Experimental Botany215, 105479.

[32]

Liu, W.J., Yang, Z.P., Ye, Q.X., Peng, Z.H., Zhu, S.X., Chen, H.L., Liu, D.H., Li, Y.D., Deng, L.J., Shu, X.Y., Huang, H., 2023. Positive effects of organic amendments on soil microbes and their functionality in agro-ecosystems. Plants12, 3790.

[33]

Lundberg, D.S., Yourstone, S., Mieczkowski, P., Jones, C.D., Dangl, J.L., 2013. Practical innovations for high-throughput amplicon sequencing. Nature Methods10, 999–1002.

[34]

Mahzoum, A.M., Villa, M., Benhadi-Marín, J., Pereira, J.A., 2020. Functional response of Chrysoperla carnea (Neuroptera: Chrysopidae) larvae on Saissetia oleae (Olivier) (Hemiptera: Coccidae): implications for biological control. Agronomy10, 1511.

[35]

Martín, J., Crespo, G., González-Menéndez, V., Pérez-Moreno, G., Sánchez-Carrasco, P., Pérez-Victoria, I., Ruiz-Pérez, L.M., González-Pacanowska, D., Vicente, F., Genilloud, O., Bills, G.F., Reyes, F., 2014. MDN-0104, an antiplasmodial betaine lipid from Heterospora chenopodii. Journal of Natural Products77, 2118–2123.

[36]

Mendes, R., Kruijt, M., De Bruijn, I., Dekkers, E., Van Der Voort, M., Schneider, J.H.M., Piceno, Y.M., Desantis, T.Z., Andersen, G.L., Bakker, P.A.H.M., Raaijmakers, J.M., 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science332, 1097–1100.

[37]

Molefe, R.R., Amoo, A.E., Babalola, O.O., 2023. Communication between plant roots and the soil microbiome; involvement in plant growth and development. Symbiosis90, 231–239.

[38]

Nguyen, L.H., Holmes, S., 2019. Ten quick tips for effective dimensionality reduction. PLOS Computational Biology15, e1006907.

[39]

Niu, H., Pang, Z.Q., Fallah, N., Zhou, Y.M., Zhang, C.F., Hu, C.H., Lin, W.X., Yuan, Z.N., 2021. Diversity of microbial communities and soil nutrients in sugarcane rhizosphere soil under water soluble fertilizer. PLoS One16, e0245626.

[40]

Noman, M., Ahmed, T., Ijaz, U., Shahid, M., Azizullah, Li, D.Y., Manzoor, I., Song, F.M., 2021. Plant-microbiome crosstalk: dawning from composition and assembly of microbial community to improvement of disease resilience in plants. International Journal of Molecular Sciences22, 6852.

[41]

Oksanen, J., Simpson, G.L., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Solymos, P., Stevens, M.H.H., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., De Caceres, M., Durand, S., Evangelista, .H. B. A, FitzJohn, R., Friendly, M., Furneaux, B., Hannigan, G., O. Hill, M., Lahti, L., McGlinn, D., Ouellette, M.H., Cunha, E.R., Smith, T., Stier, A., Braak, C.J.F.T., Weedon, J., 2024. vegan: Community Ecology Package. R package version 2.6-8 [Online]. .

[42]

Ourry, M., Lebreton, L., Chaminade, V., Guillerm-Erckelboudt, A.Y., Hervé, M., Linglin, J., Marnet, N., Ourry, A., Paty, C., Poinsot, D., Cortesero, A.M., Mougel, C., 2018. Influence of belowground herbivory on the dynamics of root and rhizosphere microbial communities. Frontiers in Ecology and Evolution6, 91.

[43]

Palomares-Pérez, M., Moreno-Rodriguez, C., Contreras-Bermúdez, Y., Arredondo-Bernal, H.C., Gallou, A., 2019. Molecular characterization of Chrysoperla carnea (Neuroptera: Chrysopidae) from commercial insectaries in Mexico. Molecular Biology Reports46, 6577–6583.

[44]

Pappalardo, S., Villa, M., Santos, S.A.P., Benhadi-Marín, J., Pereira, J.A., Venturino, E., 2021. A tritrophic interaction model for an olive tree pest, the olive moth - Prays oleae (Bernard). Ecological Modelling462, 109776.

[45]

Paredes, D., Cayuela, L., Gurr, G.M., Campos, M., 2015. Single best species or natural enemy assemblages? A correlational approach to investigating ecosystem function. BioControl60, 37–45.

