Plants communicate with microorganisms by exchanging chemical signals throughout the phytosphere. Such interactions are important not only for plant productivity and fitness, but also for terrestrial ecosystem functioning. It is known that beneficial microorganisms emit diffusible substances including volatile organic compounds (VOCs) that promote growth. Consistently, soil application of cell-free culture filtrates (CF) of beneficial soil and plant-associated microorganisms enhances plant growth and yield. However, how this treatment acts in plants and whether it alters the resident soil microbiota, are largely unknown. In this work we characterized the responses of pepper (Capsicum annuum L.) plants cultured under both greenhouse and open field conditions and of soil microbiota to soil application of CFs of beneficial and phytopathogenic fungi. To evaluate the contribution of VOCs occurring in the CFs to these responses, we characterized the responses of plants and of soil microbiota to application of distillates (DE) of the fungal CFs. CFs and their respective DEs contained the same potentially biogenic VOCs, and application of these extracts enhanced root growth and fruit yield, and altered the nutritional characteristics of fruits. High-throughput amplicon sequencing of bacterial 16S and fungal ITS rRNA genes of the soil microbiota revealed that the CF and DE treatments altered the microbial community compositions, and led to strong enrichment of the populations of the same beneficial bacterial and fungal taxa. Our findings show that CFs of both beneficial and phytopathogenic fungi can be used as biostimulants, and provide evidence that VOCs occurring in the fungal CFs act as mediators of the plants' responses to soil application of fungal CFs through stimulation of the beneficial soil microbiota.

ADM Biopolis Valencia Spain

Centre of the Region Haná for Biotechnological and Agricultural Research Czech Advanced Technology and Research Institute Olomouc Czechia

Department of Chemical Biology Faculty of Science Palacký University Olomouc Olomouc Czechia

Instituto de Agrobiotecnología Nafarroa Spain

Instituto de Hortofruticultura Subtropical y Mediterránea La Mayora Campus de Teatinos Málaga Spain

Laboratory of Growth Regulators Institute of Experimental Botany of the Czech Academy of Sciences Faculty of Science Palacký University Olomouc Olomouc Czechia

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Abarenkov K., Nilsson R. H., Larsson K. H., Alexander I. J., Eberhardt U., Erland S., et al. (2010). The UNITE database for molecular identification of fungi - recent updates and future perspectives. PubMed DOI

Ahmad M., Pataczek L., Hilger T. H., Zahir Z. A., Hussain A., Rasche F., et al. (2018). Perspectives of microbial inoculation for sustainable development and environmental management. PubMed DOI PMC

Aldesuquy H. S., Mansour F. A., Abo-Hamed S. A. (1998). Effect of the culture filtrates of DOI

Allen M. M., Allen D. J. (2020). Biostimulant potential of acetic acid under drought stress is confounded by pH-dependent root growth inhibition. PubMed DOI PMC

Ameztoy K., Baslam M., Sánchez-López ÁM., Muñoz F. J., Bahaji A., Almagro G., et al. (2019). Plant responses to fungal volatiles involve global post-translational thiol redox proteome changes that affect photosynthesis. PubMed DOI

Ameztoy K., Sánchez-López ÁM., Muñoz F. J., Bahaji A., Almagro G., Baroja-Fernández E., et al. (2021). Proteostatic regulation of MEP and shikimate pathways by redox-activated photosynthesis signaling in plants exposed to small fungal volatiles. PubMed DOI PMC

Arkhipova T. N., Veselov S. U., Melentiev A. I., Martynenko E. V., Kudoyarova G. R. (2005). Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. DOI

Badri D. V., Chaparro J. M., Zhang R., Shen Q., Vivanco J. M. (2013a). Application of natural blends of phytochemicals derived from the root exudates of PubMed DOI PMC

Badri D. V., Zolla G., Bakker M. G., Manter D. K., Vivanco J. M. (2013b). Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. PubMed DOI

Bagde U. S., Prasad R., Varma A. (2011). Influence of culture filtrate of DOI

Bahaji A., Baroja-Fernández E., Ricarte-Bermejo A., Sánchez-López ÁM., Muñoz F. J., Romero J. M., et al. (2015a). Characterization of multiple SPS knockout mutants reveals redundant functions of the four PubMed DOI

