Plant pathogens as introduced weed biological control agents: Could antagonistic fungi be important factors determining agent success or failure?

Abstract

Mycoparasitic interactions are common in nature, form part of the microbiota of plants, and are considered significant contributors to fungus-fungus antagonism. Mycoparasites kill plant pathogens, protect the plant from abiotic and biotic stressors, and reduce disease incidence and severity at the plant population level. Their exploitation as biocontrol agents in agriculture is well documented. However, mycoparasites may potentially affect classical fungal biocontrol agents of invasive weed species. Classical biological control, or biocontrol, of invasive weeds involves the intentional introduction of exotic, usually co-evolved plant pathogens and insects, for permanent establishment and long-term control of the target plant. Agent establishment, effectiveness, and safety are the critical elements for a successful weed biocontrol programme. Establishment and effectiveness of agents on the invasive plant often vary throughout the invaded range with about two-thirds of weed biocontrol agents failing to suppress their target weed. There are many documented reasons why weed biocontrol agents do not establish or are ineffective when they do, and the presence and accumulation of natural enemies in the invaded range is one of them. Endophyte-enriched, invasive weeds and those forming mutualistic associations with indigenous, native endophytes could explain the lack of consistency of some classical biological control introductions. However, another variable could be factored into the mix: mycoparasitism, where one fungus parasitises another, the natural enemies of the plant's natural enemies. In this review article, we introduce the concept of invasive weed biocontrol and the history of using plant pathogens as biocontrol agents. We discuss the success and failure of fungal agent programmes and delve into the patterns of success or failure, with a focus on the potential antagonistic role of endophytes and mycoparasites.

Keywords: classical biological control; endophytes; invasive weeds; mycoparasites; rust fungi.

Figure 1

Schematic illustration of the interactions between plant pathogens and antagonists in the classical biocontrol of invasive plants. The plant, plant pathogen, and antagonist (endophyte and hyperparasite) are all potentially present in the environment. In the native range (in the green center of the triangle), the interactions are in balance, and the plant is non-invasive. In the introduced range (orange) the plant is present as an introduced exotic species. There are three scenarios: 1) The plant pathogen, introduced as a biocontrol agent, successfully suppresses the plant (top of the triangle). Its effect is stronger than that of any present endophytes or hyperparasites. 2) A protective endophyte inhibits the plant pathogen (bottom left of the triangle). Biocontrol fails, and the plant remains an invasive weed. 3) A hyperparasite inhibits the plant pathogen (bottom right of the triangle). Biocontrol fails, and the plant remains an invasive weed. Both lower parts of the triangle are examples where outbreaks of a plant pathogen have been prevented, either intentionally (biocontrol of pathogens) or unintentionally (interference with the biocontrol of weeds).