[46]

Pascale, A., Proietti, S., Pantelides, I.S., Stringlis, I.A., 2020. Modulation of the root microbiome by plant molecules: the basis for targeted disease suppression and plant growth promotion. Frontiers in Plant Science10, 1741.

[47]

Peñaflor, M.F.G.V., Bento, J.M.S., 2013. Herbivore-induced plant volatiles to enhance biological control in agriculture. Neotropical Entomology42, 331–343.

[48]

Pérez-Hedo, M., Alonso-Valiente, M., Vacas, S., Gallego, C., Pons, C., Arbona, V., Rambla, J.L., Navarro-Llopis, V., Granell, A., Urbaneja, A., 2021. Plant exposure to herbivore-induced plant volatiles: a sustainable approach through eliciting plant defenses. Journal of Pest Science94, 1221–1235.

[49]

Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., R Core Team., 2022. nlme: Linear and Nonlinear Mixed Effects Models. R package version3, 1–153.

[50]

Põlme, S., Abarenkov, K., Nilsson, R.H., Lindahl, B.D., Clemmensen, K.E., Kauserud, H., Nguyen, N., Kjøller, R., Bates, S.T., Baldrian, P., Frøslev, T.G., Adojaan, K., Vizzini, A., Suija, A., Pfister, D., Baral, H.O., Järv, H., Madrid, H., Nordén, J., Liu, J.K., Pawlowska, J., Põldmaa, K., Pärtel, K., Runnel, K., Hansen, K., Larsson, K.H., Hyde, K.D., Sandoval-Denis, M., Smith, M.E., Toome-Heller, M., Wijayawardene, N.N., Menolli, N., Reynolds, N.K., Drenkhan, R., Maharachchikumbura, S.S.N., Gibertoni, T.B., Læssøe, T., Davis, W., Tokarev, Y., Corrales, A., Soares, A.M., Agan, A., Machado, A.R., Argüelles-Moyao, A., Detheridge, A., De Meiras-ottoni, A., Verbeken, A., Dutta, A.K., Cui, B.K., Pradeep, C.K., Marín, C., Stanton, D., Gohar, D., Wanasinghe, D.N., Otsing, E., Aslani, F., Griffith, G.W., Lumbsch, T.H., Grossart, H.P., Masigol, H., Timling, I., Hiiesalu, I., Oja, J., Kupagme, J.Y., Geml, J., Alvarez-Manjarrez, J., Ilves, K., Loit, K., Adamson, K., Nara, K., Küngas, K., Rojas-Jimenez, K., Bitenieks, K., Irinyi, L., Nagy, L.G., Soonvald, L., Zhou, L.W., Wagner, L., Aime, M.C., Öpik, M., Mujica, M.I., Metsoja, M., Ryberg, M., Vasar, M., Murata, M., Nelsen, M.P., Cleary, M., Samarakoon, M.C., Doilom, M., Bahram, M., Hagh-Doust, N., Dulya, O., Johnston, P., Kohout, P., Chen, Q., Tian, Q., Nandi, R., Amiri, R., Perera, R.H., Dos Santos chikowski, R., Mendes-Alvarenga, R.L., Garibay-Orijel, R., Gielen, R., Phookamsak, R., Jayawardena, R.S., Rahimlou, S., Karunarathna, S.C., Tibpromma, S., Brown, S.P., Sepp, S.K., Mundra, S., Luo, Z.H., Bose, T., Vahter, T., Netherway, T., Yang, T., May, T., Varga, T., Li, W., Coimbra, V.R.M., de Oliveira, V.R.T., de Lima, V.X., Mikryukov, V.S., Lu, Y.Z., Matsuda, Y., Miyamoto, Y., Kõljalg, U., Tedersoo, L., 2020. FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Diversity105, 1–16.

[51]

Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glöckner, F.O., 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research41, D590–D596.

[52]

R Core Team, 2022. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Available at the website of r-project.org.

[53]

Rani, A.S., Sulakshana, G., 2017. Herbivore-induced plant volatiles. In: Choudhary, D.K., Sharma, A.K., Agarwal, P., Varma, A., Tuteja, N., eds. Volatiles and Food Security. Singapore: Springer285–298.

[54]

Reimer, L.C., Sardà Carbasse, J., Koblitz, J., Ebeling, C., Podstawka, A., Overmann, J., 2022. BacDive in 2022: the knowledge base for standardized bacterial and archaeal data. Nucleic Acids Research50, D741–D746.

[55]

Ruano-Rosa, D., Valverde-Corredor, A., Gómez-Lama Cabanás, C., Sesmero, R., Mercado-Blanco, J., 2017. What lies beneath: root-associated bacteria to improve the growth and health of olive trees. In: Lukac, M., Grenni, P., Gamboni, M., eds. Soil Biological Communities and Ecosystem Resilience. Cham: Springer107–122.