Bahaji A., Sánchez-López ÁM., De Diego N., Muñoz F. J., Baroja-Fernández E., Li J., et al. (2015b). Plastidic phosphoglucose isomerase is an important determinant of starch accumulation in mesophyll cells, growth, photosynthetic capacity, and biosynthesis of plastidic cytokinins in PubMed DOI PMC

Belimov A. A., Dodd I. C., Safronova V. I., Hontzeas N., Davies W. J. (2007). PubMed DOI

Berestetskiy A. O. (2008). A review of fungal phytotoxins: from basic studies to practical use. PubMed DOI

Bitas V., McCartney N., Li N., Demers J., Kim J. E., Kim H. S., et al. (2015). PubMed DOI PMC

Calvo P., Nelson L., Kloepper J. W. (2014). Agricultural uses of plant biostimulants. DOI

Camarena-Pozos D. A., Flores-Núñ;ez V. M., López M. G., López-Bucio J., Partida-Martínez L. P. (2019). Smells from the desert: microbial volatiles that affect plant growth and development of native and non-native plant species. PubMed DOI

Chanclud E., Morel J. B. (2016). Plant hormones: a fungal point of view. PubMed DOI PMC

Chaurasia B., Pandey A., Palni L. M. S., Trivedi P., Kumar B., Colvin N. (2005). Diffusible and volatile compounds produced by an antagonistic PubMed DOI

Chen Y., Bonkowski M., Shen Y., Griffiths B. S., Jiang Y., Wang X., et al. (2020). Root ethylene mediates rhizosphere microbial community reconstruction when chemically detecting cyanide produced by neighbouring plants. PubMed DOI PMC

Colla G., Hoagland L., Ruzzi M., Cardarelli M., Bonini P., Canaguier R., et al. (2017). Biostimulant action of protein hydrolysates: unraveling their effects on plant physiology and microbiome. PubMed DOI PMC

Contreras-Cornejo H. A., Macías-Rodríguez L., Cortés-Penagos C., López-Bucio J. (2009). PubMed DOI PMC

Cordovez V., Mommer L., Moisan K., Lucas-Barbosa D., Pierik R., Mumm R., et al. (2017). Plant phenotypic and transcriptional changes induced by volatiles from the fungal root pathogen PubMed DOI PMC

De Mendiburu F., Simon R. (2015). Agricolae – Ten years of an open source statistical tool for experiments in breeding, agriculture and biology. DOI

De-la-Peña C., Loyola-Vargas V. M. (2014). Biotic interactions in the rhizosphere: a diverse cooperative enterprise for plant productivity. PubMed DOI PMC

Delgado-Baquerizo M., Maestre F. T., Reich P. B., Jeffries T. C., Gaitan J. J., Encinar D., et al. (2016). Microbial diversity drives multifunctionality in terrestrial ecosystems. PubMed DOI PMC

Deng S., Wipf H. M.-L., Pierroz G., Raab T. K., Khanna R., Coleman-Derr D. (2019). A plant growth-promoting microbial soil amendment dynamically alters the strawberry root bacterial microbiome. PubMed DOI PMC

Ditengou F. A., Müller A., Rosenkranz M., Felten J., Lasok H., Van Doorn M. M., et al. (2015). Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. PubMed DOI PMC

du Jardin P. (2015). Plant biostimulants: definition, concept, main categories and regulation. DOI

Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. PubMed DOI PMC

Ezquer I., Li J., Ovecka M., Baroja-Fernández E., Muñoz F. J., Montero M., et al. (2010). Microbial volatile emissions promote accumulation of exceptionally high levels of starch in leaves in mono- and dicotyledonous plants. PubMed DOI

Fincheira P., Parra L., Mutis A., Parada M., Quiroz A. (2017). Volatiles emitted by Bacillus sp. BCT9 act as growth modulating agents on PubMed DOI

Fiorentino N., Ventorino V., Woo S. L., Pepe O., De Rosa A., Gioia L., et al. (2018). Trichoderma-based biostimulants modulate rhizosphere microbial populations and improve N uptake efficiency, yield, and nutritional quality of leafy vegetables. PubMed DOI PMC

Flexas J., Díaz-Espejo A., Conesa M. A., Coopman R. E., Douthe C., Gago J., et al. (2016). Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants. PubMed DOI

