Microbial Consortia for Plant Protection against Diseases

Version	Summary	Created by	Modification	Content Size	Created at	Operation
1		Edmund Kozieł	--	2004	2023-11-27 10:52:24	\|
2	format change	Peter Tang	+ 2 word(s)	2006	2023-11-28 01:50:39	\|

This entry is adapted from the peer-reviewed paper 10.3390/ijms241512227

Biological plant protection presents a promising and exciting alternative to chemical methods for safeguarding plants against the increasing threats posed by plant diseases. This approach revolves around the utilization of biological control agents (BCAs) to suppress the activity of significant plant pathogens. Microbial BCAs have the potential to effectively manage crop disease development by interacting with pathogens or plant hosts, thereby increasing their resistance.

biocontrol crop protection biocontrol agents biopesticides plant diseases

1. Introduction

The ever-growing human population has led to an increase in food consumption, with plants serving as the primary food source worldwide. However, the combined effects of climate change and global fruit and vegetable trade have accelerated the spread of essential crop pathogens ^[1]. Therefore, to address these issues without further environmental degradation, it is crucial to explore effective and safe alternatives to chemical methods of crop protection against plant diseases ^[2]. Biocontrol, an approach involving methods that utilize natural interactions between organisms, offers a potential solution ^[3]. Extensive research has been conducted in this field, leading to multiple attempts to develop biopesticides to combat key plant pathogens ^[3]. However, despite the efforts of the scientific community and industry, the availability of biocontrol formulations remains limited, and their activity is often unsatisfactory ^[4]. Therefore, it is suggested that the combination of diverse strains of microorganisms with multidirectivemechanisms of disease suppression (which are, among others, antibiosis, competition, or induction of plant resistance) into artificial consortia can help enhance the biocontrol agents’ activity, especially in changing environmental conditions ^[5].

Microbial consortia can contain a diverse array of microorganisms that exhibit variations in their environmental preferences, such as soil type, host plant, different preferential sites of colonization, and activity against different pathogen species ^[6]. Although individual microbial strains may possess different modes of action, the amalgamation of multiple microorganisms within consortia can broaden the spectrum of their activities against a wide range of plant pathogens ^[7]. Additionally, the microorganisms present in biocontrol consortia can contribute to plant growth promotion and/or enhance the activity of the other microorganisms, further increasing the potential of such products ^[5].

Although meta-analysis has shown that the consortia activity is more significant in the greenhouse condition compared with field settings, the protective effect of the consortia remains more stable than that of single-strain inoculations ^[8]. Despite the promising potential of microbial consortia, the availability of biological control formulations based on microbial consortia on the market is currently limited ^[9].

It was demonstrated that biocontrol strains’ activity was influenced by the environmental conditions in which they were deployed ^[10]^[11]^[12]. Therefore, the utilization of microbial mixtures with diverse modes of activity was proposed as a solution to overcome the challenges related to colonization under suboptimal conditions and enhance the stability of the protective effect of biocontrol products ^[5]. By the end of the XX century, the potential of consortia to address certain challenges in the biological control of pathogens had gained acceptance ^[13]. Nevertheless, the first biocontrol product containing a mixture of microorganisms was registered only in 2015 ^[4]. After that, a few more microbial consortia were registered for biological plant protection (Table 1).

Table 1. Biological control products available on the market are registered on the list of approved plant-protecting agents ^[14] (accessed on 5 May 2023). Formulations (Form.): WP—wettable powder; WG—wettable granules.

