Abstract
The gut microbiome of plant-eaters is affected by the food they eat, but it is currently unclear how the plant metabolome and microbiome are influenced by the substrate the plant grows in and how this subsequently impacts the feeding behavior and gut microbiomes of insect herbivores. Here, we use Plutella xylostella caterpillars and show that the larvae prefer leaves of cabbage plants growing in a vermiculite substrate to those from plants growing in conventional soil systems. From a plant metabolomics analysis, we identified 20 plant metabolites that were related to caterpillar feeding performance. In a bioassay, the effects of these plant metabolites on insects’ feeding were tested. Nitrate and compounds enriched with leaves of soilless cultivation promoted the feeding of insects, while compounds enriched with leaves of plants growing in natural soil decreased feeding. Several microbial groups (e.g., Sporolactobacillus, Haliangium) detected inside the plant correlated with caterpillar feeding performance and other microbial groups, such as Ramlibacter and Methylophilus, correlated with the gut microbiome. Our results highlight the role of growth substrates on the food metabolome and microbiome and on the feeding performance and the gut microbiome of plant feeders. It illustrates how belowground factors can influence the aboveground properties of plant-animal systems, which has important implications for plant growth and pest control.
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Data availability
The authors declare that the data supporting the findings of this study are available within the paper and its supplementary information files. Raw sequence data obtained in this study have been deposited in Genome Sequence Archive in the BIG Data Center, Chinese Academy of Sciences, under accession code CRA004812. All data and code are available on GitHub (https://github.com/taowenmicro/Yuan-et-al.2021).
References
Ahuja, I., Rohloff, J., and Bones, A.M. (2011). Defence mechanisms of Brassicaceae: implications for plant-insect interactions and potential for integrated pest management. In: Lichtfouse, E., Hamelin, M., Navarrete, M., and Debaeke, P., eds. Sustainable Agriculture Volume 2. Dordrecht: Springer. 623–670.
Altieri, M.A., and Nicholls, C.I. (2003). Soil fertility management and insect pests: harmonizing soil and plant health in agroecosystems. Soil Tillage Res 72, 203–211.
Asnicar, F., Berry, S.E., Valdes, A.M., Nguyen, L.H., Piccinno, G., Drew, D.A., Leeming, E., Gibson, R., Le Roy, C., Khatib, H.A., et al. (2021). Microbiome connections with host metabolism and habitual diet from 1,098 deeply phenotyped individuals. Nat Med 27, 321–332.
Bengmark, S. (1998). Ecological control of the gastrointestinal tract. The role of probiotic flora. Gut 42, 2–7.
Bezemer, T., and van Dam, N. (2005). Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20, 617–624.
Blundell, R., Schmidt, J.E., Igwe, A., Cheung, A.L., Vannette, R.L., Gaudin, A.C.M., and Casteel, C.L. (2020). Organic management promotes natural pest control through altered plant resistance to insects. Nat Plants 6, 483–491.
Callegari, M., Jucker, C., Fusi, M., Leonardi, M.G., Daffonchio, D., Borin, S., Savoldelli, S., and Crotti, E. (2020). Hydrolytic profile of the culturable gut bacterial community associated with Hermetia illucens. Front Microbiol 11.
Chen, Y., Zeng, L., Liao, Y., Li, J., Zhou, B., Yang, Z., and Tang, J. (2020). Enzymatic reaction-related protein degradation and proteinaceous amino acid metabolism during the black tea (Camellia sinensis) manufacturing process. Foods 9, 66.
Chi, F., Shen, S.H., Cheng, H.P., Jing, Y.X., Yanni, Y.G., and Dazzo, F.B. (2005). Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71, 7271–7278.
D’Alessandro, A., Taamalli, M., Gevi, F., Timperio, A.M., Zolla, L., and Ghnaya, T. (2013). Cadmium stress responses in Brassica juncea: hints from proteomics and metabolomics. J Proteome Res 12, 4979–4997.
De Vos, M., Van Oosten, V.R., Van Poecke, R.M.P., Van Pelt, J.A., Pozo, M.J., Mueller, M.J., Buchala, A.J., Métraux, J.P., Van Loon, L.C., Dicke, M., et al. (2005). Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18, 923–937.
Ding, S., Yan, W., Fang, J., Jiang, H., and Liu, G. (2021). Potential role of Lactobacillus plantarum in colitis induced by dextran sulfate sodium through altering gut microbiota and host metabolism in murine model. Sci China Life Sci 64, 1906–1916.
Dixon, P. (2003). VEGAN, a package of R functions for community ecology. J Veg Sci 14, 927–930.
Edgar, R.C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.
Eilers, E.J., Veit, D., Rillig, M.C., Hansson, B.S., Hilker, M., and Reinecke, A. (2016). Soil substrates affect responses of root feeding larvae to their hosts at multiple levels: orientation, locomotion and feeding. Basic Appl Ecol 17, 115–124.
Flanagan, P.W., and Cleve, K.V. (1983). Nutrient cycling in relation to decomposition and organic-matter quality in taiga ecosystems. Can J For Res 13, 795–817.