Floková K., Tarkowská D., Miersch O., Strnad M., Wasternack C., Novák O. (2014). UHPLC-MS/MS based target profiling of stress-induced phytohormones. PubMed DOI

Forde B. G. (2014). Glutamate signalling in roots. PubMed DOI

Fu L., Niu B., Zhu Z., Wu S., Li W. (2012). CD-HIT: accelerated for clustering the next-generation sequencing data. PubMed DOI PMC

Fu S.-F., Sun P.-F., Lu H.-Y., Wei J.-Y., Xiao H.-S., Fang W.-T., et al. (2016). Plant growth-promoting traits of yeasts isolated from the phyllosphere and rhizosphere of PubMed DOI

García-Gómez P., Almagro G., Sánchez-López ÁM., Bahaji A., Ameztoy K., Ricarte-Bermejo A., et al. (2019). Volatile compounds other than CO2 emitted by different microorganisms promote distinct posttranscriptionally regulated responses in plants. PubMed DOI

García-Gómez P., Bahaji A., Gámez-Arcas S., Muñoz F. J., Sánchez-lópez ÁM., Almagro G., et al. (2020). Volatiles from the fungal phytopathogen PubMed

Garnica-Vergara A., Barrera-Ortiz S., Muñoz-Parra E., Raya-González J., Méndez-Bravo A., Macías-Rodríguez L., et al. (2016). The volatile 6-pentyl-2H-pyran-2-one from PubMed DOI

George T. K., SubaidaBeevi S., Asok A. K., Shaikmoideen J. M. (2019). Plant growthpromoting endophytic yeast DOI

Gu Y., Wang J., Xia Z., Wei H. L. (2020). Characterization of a versatile plant growth-promoting rhizobacterium PubMed DOI PMC

Guo Y., Jud W., Ghirardo A., Antritter F., Benz J. P., Schnitzler J.-P., et al. (2020). Sniffing fungi – phenotyping of volatile chemical diversity in PubMed DOI

Gutiérrez-Luna F. M., López-Bucio J., Altamirano-Hernández J., Valencia-Cantero E., Reyes de La Cruz H., Macías-Rodríguez L. (2010). Plant growth-promoting rhizobacteria modulate root-system architecture in DOI

Hernández-Calderón E., Aviles-Garcia M. E., Castulo-Rubio D. Y., Macías-Rodríguez L., Ramírez V. M., Santoyo G., et al. (2018). Volatile compounds from beneficial or pathogenic bacteria differentially regulate root exudation, transcription of iron transporters, and defense signaling pathways in Sorghum bicolor. PubMed DOI

Hilber-Bodmer M., Schmid M., Ahrens C. H., Freimoser F. M. (2017). Competition assays and physiological experiments of soil and phyllosphere yeasts identify Candida subhashii as a novel antagonist of filamentous fungi. PubMed DOI PMC

Huang A. C., Jiang T., Liu Y. X., Bai Y. C., Reed J., Qu B., et al. (2019). A specialized metabolic network selectively modulates PubMed DOI

Jiang C.-H., Xie Y.-S., Zhu K., Wang N., Li Z.-J., Yu G.-J., et al. (2019). Volatile organic compounds emitted by DOI

Kai M., Effmert U., Berg G., Piechulla B. (2007). Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen PubMed DOI

Kalita M., Małek W. (2017). Molecular phylogeny of PubMed DOI

Kanchiswamy C. N., Malnoy M., Maffei M. E. (2015). Chemical diversity of microbial volatiles and their potential for plant growth and productivity. PubMed DOI PMC

Kaur T., Rani R., Manhas R. K. (2019). Biocontrol and plant growth promoting potential of phylogenetically new Streptomyces sp. MR14 of rhizospheric origin. PubMed DOI PMC

Khan S., Yu H., Li Q., Gao Y., Sallam B. N., Wang H., et al. (2019). Exogenous Application of amino acids improves the growth and yield of lettuce by enhancing photosynthetic assimilation and nutrient availability. DOI

Kim J.-M., To T. K., Matsui A., Tanoi K., Kobayashi N. I., Matsuda F., et al. (2017). Acetate-mediated novel survival strategy against drought in plants. PubMed DOI

Klindworth A., Pruesse E., Schweer T., Peplies J., Quast C., Horn M., et al. (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. PubMed DOI PMC

