Research Article: Cooperation and Conflict in the Plant Immune System

Date Published: March 17, 2016

Publisher: Public Library of Science

Author(s): Eunyoung Chae, Diep T. N. Tran, Detlef Weigel, Cyril Zipfel.


Partial Text

Genetic studies of plant immunity have been tremendously influenced by Flor’s gene-for-gene hypothesis, which posits that a single host resistance gene is matched by a single effector gene from a specific pathogen strain. It was thus unexpected when two NLR genes that are located immediately adjacent to each other in the Arabidopsis thaliana genome were found to cooperatively confer resistance to the Hyaloperonospora arabidopsidis ex parasitica isolate Cala2 [1]. Since then, several more such pairs have been discovered, with one member often encoding other protein domains in addition to the canonical “NLR” moieties [2]. Two good examples are the RPS4/RRS1 protein pair, which endows A. thaliana with resistance to both bacterial and fungal pathogens, and the RGA4/RGA5 pair in rice, which confers resistance to specific races of the fungus Magnaporthe oryzae. The dual genetic requirement translates into direct physical interaction, with RPS4 and RRS1 (as well as RGA4 and RGA5) forming heterodimers [2–5]. In both cases, one protein, RRS1 or RGA5, contains an additional specific recognition domain at the C-terminus [2,6]. Binding of a pathogen effector protein to this domain alters the interaction with its respective partner, RPS4 or RGA4, and thereby leads to host immune signaling. The addition of an effector-binding domain to one of the NLR proteins may have facilitated expansion of recognition specificity, since the evolution of the recognition domain is not necessarily coupled to constraints acting on the NLR moiety.

Another common type of protein–protein interaction in the plant immune system is the one between immune receptors (often NLR proteins) and host clients that are direct targets of pathogen effectors. From the host perspective, pathogen-targeting of the NLR clients may be undesirable when it leads to enhanced pathogen virulence; in this case, clients are considered NLR-guardees. In other cases, however, targeting may be desirable, because the NLR-clients are merely decoy versions of true targets [10]. The interaction between the NLR-guard and its guardee/decoy mediates indirect recognition of pathogen effectors [9]. Similar to the NLR–NLR interaction discussed above, the guardee/decoy partner modulates signaling of the NLR protein; if the guardee/decoy is compromised, either by effector-dependent modification or mutation, immune responses are activated. This can also occur when the NLR (or a non-NLR immune receptor) and its host client have not coevolved and are mismatched [11,12]. Such spontaneous, pathogen-independent autoimmune reactions can be observed in many genetic intra- and interspecific crosses, a phenomenon that breeders have known as hybrid necrosis for decades [13].

Individual NLR genes can incur substantial fitness costs in the absence of the pathogen they recognize, not only in the greenhouse but also in the field (e.g., [20]). Ideally, immune receptors would, of course, be perfectly “off” in the absence of a trigger. The fact that there are apparent NLR effects, even without pathogen effectors, points to a biochemical trade-off between the robustness of the on/off switch and sensitive, highly specific activation of immune receptors. Still, knocking out common components of NLR downstream signaling does not lead to enormous increases in growth. One can think of several explanations for why this is the case; for example, it could be that NLR genes with substantial fitness costs are the exception, with aberrant NLR activity being often suppressed by other NLR genes, or that there is an inherent limit to the resources that will normally be diverted to defense upon NLR activation. No matter what the right answer is, we certainly need a better understanding of the trade-offs both within the immune system and between immunity and growth. One approach is to investigate biochemical details of immune receptor activation, and of the connection between immune receptors and hormone signaling [21]. Similarly, phenotypic differences among different autoactive NLR mutants (e.g., [22]) and between different hybrid necrosis cases [15] may be illuminating in this regard.




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