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Applied Soil Ecology 168 (2021) 104118
Available online 19 June 20210929-1393/© 2021 The Author. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Review
Beneficial effects of microbial volatile organic compounds (MVOCs) in plants
Jorge Poveda *
Institute for Multidisciplinary Research in Applied Biology (IMAB), Universidad Pública de Navarra, Campus Arrosadía, 31006 Pamplona, Spain
A R T I C L E I N F O
Keywords: Volatile organic compounds Microbial volatile organic compounds Biocontrol Antifungal activity Plant growth
A B S T R A C T
Volatile organic compounds (VOCs) are chemical compounds whose saturation vapor pressures are greater than 102 kPa at 25 ◦C. Both plants and microorganisms produce VOCs that allow them to communicate intra- and inter-specifically. By emitting VOCs, plants defend themselves against herbivores and pathogens, warn their neighbors of the attack, compete with other plants, and/or feed microbial populations. Microorganisms emit VOCs to communicate or attack each other. Microbial VOCs (MVOCs) can be of great benefit to plants and their use in agriculture thanks to their ability to inhibit the growth and development of plant pathogens, induce the activation of plant defenses, or promote plant growth and development. In recent years, advances in under-standing the importance of microbial volatilome have placed MVOCs as important biotechnological resources in plant production systems.
1. Introduction
Volatile organic compounds (VOCs) are man-made and/or naturally occurring highly reactive hydrocarbons (WHO, 1992). VOCs are defined as any organic compound whose boiling point is in the range from (50–260 ◦C), corresponding to having saturation vapor pressures greater than 102 kPa at 25 ◦C (ISO16000-6, 1989). Many types of VOCs are toxic or even deadly to humans and can be detrimental to the environment (Berenjian et al., 2012). A majority of VOCs are created from anthro-pogenic activities consisting of manufacturing industries, petrochemical industries and vehicular emissions (EPA, 2012). Natural origins of VOCs include wetlands, forests, oceans and volcanoes (Atkinson and Arey, 2003). Human exposure to VOCs of anthropogenic origin may result in a spectrum of illnesses ranging from mild, such as irritation, to very severe effects, including cancer (Rumchev et al., 2007). In this sense, both microorganisms and plants have the ability to biodegrade these toxic chemical compounds and remove them from the air (Qi et al., 2002; Kim et al., 2018); and can be used as bioindicators of their toxicity, such as the case of the model organisms Escherichia coli (Yung et al., 2016) and Arabidopsis thaliana (Lee et al., 2014).
The terrestrial biosphere acts as a source of biogenic volatile organic compounds (BVOCs) to the atmosphere. BVOCs possess special struc-tures and contain much useful and crucial bio-information, deeply regulating inter- and intra-specific interactions. Most of these BVOCs are
synthesized by one of three major biochemical routes: the isoprenoid, the lipoxygenase or the shikimic acid pathways (Laothawornkitkul et al., 2009; Zhang and Li, 2010). This group of chemical compounds serves, for example, insects to communicate with their symbiont microorgan-isms, as happens with the Eurasian spruce bark beetle (Ips typographus) with its fungal symbionts (Kandasamy et al., 2019). But they can also be used for the diagnosis of plants attacked by pests, such as trees of the genus Acer attacked by the Asian longhorn beetle (Anoplophora glabri-pennis) (Makarow et al., 2020). Or in the geographical determination of the organisms used in food origin, such as the white truffle (Tuber magnatum) (Gioacchini et al., 2008). Even in the diagnosis of human diseases of the type infection, inflammation, cancer or metabolic by means of the analysis of breath (Dummer et al., 2011), or to differentiate human corpses thanks to their profile of BVOCs (Kusano et al., 2013).
2. Microbial VOCs
Microorganisms are capable of synthesizing a number of various volatile substances called as microbial VOCs (MVOCs) with low boiling points and small molecular masses (on average 300 Da) (Veselova et al., 2019). MVOCs of bacterial and fungal origin are responsible for the aroma of such foodstuffs as cheese, wine, yogurt, etc., as well as for unpleasant smell of degrading foodstuffs (Veselova et al., 2019). They are propagated in air and liquid media, as well as in soil, and act at short
* Institute of Environment, Natural Resources and Biodiversity, University of Leon, Leon, Spain. E-mail address: [email protected].
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Applied Soil Ecology
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https://doi.org/10.1016/j.apsoil.2021.104118 Received 9 November 2020; Received in revised form 7 June 2021; Accepted 11 June 2021
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and long distances (Veselova et al., 2019). MVOCs were found to modulate plant and microbial growth, cause systemic resistance in plants, affect insects, nematodes, and other organisms, and act as at-tractants or repellents (Veselova et al., 2019). Their profiles are studied using gas chromatography–mass spectrometry (GS-MS), a method providing for efficient separation of the components of complex mix-tures, their identification, and assessment of the relative content of their components (Veselova et al., 2019). A totality of volatile compounds synthesized by an organism or an ecosystem is termed volatilome (Veselova et al., 2019).
A published database of identified MVOCs (MVOCs 2.0 database, http://bioinformatics.charite.de/mvoc/) includes over 2000 com-pounds produced by almost 1000 microbial species (Lemfack et al., 2014, 2018). Bacterial volatiles are typically dominated by alkenes, al-cohols, ketones, terpenes, benzenoids, pyrazines, acids and esters, whereas fungal volatiles are dominated by alcohols, benzenoids, alde-hydes, alkenes, acids, esters and ketones. Most microbial volatiles are considered as products of primary and secondary metabolism, formed mainly by oxidation of glucose from various intermediates (Morath et al., 2012; Schmidt et al., 2015).
The functions that MVOCs can have for their emitting organisms and for the ecosystem are very different and characteristic. Furthermore, MVOCs exhibit dynamic changes across microbial growth phases, resulting in variance of composition and emission rate of species-specific and generic MVOCs (Misztal et al., 2018). The main function of the MVOCs is based on the interplay between microorganisms, generally between bacteria and fungi in a cross way (Schmidt et al., 2016). These interactions are often based on antagonism by MVOCs with antifungal activity (caryophyllene, hydrogen cyanide, 1-undecen, dimethyl disul-fide, dimethyl trisulphide, S-methyl thioacetate, benzonitrile, etc.) or antibacterial (γ-butyrolactones, albaflavenone, dihydro-β-agarofuran, 1- undecene, methanthiol, dimethyl disulfide, etc.), although there may also be effective beneficial communication by such compounds, having an important role in interactions between physically separated micro-organisms (Schmidt et al., 2015). On the other hand, in relation with insects, MVOCs may signal aspects of habitat suitability or potential exposure to entomopathogens, can incite insect aggregations, can resemble sexual pheromones that elicit mating and oviposition behav-iors from responding insects (Davis et al., 2013).
From the human point of view, there are different MVOCs that have been described as potential allergenic and asthmatic agents, such as 1- octen-3-ol exposure (Araki et al., 2012). However, many MVOCs are used in different industries, such as pharmaceuticals with antimicrobials as 13-epi-manoyl oxide, manool, 15,16-dinorlabd-8(20)-en-13-one, labda-8(17),13Z-dien-15-ol or 3α-hydroxy-13-epi-manoyl oxide (Hami-che et al., 2019), or perfumery and cosmetic industries with compounds as β-agarofuran, α-agarofuran, δ-eudesmol, oxo-agarospirol, or β-dihy-dro agarofuran (Monggoot et al., 2017). Furthermore, thanks to the identification and quantification of MVOCs we can diagnose different harmful situations, such as food safety (Wang et al., 2016), fungi growing on walls and ceilings (Betancourt et al., 2013) or decomposing wood materials (Konuma et al., 2015).