Koprna R., De Diego N., Dundálková L., Spíchal L. (2016). Use of cytokinins as agrochemicals. PubMed DOI

Kottb M., Gigolashvili T., Großkinsky D. K., Piechulla B. (2015). PubMed DOI PMC

Kröber M., Wibberg D., Grosch R., Eikmeyer F., Verwaaijen B., Chowdhury S. P., et al. (2014). Effect of the strain PubMed DOI PMC

Lebeis S. L., Paredes S. H., Lundberg D. S., Breakfield N., Gehring J., McDonald M., et al. (2015). Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. PubMed DOI

Lee S. A., Kanth B. K., Kim H. S., Kim T.-W., Sang M. K., Song J., et al. (2019). Complete genome sequence of the plant growth-promoting endophytic bacterium DOI

Li N., Wang W., Bitas V., Subbarao K., Liu X., Kang S. (2018). Volatile compounds emitted by diverse PubMed DOI

Loiret F. G., Grimm B., Hajirezaei M. R., Kleiner D., Ortega E. (2009). Inoculation of sugarcane with PubMed DOI

López-Bucio J., Pelagio-Flores R., Herrera-Estrella A. (2015). DOI

Lou J., Fu L., Peng Y., Zhou L. (2013). Metabolites from PubMed DOI PMC

Love M. I., Huber W., Anders S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. PubMed DOI PMC

Luziatelli F., Ficca A. G., Colla G., Baldassarre Švecová E., Ruzzi M. (2019). Foliar application of vegetal-derived bioactive compounds stimulates the growth of beneficial bacteria and enhances microbiome biodiversity in lettuce. PubMed DOI PMC

Mahnert A., Haratani M., Schmuck M., Berg G. (2018). Enriching beneficial microbial diversity of indoor plants and their surrounding built environment with biostimulants. PubMed DOI PMC

Mannaa M., Park I., Seo Y. S. (2019). Genomic features and insights into the taxonomy, virulence, and benevolence of plant-associated PubMed DOI PMC

Martin M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. DOI

McLean M. (1996). The phytotoxicity of PubMed DOI

Moisan K., Cordovez V., van de Zande E. M., Raaijmakers J. M., Dicke M., Lucas-Barbosa D. (2019). Volatiles of pathogenic and non-pathogenic soil-borne fungi affect plant development and resistance to insects. PubMed DOI PMC

Novák O., Hauserová E., Amakorová P., Doležal K., Strnad M. (2008). Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. PubMed DOI

Ogórek R. (2016). Enzymatic activity of potential fungal plant pathogens and the effect of their culture filtrates on seed germination and seedling growth of garden cress ( DOI

Op De Beeck M., Lievens B., Busschaert P., Declerck S., Vangronsveld J., Colpaert J. V. (2014). Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. PubMed DOI PMC

Ortíz-Castro R., Contreras-Cornejo H. A., Macías-Rodríguez L., López-Bucio J. (2009). The role of microbial signals in plant growth and development. PubMed DOI PMC

Palou L., Smilanick J., Crisosto C. (2009). Evaluation of food additives as alternative or complementary chemicals to conventional fungicides for the control of major postharvest diseases of stone fruit. PubMed DOI

Parveen S., Wani A. H., Bhat M. Y. (2019). Effect of culture filtrates of pathogenic and antagonistic fungi on seed germination of some economically important vegetables. DOI

Pěnčík A., Rolčík J., Novák O., Magnus V., Barták P., Buchtík R., et al. (2009). Isolation of novel indole-3-acetic acid conjugates by immunoaffinity extraction. PubMed DOI

Perin L., Martínez-Aguilar L., Paredes-Valdez G., Baldani J. I., Estrada-de los Santos P., Reis V. M., et al. (2006). PubMed DOI

Philippot L., Raaijmakers J. M., Lemanceau P., Van Der Putten W. H. (2013). Going back to the roots: the microbial ecology of the rhizosphere. PubMed DOI

Podlešáková K., Ugena L., Spíchal L., Doležal K., De Diego N. (2019). Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. PubMed DOI

Prudent M., Dequiedt S., Sorin C., Girodet S., Nowak V., Duc G., et al. (2020). The diversity of soil microbial communities matters when legumes face drought. PubMed DOI

Rabhi N. E. H., Silini A., Cherif-Silini H., Yahiaoui B., Lekired A., Robineau M., et al. (2018). PubMed DOI

