Three-way interactions between crop plants, phytopathogenic fungi, and mirid bugs. A review

Miridae is the largest Heteroptera family, with a tremendous worldwide economic impact, both as pests and natural enemies. Unlike most Hemiptera, herbivorous and omnivorous mirid bugs are lacerate/macerate and flush feeders, not phloem feeders. Plant responses to damage by arthropods of this feeding guild therefore occur via jasmonic acid or ethylene signaling pathways rather than the salicylic acid pathway. Moreover, unlike most other Heteroptera that lay eggs on the plant surface, mirids insert their eggs in plant tissues, resulting in oviposition injury. Similarly, regarding phytopathogenic fungi and oomycetes, a distinction should be made between biotrophic fungi (triggering the salicylic acid pathway plant response), and necrotrophic and/or hemibiotrophic fungi or oomycetes (triggering jasmonic acid or ethylene pathway plant responses). In that respect, phytopathogenic fungi or oomycetes (PFO) differ from phytopathogenic viruses and bacteria, the former being all biotrophic while the latter are theoretically hemibiotrophic. Here, for the first time, we review tripartite interactions between mirids, PFO, and crop plants. The major deliverables are as follows: Five major interaction frameworks are identified: (i) crop plant infection by PFO mechanically facilitated by prior mirid infestation; (ii) crop plant infection by PFO hampered by prior mirid infestation via crop plant signaling; (iii) crop plant infestation by mirids facilitated by prior PFO infection via crop plant signaling; (iv) crop plant infestation by mirids hampered by prior PFO infection via crop plant signaling; (v) crop plant infestation by mirids and/or infection by PFO hampered by prior mirid infestation and/or PFO infection via crop plant resource quality alteration. PFO and mirids may also occur concomitantly, favored by the same conditions, i.e., climatic or linked to endogeneous factors (e.g., redox status) in crop plant. Instances from each framework are described, and highlighted interactions are examined in view of managing mirid–PFO complexes on crop plants.