Forcat, S., Bennett, M.H., Mansfield, J.W., and Grant, M.R. (2008). A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods 4, 16.
Gill, S.R., Pop, M., DeBoy, R.T., Eckburg, P.B., Turnbaugh, P.J., Samuel, B.S., Gordon, J.I., Relman, D.A., Fraser-Liggett, C.M., and Nelson, K. E. (2006). Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359.
Gomes, S.I.F., Kielak, A.M., Hannula, S.E., Heinen, R., Jongen, R., Keesmaat, I., De Long, J.R., and Bezemer, T.M. (2020). Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities. Anim Microbiome 2, 1–2.
Hammer, T.J., and Bowers, M.D. (2015). Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179, 1–14.
Hannula, S.E., Zhu, F., Heinen, R., and Bezemer, T.M. (2019). Foliar-feeding insects acquire microbiomes from the soil rather than the host plant. Nat Commun 10, 1–9.
Hansen, J., and Møller, I. (1975). Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone. Anal Biochem 68, 87–94.
He, F. (2011). Bradford protein assay. Bio-protocol, 1, e45.
Kikuchi, Y., Hosokawa, T., and Fukatsu, T. (2007). Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol 73, 4308–4316.
Kimura, I., Miyamoto, J., Ohue-Kitano, R., Watanabe, K., Yamada, T., Onuki, M., Aoki, R., Isobe, Y., Kashihara, D., Inoue, D., et al. (2020). Maternal gut microbiota in pregnancy influences offspring metabolic phenotype in mice. Science 367, eaaw8429.
Kind, T., Wohlgemuth, G., Lee, D.Y., Lu, Y., Palazoglu, M., Shahbaz, S., and Fiehn, O. (2009). FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Anal Chem 81, 10038–10048.
Kollner, T.G., Held, M., Lenk, C., Hiltpold, I., Turlings, T.C.J., Gershenzon, J., and Degenhardt, J.. (2008). A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20, 482–494.
Maidak, B.L., Cole, J.R., Lilburn, T.G., Parker, C.T., Saxman, P.R., Stredwick, J.M., Garrity, G.M., Li, B., Olsen, G.J., Pramanik, S., et al. (2000). The RDP (ribosomal database project) continues. Nucleic Acids Res 28, 173–174.
Marti, G., Erb, M., Boccard, J., Glauser, G., Doyen, G.R., Villard, N., Robert, C.A.M., Turlings, T.C.J., Rudaz, S., and Wolfender, J.L. (2013). Metabolomics reveals herbivore-induced metabolites of resistance and susceptibility in maize leaves and roots. Plant Cell Environ 36, 621–639.
Mattson, W.J. (1980). Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11, 119–161.
Megali, L., Glauser, G., and Rasmann, S. (2014). Fertilization with beneficial microorganisms decreases tomato defenses against insect pests. Agron Sustain Dev 34, 649–656.
Mewis, I., Appel, H.M., Hom, A., Raina, R., and Schultz, J.C. (2005). Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138, 1149–1162.
Mikulska, M., Bomsel, J.L., and Rychter, A.M. (1998). The influence of phosphate deficiency on photosynthesis, respiration and adenine nucleotide pool in bean leaves. Photosynthetica 35, 79–88.
Miyauchi, E., Kim, S.W., Suda, W., Kawasumi, M., Onawa, S., Taguchi-Atarashi, N., Morita, H., Taylor, T.D., Hattori, M., and Ohno, H. (2020). Gut microorganisms act together to exacerbate inflammation in spinal cords. Nature 585, 102–106.
Muratore, M., Sun, Y., and Prather, C. (2020). Environmental nutrients alter bacterial and fungal gut microbiomes in the common meadow katydid, Orchelimum vulgare. Front Microbiol 11, 557980.
Nemet, I., Saha, P.P., Gupta, N., Zhu, W., Romano, K.A., Skye, S.M., Cajka, T., Mohan, M.L., Li, L., Wu, Y., et al. (2020). A cardiovascular disease-linked gut microbial metabolite acts via adrenergic receptors. Cell 180, 862–877.e22.
Norman, R.J., and Stucki, J.W. (1981). The determination of nitrate and nitrite in soil extracts by ultraviolet spectrophotometry. Soil Sci Soc Am J 45, 347–353.
Nosarzewski, M., Downie, A.B., Wu, B., and Archbold, D.D. (2012). The role of SORBITOL DEHYDROGENASE in Arabidopsis thaliana. Funct Plant Biol 39, 462.
Ohgushi, T. (2005). Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36, 81–105.
Pan, X., Welti, R., and Wang, X. (2008). Simultaneous quantification of major phytohormones and related compounds in crude plant extracts by liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69, 1773–1781.
Pichersky, E., and Gershenzon, J. (2002). The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5, 237–243.
Raza, M.F., Wang, Y., Cai, Z., Bai, S., Yao, Z., Awan, U.A., Zhang, Z., Zheng, W., and Zhang, H. (2020). Gut microbiota promotes host resistance to low-temperature stress by stimulating its arginine and proline metabolism pathway in adult Bactrocera dorsalis. PLoS Pathog 16, e1008441.
