Plant pathogen effector proteins as manipulators of host microbiomes?

To understand the mechanisms underlying disease development in plants, molecular plant pathology research has mostly focused on the characterization of direct interactions between plant pathogens and their hosts. Collectively, this research has demonstrated that plants sense microbial invaders using various types of receptors (recently coined as ‘invasion pattern receptors’, IPRs) that sense microbial invasion and activate defence responses upon recognition of various molecular patterns that betray microbial invasion (recently coined as ‘invasion patterns’, IPs) (Cook et al., 2015). While these IPRs comprise cell surface-localized as well as intracellular receptors, IPs comprise microbe-associated molecular patterns (MAMPs) and other microbially secreted components, as well as host-derived damage-associated molecular patterns (DAMPs) (Cook et al., 2015). In order to successfully colonize their hosts and subvert immune responses, plant pathogens secrete molecules, so-called effectors, during attempted host ingress (Cook et al., 2015; Rovenich et al., 2014). According to the initial, narrowest, definitions, effectors are small, cysteine-rich proteins that function through the manipulation of plant immune responses. However, ongoing research has revealed that effectors may have other functions as well, such as roles in pathogen self-defence or liberation of nutrients from host tissues (Fatima and Senthil-Kumar, 2015; Rovenich et al., 2014). Moreover, it is generally appreciated that other types of microbially secreted molecules, such as secondary metabolites and small RNAs (Wang et al., 2016), may exert prototypical effector functions. Furthermore, it is accepted that effectors are not exclusively secreted by pathogens, as homologous molecules are employed by other types of symbiotic organisms, such as endophytes and mutualists, and even by saprophytes (Rovenich et al., 2014). Consequently, more recently, it has been proposed that rather than being small, cysteine-rich proteins that function through the manipulation of plant immune responses, effectors should be defined as microbially secreted molecules that contribute to niche colonization (Rovenich et al., 2014). Similar to other higher organisms, plants associate with a plethora of microbes that collectively form its microbiome. The phyllosphere comprises all aerial parts of the plant and is commonly colonized by diverse microbial communities (Vorholt, 2012). However, the most extensive microbial host colonization occurs below ground. The soil is a hotspot of microbial life, as microbial communities generally display great diversity and reach high densities. In particular, the narrow zone in close proximity to the roots, also known as the rhizosphere, is extremely microbe rich as it attracts microbes from the surrounding soil and allows them to thrive on plant-derived root exudates (Bais et al., 2006). Over recent years, the plant microbiome has gained increasing attention. Metagenomic studies have greatly enriched our knowledge of the composition of plant microbiomes and have led to its recognition as a key factor for plant health (Berendsen et al., 2012). The role of the rhizosphere microbiome in disease suppression has been particularly well described. It is currently generally appreciated that plants exploit root exudates to increase microbial activity on pathogen attack, and specifically attract beneficial microbes from the very diverse microbial community residing in the bulk soil (Berendsen et al., 2012). Consequently, plants select microbial communities around their roots that function as an additional layer of defence. One of the best-studied examples is the reduced incidence and severity of take-all disease caused by the fungus Gaeumannomyces graminis var. tritici which typically follows a severe disease outbreak in a monoculture of wheat or barley. This phenomenon is known as the so-called ‘take-all decline’ and is associated with the elevated presence of antagonistic Pseudomonas spp. that suppress the soil-borne fungal pathogen. Like all microbes, plant pathogens are under strong selective pressure exerted by co-inhabiting microorganisms. These microbiota members influence each other, both positively and negatively, through secreted molecules. A significant part of these molecules function through their antimicrobial activity and involve hydrolytic enzymes, antibiotics, toxins and volatiles (Compant et al., 2005). In addition, microbes strongly compete with each other for nutrients and essential elements. Importantly, these processes often involve secreted molecules. Siderophores and haemophores are well-studied molecules secreted by plants and soil microbes to scavenge metal ions and facilitate their uptake *Correspondence: Email: bart.thomma@wur.nl †These authors contributed equally to this work.