Abstract

Plants are exposed to diverse abiotic and biotic stimuli. These require fast and specific integrated responses. Such responses are coordinated at the protein and transcript levels and are incorporated into larger regulatory networks. Here, we focus on the evolution of transcriptional regulatory networks involved in plant–pathogen interactions. We discuss the evolution of regulatory networks and their role in fine-tuning plant defense responses. Based on the observation that many of the cornerstones of immune signaling in angiosperms are also present in streptophyte algae, it is likely that some regulatory components also predate the origin of land plants. The degree of functional conservation of many of these ancient components has not been elucidated. However, ongoing functional analyses in bryophytes show that some components are conserved. Hence, some of these regulatory components and how they are wired may also trace back to the last common ancestor of land plants or earlier. Of course, an understanding of the similarities and differences during the evolution of plant defense networks cannot ignore the lineage-specific coevolution between plants and their pathogens. In this review, we specifically focus on the small RNA regulatory networks involved in fine-tuning of the strength and timing of defense responses and highlight examples of pathogen exploitation of the host RNA silencing system. These examples illustrate well how pathogens frequently target gene regulation and thereby alter immune responses on a larger scale. That this is effective is demonstrated by the diversity of pathogens from distinct kingdoms capable of manipulating the same gene regulatory networks, such as the RNA silencing machinery.

Highlights

  • Plants face a plethora of different environmental stimuli throughout their lifetimes

  • The fine-tuning of plant immunity is achieved through the regulation of NBS-LRRs and through the regulation of independent immune signalling pathways. Some of those immunity-associated pathways are regulated by miRNAs [85,86]. These include the regulation of the auxin response factor (ARF)-encoding and other genes involved in auxin signalling by miRNA

  • These phasiRNAs have a target in Phytophthora and targeting impacts the virulence and sporulation of the pathogen [98]. (c) The function of the recently identified RNA silencing suppressor of Puccinia graminis f. sp. tritici (Pgt)

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Summary

Introduction

Plants face a plethora of different environmental stimuli throughout their lifetimes These can originate from abiotic and biotic sources and both can induce changes in plant gene and protein regulation. Altering transcription can allow pathogens to downregulate specific immunity-associated genes and to dysregulate multiple pathways simultaneously or to reprogram transcript investments away from immunity-associated pathways to growth-associated metabolism. That these mechanisms are effective is evident when looking across the diversity of pathogens—similar plant regulatory networks are often targeted convergently by pathogens of different kingdoms [19,20,21]. We will discuss how pathogens can exploit and shape such gene regulatory mechanisms to their own advantage

Evolution of Plant–Microbe Interaction Networks
The Evolution of microRNA-Mediated Regulation of Resistance Genes
Additional microRNAs Regulating Plant Immunity
The RNA Silencing Machinery as a Common Target of Pathogens
Findings
Conclusions

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