Reyes, R.D.H., and Cafaro, M.J. (2015). Paratrechina longicornis ants in a tropical dry forest harbor specific Actinobacteria diversity. J Basic Microbiol 55, 11–21.
Rognes, T., Flouri, T., Nichols, B., Quince, C., and Mahé, F. (2016). VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584.
Rosen, C.J., and Allan, D.L. (2007). Exploring the benefits of organic nutrient sources for crop production and soil quality. HortTechnology 17, 422–430.
Russolillo, G. (2012). Non-metric partial least squares. Electron J Stat 6, 1641.
Santos-Garcia, D., Mestre-Rincon, N., Zchori-Fein, E., and Morin, S. (2020). Inside out: microbiota dynamics during host-plant adaptation of whiteflies. ISME J 14, 847–856.
SharathKumar, M., Heuvelink, E., and Marcelis, L.F.M. (2020). Vertical farming: moving from genetic to environmental modification. Trends Plant Sci 25, 724–727.
Shelp, B.J., Bown, A.W., and McLean, M.D. (1999). Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4, 446–452.
Shepherd, E.S., DeLoache, W.C., Pruss, K.M., Whitaker, W.R., and Sonnenburg, J.L. (2018). An exclusive metabolic niche enables strain engraftment in the gut microbiota. Nature 557, 434–438.
Sugio, A., Dubreuil, G., Giron, D., and Simon, J.C. (2015). Plant-insect interactions under bacterial influence: ecological implications and underlying mechanisms. J Exp Bot 66, 467–478.
Tenenboim, H., and Brotman, Y. (2016). Omic relief for the biotically stressed: metabolomics of plant biotic interactions. Trends Plant Sci 21, 781–791.
van der Heijden, M.G.A., Bardgett, R.D., and van Straalen, N.M. (2008). The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11, 296–310.
Van Poecke, R.M.P., Posthumus, M.A., and Dicke, M. (2001). Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol 27, 1911–1928.
Walters, W., Hyde, E.R., Berg-Lyons, D., Ackermann, G., Humphrey, G., Parada, A., Gilbert, J.A., Jansson, J.K., Caporaso, J.G., Fuhrman, J.A., et al. (2016). Improved bacterial 16S rRNA gene (V4 and V4–5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1, e00009–15.
Wen, T., Xie, P., Yang, S., Niu, G., Liu, X., Ding, Z., Xue, C., Liu, Y., Shen, Q., and Yuan, J. (2022). ggClusterNet: An R package for microbiome network analysis and modularity-based multiple network layouts. iMeta 1, e32.
Winter, H., Lohaus, G., and Heldt, H.W. (1992). Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiol 99, 996–1004.
Yang, X., Feng, L., Zhao, L., Liu, X., Hassani, D., and Huang, D. (2018). Effect of glycine nitrogen on lettuce growth under soilless culture: a metabolomics approach to identify the main changes occurred in plant primary and secondary metabolism. J Sci Food Agric 98, 467–477.
Yuan, J., Wen, T., Zhang, H., Zhao, M., Penton, C.R., Thomashow, L.S., and Shen, Q. (2020). Predicting disease occurrence with high accuracy based on soil macroecological patterns of Fusarium wilt. ISME J 14, 2936–2950.
Yuan, J., Zhao, J., Wen, T., Zhao, M., Li, R., Goossens, P., Huang, Q., Bai, Y., Vivanco, J.M., Kowalchuk, G.A., et al. (2018). Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6, 1–2.
Zeisel, A., Zuk, O., and Domany, E. (2011). FDR control with adaptive procedures and FDR monotonicity. Ann Appl Stat 5, 943.
Zhu, Y.X., Song, Z.R., Zhang, Y.Y., Hoffmann, A.A., and Hong, X.Y. (2021). Spider mites singly infected with either Wolbachia or Spiroplasma have reduced thermal tolerance. Front Microbiol 12, 706321.
Zogli, P., Pingault, L., Grover, S., and Louis, J. (2020). Ento(o)mics: the intersection of ‘omic’ approaches to decipher plant defense against sapsucking insect pests. Curr Opin Plant Biol 56, 153–161.
Zytynska, S.E., Eicher, M., Rothballer, M., and Weisser, W.W. (2020). Microbial-mediated plant growth promotion and pest suppression varies under climate change. Front Plant Sci 11, 573578.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (42090060, 42277297), Natural Science Foundation of Jiangsu Province (BK20211577), and Innovative Research Team Development Plan of the Ministry of Education of China (IRT_17R56). J. Y. was supported by the Qing Lan Project of Jiangsu Province. We thank Dr. Xiaoli Bing, Xiaofeng Xia, and Dr. Stefan Geisen for their comments.
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Yuan, J., Wen, T., Yang, S. et al. Growth substrates alter aboveground plant microbial and metabolic properties thereby influencing insect herbivore performance. Sci. China Life Sci. 66, 1728–1741 (2023). https://doi.org/10.1007/s11427-022-2279-5
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DOI: https://doi.org/10.1007/s11427-022-2279-5