Herbivorous insects, likewise, other organisms, are exposed to diverse communities of microbes, including bacteria, fungi, viruses, Oomycota, from the surrounding environment (Hammer et al., 2017; Gurung et al., 2019). Many microbes acquired by insects via the diet or soil may not impact insect hosts (Hammer et al., 2017; Zhao et al., 2019). However, some can colonize insects and share with them symbiotic (mutualism, commensalism, and parasitism) or pathogenic relationships. Insects-associated microbes can have diverse roles in mediating insect interactions with plants, other insects, or other microbes (Chung et al., 2013; Mason et al., 2019). It has been shown that insect’s oral secretions or regurgitants contain diverse microbial communities, effectors, proteins, and small molecules that can affect plant defense response to insect feeding (Figure 1; Acevedo et al., 2017; Gedling et al., 2018).

Insects can be considered as both pests and reservoirs or even vectors of plant pathogens because they damage the plant directly by feeding and indirectly by delivering plant pathogens to wounded places, from where pathogens spread throughout the plant (Figure 1; Agrios, 2008).

Hemipteran insects, including leafhoppers and psyllids, are considered by far the most important vectors of bacteria (Perilla-Henao and Casteel, 2016) due to their wide host range and rapid reproduction. In turn, whiteflies and aphids are considered important vectors of viruses (Jones, 2003; Perilla-Henao and Casteel, 2016; Ghosh et al., 2017).

Coleoptera is the largest insect order accounting for over 360,000 species, which constitutes 40% of the known insect species in the world. Beetles are not mentioned in the first place as disease vectors, but some of them cause considerable damages through the transmission of plant pathogens. Here, we present an overview of beetles as vectors of plant pathogens, including viruses, bacteria, nematodes, fungi, and Oomycota, which are responsible for developing plant diseases with a significant impact on crop yield, and quality (Salaau Rojas, 2013; Pan et al., 2018). The successful management of plant diseases requires knowledge on the plant–pathogen–insect vector interactions which is fundamental to reduce the occurrence and spread of the plant diseases, and to limit yield losses as well as the amount of used plant protection chemistry which is very important for the environment.

Plants are rooted and motionless, and thus the pathogen must be delivered to them (Agrios, 2008). Natural plant openings or wounds are necessary for the pathogen to penetrate the plant. Insects are considered part of the disease complex because feeding wounds constitute the point of entry for plant pathogens (Willsey et al., 2017). Insects are frequently involved in the transmission of plant pathogens from one plant or organ to another. The way of transmission depends on both, the insect species, and pathogens. In some cases, insects carry pathogens incidentally, without any special relationship between them. For instance, the bacterial and fungal spores are often sticky and cling to the insect’s body during feeding or walking through a plant area where pathogens are deposited. The insect can also acquire the pathogen with food. Ingested pathogen circulates within the insect body, reaches the salivary glands, mouthparts, and finally enters the plant host through the wounds resulting from insect feeding. Overall, insects can carry plant pathogens externally on their legs, mouthparts, bodies, and internally in their digestive tract, and hemocoel (Figure 2; Agrios, 2008; Gedling et al., 2018).

Insects select plant hosts based on the number of sensory cues including visual (e.g., leaf color), olfactory (emission of volatile organic compounds – VOCs; Heard, 1999; Mauck et al., 2014), gustatory, or tactile stimuli (Heard, 1999). Numerous studies suggest that plant pathogens, including viruses, induce changes in plant phenotypes, their palatability, and nutrients components, to enhance visiting of the plants by insect vectors and to increase pathogens acquisition and transmission to other plants (Lieutier et al., 2009; Chesnais et al., 2020). It was reported that beetle vectors have a preference for pathogen-infected plants (Musser et al., 2003). For instance, the induction of changes in the plant VOCs enhances the aggregation of insect vectors on infected plants (Mauck et al., 2010). This phenomenon is observed in many insect species, including these belonging to the Coleoptera order. Pathogens can also affect the quality of the primary plant host as the resource for the insect vector (Mauck et al., 2010; Chesnais et al., 2019) and can have a direct effect on insect behavior (Figure 2; Coplin et al., 2002; Mann et al., 2012; Shapiro et al., 2012). In addition, the increased attraction of insect vectors to infected plant hosts has been documented in response to visual changes in plant phenotype elicited by plant pathogens (Chesnais et al., 2020). Musser et al. (2003) indicated that Epilachna varivestis (Coccinellidae) prefers to feed on visually changed plants infected by bean pod mottle virus (BPMV, Secoviridae) and southern bean mosaic virus (SBMV, Solemoviridae).