In soils, MVOCs can be used as nondestructive indicators of subsur-face microbial activity and community composition as a function of varying environmental factors, similar to how it is done by CO2 evolu-tion, as a measure of microbial activity, and by community-level phys-iological profiles (CLPPs) and fatty acid methyl ester (FAME) community structure techniques (McNeal and Herbert, 2009). There-fore, volatilomics would have the advantage of avoiding extraction steps that are often a limit in genomic or proteomic approaches (Insam and Seewald, 2010). Furthermore, the portion MVOCs emitted by the microbiota present in a soil have the capacity to actively modify the quantity and diversity of microorganisms present (Yuan et al., 2017). In this sense, it has been reported how reduced levels of microbial diversity in soils increased MVOCs emissions from soils, while the number of different MVOCs emitted decreased (Letizia et al., 2020).
3. MVOCs and plants
Even today, the ecological functions of microbial volatiles are not understood in detail, still needing a lot of research. Its functions are always based on highly competitive but symbiotic conditions that mainly lead to antibiosis processes against plant pathogens, activation of plant defense responses and increased growth. Both in plants and in other microorganisms, MVOCs are capable of modulating the metab-olome, genome, and proteome, having great potential to serve as effective biostimulants and bioprotectants, even under open-field con-ditions (Kanchiswamy et al., 2015; Chung et al., 2016).
MVOCs are capable to modulate plant physiological and hormonal pathways to increase biomass and yield production, via increased root volume, leaf number, leaf size and flower number, allowing for higher fruit and seed production (Sharifi and Ryu, 2018; Tyagi et al., 2018). Furthermore, they are capable to improve plant health through anti-fungal, antibacterial, oomyceticidal, nematicidal activity, and as elici-tors of plant immunity through the routes of salicylic acid (SA) and jasmonic acid (JA) (Bitas et al., 2013; Schalchli et al., 2016). The different beneficial (and harmful) effects reported for MVOCs in plants are found collected in an orderly manner by groups of microorganisms in Table 1 and are represented schematically in a infographic in Fig. 1.
3.1. Plant growth promoting MVOCs
The plant model in plant sciences Arabidopsis thaliana has also been proposed as a study model of the effect of MVOCs on it (Li et al., 2019), being the plant system where the promotion of plant growth by them has been most studied. Within the bacterial genus Bacillus, the main re-ported MVOCs with the ability to promote the growth of A. thaliana, for example, by increasing shoot biomass, are 2,3-butanediol and acetoin (3-hydroxy-2-butanone). 2,3-butanediol synthesized by B. amyloliquefaciens (Ryu et al., 2003; Asari et al., 2016), B. mojavensis (Rath et al., 2018) or B. subtilis (Ryu et al., 2003), and acetoin produced by B. amyloliquefaciens (Asari et al., 2016) or B. mojavensis, which can cause phytotoxic effects in large quantities (Rath et al., 2018), but it is also capable of promoting growth in lettuce by an increase in the number of lateral roots, dry weight, root growth and shoot length (Fincheira et al., 2016). Other MVOCs from Bacillus sp. such as tetrahydrofuran-3-ol and 2-heptanone 2-ethyl-1-hexanol promote the growth of A. thaliana through the action of auxins and strigolactones, increasing endogenous levels, also in tomato (Jiang et al., 2019). Or as 6,10,14-trimethyl 2-pentadecanone, benzaldehyde and 9-octadecanone released by different Bacillus species and that stimulate biomass pro-duction, which was related to differential modulation of root-system architecture in A. thaliana (Gutierrez-Luna et al., 2010). Indole MVOC produced by Proteus vulgaris stimulates the growth of A. thaliana through an interplay between the auxin, cytokinin, and brassinosteroid pathways (Bhattacharyya et al., 2015). Therefore, there are different MVOCs produced by Bacillus species which have been shown to have the ability to promote plant growth. The agricultural application of these bacteria as plant growth promoters (PGPBs) must take into account the role played by these MVOCs, in order to enhance the benefits.
With respect to MVOCs of fungal origin, it has been determined as those synthesized by Alternaria alternata stimulate starch biosynthesis during illumination (Li et al., 2011) and enhance photosynthesis and accumulation of high levels of cytokinins (CKs) and sugars in A. thaliana (Sanchez-Lopez et al., 2016), but without having been identified. In Trichoderma genus there are several species whose MVOCs have been described with the ability to promote plant growth in A. thaliana. Through an increase in root branching by exposure to δ-cadinene pro-duced by T. virens (Contreras-Cornejo et al., 2014), an increase in total biomass, chlorophyll content and acceleration of flowering by isobutyl alcohol, isopentyl alcohol and 3-methylbutanal from T. viride (Hung et al., 2013), in addition to many other chemical compounds of different species that at the same time increase the development of lateral roots,
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Table 1 Plant effects of MVOCs.
Microorganism VOC Effects Reference
Bacteria Arthrobacter agilis Dimethylhexadecylamine Medicago sativa growth promotion Velazquez-Becerra et al., 2011
Antifungal activity against Botrytis cinerea Oomyceticidal activity against Phytophthora cinnamomi
Velazquez-Becerra et al., 2013
Azospirillum brasilense Unidentified Mentha piperita change in essential oils composition Santoro et al., 2011 Bacillus amyloliquefaciens 2,5-Dimethyl pyrazine
2-Dodecanone 2-Tetradecanone
Antifungal activity against Fusarium sp. and Colletotrichum gloeosporioides Oomyceticidal activity against Phytophthora cinnamomi
Guevara-Avendano et al., 2019
Unidentified A. thaliana growth promotion Raza et al., 2016b 2,3-Butanediol A. thaliana growth promotion Ryu et al., 2003 2,3-Butanediol Induction of systemic resistance in A. thaliana against Erwinia
carotovora subsp. carotovora Ryu et al., 2004
3-Pentanol Induction of systemic resistance in pepper against Xanthomonas axonopodis pv. vesicatoria
Choi et al., 2014
Benzothiazole phenol 2,3,6-Trimethylphenol
Antifungal activity against Fusarium oxysporum f. sp. cubense Yuan et al., 2012
Acetoin Increase tolerance to salinity in Mentha piperita del Rosario-Cappellari and Banchio, 2019
2,3-Butanedione Acetoin
A. thaliana growth promotion Antifungal activity against Botrytis cinerea, Alternaria brassicicola, A. brassicae and Sclerotinia sclerotiorum
Asari et al., 2016
1,3 Pentadiene Acetoin Thiophene
Antifungal activity against Monilinia laxa, M. fructicola and B. cinera
Gotor-Vila et al., 2017
