Insect effectors and gene-for-gene interactions with host plants

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Highlights

  • Important insect pests continue to conform to the gene-for-gene hypothesis.

  • New insect NB-LRR-encoding resistance genes have been identified.

  • Insect avirulence genes have been cloned.

  • Large families of effector-encoding genes are present in gall midge genomes.

Within the context of the four-phase model of plant immunity, gene-for-gene interactions have gained new relevance. Genes conferring resistance to the Asian rice gall midge (Orseolia oryzae) and the small brown planthopper (Nilaparvata lugens) have been cloned in rice (Oryza sativa). Mutations in insect avirulence genes that defeat plant resistance have been identified and cloned. Results are consistent with both the gene-for-gene hypothesis and the new model of plant immunity. Insect resistance genes encode proteins with nucleotide binding sites and leucine-rich repeats. Insects use effectors that elicit effector-triggered immunity. At least seven-percent of Hessian fly genes are effector encoding.

Graphical abstract

The gene-for-gene interaction is a battle whose outcome depends on genetic variation at specific resistance genes (R/– and r/r) and cognate parasite avirulence genes (A/– and a/a). Parasites use a host of effector proteins, represented as small shapes, to attack specific targets (T1 and T2) in plant cells. In the red panel, resistance proteins (R) that perceive the presence of a cognate effector (E) elicit effector-triggered immunity. In the green panels, perception fails due to the absence of R or E, and susceptibility results.

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Introduction

The gene-for-gene (GFG) hypothesis has been a major focus of investigation in plant pathology [1]. It weathered intensive experimental examination, and from both economic and mechanistic standpoints, it is still recognized as an important component of plant-associated interactions when it is observed [2, 3]. However, recent improvements in our understanding of plant induced immunity have transformed the GFG hypothesis [4]. A new four-phased model holds that plant parasites in every taxon use effector proteins as virulence factors to modulate plant cell biology and that plants perceive and respond to effector activity using resistance (R) proteins. This model has had a unifying effect within those communities that study plant-associate biological interactions and evidence of arthropod and arthropod-associated effectors is now substantial; some of the more interesting examples are referenced here: [5, 6•, 7, 8••, 9•, 10, 11••, 12•]. New methods for arthropod effector discovery have also highlighted the importance of fully sequenced insect genomes [13, 14]. As a consequence of these activities, several recent and comprehensive reviews that describe the roles effectors play across a host of plant–arthropod interactions have been published [15, 16, 17, 18, 19, 20, 21]. This review is limited to a brief description of the transition from the GFG concept to the effector-based paradigm in entomology. Arthropod interactions that conform to both the classical GFG hypothesis and the new paradigm are the central focus.

Section snippets

The GFG hypothesis

Plant resistance (R) genes protect plants from the damage caused by specific pathogens and pests. As such, they have long been recognized as a valuable natural resource in agriculture. Their major limitation has been their durability in monoculture, as their efficacy is typically lost over time due to the evolution of ‘virulent’ pathogens and pests. Many plant pathogenic microorganisms are genetically tractable. This makes it possible to examine the genetics of both resistance in the plant and

The new model

Currently, plant pathologists recognize two related categories of immunological mechanisms: basal and R-gene-mediated immunity [4]. Basal immunity uses transmembrane pattern recognition receptors (PRRs) that elicit pathogen-triggered immunity (PTI) when they detect pathogen-associated molecular patterns (PAMPs). PAMPs are essential, highly conserved, slowly evolving molecules that exist across a broad range of taxa. PRRs are therefore capable of protecting the plant from most non-adapted

The Asian rice gall midge (RGM, Orseolia oryzae; Diptera: Cecidomyiidae)

Rice (Oryza sativa), the primary host of RGM, is a model monocot for functional genomics [36]. This makes the rice–RGM interaction a particularly attractive system for studies focused on insect-induced plant-gall formation. RGM larvae attack rice cells at the apical shoot meristem where they introduce substances that induce the formation of a tube-like gall, called a silver shoot. The gall supplants grain development [37]. Considerable effort has been made to identify rice genes responding to

The small brown planthopper (BPH, Nilaparvata lugens; Homoptera: Delphacidae)

The BPH is one of the most important insect pests of rice in Asia. It causes serious physical damage to the plant and is a vector of viral disease. The insect is fully adapted to only rice and cutgrass (Leersia hexandra). Modern and innovative approaches focused on rice–BPH interactions are revealing the genetic and metabolic responses of the plant in both susceptible and resistant interactions [52, 53, 54•, 55]. These indicate the insect shifts the metabolic profile of the plant in susceptible

The Hessian fly (HF, Mayetiola destructor; Diptera: Cecidomyiidae)

The HF is a gall-forming parasite of wheat (Triticum spp.) and the first notable invasive insect pest in the United States [61]. At least 35 different HF R genes, named H1-H34 and Hdic, have been identified genetically [62, 63]. Although no HF R genes have yet been cloned, several have been mapped within clusters of NB-LRR-encoding genes [64, 65]. A sequenced wheat genome [66] and new approaches to R gene mapping promise to remedy this deficiency [67, 68, 69].

Putative HF effector-encoding

Conclusions and future directions

In the context of the new four-phase plant immunity model, plant–arthropod GFG interactions continue to provide a window through which plant susceptibility, plant resistance and arthropod virulence can be examined. Ongoing and future investigations will focus on identifying the targets of effector proteins. These efforts will focus on the identification of common targets so that mechanisms of control might be developed against multiple plant pests. We can anticipate that effectors will take new

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The author gratefully acknowledges support for this work from USDA-NIFA AFRI Grant 2008-35302-18816, USDA-NIFA Grant AFRI2010-03741, and a fellowship supported by Fulbright-Colombia.

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