Several plant viruses are spread by plant contact or their vegetative reproduction, but many of them depend on vectors. More than 70 species of beetles (Smith et al., 2017) are known to transmit viruses that infect economically important vegetables and grain crops. It is estimated that beetles transmit approximately 11% of insect-borne viruses (Smith et al., 2017; Bhat and Rao, 2020). Beetle vectors of plant viruses belong to Chrysomelidae, Coccinellidae, Curculionidae, Meloidae families (Gergerich, 2001; Fereres and Raccah, 2015) and have a unique mode of transmission of at least six groups of plant virus genera: Machlomovirus, Bromovirus, Carmovirus, Comovirus, Sobemovirus, and Tymovirus (Scott and Fulton, 1978; Gedling et al., 2018). Mechanisms of virus acquisition and transmission are associated with the fact that most of the beetle vectors eat plant cells between the leaf veins and regurgitate during feeding, bathing their mouthparts with sap and virus particles, therefore beetle-associated viruses can be deposited into a chewing wound. Virus particles are translocated in the xylem elements to parts of the plants away from the site where they were deposited by an insect (Gergerich and Scott, 1988, 1991; Gedling et al., 2018).

Noncirculative viruses can be transmitted in a semipersistent manner by many groups of insects including beetles (Raccah and Fereres, 2009). These viruses are retained in the foregut, a chitinous anterior region of the insect alimentary canal (Mauck et al., 2018). Some viruses move into the beetle hemolymph immediately after ingestion (Fereres and Raccah, 2015), wherein probably virus is retained for extended periods (Fulton and Scott, 1977; Scott and Fulton, 1978). It was indicated that a beetle could get viruses after a single bite of plant tissue, but the efficiency of acquisition increases with more extensive feeding (Fulton and Scott, 1977). Beetles can acquire and transmit the virus after feeding for a few seconds and can retain the virus from 1 to 10days (Agrios, 2008), depending on the beetle species. For instance, E. varivestis retains cowpea severe mosaic virus (CPSMV, Secoviridae) for 1day, whereas Cerotoma trifurcate (Chrysomelidae) retains the same virus for several days (Fereres and Raccah, 2015), and in turn, Diabrotica balteata (Chrysomelidae) vectors bean rugose mosaic virus (BRMV, Secoviridae; Table 1) for 3days (Fulton and Scott, 1977).

Adult beetles and, in some cases, also larvae are very important vectors of plant viruses (Table 1). Nault (1978) found that larvae of Oulema melanopus (Chrysomelidae) transmitted maize chlorotic mottle virus (MCMV, Tombusviridae) more efficiently in comparison with adults (Nault, 1978). Additionally, O. melanopus, as well as Oulema gallaeciana (Chrysomelidae), can transmit effectively cocksfoot mottle virus (CfMV, Solemoviridae; Catherall, 1987; Table 1) for up to 15days after its acquisition. CfMV is transmitted more efficiently by adults than in the larval stage.

BPMV, a widespread pathogen in the major soybean-growing areas, can be effectively transmitted by several species of the Chrysomelidae family (Table 1; Giesler et al., 2002). BPMV infection can lead to yield reduction and a deterioration in the quality of the soybean seeds. Reduction of crop yield depends on the time of virus infection relative to plant development (Gergerich and Scott, 1996; Gergerich, 1999) and can range between 36 and 52% (Hopkins and Mueller, 1984).

Epilachna varivestis is considered to be a severe pest among others of soybean (Fan et al., 1992; Nakamura and Chavez, 2007). Gedling et al. (2018) showed that E. varivestis regurgitant is fundamental to the specificity of beetle transmissible viruses. This pest can transmit several plant viruses, including cowpea severe mosaic (CPMV, Secoviridae; Fulton and Scott, 1974), SBMV (Musser et al., 2003), or blackgram mottle virus (BMoV, Tombusviridae; Scott and Fulton, 1978; Scott and Phatak, 1979; Table 1).

Plant bacterial disease can be manifested by several types of symptoms, including blights, galls, and soft rots. Bacteria can be present on the plant surface in droplets and sticky exudates released through cracks, wounds in the infected area, or through natural openings (including stomata, nectar rhodes, and hydathodes). Insects can be attracted by sweet bacterial exudates. During insect feeding, bacteria stick to mouthparts and other parts of the insect body (Agrios, 2008). Some bacteria obtained with plant material migrate to the insect gut epithelium and are deposited on wounds through infected fecal droppings (Mitchell and Hanks, 2009; Figure 2). For the development of a new bacterial infection, a fresh wound or the natural opening and enough moisture in the plant surface are needed. Thanks to this, bacteria multiply and move into the plant, and bacterial infection is developing (Agrios, 2008).

There are much more currently known and described beetles as vectors of viruses and fungal pathogens than beetles that transmit bacterial pathogens. However, metagenomic studies, including microbiome analyses, may soon provide a lot of valuable information about beetles as reservoirs or even vectors of other plant pathogenic bacteria.