Butylated hydroxy toluene p-Xylene 2-Nonanone 2-Undecanone 2-Dodecanone 2-Tridecanone Undecanal Heptadecane Oleic acid
Antibacterial activity against Ralstonia solanacearum Raza et al., 2016c
2-Undecanone 2-Tridecanone Heptadecane Undecanal
Antibacterial activity against R. solanacearum Raza et al., 2016d
1-(2-Aminophenyl)ethanone Benzothiazole α-Farnesene
Antifungal activity against Peronophythora litchi Induction of fruit defenses
Zheng et al. 2019
Bacillus atrophaeus Chloroacetic acid Octadecane Hexadecanoic acid
Antifungal activity against Colletotrichum gloeosporioides Rajaofera et al., 2019
Bacillus megaterium Heneicosane Heptacosane Octacosane
Antifungal activity against Botrytis cinerea, F. solani, Rhizoctonia solani, Sclerotinia sclerotiorum and Verticillium dahliae Oomyceticidal activity against Pythium ultimum
Giorgio et al., 2015
Bacillus mojavensis 2,3-Butanediol Acetoin
A. thaliana growth promotion Rath et al., 2018
Bacillus mycoides Dimethyl disulfide Antifungal activity against C. gloeosporioides Guevara-Avendano et al., 2019
Bacillus pumilus 1-(2-Aminophenyl)ethanone Benzothiazole α-Farnesene
Antifungal activity against Peronophythora litchi Induction of fruit defenses
Zheng et al. 2019
Bacillus subtilis Benzaldehyde Nonanal Benzothiazole Acetophenone
Antibacterial activity against Clavibacter michiganensis ssp. sepedonicus
Rajer et al., 2017
2,3-Butanediol A. thaliana growth promotion Ryu et al., 2003 2,3-butanediol Induction of systemic resistance in A. thaliana against Erwinia
carotovora subsp. carotovora Ryu et al., 2004
Acetoin Induction of systemic resistance in A. thaliana against Pseudomonas syringae pv. tomato
Rudrappa et al., 2010
Unidentified Soybean growth promotion Bavaresco et al., 2020 Albuterol 1,3-Propanediole
Tomato growth promotion Tahir et al., 2017
2,4-Di-tert-butylphenol 1-Octanol Benzothiazole Benzoic acid Benzaldehyde 3-Methylbutanal
Antifungal activity against B. cinerea, C. gloeosporioides, Penicillium expansum, Monilinia fructicola and A. alternata
Gao et al., 2018
2,3-Butanediol Increase tolerance to salinity in A. thaliana Zhang et al., 2008 Unidentified Mentha piperita growth promotion Santoro et al., 2011
Bacillus velezensis Gao et al., 2017
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Table 1 (continued )
Microorganism VOC Effects Reference
Pyrazine (2,5-dimethyl) Benzothiazole 4-Chloro-3-methyl Phenol-2,4-bis (1,1-dimethylethyl)
Antifungal activity against Alternaria solani, B. cinerea, Valsa mali, M. fructicola, F. oxysporum f. sp. capsicum and Colletotrichum lindemuthianum
Bacillus sp. Acetoin Lettuce growth promotion Fincheira et al., 2016 Tetrahydrofuran-3-ol, 2-heptanone 2-Ethyl-1-hexanol
A. thaliana and tomato growth promotion Jiang et al., 2019
Bacillus spp. 6,10,14-Trimethyl 2-pentadecanone Benzaldehyde 9-Octadecanone
A. thaliana growth promotion Gutierrez-Luna et al., 2010
Corrallococcus sp. Isooctanol Antifungal activity against F. oxysporum f. sp. cucumerinum and Penicillum digitatum
Ye et al., 2020
Enterobacter aerogenes 2,3-Butanediol Induction of systemic resistance in maize Parasitoid attraction
D’Alessandro et al., 2014
Exiguobacterium acetylicum 1-(2-Aminophenyl)ethanone Benzothiazole α-Farnesene
Antifungal activity against P. litchi Induction of fruit defenses
Zheng et al. 2019
Lysinibacillus sp. 2-Ethyl-1-hexanol Antifungal activity against Colletotrichum acutatum Che et al., 2017 Paenibacillus polymyxa 2-Nonanone
3-Hydroxy-2-butanone Antifungal activity against Verticillium longisporum Rybakova et al., 2017
Acetone 2-Decanol 2-Nonanone 2-Decanone
Nematicidal activity against Meloidogyne incognita Cheng et al., 2017
Proteus vulgaris Indole A. thaliana growth promotion Bhattacharyya et al., 2015
Pseudomonas brassicacearum
2-Undecanone 1-undecene
Antifungal activity against B. cinerea, Fusarum equiseti, F. oxysporum, F. solani, Macrophomina phaseolina, R. solani, Rosellinia necatrix, S. sclerotiourm and V. dahliae Oomyceticidal activity against Phytophthora cactorum, P. nicotianae and Pythium ultimum
Giorgio et al., 2015
Pseudomonas chlororaphis 2,3-Butanediol Induction of systemic resistance in tobacco against E. carotovora
Han et al., 2006
2,3-Butanediol Increase tolerance to drought in A. thaliana Cho et al., 2008 Pseudomonas chlororaphis subsp. aureofaciens
3-Methyl-1-butanol 2-Methyl-1-butanol Phenylethyl alcohol
Antifungal activity against Ceratocystis fimbriata Zhang et al., 2019
Pseudomonas donghuensis Hydrogen cyanide Dimethyl sulfide S-Methyl thioacetate Methyl thiocyanate Dimethyl trisulfide 1-Undecan
Antifungal activity against R. solani, Fusarium culmorum and V. dahliae Oomyceticidal activity against P. ultimum
Ossowicki et al., 2017
Pseudomonas fluorescens Toluene Ethyl benzene m-Xylene Benzothiazole
Bacteriostatic effect against Ralstonia solanacearum Raza et al., 2016a
Unidentified A. thaliana growth promotion Raza et al., 2016b Dimethyl disulfide Antifungal activity against B. cinerea
Medicago truncatula growth promotion Hernandez-Leon et al., 2015
3-Nonene 4-Undecyne 1-Undecene
A. thaliana growth promotion Induction of systemic resistance
Cheng et al., 2016
Undecene Antifungal activity against R. solani Kai et al., 2007 Unidentified Mentha piperita growth promotion and change in essential oils
composition Santoro et al., 2011
Pseudomonas putida 1-Undecene Dimethyldisulfide
Antifungal activity against B. cinerea, Fusarum equiseti, F. oxysporum, F. solani, M. phaseolina, R. solani, R. necatrix, S. sclerotiourm and V. dahliae Oomyceticidal activity against P. cactorum, P. nicotianae and P. ultimum
Giorgio et al., 2015
Dimethyl trisulphide Antifungal activity against R. solani, C. gloeosporioides, Athelia rolfsii, Gibberella moniliformis and Magnaporthe oryzae Oomyceticidal activity against Phytophthora capsici and Pythium myriotylum Nematicidal activity against Radopholus similis
Agisha et al., 2019
4-Octylbutan-4-olide Mentha piperita growth promotion and an increase in menthol production
Santoro et al., 2016
Pseudomonas simiae Phenol-2-methoxy Stearic acid Tetracontane Myristic acid
Increase tolerance to salinity in soybean Vaishnav et al., 2015, 2016
Pseudomonas stutzeri Dimethyl disulfide Antifungal activity against B. cinerea Tomato growth promotion
Rojas-Solís et al., 2018
Pseudomonas trivialis Antifungal activity against R. solani Kai et al., 2007
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Table 1 (continued )
Microorganism VOC Effects Reference
Undecadienea Undecenea Benzyloxybenzonitrile
Pseudomonas spp. Pyrrolo[1,2-a]pyrazine-1,4-dione, hexahydro-3-(phenylmethyl) Hexadecane n-Hexadecanoic acid
Vigna radiata growth promotion Jishma et al., 2017
Serratia plymuthica Dimethyl trisulfide β-Phenylethanol
Antifungal activity against R. solani Kai et al., 2007
Serratia odorifera Trans-9-hexadecene-1-ol β-Phenylethanol Benzylnitrile
