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Fungi–Nematode Interactions: Diversity, Ecology, and Biocontrol Prospects in Agriculture

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Fungi–Nematode Interactions: Diversity, Ecology, and Biocontrol Prospects in Agriculture Journal of Fungi Review Fungi–Nematode Interactions: Diversity, Ecology, and Biocontrol Prospects in Agriculture Ying Zhang 1, Shuoshuo Li 1,2, Haixia Li 1,2, Ruirui Wang 1,2, Ke-Qin Zhang 1,* and Jianping Xu 1,3,* 1 State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, and Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University, Kunming 650032, China; [email protected] (Y.Z.); [email protected] (S.L.); [email protected] (H.L.); [email protected] (R.W.) 2 School of Life Science, Yunnan University, Kunming 650032, China 3 Department of Biology, McMaster University, Hamilton, ON L8S 4K1, Canada * Correspondence: [email protected] (K.-Q.Z.); [email protected] (J.X.) Received: 15 September 2020; Accepted: 2 October 2020; Published: 4 October 2020 Abstract: Fungi and nematodes are among the most abundant organisms in soil habitats. They provide essential ecosystem services and play crucial roles for maintaining the stability of food-webs and for facilitating nutrient cycling. As two of the very abundant groups of organisms, fungi and nematodes interact with each other in multiple ways. Here in this review, we provide a broad framework of interactions between fungi and nematodes with an emphasis on those that impact crops and agriculture ecosystems. We describe the diversity and evolution of fungi that closely interact with nematodes, including food fungi for nematodes as well as fungi that feed on nematodes. Among the nematophagous fungi, those that produce specialized nematode-trapping devices are especially interesting, and a great deal is known about their diversity, evolution, and molecular mechanisms of interactions with nematodes. Some of the fungi and nematodes are significant pathogens and pests to crops. We summarize the ecological and molecular mechanisms identified so far that impact, either directly or indirectly, the interactions among phytopathogenic fungi, phytopathogenic nematodes, and crop plants. The potential applications of our understanding to controlling phytophagous nematodes and soilborne fungal pathogens in agricultural fields are discussed. Keywords: nematophagous fungi; cross-kingdom interactions; food-web cycling; phytophagous nematodes; soilborne fungal pathogens 1. Introduction Ecosystems consist of many types of organisms, including different types of microscopic organisms such as bacteria, archaea, protozoa, fungi, and small animals such as nematodes. Together, these organisms interact with each other and with macroscopic organisms such as plants and large animals to perform ecosystem functions. Their interactions happen in multiple ways, can be direct or indirect, involving two or more partners, and occur through different mechanisms such as predation, parasitism, mutualism, or competition. These interactions are critical for maintaining ecosystem balance [1]. Fungi and nematodes are among the most abundant organisms in the terrestrial ecosystem. The phylum Nematoda, also known as the roundworms, is the second largest phylum in the animal kingdom, encompassing an estimated 500,000 species [2]. Ninety percent of terrestrial nematodes reside in the top 15 cm of soil, and they play an important role in the nitrogen cycle by way of J. Fungi 2020, 6, 206; doi:10.3390/jof6040206 www.mdpi.com/journal/jof J. Fungi 2020, 6, 206 2 of 24 J. Fungi 2020, 6, x 2 of 25 nitrogenorganisms mineralization. that feed on living Nematodes materials do [3]. not On decompose the other organichand, fungi matter are butthe insteadprincipal are decomposers parasitic or free-livingof dead organic organisms matter; that they feed perform on living fundamental materials [3 ].roles On thein nutrient other hand, cycling fungi in are the the ecosystem. principal decomposersAlthough fungi of may dead look organic like plants, matter; they they are perform in fact evolutionarily fundamental rolesmore inclosely nutrient related cycling to animals in the ecosystem.than to plants. Although Both fungifungi mayand looknematodes like plants, (as theywell areas inall fact animals) evolutionarily are heterotrophs. more closely They related are tocommonly animals found than to co-existing plants. Both in a fungidiversity and of nematodes natural and (as man-made well as all ecosystems animals), areespecially heterotrophs. in the Theyrhizosphere are commonly of plants, found including co-existing crops, in a diversity with significant of natural andimpacts man-made on agriculture ecosystems, and especially forestry. in theConsequently, rhizosphere interactions of plants, among including fungi crops, and nematodes with significant have attracted impacts significant on agriculture