Active Substance	Trade Name	Distributor	Country	Form.	Target Crops	Target Disease
Aureobasidium pullulans DSM 14940 + DSM 14941	BLOSSOM PROTECT; BONI PROTECT; BOTECTOR	Bio-ferm Biotechnologische Entwicklung und Produktion GmbH	US; CA; EU; SK; TN; GB; NI; BE; DE; EL; ES; FR; HU; IT; LU; NL; PT; PL; RO; SI; SK	WP	Apple, medlar, pear, quince	Fire blight Erwinia amylovora
Trichoderma virens G-41 + T. harzianum Rifai T-22	RootShield^® PLUS WP	BioWorks, Inc.	US; CA	WG	Greenhouse and nursery vegetables, herbs, ornamentals, fruits, conifer tree seedlings, various trees, legumes, oil seeds, and peanuts	Phytophthora, Rhizoctonia, Pythium, Fusarium, Thielaviopsis, Cylindrocladium
Trichoderma asperellum ICC012 + T25 + TV1	XEDAVIR; PATRIOT GOLD; BIOTRIX; XEDAVIR PFNPE	Xeda International S.A.; Timac AGRO Espańa SA	IT; PT; FR; EU;	WP, WG	Greenhouse and open field vegetables	Pythium spp., Phytophthora capsici, Rhizoctonia solani
Trichoderma atroviride IMI 206040 + T11	Binab TF WP; Binab T Vector;	Borregaard Bioplant	SE; EU	WP	Tomatoes, strawberries, ornamental trees	Botrytis cinerea, Chondrostereum purpureum
Trichoderma asperellum ICC012 + T. gamsii ICC080	Tellus; Foretryx; Bio-Tam2.0; DonJon; Bioten WP; Blindar; Remedier	Syngenta; Isagro S.p.A.; Bayer; Gowan	NL; CA; PL; US; PT; FR; TN; CY	WP	Tomatoes, horticultural flowers, ornamental and tree crops	Verticillium dahliae, Rhizoctonia solani, Sclerotinia sclerotiorum, Thielaviopsis basicola, Phytophthora capsici
Trichoderma asperellum T25 + T. atroviride T11	Tusal	Newbiotechnic S.A.	FR; EL; GB; EU	WG	Strawberry, tomato, eggplant, pepper, cucumber, courgetti, melon, watermelon, pumpkin, cut flowers, lettuce, escarole, similars, trees, and shrubs	Phytophthoracactorum, Rhizoctonia solani, Sclerotinia sclerotiorum, Phytophthora spp., Fusarium spp., Pythium spp., Phomopsis sp.,

2. Ecological Interactions: Mechanisms of Plant Disease Control

Biological control agents (BCAs) have the ability to protect plants against diseases either by direct or indirect means. Direct protection involves the BCA acting on the disease-causing agent—a pathogen. This can be achieved via parasitism, predation antibiosis or production of lytic enzymes, and it can suppress pathogens before as well as during invasion. On the other hand, indirect activity alters the environment to decrease the presence of pathogens and the chance of disease development. This can be achieved through various mechanisms, such as inducing plant resistance or competition between the BCA and pathogens ^[14] (Figure 1). It is proposed that microorganisms can enhance plant resistance to pathogens by promoting plant growth, increasing the overall fitness of the plant, and decreasing the chance of disease development according to the disease triangle concept ^[15]. Biological control agents can also disrupt pathogenesis via the digestion of pathogens virulence factors or the disruption of their communication ^[16].

Figure 1. Possible mechanisms used by biological control agents (BCAs) (bolded and framed in blue) to prevent plant diseases. BCAs can directly protect plants from pathogen invasion by killing the pathogens before or during invasion by parasitism, predation, production of lytic enzymes, or antibiosis. They can also prevent or slow down pathogens’ invasion by blocking their ecological niche and/or competing for essential nutrients. The pathogen attack induces natural plant defenses, leading to systematic acquired resistance (SAR). These defenses can also be induced by nonpathogenic bacteria such as BCAs, leading to increased resistance through induced systemic resistance (ISR). It is also suggested that BCAs can increase plant resistance to pathogen attack by inducing plants’ general fitness via growth promotion through the inter alia production of plant hormones. Repeated induction of plant defenses, either by ISR or SAR, leads to the development of a state of increased resistance: a primed state. Pathogens that successfully invade plants coordinate the production of the virulence factors responsible for the development of the disease by a mechanism called quorum sensing. BCAs may disrupt this microbial communication through quorum quenching, which relies, among other things, on the digestion of signal molecules. BCAs can also disrupt pathogenesis via the digestion of virulence factors, thus preventing disease development. Red arrows demonstrate inhibition and green arrows represent induction.