Antifungal activity against R. solani Kai et al., 2007
Ammonia Dimethyl disulfide
A. thaliana toxicity Kai et al., 2010
Stenotrophomonas maltophilia
Dimethyl disulfide Antifungal activity against B. cinerea Tomato growth promotion
Rojas-Solís et al., 2018
Stenotrophomonas rhizophila
Dodecanal β-Phenylethanol
Antifungal activity against R. solani Kai et al., 2007
Streptomyces alboflavus 2-Methylisoborneol Antifungal activity against Fusarium moniliforme, Aspergillus flavus, A. ochraceus, A. niger and Penicillum citrinum
Wang et al., 2013
Dimethyl disulfide Antifungal activity against F. moniliforme Wang et al., 2013 Dimethyl trisulfide Benzenamine
Antifungal activity against A. flavus Yang et al., 2019
Streptomyces fimicarius Phenylethyl Alcohol Ethyl phenylacetate Methyl anthranilate α-Copaene Caryophyllene Methyl salicylate 4-Ethylphenol
Oomyceticidal activity against P. litchii Xing et al., 2018
Streptomyces yanglinensis Methyl 2-methylbutyrate 2-Phenylethanol b-Caryophyllene
Antifungal activity against A. flavus and A. parasiticus Lyu et al., 2020
Streptomyces spp. 1,3,5-Trichloro-2-methoxy benzene Antifungal activity against R. solani A. thaliana growth promotion
Cordovez et al., 2015
Yeasts Aureobasidium pullulans 2-Phenethyl alcohol Antifungal activity against B. cinerea, Colletotrichum acutatum, Penicillium expansum, P. digitatum and P. italicum
Di Francesco et al., 2015
2-Phenethyl alcohol Antifungal activity against Monilinia laxa, M. fructicola, M. polystroma and M. fructigena
Di Francesco et al., 2020
2-Methyl-1-butanol 3-Methyl-1-butanol
Attraction of pest insect predatory wasps Davis et al., 2012
Unidentified Antifungal activity against B. cinerea, P. digitatum and P. italicum
Parafati et al., 2017
Candida intermedia 1,3,5,7-Cyclooctatetraene 3-Methyl-1-butanol 2-Nonanone Pentanoic acid 4-Methyl-ethyl ester 3-Methyl-1-butanol Acetate Acetic acid Pentyl ester Hexanoic acid Ethyl ester
Antifungal activity against B. cinerea Huang et al., 2011
Geotrichum candidum 2-Penylethanol Isopentyl acetate Naphthalene
Antifungal activity against R. solani Mookherjee et al., 2018
Hanseniaspora uvarum Ethyl caproate Ethyl acetate
Increase strawberry fruit flavor and defense Wang et al., 2019
Metschnikowia pulcherrima Ethyl acetate Antifungal activity against B. cinerea, M. fructicola, A. alternata, Aspergillus carbonarius, P. digitatum, Cladosporium spp. and Colletotrichum spp.
Oro et al., 2018
Saccharomyces cerevisiae Ethanol Antifungal activity against Phyllosticta citricarpa Fialho et al., 2016 Ethanol Antifungal activity against Guignardia citricarpa Fialho et al., 2011 Ethyl acetate Antifungal activity against B. cinerea, M. fructicola, A. alternata,
A. carbonarius, P. digitatum, Cladosporium spp. and Colletotrichum spp.
Oro et al., 2018
3-Methyl-1-butanol 2-Methyl-1-butanol
Antifungal activity against P. citricarpa Toffano et al., 2017
Wickerhamomyces anomalus
Ethyl acetate Antifungal activity against B. cinerea, M. fructicola, A. alternata, A. carbonarius, P. digitatum, Cladosporium spp. and Colletotrichum spp.
Oro et al., 2018
Unidentified Antifungal activity against B. cinerea, P. digitatum and P. italicum
Parafati et al., 2017
Alternaria alternata Unidentified Increased starch synthesis in A. thaliana Li et al., 2011
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Table 1 (continued )
Microorganism VOC Effects Reference
Filamentous fungi
Unidentified A. thaliana growth and flowering promotion Sanchez-Lopez et al., 2016
Ampelomyces sp. m-Cresol Induction of systemic resistance in A. thaliana against Pseudomonas syringae pv. tomato
Naznin et al., 2014
Cladosporium sp. Methyl benzoate Induction of systemic resistance in A. thaliana against P. syringae pv. tomato
Naznin et al., 2014
Cochliobolus sativus 2-Methylbutan-1-ol Decreased barley growth Fiers et al. 2013 Cryptosporiopsis ericae 12-Methyloxacyclododec-9-en-2-one
3,5,5,9-Tetramethyl-2,4a,5,6,7,8- Hexahydro-1H-benzo[7]annulene Bisabolene
Antifungal activity against S. sclerotiorum and S. turcica Zhang et al., 2018
Daldinia bambusicola Benzeneethanol 2H-1-Benzopyran-2-One,4,7- dihydroxy
Antifungal activity against Colletotrichum lagenarium Oomyceticidal activity against Phytophthora palmivora
Pandey and Banerjee, 2014
Fusarium culmorum 2-Methylbutan-1-ol Decreased barley growth Fiers et al. 2013 Fusarium oxysporum Dimethyl disulfide Lettuce growth promotion Minerdi et al., 2011
Unidentified Induction of resistance against P. syringae Li and Kang, 2018 3-Methyl-1-butanol 2-Methyl-1-butanol
Antifungal activity against V. dahliae and V. longisporum Mulero-Aparicio et al., 2019
5,8-Cyclocaryophyllan-4-olo Butylated hydroxyanisole
Antifungal activity against F. xysporum f. sp. lactucae Minerdi et al., 2009
2-Methylbutyl acetate 3-Methylbutyl acetate Ethyl acetate 2-Methylpropyl acetate
Nematicidal activity against M. incognita Terra et al., 2018
Fusarium verticillioides 1-Octen-3-ol 3-Octanol
Insect-pest repellent against Sitophilus zeamais Usseglio et al., 2017
Fusarium spp. Furfural 5-Methyl-2-furancarboxaldehyde
A. thaliana growth promotion Schenkel et al., 2018
Gliocladium sp. 1-Butanol 3-Methyl-phenylethyl alcohol Acetic acid 2-Phenylethyl ester
Antifungal activity against V. dahliae Oomyceticidal activity against P. ultimum
Stinson et al., 2003
Hypoxylon anthochroum Eucalyptol Antifungal activity against F. oxysporum Macías-Rubalcava et al., 2018
2-Methyl-1-butanol 3-Methyl-1-butanol Eucalyptol Ocimene Terpinolene
Antifungal activity against F. oxysporum Medina-Romero et al., 2017
Muscodor albus Naphthalene Antifungal activity against Aspergillus fumigatus and A. ochraceus
Ezra et al., 2004
Muscodor brasiliensis Pogostol 2-Phenylethylacetate Phenylethyl alcohol
Antifungal activity against P. digitatum Pena et al., 2019
Muscodor heveae 3-Methylbutan-1-ol 3-Methylbutyl acetate 2-Methylpropanoic acid
Antifungal activity against Rigidoporus microporus Reduces the growth and inhibits the germination of A. thaliana and tomato
Siri-Udom et al., 2017
Myrothecium inundatum 3-Octanone 3-Octanol 7-Octen-4-ol
Antifungal activity against S. sclerotiorum Oomyceticidal activity against P. ultimum
Banerjee et al., 2010
Nodulisporium sp. Eucalyptol Limonene
Oomyceticidal activity against Pythium aphanidermatum Sanchez-Fernandez et al., 2016
1,8 Cineole 1-Butanol 2-Methyl Phenylethanol alcohol.
Antifungal activity against R. solani and S. sclerotiorum Oomyceticidal activity against Phytophthora palmivora and P. cinnamomi
Hassan et al., 2013
Phoma sp. Methyl-propanol 3-Methyl-butanol
Tobacco growth promotion Naznin et al., 2013
Phomopsis sp. 1-Butanol 3-Methyl Benzeneethanol 1-Propanol 2-Methyl 2-Propanone
Antifungal activity against Sclerotinia sp., Rhizoctonia sp., Fusarium sp., Botrytis sp., Verticillium sp. and Colletotrichum sp. Oomyceticidal activity against Pythium sp. and Phytophthora sp.
