Effectors of Filamentous Plant Pathogens: Commonalities amid Diversity

Abstract

Fungi and oomycetes are filamentous microorganisms that include a diversity of highly developed pathogens of plants. These are sophisticated modulators of plant processes that secrete an arsenal of effector proteins to target multiple host cell compartments and enable parasitic infection. Genome sequencing revealed complex catalogues of effectors of filamentous pathogens, with some species harboring hundreds of effector genes. Although a large fraction of these effector genes encode secreted proteins with weak or no sequence similarity to known proteins, structural studies have revealed unexpected similarities amid the diversity. This article reviews progress in our understanding of effector structure and function in light of these new insights. We conclude that there is emerging evidence for multiple pathways of evolution of effectors of filamentous plant pathogens but that some families have probably expanded from a common ancestor by duplication and diversification. Conserved folds, such as the oomycete WY and the fungal MAX domains, are not predictive of the precise function of the effectors but serve as a chassis to support protein structural integrity while providing enough plasticity for the effectors to bind different host proteins and evolve unrelated activities inside host cells. Further effector evolution and diversification arise via short linear motifs, domain integration and duplications, and oligomerization

An RXLR effector PlAvh142 from Peronophythora litchii triggers plant cell death and contributes to virulence

“…In plants, perception of PAMPs or effectors activates a complicated signal transduction network, including mitogen‐activated protein kinase (MAPK) cascades, and/or chemical signalling by plant hormones and transcriptional regulation via transcription factors (Pitzschke et al , ; Wang et al ., ). The immune activation culminates in a series of physiological changes in the plant, such as reactive oxygen species (ROS) production, cell wall fortification, and the localized rapid cell death known as the hypersensitive response (HR) (Ingle et al , ; Franceschetti et al , ).…”

The emergence of the multi‐species NIP1 effector in Rhynchosporium was accompanied by high rates of gene duplications and losses

“…Recent studies showed that hybridization and introgression enabling pathogens to expand their host ranges is more common than previously thought (Lemaire et al, 2015;Depotter et al, 2016;Menardo et al, 2016). In comparison to a large number of evolutionarily young effectors, relatively few effectors are conserved across fungal taxa (Kohler et al, 2016;Franceschetti et al, 2017). Coevolution between hosts and pathogens led to the diversification of specific fungal effectors across pathogen lineages (Jiang et al, 2008;Huang et al, 2014;Sperschneider et al, 2014).…”

The WY domain in the Phytophthora effector PSR1 is required for infection and RNA silencing suppression activity

“…Furthermore, three PSR1‐like effectors (PcPSR1L, PiPSR1L and PpPSR1L) found in Phytophthora species shared conserved biological functions with PSR1, but did not bind to PINP1 or PINP1 homologs in their host plants in the Y2H assay (Fig. S4a,b), suggesting that PSR1 and PSR1‐like effectors share a similar function and conserved WY domain; however, they are not real orthologous effectors, they might suppress RNA silencing and contribute to infection by binding to different host targets (Franceschetti et al ., ). Together, these findings expand our understanding of oomycete WY domain effectors, which possess structural flexibility and diverse biological functions to suppress plant immunity.…”

“…Collectively, these findings suggest that rapid evolution of the protein sequence encoding the WY motif led to diversification of these effectors. This in turn may have facilitated the acquisition of new effector functions and evasion from host immunity pathways (Franceschetti et al ., ).…”