Translational biology of nematode effectors. Or, to put it another way, functional analysis of effectors – what’s the point?

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There has been a huge amount of work put into identifying and characterising effectors from plant-parasitic nematodes in recent years. Although this work has provided insights into the mechanisms by which nematodes can infect plants, the potential translational outputs of much of this research are not always clear. This short article will summarise how developments in effector biology have allowed, or will allow, new control strategies to be developed, drawing on examples from nematology and from other pathosystems.

Nematology

International Journal of Fundamental and Applied Nematological Research

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References

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Figures

  • The zigzag model in context of plant-nematode interactions. In 2006, Jones & Dangl established the zigzag model to illustrate the quantitative output of the plant immune system in response to microbes but the concept has proven to be more broadly applicable to pests and pathogens. Components of the zigzag model that have been identified in plant-nematode interactions are shown in bold red type. The conceptual arms-race between host and pathogens can be depicted in four major phases. In phase I, conserved pathogen-associated molecular patterns (PAMPs; represented by the letter P in the pink forms) are recognised in plants by cell surface pattern-recognition receptors (PRRs) leading to induction of PAMP-triggered immunity (PTI). The only PAMP from plant-parasitic nematodes identified to date is a pheromone, the ascaroside 18 (Ascr#18; Manosalva et al., 2015), but its cognate PRR is not yet known. In phase II, adapted pathogens secrete effectors into the host that interfere with PTI, leading to effector-triggered susceptibility (ETS). Several nematode effectors (represented by the letter E in the blue clouds) have been characterised that can suppress PTI responses (see review by Mantelin et al., 2015). In phase III, particular effectors (represented in the blue clouds by the letter A for ‘Avirulence factors’) are detected by a second layer of plant resistance receptors (products of the R genes), activating effector-triggered immunity (ETI), which in most cases leads to the induction of a hypersensitive plant cell-death reaction (HR). Very few nematode R genes have been cloned (see review by Goverse & Smant, 2014) and only one avirulence effector has been identified so far, the Globodera pallida RBP-1 SPRYSEC effector AvrGpa2 (Sacco et al., 2009). In phase IV, as pathogen and host coevolve new effectors and R genes, susceptibility or resistance predominate in turn. Avirulence factors (A) maybe lost or modified to avoid recognition by cognate R proteins (as is the case for RBP-1) and perhaps new effectors are gained (B, C, D) that are able to suppress ETI. Such activity has been demonstrated for the ubiquitin carboxyl extension protein GrUBCEP12 and many SPRYSEC effectors (see review by Mantelin et al., 2015). Based on a figure in Smant & Jones (2011).

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  • Effector-mediated cell death in plants. A, B: A typical hypersensitive reaction is elicited by recognition of Globodera pallida effector Gp-RBP-1 (StGpa2-cognate avirulence factor) in Agrobacterium tumefaciens-based transient expression assay in potato accession Cara containing the StGpa2 resistance gene (A) or by transient co-expression of both StGpa2 and Gp-RBP-1 in Nicotiana benthamiana leaf (B). Conversely, eGFP control in potato and either StGpa2 or Gp-RBP-1 expressed alone in N. benthamiana do not induce a response in plants. Transient expressions were performed with untagged constructs for StGpa2, Gp-RBP-1 (Sacco et al., 2009) and eGFP control as described in Mei et al. (2015), by infiltration of A. tumefaciens strains at an OD600nm of 0.5. Symptoms observed under white light 7 days post infiltration. Infiltrated areas are indicated by dashed circles. C, D, E: Effectors also participate in non-host resistance. C: Wild-type Pseudomonas syringae pathovar tomato (Pst) strain DC3000 can barely infect N. benthamiana, whilst Pst mutant strain CUCPB5460 lacking the type-III effector HopQ1-1 is able to cause disease in the non-host plant (demonstrated by Wei et al., 2007). Necrotic disease symptoms observed 7 days after bacteria infiltration at OD600nm of 1.10−4 in 10 mM MgSO4 solution. Infiltrated areas are circled. D, E: Cell death is triggered specifically in non-host N. sylvestris (D) by a Phytophthora infestans RXLR effector (Pi-A) while transient expression of the same effector in the host plant N. benthamiana (E) does not induce symptoms in the leaf. Another effector (Pi-B) as well as the Td-Tomato construct used as control do not induce symptoms. Conversely, a typical hypersensitive reaction is elicited by recognition of P. infestans effector Pi-Avr3a in the presence of the potato resistance protein StR3a in N. benthamiana leaf (E). Effectors and controls in binary vector pGRAB were transformed in A. tumefaciens GV3101 and agro-infiltrated at an OD600nm of 0.1 in Nicotiana leaves (Mantelin & Hein, pers. comm.). Symptoms were observed under white light 7 days post inoculation. Infiltrated areas are indicated by dashed circles.

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