Singh et al., 2011
Trichoderma atroviride Isopropanol Acrylonitrile 2-Pentanone 1-Butanol Propyl acetate Butyl acetate Pentyl acetate Styrene Furfural Heptanal 2-Heptanol
A. thaliana growth promotion Lee et al., 2015
(continued on next page)
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such as limonene (Lee et al., 2016; Nieto-Jacobo et al., 2017; Lee et al., 2019). A wide diversity of MOCs produced by T. atroviride also increase the growth of A. thaliana independently of the age of the plant, but with different effects (including growth inhibition) depending on the age of the fungal cultures (Lee et al., 2015). Also in A. thaliana, furfural and 5- methyl-2-furancarboxaldehyde from various Fusarium species increase the length of the primary roots (Schenkel et al., 2018), in the same way
that 1-naphthylphthalamic acid does from various Verticillum species, thanks to increase the auxins biosynthesis (Li et al., 2018b). In recent years, the use of Trichoderma species as plant growth promoting fungi (PGPFs) has been arousing more and more interest. In its PGP capacity, it has been demonstrated how the produced MVOCs can play a key role, being an important axis of research and agricultural application.
In crops of agronomic interest such as tabacco, it has been
Table 1 (continued )
Microorganism VOC Effects Reference
Furfuryl alcohol 2-Acetylfuran 2-Ethylhexyl alcohol Nonyl alcohol Methyl salicylate Undecanal 1,2,3,4-Tetrahydro-5- methylnaphthalene 1112 2-Phenoxyethanol Sesquiterpene Isocaryophyllene n-Heptadecane Methyl dihydrojasmonate Isopropyl laurate Octanal-2-(phenylmethylene)
Trichoderma gamsii Dimethyl disulfide Antifungal activity against Epicocum nigrum and Scytalidium lignicola
Chen et al., 2016a
2-Undecanone Antifungal activity against Phoma herbarum Chen et al., 2016a 3-Octanone Antifungal activity against Fusarium flocciferum Chen et al., 2016a
Trichoderma koningiopsis Cycloocta-2,4-dien-1-ol cis-1-Butyl-2-methylcyclopropane
Antifungal activity against P. herbarum, F. flocciferum, S. lignicola and E. nigrum
Chen et al., 2016b
Trichoderma longibrachiatum
Longifolene Caryophyllene
Antifungal activity against Sclerotium rolfsii and Macrophomina phaseolina
Sridharan et al., 2020
Trichoderma virens Caryophyllene Thujopsene
Antifungal activity against R. solani Inayati et al., 2019
δ-Cadinene A. thaliana growth promotion Induction of resistance against B. cinerea
Contreras-Cornejo et al., 2014
Trichoderma viride Isobutyl alcohol Isopentyl alcohol 3-Methylbutanal
A. thaliana growth promotion Hung et al., 2013
Trichoderma spp. 4-Heptanone Nonane 2-Octanone Limonene
A. thaliana growth promotion Nieto-Jacobo et al., 2017
3-Octanone Acetic acid 1-Octen-3-ol
Antifungal activity against F. oxysporum Li et al., 2018a
Heptanal Antifungal activity against Neolentinus lepideus, Postia placenta, Gloeophyllum trabeum and Trametes versicolor
Humphris et al., 2001
Unidentified Increase tolerance to salinity in A. thaliana Jalali et al., 2017 3-Methyl-1-butanol 1-Decene 2-Heptylfuran
A. thaliana growth promotion Lee et al., 2019
Butane-2,3-dione 2-Methylpropan-1-ol 3-Methylbutan-1-ol Limonene Undecane Camphor Benzoic acid Nonanoic acid β-Acoradiene
A. thaliana and tomato growth promotion Lee et al., 2016
Urnula sp. 4-Decene Tridecane 2-Decene (E) 2-Dodecene (Z,E)-alpha-Farnesene Butanoic acid Pentyl ester 1-Hexanol,2-ethyl
Antifungal activity against B. cinerea, Ceratocystis ulmi, Fusarium solani, and R. solani Oomyceticidal activity against P. ultimum
Strobel et al., 2017
Verticillium dahliae Unidentified Increase tolerance to salinity in A. thaliana Li and Kang, 2018 Verticillium spp. 1-Naphthylphthalamic acid A. thaliana and Nicotiana benthamiana growth promotion Li et al., 2018b Xylaria sp. 3-Methyl-1-butanol
2-Methyl-1-butanol 2-Methyl-1-propanol Thujopsene
Oomyceticidal activity against Pythium aphanidermatum and P. capsici Antifungal activity against A. solani and F. oxysporum
Sanchez-Ortiz et al., 2016
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determined that the MVOCs methyl-propanol and 3-methyl-butanol produced by fungi such as Phoma sp. are capable of increasing their growth (Naznin et al., 2013), or dimethyl disulfide in lettuce from Fusarium oxysporum, capable of increasing root length, fresh weight and chlorophyll content (Minerdi et al., 2011). Similarly, dimethyl disulfide from the bacteria Stenotrophomonas maltophilia and Pseudomonas stutzeri increases the growth of tomato plants (Rojas-Solís et al., 2018), as does albuterol and 1,3-propanediole from B. subtilis, thanks to an increase in photosynthetic activity, the content of gibberellins, auxins, and cytoki-nins, and a decrease in ethylene (Tahir et al., 2017). Also from B. subtilis, unidentified MVOCs have been found to significantly increase plant biomass in soybean, changing the root architecture, exhibiting roots with higher length, diameter, surface area and volume (Bavaresco et al., 2020), as in Mentha piperita (Santoro et al., 2011).
In M. piperita, it has been proven that the MVOCs emitted by bacteria such as Pseudomonas fluorescens, Azospirillum brasilense and Pseudomonas putida, including 4-octylbutan-4-olide, are capable of promoting plant growth and increasing the content of compounds of interest in its essential oils, such as (+) pulegone and (− ) menthone (Santoro et al., 2011; Santoro et al., 2016). In this sense, it has been determined how different MVOCs are capable of increasing the sugar content (therefore, the flavor) and their tolerance to cold storage in strawberries, such as ethyl caproate and ethyl acetate issued by the yeast Hanseniaspora uvarum (Wang et al., 2019).
So far, numerous examples of MVOCs with the ability to promote plant growth of important crops have been reported. Despite this, the mechanisms involved are unknown and a great research effort is needed to develop tools that allow the controlled, efficient and profitable application of these secondary metabolites in the greenhouse and in the
field. On the other hand, negative effects on plant growth have also been
reported as a consequence of different MVOCs. In A. thalaiana, amounts of 20 μmol or 2.5 μmol of ammonia or dimethyl disulfide, respectively, from the bacteria Serratia odorifera, represent the IC50 concentrations (concentration that leads to 50% inhibition) (Kai et al., 2010), as well as 3-methylbutan-1-ol, 3-methylbutyl acetate and 2-methylpropanoic acid from the fungus Muscodor heveae that inhibit its germination and that of tomato (Siri-Udom et al., 2017). In barley, 2-methylbutan-1-ol produced by the fungi Cochliobolus sativus and Fusarium culmorum significantly decreases the length of roots and the surface of aerial parts (Fiers et al., 2013). The existence of possible negative effects of MVOCs in plants requires detailed studies on the volatilome of PGPBs and PGMFs used in crops.