attention. and forestry. Consequently,Nematode interactions and fungi arose among about fungi 550–600 and nematodes mya and 1050 have mya, attracted respectively. significant They attention. likely co-existed and interactedNematode with and each fungi other arose in about soils 550–600before plants myaand colonized 1050 mya, terrestrial respectively. habitats They about likely 450 co-existedmya [4,5]. andThe co-existence interacted with and each interactions other in soilsbetween before nematodes plants colonized and fungi, terrestrial whether habitats antagonistic about or 450 mutualistic, mya [4,5]. Thedirect co-existence or indirect, and are interactions fundamental between for understanding nematodes and their fungi, ecosystem whether antagonisticeffects and their or mutualistic, potential directmanipulations or indirect, in areagriculture. fundamental An important for understanding long-term their goal ecosystem in agriculture effects pest and theirand pathogen potential manipulationsmanagement is into identify agriculture. novel Ancontrol important strategies long-term against phytophagous goal in agriculture nematodes pestand and pathogensoilborne managementfungal pathogens, is to identifyto help novelincrease control both strategiesthe qualit againsty and quantity phytophagous of agricultural nematodes products. and soilborne In this fungalreview, pathogens, we summarize to help our increase current bothknowledge the quality of the and interactions quantity of between agricultural nematodes products. and Infungi. this review,Specifically, we summarizewe focus on our the current interactions knowledge between of these the interactions two groups between of organisms nematodes that have and shown fungi. Specifically,both antagonistic we focus and onmutualistic the interactions interactions between to each these other, two groupseither directly of organisms or indirectly that have (Figure shown 1). bothWe note antagonistic that the andnature mutualistic of their interactionsinteractions tocan each vary other, greatly either among directly the or different indirectly fungal (Figure and1). Wenematode note that species. the nature Furthermore, of their interactions the interactions can vary between greatly amongtwo organisms the different are fungalnot static and but nematode can be species.impacted Furthermore, by environmental the interactions factors to influence between both two organismsthe type and are magnitude not static butof their can beinteractions impacted [6]. by environmental factors to influence both the type and magnitude of their interactions [6]. Figure 1. Fungi-nematode interactions in soil. a: Endophytic fungi trigger host plant defense againstFigure 1. plant Fungi-nematode pathogenic nematodes interactions (PPNs). in soil. b: a: Plants Endoph helpytic nematodes fungi trigger escape host fungal plant attacksdefense through against volatileplant pathogenic training. nematodes (PPNs). b: Plants help nematodes escape fungal attacks through volatile 2. Antagonistictraining. Interactions 2. AntagonisticAntagonistic Interactions interactions between fungi and nematodes are as numerous as they are varied. For example, many nematodes, such as Aphelenchus avenae, Aphelenchoides spp., and Paraphelenchus Antagonistic interactions between fungi and nematodes are as numerous as they are varied. For acontioides, can feed on a diversity of fungi. These are commonly referred to as fungivorous example, many nematodes, such as Aphelenchus avenae, Aphelenchoides spp., and Paraphelenchus nematodes [7]. In contrast, a number of fungal species such as Arthrobotrys oligospora can prey acontioides, can feed on a diversity of fungi. These are commonly referred to as fungivorous on nematodes and their eggs, consuming them as food. Such fungi are known as nematophagous nematodes [7]. In contrast, a number of fungal species such as Arthrobotrys oligospora can prey on fungi [8]. nematodes and their eggs, consuming them as food. Such fungi are known as nematophagous fungi [8]. J. Fungi 2020, 6, 206 3 of 24 2.1. Nematodes Feeding on and Antagonizing Fungi Many of the nematodes have fungi in their diets or feed exclusively on fungi [9]. Thus, as a major component of the soil food web, nematodes can influence both the fungal diversity and abundance and community structure, including crop growth and tolerance to soil pollution. Fungivorous nematodes commonly exist in soil containing many different fungal species. Nematodes in the genera Aphelenchus, Aphelenchoides, Ditylenchus, and Tylenchus are among the most common fungivorous nematodes [10]. Generally, fungivorous nematodes feed on a diversity of soil fungi, including saprophytic, plant-pathogenic, and plant-beneficial (such as mycorrhizal) fungi and are known as polyphagous nematodes [11]. While the population densities of fungivorous nematodes in soil may
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