Radhakrishnan R., Kang S.-M., Baek I.-Y., Lee I.-J. (2014). Characterization of plant growth-promoting traits of DOI

Rahman A., Sultana R., Ferdousi Begum M., Firoz Alam M. (2012). Effect of culture filtrates of

Rao V. K., Girisham S., Reddy S. M. (2014). Influence of different species of

Renaut S., Masse J., Norrie J. P., Blal B., Hijri M. (2019). A commercial seaweed extract structured microbial communities associated with tomato and pepper roots and significantly increased crop yield. PubMed DOI PMC

Ryu C.-M., Farag M. A., Hu C.-H., Reddy M. S., Wei H.-X., Paré P. W., et al. (2003). Bacterial volatiles promote growth in PubMed DOI PMC

Sánchez-López ÁM., Baslam M., De Diego N., Muñoz F. J., Bahaji A., Almagro G., et al. (2016). Volatile compounds emitted by diverse phytopathogenic microorganisms promote plant growth and flowering through cytokinin action. PubMed DOI

Sasse J., Martinoia E., Northen T. (2018). Feed your friends: do plant exudates shape the root microbiome? PubMed DOI

Schmidt R., Etalo D. W., de Jager V., Gerards S., Zweers H., de Boer W., et al. (2016). Microbial small talk: volatiles in fungal–bacterial interactions. PubMed DOI PMC

Schulz-Bohm K., Martín-Sánchez L., Garbeva P. (2017). Microbial volatiles: small molecules with an important role in intra- and inter-kingdom interactions. PubMed DOI PMC

Spaepen S., Vanderleyden J., Remans R. (2007). Indole-3-acetic acid in microbial and microorganism-plant signaling. PubMed DOI

Sudadi S. (2012). Exogenous application of tryptophan and indole acetic acid (IAA) to induce root nodule formation and increase yield of soybean.

Sung G. H., Shrestha B., Park K. B., Han S. K., Sung J. M. (2011). Enhancing effect of PubMed DOI PMC

Talibi I., Askarne L., Boubaker H., Boudyach E. H., Msanda F., Saadi B., et al. (2012). Antifungal activity of some Moroccan plants against DOI

Tarkowski P., Vereecke D. (2014). Threats and opportunities of plant pathogenic bacteria. PubMed DOI

Varma A., Savita V., Sudha, Sahay N., Butehorn B., Franken P. (1999). Piriformospora indica, a cultivable plant-growth-promoting root endophyte. PubMed DOI PMC

von Caemmerer S., Farquhar G. D. (1981). Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. PubMed DOI

Wang D., Deng X., Wang B., Zhang N., Zhu C., Jiao Z., et al. (2019). Effects of foliar application of amino acid liquid fertilizers, with or without PubMed DOI PMC

Waqas M., Kim Y.-H., Khan A. L., Shahzad R., Asaf S., Hamayun M., et al. (2017). Additive effects due to biochar and endophyte application enable soybean to enhance nutrient uptake and modulate nutritional parameters. PubMed DOI PMC

Werner S., Polle A., Brinkmann N. (2016). Belowground communication: impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms. PubMed DOI

Wu Y., He Y., Yin H., Chen W., Wang Z., Xu L., et al. (2012). Isolation of phosphate-solubilizing fungus and its application in solubilization of rock phosphates. PubMed DOI

Yandigeri M. S., Meena K. K., Singh D., Malviya N., Singh D. P., Solanki M. K., et al. (2012). Drought-tolerant endophytic actinobacteria promote growth of wheat ( DOI

Yu K., Pieterse C. M. J., Bakker P. A. H. M., Berendsen R. L. (2019). Beneficial microbes going underground of root immunity. PubMed DOI PMC

Zahir Z. A., Shah M. K., Naveed M., Akhter M. J. (2010). Substrate-dependent auxin production by PubMed DOI

Zhang H., Sun Y., Xie X., Kim M. S., Dowd S. E., Paré P. W. (2009). A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. PubMed DOI

Zhang H., Xie X., Kim M. S., Kornyeyev D. A., Holaday S., Paré P. W. (2008). Soil bacteria augment PubMed DOI

Glucose-6-P/phosphate translocator2 mediates the phosphoglucose-isomerase1-independent response to microbial volatiles