3.2. Abiotic stress tolerance-enhancing MVOCs
Regarding the increase in tolerance to abiotic stresses in plants by the action of MVOCs, there are few studies carried out so far. Mainly, the ability of different MVOCs to increase plant tolerance against salinity stress has been studied. It has been determined how different species of the fungal genus Trichoderma are capable of inducing salt tolerance in A. thaliana plants through protection against oxidative damage, by reducing the accumulation of H2O2 accumulation under salt stress, although the exact MVOCs involved have not been determined (Jalali et al., 2017). MVOCs produced by Verticillium dahliae that are capable of increasing signaling by auxins against salt stress, increasing A. thaliana growth and their chlorophyll content (Li and Kang, 2018), either un-known. Therefore, to determine the mechanisms involved in increasing tolerance to salinity in plants through the action of MVOCs from fungi, further studies are necessary.
In bacteria, several mechanisms possibly involved in the increase of tolerance against salinity in plants by MVOCs have been described. Acetoin released by B. amyloliquefaciens is able to increase tolerance against salinity in M. piperita, thanks to an increase in SA content (del Rosario-Cappellari and Banchio, 2019). In soybean, phenol-2-methoxy, stearic acid, tetracontane and myristic acid released by Pseudomonas simiae are able to significantly reduce Na+, and increase K+ and P, content in roots of soybean seedlings under salt stress, due to an increase in expression of peroxidase, catalase, vegetative storage protein and nitrite reductase genes (Vaishnav et al., 2015, 2016). 2,3-Butanediol released by B. subtilis increases tolerance to salinity in A. thaliana by downregulating expression of high-affinity K+ transporter 1 in roots, while at the same time inducing its upregulation in shoots. This change in expression (upregulation vs downregulation) served to mediate Na+
accumulation in the plant, and hence improved tolerance to salt stress (Zhang et al., 2008). Same MVOC issued by Pseudomonas chlororaphis that is capable of inducing tolerance to drought in A. thaliana through an SA-dependent response (Cho et al., 2008).
The ability of MVOCs to increase plant tolerance to abiotic stresses such as salinity and drought has been reported in different systems. However, the true application of MVOCs in agriculture in order to in-crease the productivity of crops under unfavorable conditions needs specific studies.
3.3. Plant defense inducing MVOCs
The ability of different MVOCs to activate plant defenses against different pathogens and pests has been reported in different microbial and plant species. Against the pathogenic bacteria Pseudomonas syringae pv. tomato has been determined how different fungal MVOCs from Fusarium oxysporum are able to induce a systemic resistance in A. thaliana by SA-signaling pathway (Li and Kang, 2018); how has been observed for m-cresol from Ampelomyces sp. using SA- and JA-signaling pathways, or methyl benzoate emitted by Cladosporium sp. via JA- signaling pathway (Naznin et al., 2014). Also, acetoin from the
Fig. 1. Graphic representation of the beneficial effects of MVOCs in plants.
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bacteria B. subtilis induces systemic resistance in A. thaliana against P. syringae through SA-signaling pathway (Rudrappa et al., 2010), how observed with 3-nonene MVOCs, 4-undecyne and 1-undecene emitted by P. fluorescens, also capable of promoting plant growth (Cheng et al., 2016).
2,3-Butanediol is a VOC emitted by various species of microorgan-isms that, in addition to other functions, is capable of activating plant defenses against different pathogens. Against Erwinia carotovora subsp. carotovora this MVOC emitted by B. subtilis and B. amyloliquefaciens is capable of activating a systemic resistance in A. thaliana mediated by ethylene- (ET) signaling pathway (Ryu et al., 2004), same result ob-tained when is emitted by Pseudomonas chlororaphis, although without to know the exact mechanism by which the defensive response is activated, and not being effective against P. syringae pv. tabaci in tobacco plants (Han et al., 2006). Same MVOC from Enterobacter aerogenes involved in the induction of plant resistance against the Northern corn leaf blight fungus Setosphaeria turcica (D’Alessandro et al., 2014). Also in field conditions, the effectiveness of bacterial MVOCs against bacterial dis-eases has been verified, as is the case of 3-pentanol emitted by B. amyloliquefaciens, which increases the resistance of pepper plants against the bacterial spot disease (Xanthomonas axonopodis pv. ves-icatoria) by SA- and JA-signaling pathways (Choi et al., 2014).
On the other hand, anti-fungal plant pathogens have been shown in A. thaliana how exposure to δ-cadinene released by the fungus T. virens is able to increase plant growth and its resistance to attack by B. cinerea, thanks to an increase in biosynthesis of terpenes and accumulation of jasmonic acid and hydrogen peroxide (Contreras-Cornejo et al., 2014). In postharvest, the fungus Peronophythora litchi severely affects litchi fruits, and it has been proven that the resistance of fruits is increased when exposed to MVOC α-farnesene from the bacteria B. pumilus, B. amyloliquefaciens and Exiguobacterium acetylicum (Zheng et al., 2019).
The activation of plant defenses by MVOCs has been extensively studied, including in vitro and even in field assays. Future lines of research should be carried out to develop formulations and methodol-ogies for direct use in agriculture.
3.4. MVOCs against insect-pest
Against insects, the main mechanisms that have been reported by MVOCs in plants are the direct effect as a repellent or the attraction of natural enemies. In stored maize kernels it has been verified how when they are infected by the pathogenic fungus Fusarium verticillioides they are not consumed by the insect-pest Sitophilus zeamais, as a consequence of the emission of repellent MVOCs, such as 1-octen-3-ol and 3-octanol (Usseglio et al., 2017). In the case of attraction of predatory insects, it has been proven that the emission of 2-methyl-1-butanol and 3-methyl- 1-butanol by the yeast Aureobasidium pullulans causes the active attrac-tion of species of predatory insect-pest wasps such as the western yel-lowjacket (Vespula pensylvanica) and the German yellowjacket (V. germanica) (Davis et al., 2012). While in the attraction of parasitoid insects it has been reported as 2,3-butanediol from the bacterium E. aerogenes when it is in interaction with maize roots, it actively in-creases the attraction of parasitoid insect-pest wasps such as Cotesia marginiventris (D’Alessandro et al., 2014).
The use of MVOCs against insect-pest in plants requires in-depth research. Until now, the capacity of various MVOCs as repellants of insect-pests and/or attractants of natural enemies has been described, but it is necessary to know the mechanisms involved and the possibility of their applied use.
3.5. MVOCs in plant pathogens control
The direct antibiosis of different MVOCs against plant pathogens is one of the most studied benefits for plants. There are a large number of interaction studies between different MVOCs, mostly from antagonistic microorganisms used in biocontrol, and plant pathogenic
microorganisms. The main microorganisms producing antibacterial MVOCs are bac-
teria of the Bacillus genus. Against the causal agent of bacterial ring rot of potato, Clavibacter michiganensis ssp. sepedonicus, has been reported as the compounds benzaldehyde, nonanal, benzothiazole and acetophe-none, from B. subtilis, are capable of producing a reduction in the size of the colonies and a wide range of abnormalities in C. michiganensis cells (Rajer et al., 2017). Or against the tomato wilt pathogen Ralstonia sol-anacearum, both in vitro and in vivo, has been determined as several MVOCs produced by B. amyloliquefaciens, such as 2-undecanone, 2-tri-decanone and heptadecane that are capable of inhibiting motility, bio-film formation and root colonization of pathogenic bacteria, in addition to increasing oxidative stress (Raza et al., 2016c, 2016d). Bacteriostatic effect also reported by MVOCs toluene, ethyl benzene, m-xylene and benzothiazole from P. fluorescens, restricting the growth and virulence (Raza et al., 2016a).
