Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation

Abstract

Biotic stress has a major impact on the process of natural selection in plants. As plants have evolved under variable environmental conditions, they have acquired a diverse spectrum of defensive strategies against pathogens and herbivores. Genetic variation in the expression of plant defence offers valuable insights into the evolution of these strategies. The 'zigzag' model, which describes an ongoing arms race between inducible plant defences and their suppression by pathogens, is now a commonly accepted model of plant defence evolution. This review explores additional strategies by which plants have evolved to cope with biotic stress under different selective circumstances. Apart from interactions with plant-beneficial micro-organisms that can antagonize pathogens directly, plants have the ability to prime their immune system in response to selected environmental signals. This defence priming offers disease protection that is effective against a broad spectrum of virulent pathogens, as long as the augmented defence reaction is expressed before the invading pathogen has the opportunity to suppress host defences. Furthermore, priming has been shown to be a cost-efficient defence strategy under relatively hostile environmental conditions. Accordingly, it is possible that selected plant varieties have evolved a constitutively primed immune system to adapt to levels of disease pressure. Here, we examine this hypothesis further by evaluating the evidence for natural variation in the responsiveness of basal defence mechanisms, and discuss how this genetic variation can be exploited in breeding programmes to provide sustainable crop protection against pests and diseases.

Figure 1

Priming of basal resistance provides protection against virulent pathogens. (A) Basal resistance against virulent pathogens results from a residual level of host defence after defence suppression by disease‐promoting pathogen effectors (blue arrows). Priming of basal resistance leads to a faster and stronger induction of basal defence mechanisms, providing enhanced resistance against the invading pathogen. In most cases, priming of basal resistance cannot prevent the delivery of pathogen effectors entirely, and thereby only slows down the introgression of the pathogen (‘moderately primed defence response’). However, if the primed defence response precedes the delivery of pathogen effectors, this defence strategy can prevent pathogen infection and provide full protection against otherwise virulent pathogens (‘strongly primed defence response’). Red plant cells indicate the expression of basal defence mechanisms. (B) The ‘zigzag’ model describes basal resistance as the sum of pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI) and weak effector‐triggered immunity (ETI) minus effector‐triggered susceptibility (ETS) (Jones and Dangl, 2006). Apart from newly evolved R proteins that recognize effectors or their activities, ETS can be counteracted by the priming of defence, causing faster and stronger induction of basal defence mechanisms after pathogen attack. A moderately primed defence response merely augments the PTI/ETI response, but would still allow ETS to take place (shown in orange), whereas a strongly primed defence reaction can prevent ETS entirely (shown in red).

Figure 2

Model of plant defence strategies and their adaptive values under different biotic stress conditions. Plants in environments with relatively high disease pressure from a wide array of different attackers benefit from constitutive priming of basal resistance mechanisms, which provide broad‐spectrum protection against pests and diseases (strategy A). However, this defence strategy may affect the plant's ability to associate with plant‐beneficial microbes, such as mycorrhizae or nitrogen‐fixing bacteria. In this situation, plants would benefit more from an increased ability to attract and associate with disease‐suppressing plant‐beneficial microbes (strategy B). Plants in environments with a constant pressure from one dominant biotrophic pathogen benefit from effector‐triggered immunity (ETI; strategy C). ETI can be broken and give rise to an ongoing ‘zigzag’ evolution, as described by Jones and Dangl (2006). Inducible defence priming on perception of stress‐indicating signals provides a cost‐efficient adaptation to environments with variable degrees of disease pressure (strategy D). Because priming of defence and induction of defence are both associated with costs on plant growth and reproduction, a relatively unresponsive immune system would be beneficial in environments with relatively low disease pressure (strategy E).