A catalogue of virulence strategies mediated by phytopathogenic effectors

Abstract

Plant diseases cause dramatic economic loss, posing a major challenge to modern agriculture. Plant pathogenic organisms secret effectors that utilize fascinating and intricate stratagems to facilitate infection. The consequences of plant-pathogen interactions are largely determined by effectors. The effector research has made great strides since its inception in the 1990s and the importance of effectors is increasingly noticed. Molecular investigation of effectors has provided critical insights into how plant pathogens manipulate their hosts to cause diseases. Thus far, numerous excellent reviews concerning effectors have focused on their targeting host pathways, recognition by host receptors, and evasion mechanisms, but few have ever summarized all known effector action modes. Here, we distinguish ten different stratagems of effector function from all types of pathogens, including damage, inhibition, hijacking, promotion, subversion, mimicry, reprogramming, evasion, decoying, and adaption. Furthermore, we discuss examples of these ten stratagems, refine the effector definition, and propose future directions of phytopathogenic effector research.

Keywords: Effector; Effector action mode; Host immunity; Pathogen-host interaction; Plant pathogenic organism.

Fig. 1

A bird's-eye view of effectors in plant pathogenic organisms. (A) Effector characterization from plant pathogenic organisms. Known types of pathogens, effectors and their targets are shown. (B) A historic overview of effector studies. The number of pathogenic effector-related papers per year is shown. Data were obtained from Web of Science (https://www.webofscience.com/wos/alldb/basic-search).

Fig. 2

Summarization of the ten action stratagems of phytopathogenic effectors. The ten stratagems are damage, inhibition, hijacking, promotion, subversion, mimicry, reprogramming, evasion, decoying, and adaption. The stratagems of the effectors are written in blue, with an upward arrow denoting increase and a downward arrow denoting decrease. Effectors can interfere with target functions through damage, inhibition, and hijacking stratagems. They also promote target functions through promotion, subversion, and mimicry stratagems. Meanwhile, they could also manipulate plant immunity by the reprogramming stratagem. Effectors may also prevent recognition of another effector by host through evasion and decoying stratagems. Additionally, effectors can target other species in the same niche, directly change environment conditions to facilitate colonization, or acquire nutrients through the adaption stratagem.

Fig. 3

Plant targets and effector stratagems: damage, inhibition, and hijacking. The description of the indicated stratagems and the illustration of examples for these stratagems are shown. Effectors are shown in red. The targets of effectors are shown in green. The stratagems of the effectors are written above, with an upward arrow denoting increase and a downward arrow denoting decrease. The detailed target categories of the indicated effectors are written below.

Fig. 4

Plant targets and effector stratagems: promotion, subversion, and mimicry. The description of the indicated stratagems and the illustration of examples for these stratagems are shown. Effectors are shown in red. The targets of effectors are shown in green. Effector stratagems are written in above, with an upward arrow denoting increase and a downward arrow denoting decrease. The detailed target categories of the indicated effectors are written below.

Fig. 5

Plant targets and effector stratagems: reprogramming, evasion, and decoying. The description of the indicated stratagems and the illustration of examples for these stratagems are shown. Effectors are shown in red. The targets of effectors are shown in green. Effector stratagems are written in above, with an upward arrow denoting increase and a downward arrow denoting decrease. The detailed target categories of the indicated effectors are written below.

Fig. 6

Plant targets and effector stratagems: adaption. The description of the indicated stratagems and the illustration of examples for these stratagems are shown. Effectors are shown in red. The targets of effectors are shown in green. Effector stratagems are written in above, with an upward arrow denoting increase and a downward arrow denoting decrease. The detailed target categories of the indicated effectors are written below.