As far as oomycetes are concerned, there is a great diversity of bac-terial MVOCs with oomyceticidal capacity. From P. putida several MVOCs with oomyceticidal capacity have been described in vitro, such as 1-undecene and dimethyldisulfide against Phytophthora cactorum, P. nicotianae and Pythium ultimum (Giorgio et al., 2015), or dimethyl-trisulphide against Phytophthora capsici and Pythium myriotylum (Agisha et al., 2019). Effects also reported from Pseudomonas brassicacearum 2- undecanone and 1-undecene (Giorgio et al., 2015), various MVOCs from P. donghuensis (Ossowicki et al., 2017), and from Bacillus mega-terium heneicosane, heptacosane and octacosane (Giorgio et al., 2015). Dimethylhexadecylamine from Arthrobacter agilis is able to inhibit the growth of Phytophthora cinnamomi by decreasing the number of mem-brane lipids present in the mycelium of the pathogen (Velazquez- Becerra et al., 2013), also by 2,5-dimethyl pyrazine, 2-dodecanone and 2-tetradecanone from B. amyloliquefaciens (Guevara-Avendano et al., 2019). Against litchi downy blight, caused by the oomycete pathogen Peronophythora litchi, various MVOCs from Streptomyces fimicarius resulted in severe damage to the endomembrane system and cell wall pathogen cells in vitro and abnormal morphology of appressoria, as well as deformed new hyphae in infection process, suppressing mycelial growth and sporulation (Xing et al., 2018).
In the group of filamentous fungi there is a great diversity of MVOCs with oomyceticidal capacity. Eucalyptol, limonene or 1,8 cineole pro-duced by Nodulisporium sp. are able to inhibit the in vitro growth of Pythium aphanidermatum (Sanchez-Fernandez et al., 2016), Phytophthora palmivora and P. cinnamomi (Hassan et al., 2013), same results reported by several MVOCs from Phomopsis sp. (Singh et al., 2011), Daldinia bambusicola (Pandey and Banerjee, 2014), and Xylaria sp. (Sanchez- Ortiz et al., 2016). Against P. ultimum, 1-butanol or 3-methyl-phenyl-ethyl alcohol from Gliocladium sp. (Stinson et al., 2003), 4-decene or butanoic acid from Urmula sp. (Strobel et al., 2017), and several octanols from Myrothecium inundatum present oomyceticidal capacity; the vola-tiles produced by the latter being of great interest, since when grown in microaerophilic conditions, it produces a number of hydrocarbons of interest as fuel related hydrocarbons including octane (Banerjee et al., 2010).
Against pathogenic fungi there are many different studies that demonstrate the antifungal capacity of different MVOCs. In the case of Rhizoctonia solani, inhibition of mycelial growth in vitro by MVOCs has been reported as undecene, benzyloxybenzonitrile, dimethyltrisulfide, β-phenylethanol or dodecanal from P. fluorescens, P. trivialis, Serratia plymuthica, S. odorifera or Stenotrophomonas rhizophila (2007). Also in soil, where 1,3,5-trichloro-2-methoxy benzene emitted by several spe-cies of the bacterial genus Streptomyces eliminate the presence of the pathogen, while promoting the growth of A. thaliana (Cordovez et al., 2015). Antifungal effects against R. solani in vitro also reported by yeasts such as Geotrichum candidum when releasing MVOCs 2-penylethanol, isopentyl acetate and naphthalene (Mookherjee et al., 2018), or the filamentous fungus T. virens thanks to the release of thujopsene (Inayati et al., 2019).
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In the case of pathogenic fungi of the genus Fusarium, the ability to inhibit the growth of F. oxysporum, both in vitro and on cherry tomatoes, has been described for changes in cell membrane permeability, damage to the hyphal morphology, and an inhibitory effect on the respiration, by MVOCs as eucalyptol or 3-methyl-1-butanol from the filamentous fun-gus Hypoxylon anthochroum (Medina-Romero et al., 2017; Macías- Rubalcava et al., 2018). The same effect has been described by 3-octa-none, acetic acid and 1-octen-3-ol emitted by several Trichoderma spe-cies (Li et al., 2018a), 5,8-cyclocaryophyllan-4-olo and butylated hydroxyanisole emitted by endophytic strains of F. oxysporum (Minerdi et al., 2009), or benzothiazole phenol and 2,3,6-trimethylphenol released by the bacterium B. amyloliquefaciens (Yuan et al., 2012). Also against other species within the Fusarium genus, such as the post-harvest pathogen F. moniliforme by the action of dimethyldisulfide emitted by bacteria S. alboflavus (Wang et al., 2013), or F. flocciferum by the MVOC 3-octanone from fungus Trichoderma gamsii (Chen et al., 2016a).
In addition to R. solani and Fusarium, there are many other patho-genic soil-borne against which different MVOCs are highly effective. For example, against Verticillium dahliae and V. longisporum the MVOCs emitted by F. oxysporum 3-methyl-1-butanol and 2-methyl-1-butanol cause an inhibition of mycelial growth and microsclerotia viability (Mulero-Aparicio et al., 2019). As it happens with different MVOCs released by bacterial species like Paenibacillus polymyxa (Rybakova et al., 2017) or filamentous fungi like Gliocladium sp. (Stinson et al., 2003).
Regarding fungal diseases mainly produced in postharvest, there are a large number of bacterial MVOCs with antifungal capacity. Against the postharvest litchi fruit pathogen P. litchi the MVOCs 1- (2-aminophenyl) ethanone, benzothiazole and α-farnesene from B. amyloliquefaciens, B. pumilus and Exiguobacterium acetylicum have been shown to inhibit the growth of the pathogen in vitro and to the incidence of the disease in vivo (Zheng et al. 2019). Against the fungus Ceratocystis fimbriata, the caus-ative agent of black rot disease in sweet potato tuber-roots in post-harvest, has been reported as Pseudomonas chlororaphis subsp. aureofaciens by emitting the MVOCs 3-methyl-1-butanol, 2-methyl-1- butanol and phenylethyl alcohol is capable of causing morphological changes and loss of content at the cellular level in the hyphae (Zhang et al., 2019). Also against pathogens within the genus Colleotrichum, such as C. gloeosporioides or C. acutatum, the production of bacterial MVOCs has great growth inhibition capacity in vitro, such as chloro-acetic acid from Bacillus atrophaeus (Rajaofera et al., 2019), dime-thyldisulfide from B. mycoides (Guevara-Avendano et al., 2019), or 2- ethyl-1-hexanol from Lysinibacillus sp. (Che et al., 2017). And within the genus Aspergillus, such as A. flavus and A. parasiticus, against which strong inhibitory effects against mycelial growth, sporulation, conidial germination and aflatoxin production have been described, by the MVOCs dimethyl trisulfide and benzenamine from S. alboflavus (Yang et al., 2019), or methyl 2-methylbutyrate, 2-phenylethanol and β-car-yophyllene from S. yanglinensis (Lyu et al., 2020). Meanwhile, B. cinerea is a fungus of great importance in postharvest that also attacks plant aerial part in a widespread manner. It has been reported as dime-thyldisulfide, from P. fluorescens, P. stutzeri and Stenotrophomonas mal-tophilia, acts efficiently against B. cinerea in tomato plants and Medicago truncatula (Hernandez-Leon et al., 2015; Rojas-Solís et al., 2018). Also in postharvest, reducing decay of cherry by MVOCs issued by B. amyloliquefaciens 1,3 pentadiene, acetoin and thiophene, being equally effective in the case of the pathogens Monilinia laxa and M. fructicola (Gotor-Vila et al., 2017).