The transmission of fungi by insects occurs usually accidentally. Insects can be contaminated with the fungus or its spores during visiting infected plants, externally (for instance during walking) or internally (through feeding). Spores and mycelia adhering to insect bodies or ingested by insects are transported to healthy plant tissues (Willsey et al., 2017; Figure 2). Some of the beetles have special organs, namely mycangia, for carrying fungi (Amman, 1983).

Epitrix sp. (Chrysomelidae) are considered a serious pest of various species of plants. For instance, Epitrix tuberis is primarily associated with members of Solanaceae family, especially with potato plants (Malumphy et al., 2016). Both adults and larvae of E. tuberis are harmful to plants. It was noted that E. tuberis may enhance dispersal of the Phytophthora infestans (Peronosporacea; Leach, 1940; Table 1), causing the potato blight. Interestingly, E. tuberis can act as a multivector. The role of this insect in spreading various plant pathogens was reported in the past in the literature. It was indicated that E. tuberis can transmit bacteria Raltsonia solanacearum (Burkholderiaceae) responsible for potato brown rot, Streptomyces scabiei (Streptomycetaceae) causing potato scab, and potato spindle tuber viroid (PSTV, Pospiviroidae; Table 1; Leach, 1940). Generally, all species of Epitrix sp. can transmit plant pathogens that may have a negative impact on crop yield.

Transmission of nematodes can take several ways including direct contact between plant roots, through contaminated tools, or insect vectors. Generally, nematodes transmitted by beetles migrate to trees through wounds caused by beetle feeding and through the oviposition slits in the bark (Agrios, 2008). Healthy plants may also become contaminated by nematodes through insect feces (Bierhals et al., 2018).

The transmission of plant pathogens can affect all the components of the pathogen – plant – beetle vector system. The components of this system are additionally affected by environmental factors and the plant protection strategies aimed to reduce the spread of pathogens and pests. In general, the consequences of these three-way interactions are manifold. The examples are listed below.

For the plant, both beetle feeding and damages caused by pathogens are harmful and can have a negative impact on the crop quantity and quality as well as plant growth and development. Sometimes damages may result in the death of the plant. Importantly, in this situation, the plant has to deal with two stressors (pathogens and beetles) at the same time, and fine-tune its defence response at the lowest possible cost of energy (Wielkopolan and Obrępalska-Stęplowska, 2016).

The microbes influence many aspects of insect host life, including adaptation to new environmental niches or plant hosts (Henry et al., 2021), which is beneficial for both insects and microorganisms. From the ecological point of view, the plant pathogens dispersal by vectors is a key factor of distribution and incidence of some plant diseases. Insect vectors may benefit from insect-associated microorganisms (Musser et al., 2003) because microbes can modulate plant defence mechanisms in favour of their insect vector (Paine et al., 1997; Wielkopolan and Obrępalska-Stęplowska, 2016; Pan et al., 2018). It was shown that insect-associated bacteria can cause that the plant defence against insects is milder. For instance, it was indicated that O. melanopus-associated bacteria suppressed the expression of wheat genes encoding of harmful to insects serine protease inhibitors (Wielkopolan et al., 2018). This situation might also apply to pathogens.

Vector-borne pathogens can also alter the phenotype of the plant, including its palatability and quality to enhance the aggregation of insect vectors on the infected plant (Mauck et al., 2010). For instance, larvae of E. varivestis grow faster on virus-infected leaf tissue. This suggests that the virus – E. varivestis relationship might be potentially beneficial for insects since larger insects typically have a higher reproductive potential and they are more likely to escape natural enemies, which increases the chances of transmitting pathogens (Musser et al., 2003).

Beetles with chewing mouthparts disrupt tissue continuity during feeding and wounding caused by them can constitute a point of entry to plant pathogens. This article presented examples and mechanisms of phytopathogen transmission by beetles. For a plant disease to initiate and develop, the common host for pest and pathogen is required as well as the synchronization between the plant development and the appearance of beetle vector and the pathogen. Climate changes may affect the spread of new alien species of beetle and pathogens to new areas, as a result, new trophic relationships between them can be established. There are still significant gaps in our understanding of beetle-plant-pathogen interactions and their consequence for disease incidence and pathogen spread. Therefore, the main challenges for future research are to understand the mechanism of (a) the acquisition and transmission of the plant pathogens by the insect vectors, (b) plant defense response against insects and associated with them pathogens, and (c) the impact of the pathogen on its insect vector. Research at the molecular level and metagenomic studies may provide a lot of valuable information about three-trophic interactions. Obtained knowledge should provide a more holistic understanding of disease dynamics and will allow for guiding effective monitoring and developing effective tools to limit pathogen transmission and disease incidence.

AO-S and BW: conceptualization, literature review, data analysis, and writing – original draft preparation. BW, MJ, and AO-S: writing – review and editing. AO-S: funding acquisition. All authors contributed to the article and approved the submitted version.

This work was supported by the Polish National Science Centre within the UMO-2016/23/B/NZ9/03503 agreement.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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