[56]

Sato, H., Mizoi, J., Shinozaki, K., Yamaguchi-Shinozaki, K., 2024. Complex plant responses to drought and heat stress under climate change. The Plant Journal117, 1873–1892.

[57]

Sciubba, F., Chronopoulou, L., Pizzichini, D., Lionetti, V., Fontana, C., Aromolo, R., Socciarelli, S., Gambelli, L., Bartolacci, B., Finotti, E., Benedetti, A., Miccheli, A., Neri, U., Palocci, C., Bellincampi, D., 2020. Olive mill wastes: a source of bioactive molecules for plant growth and protection against pathogens. Biology9, 450.

[58]

Sharma, I., Kashyap, S., Agarwala, N., 2023. Biotic stress-induced changes in root exudation confer plant stress tolerance by altering rhizospheric microbial community. Frontiers in Plant Science14, 1132824.

[59]

Shree, P., Kumar, M., Singh, D.K., 2021. Molecular and biochemical aspect of insect-plant interaction: a perspective for pest management. In: Singh, I. K., Singh, A., eds. Plant-Pest Interactions: from Molecular Mechanisms to Chemical Ecology. Singapore: Springer417–436.

[60]

Snoeck, S., Guayazán-Palacios, N., Steinbrenner, A.D., 2022. Molecular tug-of-war: plant immune recognition of herbivory. The Plant Cell34, 1497–1513.

[61]

Song, C.X., Zhu, F., Carrión, V.J., Cordovez, V., 2020. Beyond plant microbiome composition: exploiting microbial functions and plant traits via integrated approaches. Frontiers in Bioengineering and Biotechnology8, 896.

[62]

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 One9, e105592.

[63]

Tzanakakis, M.E., 2003. Seasonal development and dormancy of insects and mites feeding on olive: a review. Netherlands Journal of Zoology52, 87–224.

[64]

Villa, M., Santos, S.A.P., Benhadi-Marín, J., Mexia, A., Bento, A., Pereira, J.A., 2016. Life-history parameters of Chrysoperla carnea s.l. fed on spontaneous plant species and insect honeydews: importance for conservation biological control. BioControl61, 533–543.

[65]

Vivas, A., Moreno, B., Garcia-Rodríguez, S., Benitez, E., 2009. Assessing the impact of composting and vermicomposting on bacterial community size and structure, and microbial functional diversity of an olive-mill waste. Bioresource Technology100, 1319–1326.

[66]

Wang, H.Y., Shi, S.J., Hua, W., 2023. Advances of herbivore-secreted elicitors and effectors in plant-insect interactions. Frontiers in Plant Science14, 1176048.

[67]

Waterman, J.M., Cazzonelli, C.I., Hartley, S.E., Johnson, S.N., 2019. Simulated herbivory: the key to disentangling plant defence responses. Trends in Ecology & Evolution34, 447–458.

[68]

Wei, L.P., Bergeron, Y., De Frenne, P., Verheyen, K., Tian, L.M., Ren, H., Jian, S.G., 2024. Above- and belowground composition and diversity of subtropical plantations and their relationships with soil nutrient stocks. Plant and Soil495, 235–252.

[69]

Wright, M.N., Ziegler, A., 2017. ranger: a fast implementation of random forests for high dimensional data in C++ and R. Journal of Statistical Software77, 1–17.

[70]

Yamamichi, M., Gibbs, T., Levine, J.M., 2022. Integrating eco-evolutionary dynamics and modern coexistence theory. Ecology Letters25, 2091–2106.

[71]

Yang, M., Cheng, J.B., Yin, M., Wu, J.S., 2023. NaMLP, a new identified Kunitz trypsin inhibitor regulated synergistically by JA and ethylene, confers Spodoptera litura resistance in Nicotiana attenuata. Plant Cell Reports42, 723–734.

[72]

Zhang, H.M., Kaushal, R., Singh, S.K., Paré, P.W., 2020. Bacterial volatile-mediated plant abiotic stress tolerance. In: Ryu, C.M., Weisskopf, L., Piechulla, B., eds. Bacterial Volatile Compounds as Mediators of Airborne Interactions. Singapore: Springer187–200.

RIGHTS & PERMISSIONS

The Author(s) 2024. This article is published with open access at link.springer.com and journal.hep.com.cn

AI Summary AI Mindmap
PDF (1921KB)

Supplementary files

SEL-00281-OF-BE_suppl_1

842

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/