Continuing with postharvest fungal diseases, different fungal MVOCs are also very effective in reducing their incidence. From yeast S. cerevisiae ethanol, 3-methyl-1-butanol and 2-methyl-1-butanol inhibiting completely the mycelial growth and the germination and appressorium formation of the causal agents of citrus black spot (Phyl-losticta citricarpa and Guignardia citricarpa) because essential metabolic pathways, such as the production of the morphogenesis related enzymes
interference (Fialho et al., 2011, 2016; Toffano et al., 2017). While from the fungi Muscodor albus and M. brasiliensis the MVOCs naphthalene, pogostol, 2-phenylethylacetate and phenylethyl alcohol inhibit the development of the disease caused by postharvest fungi Aspergillus fumigatus, A. ochraceus and Penicillium digitatum (Ezra et al., 2004; Pena et al., 2019).
On the other hand, against wood diseases there are also several studies on the effect of fungal MVOCs. Against white root rot disease in rubber trees (Hevea brasiliensis) it has been determined that, both in vitro and in vivo, 3-methylbutan-1-ol, 3-methylbutyl acetate and 2-methylpro-panoic acid from Muscodor heveae decrease the growth of the pathogen and they cause a great suppression of the disease in trees (Siri-Udom et al., 2017). Similarly, heptanal released by various Trichoderma species inhibits of wood decay fungi Neolentinus lepideus, Postia placenta, Gloeophyllum trabeum and Trametes versicolor (Humphris et al., 2001).
There are many other MVOCs that have been proven to have anti-fungal activity against a wide variety of plant pathogens. As are those of bacterial origin 2,3-butanedione and acetoin from B. amyloliquefaciens (Asari et al., 2016), heneicosane, heptacosane and octacosane from B. megaterium (Giorgio et al., 2015), issoctanol from Corrallococcus sp. (Ye et al., 2020), 2-undecanone, 1-undecene, dimethyldisulfide and dimethyltrisulfide from B. brassicacearum and P. putida (Giorgio et al., 2015; Agisha et al., 2019), 2-methylisoborneol from Streptomyces albo-flavus (Wang et al., 2013), and many other MVOCs from species such as Bacillus velezensis (Gao et al., 2017), B. amyloliquefacines (Guevara- Avendano et al., 2019), B. subtilis (Gao et al., 2018), or Pseudomonas donghuensis (Ossowicki et al., 2017). From yeasts such as 2-phenethyl alcohol from A. pullulans (Di Francesco et al., 2015, 2020), or ethyl acetate from Metschnikowia pulcherrima, Wickerhamomyces anomalus and S. cerevisiae (Oro et al., 2018). Or of fungal-filamentous origin, such as 1- butanol, 2-methyl, caryophyllene, 3-methyl-1-butanol or 4-decene, from fungi such as Trichoderma koningiopsis (Chen et al., 2016b), T. longibrachiatum (Sridharan et al., 2020), Cryptosporiopsis ericae (Zhang et al., 2018), Myrothecium inundatum (Banerjee et al., 2010), Nod-ulisporium sp. (Hassan et al., 2013), Phomopsis sp. (Singh et al., 2011), Urnula sp. (Strobel et al., 2017) or Xylaria sp. (Sanchez-Ortiz et al., 2016).
As far as the nematicidal capacity of MVOCs are concerned, it has been described for acetone, 2-decanol, 2-nonanone and 2-decanone from Paenibacillus polymyxa against Meloidogyne incognita, acting as “honey-traps” attracting and destroying the integrity of the intestine and pharynx (Cheng et al., 2017). Same mortality reported in second-stage juveniles due to the volatiles emitted by the fungus F. oxysporum, as various methylbutyl acetates (Terra et al., 2018), and against the nem-atode Radopholus similis by dimethyltrisulphide emitted by the bacteria P. putida (Agisha et al., 2019).
Despite the large number of studies that demonstrate the ability of different MVOCs to inhibit the growth and development of plant path-ogens in vitro, there are still few studies in planta. The development of tools for real use in agriculture requires demonstrating in planta and in field the effectiveness of the different MVOCs to reduce the disease caused by plant pathogens.
4. Future challenges and perspectives
One of the fundamental aspects of studying MVOCs for their true use in agriculture in the future is how to transfer all the results obtained in controlled laboratory conditions to agro-system, where there are numerous factors that can reduce and even nullify the effects of these volatiles. Knowing the best way to apply MVOCs in the field is a fundamental aspect for their true use in agriculture. There are several studies that have carried out some MVOCs described with great potential in the laboratory, using different methodologies. As described in the text, 3-pentanol is an MVOC capable of acting as an activator of plant defenses against different pathogens. The application in irrigation of synthetic 3-pentanol has been described as an optimal methodology for
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obtaining systemic plant resistance against the attack of bacteria and pests (Song and Ryu, 2013). The direct application in soil of MVOC 2,3- butanediol, described throughout the text as a promoter of plant growth and inducer of systemic resistance, has also been tested. The application of synthetic 2,3-butanediol directly to the soil has been described as an efficient methodology in the field, reporting activation of systemic resistance in Nicotiana benthamiana and Agrostis stolonifera against different fungal diseases (Cortes-Barco et al., 2010a, 2010b). Future research should analyze the development of new methodologies for the application of MVOCs in the agro-system, for example, through mate-rials that achieve their controlled release.
Although the effects of different MVOCs in plants have been widely described, the true mechanisms involved are still unknown. This rep-resents a great field of future development for MVOCs and plant research. In 2018, Tyagi et al. proposed the hypothesis that MVOCs are capable of penetrating plant tissues, specifically through roots, where they modulate different hormonal signaling routes, modifying plant health and developmental processes (Tyagi et al., 2018). However, this statement continues to be a hypothesis that requires future studies to describe the plant receptors capable of perceiving MVOCs, how these compounds are capable of penetrating plant tissues, how they are perceived by plant cells (receptors, signaling pathways, etc.), the possible existence of active transport from the site of penetration to the site of action, in addition to their role as regulators of plant physiology. In this sense, research on all these aspects in plant-VOCs has reported relevant information in this regard, allowing in-depth knowledge of their receptors, their mode of transport in tissues, or how they are stored in cavities (Tissier et al., 2017; Ninkovic et al., 2021).
An important aspect that will require future studies is the application of several combined MVOCs and their interaction with plant-VOCs. So far, no studies have been carried out regarding the possible functional modifications derived from the combination of several MVOCs, being an area of future study that may provide important information. It has been described how MVOCs can be combined with different plant-VOCs capable of completely canceling their function, mainly with MVOCs involved in pathogen-pathogen communication (Quintana-Rodriguez et al., 2018). Therefore, the knowledge of the profile of MVOCs and plant-VOCs becomes essential in the design of a correct application strategy.
5. Conclusions
As far as MVOCs are concerned, one of its main functions is inter- and intra-specific communication. In a beneficial way for plants, there are numerous in vitro, in planta and in field studies that demonstrate how the incidence of diseases in crops can be reduced in a sustainable way for the environment and health by using VOCs of certain microbial species.
Despite the existence of considerable literature on plant-MVOCs interaction and the effects and benefits that occur, the understanding of the exact mechanisms by which they occur are often very limited. In this sense, it is worth noting the few existing studies in the study of plant tolerance to abiotic stresses by MVOCs, being a study area with great potential in the coming years.
Finally, in the field of nanotechnology, great advances are being made in the development of tools that allow the use of MVOCs in agri-culture in a specific and controlled way. For example, by using molec-ularly imprinted polymers as a solid sorbent from MVOCs, such as dibutyl phthalate, allowing the metabolite of interest to be separated from the rest of volatilome (Rahnama et al., 2016).
Declaration of competing interest
The author declares that he has no known competing financial in-terests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
Thanks to Darío Rodríguez-Prieto for preparing the infographic summary of the entire manuscript.
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