3. Interactions between Components: Menace or a New Hope

Even individual microbial strains can employ different modes of action to protect plants from diseases ^[17]^[18]. However, it has been proposed that using a mixture of bacteria can enhance the biocontrol effect in terms of not only its stability and the spectrum of application (in terms of the plant, soil type, and pathogen) but also its magnitude ^[19]^[20]. In nature, bacteria exist in complex, multispecies consortia with numerous interspecies and interkingdom interactions ^[21]. Therefore, employing multiple microorganisms as a consortium is expected to benefit their performance due to these interactions ^[5]. Therefore, this is why microbial consortia are commonly used as biofertilizers ^[22]. However, there are relatively few biocontrol products containing microbial consortia ^[23], not only due to the more problematic registration ^[24] of multiple-component-containing products but also to difficulties in the prediction of interactions between their components ^[25]. Microorganisms used for biocontrol usually produce a wide array of antimicrobial compounds, and the same modes of action used to fight the pathogens can negatively affect other consortium components ^[26]. For example, Pseudomonas fluorescens A506 degrades the antibiotics produced by strains Pantoea vagans C9-1 and Pantoea agglomerans Eh252, reducing their activity against the fire blight of pear ^[27]. This indicates incompatibility between the tested strains, highlighting the importance of confirming compatibility when composing consortia for biological plant protection. The same mechanisms used by biological control agents against plant pathogens (such as parasitism, predation, antibiosis, competition, and production of lytic enzymes but also digestion of substances responsible for their activity) can reduce the activity of other BCAs. On the other hand, BCAs can increase the protective effect with the use of alternative modes of action, different environmental preferences or by the induction of the secondary metabolism of other consortium components (Figure 2). There are various methods for assessing strain compatibility, each with its own advantages and disadvantages. However, the most commonly used approach to evaluate the biocompatibility of strains and their activity against selected pathogens relies on direct antagonism on artificial media ^[23]. Since microbial secondary metabolisms are highly dependent on the nutrients available ^[28], it has been suggested that strains for biological plant protection should be selected based on their in vivo rather than in vitro activity ^[29]. The researchers believe that this principle should be applied to the selection and composition of microbial consortia, as the interactions within the consortium have a significant impact on its overall performance ^[5].

Figure 2. Possible mechanisms by which biological control agents can interact with other BCAs present in the applied consortium (bolded and framed in blue). BCAs can directly suppress other BCAs by killing them before or during colonization by parasitism, predation, production of lytic enzymes, or antibiosis. They can also prevent or slow down other components’ colonization by blocking their ecological niches and/or competing for essential nutrients. BCAs can also degrade the compounds responsible for other BCAs’ activity. On the other hand, use of multiple strains of BCAs has a positive effect of biocontrol activity thanks to the utilization of alternative modes of action, different environmental preferences and induction of BCAs’ secondary metabolism due to competitive conditions. Red arrows demonstrate inhibition and green arrows represent induction.

4. Successful Solutions

Table 1 provides an overview of the biocontrol products available on the market. Although knowledge transfer from science to industry may not occur rapidly, and various factors impact the selection of products on the shelves, it offers valuable insights into the potential for success. In the literature, numerous examples of complex consortia involving different microorganisms for combating various diseases can be found ^[5]. However, this diversity is not fully reflected in the range of biocontrol products registered for crop protection (Table 1). Farmers have access to multiple approved biological control products based on only a limited number of different microbial consortia. The challenges in registering products with multiple active ingredients contribute to this situation. Additionally, it is noteworthy that the current solutions for biocontrol predominantly rely on the use of Trichoderma spp. ^[30], despite the wide array of microorganisms available for such purposes.

Trichoderma is an extensively studied genus for biological plant protection, and numerous studies focus on identifying new isolates with promising biocontrol potential ^[31]^[32]. The popularity of this genus stems from the number of modes of action utilized by Trichoderma spp. ^[33] and the resulting potential to not only protect plants from important pathogens ^[34] but also to produce spores with a high survival rate during formulation ^[35]. Additionally, their ability to promote plant growth enables the use of Trichoderma strains as both biocontrol agents and biofertilizers ^[36]. The researchers anticipate that this newly discovered Trichoderma species will quickly find their way onto the market of biocontrol products ^[37].

On the other hand, there are a wider range of species utilized in consortia for biofertilizers or biostimulants ^[38]^[39]. However, the legal status of these consortia, similar to biocontrol products, is in urgent need of revision ^[12]^[13]^[15]^[40]. Nevertheless, the relatively low number of biocontrol formulations can also be attributed to inadequate knowledge exchange between industry and academia ^[41]^[42]. Therefore, it is imperative to improve communication among scientists, plant protection product producers, farmers, and regulatory authorities. By enhancing collaboration, we can meet technological demands, address pressing agricultural challenges, and establish a safe and efficient environment for the registration of biocontrol products.

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