Plants versus pathogens: an evolutionary arms race

Abstract

The analysis of plant-pathogen interactions is a rapidly moving research field and one that is very important for productive agricultural systems. The focus of this review is on the evolution of plant defence responses and the coevolution of their pathogens, primarily from a molecular-genetic perspective. It explores the evolution of the major types of plant defence responses including pathogen associated molecular patterns and effector triggered immunity as well as the forces driving pathogen evolution, such as the mechanisms by which pathogen lineages and species evolve. Advances in our understanding of plant defence signalling, stomatal regulation, R gene-effector interactions and host specific toxins are used to highlight recent insights into the coevolutionary arms race between pathogens and plants. Finally, the review considers the intriguing question of how plants have evolved the ability to distinguish friends such as rhizobia and mycorrhiza from their many foes.

Fig. 1

Activity of the Pseudomonas syringae pv. tomato effector protein AvrPtoB in suppressing both PAMP triggered immunity (PTI) and effector triggered immunity (ETI). The N-terminal kinase interaction domain (1–307) suppresses the activity of PTI. Plants have evolved the resistance protein Pto to recognise AvrPtoB residues 307 and 387 and to activate ETI through the host proteins Prf and Fen. AvrPtoB acquired a C-terminal E3 ubiquitin ligase domain (400–550) that promotes degradation of Fen and therefore inhibits ETI triggered by Pto binding.

Fig. 2

Interaction of pathogen and host components, and the selection pressures to which they may be exposed. Effectors from biotrophs suppress PTI in the host, which may, in turn, activate resistance (ETI) through direct interaction with host R proteins or through R protein detection of effector activity. Effectors or host specific toxins (HST) from necrotrophs activate PCD (or HR) through interaction with host R proteins, thereby inducing susceptibility in the host. The host R proteins may therefore be under opposing selection pressures to (1) multiply in order to detect additional biotroph effectors, or their activity, and (2) restrict the number of genes to minimise targets for necrotroph HSTs and effectors. Pathogen associated molecular patterns (PAMP) and host pattern recognition receptors (PRR) are under diversifying selection to evade and facilitate detection respectively. Effectors from biotrophs may be under pressure to diversify to avoid detection by host R proteins but maintain function, while effectors and HSTs from necrotrophs may be under pressure to maintain detection by host R proteins. Host R proteins involved in direct interaction with effectors may be under selection pressure to diversify to detect changing biotroph effectors and avoid necrotroph HSTs. R proteins involved in indirect interaction with effectors, e.g. ‘guarding’ host proteins, may be under stabilising pressure to maintain interaction between R protein and guarded host protein or under pressure to coevolve with the guarded protein, which may itself be under pressure to avoid interaction with effectors. The figure is based on references cited in the text.

Fig. 3

General signalling responses during plant interactions with symbionts and pathogens. Rhizobia and AM fungi produce signals (Nod factor for Rhizobia and Myc factor for AM fungi) that are perceived by the plant’s cognate receptor(s). These signals activate downstream responses via a common symbiosis (SYM) pathway (grey box). The CCamK may be differentially perceiving or transmitting the calcium signal, leading to activation of rhizobia and AM specific transcription factors and subsequent downstream responses. For more details of AM and rhizobial symbioses, refer to the recent reviews of Parneske (2008) and Oldroyd et al. (2009). Plant pathogens are also perceived by the plant by receptors and during incompatible interactions, they trigger many downstream responses, including the production of defence signalling hormones such as ET, SA and JA. Interestingly, certain rhizobia and Nod factors can negatively regulate production or accumulation of these hormones (Soto et al. 2006; Penmetsa et al. 2008). ET, SA and JA negatively regulateCa²⁺ spiking and other Nod factor induced responses (Ding and Oldroyd 2009). Auxin and cytokinin signalling pathways can be manipulated by certain pathogens to facilitate infection processes. They also regulate nodule specific transcription factors and are required for nodule organogenesis (Frugier et al. 2008; Grunewald et al. 2009). AM, arbuscular mycorrhiza; LRR-RLK, leucine rich repeat receptor-like kinase; CCamK, calcium-calmodulin dependent protein kinase; ET, ethylene; JA, jasmonic acid; SA, salicylic acid; PPA, pre-penetration apparatus; TF, transcription factors.