JOURNAL OF NEMATOLOGY Article | DOI: 10.21307/jofnem-2020-022 e2020-22 | Vol. 52 Fungal communities associated with Heterodera glycines and their potential in biological control: a current update Deepak Haarith1,*, Kathryn E. Bushley2 and Senyu Chen1 Abstract The soybean cyst nematode (SCN) is the most important pest on 1Department of Plant Pathology, soybean, a major crop worldwide. The SCN is considered both University of Minnesota, St. Paul, parasitic and pathogenic as it derives nutrition from the host and MN 55108. manipulates host physiology to do so. Currently, there are no com- 2Department of Plant and Microbial mercially available chemicals that are specific, environmentally safe Biology, University of Minnesota, and cost effective to control SCN levels. Crop rotation, use of host St. Paul, MN 55108. resistance and other cultural practices remain the main management strategies. The need for bioprospecting other methods of controlling *E-mail: [email protected] SCN is paramount, and fungi show promise in that respect. Sever- This paper was edited by Horacio al studies have evaluated fungi and fungal products as biocontrol Lopez-Nicora. options against plant-parasitic nematodes. This review discusses fungal genera isolated from the SCN with potential for use as bio- Received for publication June 21, control agents and the effects of their secondary metabolites on vari- 2019. ous stages of SCN development. The review also summarizes efforts to control SCN using soil amendments that could potentially impact fungal communities in the soil. Keywords Soybean cyst nematode, SCN, Biocontrol, Biological control, Fungi, Fungal metabolites, Mycobiome, Heterodera spp., Heterodera glycines, Review. The soybean cyst nematode (Heterodera glycines, The lifecycle of SCN includes several life stages SCN) was discovered as a significant pest of soybean that can be targeted by natural antagonists. However, in 1954 in North Carolina in the USA, and subse- the survival structures or cysts, which consist of the quently spread across a few counties in Arkansas, female bodies containing hundreds of eggs protected Missouri, Kentucky and Tennessee, as well as few by a melanized layer of cuticle, are an important target other pockets in North Carolina (Winstead and Skot- stage for biocontrol. The eggs in cysts can survive up land, 1955). In 2014, bolstered by the increase in to 10 years or longer in soil and can produce viable planting of soybean, the SCN has become a signif- and infective second-stage juvenile nematodes (J2) icant plant health issue all over the agrarian east- when conditions are favorable. Thus, reducing the ern continental United States as well as Hawaii and egg numbers in cysts in soil will ensure significant Puerto Rico, and southern Canada (Tylka and Ma- reduction in nematode inoculum. rett, 2014). In the USA, SCN accounts for up to 30% The idea of using biological agents to control of all soybean yield lost to disease, amounting to a nematodes is as old as nematology itself, as Nathan little over 2.7 m metric tons a year (Allen et al., 2017). Cobb, the father of nematology, first suggested It is a major problem of this important protein and using predatory nematodes to control plant- oilseed crop of the USA, the largest producer of soy- parasitic nematodes (Cobb, 1917). Biological control bean with an annual output of 117.3 m metric tons in or biocontrol is scientifically attractive goal, albeit 2016 (White and Honig, 2017). often not as commercially successful in most cases © 2020 Authors. This is an Open Access article licensed under the Creative 1 Commons CC BY 4.0 license, https://creativecommons.org/licenses/by/4.0/ SCN fungi and biocontrol: Haarith et al. compared to chemical control methods. It has studies that have tried to understand the fungal become increasingly attractive since methyl bromide communities associated with one nematode, SCN, has been proven harmful to the environment, livestock in the USA. A detailed review of biocontrol of all and humans and subsequently banned from use plant-parasitic nematodes by different kinds of (Duniway, 2002). Although there are several chemical fungal parasites such as nematode-trapping fungi, alternatives to methyl bromide available in the market obligate endoparasites of SCN juveniles, and female today, their mechanisms are either poorly understood and egg parasites, on different stages of nematode or not extremely specific to the target nematodes. development, is presented in a book chapter by Furthermore, biocontrol also offers the option to Chen and Dickson (2012). Therefore, this review isolate bioactive metabolites from microorganisms will focus mainly on members of culturable fungal and develop them into bionematicides, in addition communities from SCN that can be studied in vitro to using the organism by itself. It is also a good idea as well as in vivo for their biocontrol properties. to develop biocontrol agents and bionematicides to For a good biological control agent, in addition to work synergistically with currently employed practices being able to colonize nematodes in vitro, the ability such as genetic resistance, crop rotation and other to tolerate abiotic and biotic stresses to survive in chemical nematicides as well, for a well-rounded, soil or colonize roots is an important consideration. integrated nematode management. Fungistasis, or competition between fungi, as Several microorganisms have been tested as well as host preferences (Mauchline et al., 2004) potential antagonists against SCN, including both and abiotic stresses such as varying conditions of fungi and bacteria, with Pasteuria spp. being the temperature, humidity, pH and moisture in the soil most important bacterial agent. However, only a few environment must be evaluated before a biocontrol bacterial and fungal biocontrol agents have been agent is tested in the field. Several reviews have commercialized thus far, mostly in the genera Bacillus discussed the role of nematode-trapping fungi or Pasteuria for bacteria, and Paecilomyces and that utilize various trapping devices, such as nets, Pochonia for fungi (Li et al., 2015; Chen and Dickson, rings and knobs, in control of nematodes (Mankau, 2012). Bionematicides of bacterial origin, especially 1980; Kerry, 1988; Siddiqui and Mahmood, 1996; Abemectin, have seen some commercial success, Chen and Dickson, 2012). This review will not including for use on Heterodera avenae (Zhang discuss trapping fungi as they often are influenced et al., 2017). However, eukaryotic fungi and other by other soil organisms and competition, and are fungal-like organisms that can sporulate, have only often fastidious to culture (Persmark et al., 1996; been increasingly reported as potential biocontrol Jaffee et al., 1998; Li et al., 2011). This paper aims agents, especially on root-knot nematodes, but have to summarize some of the common fungal taxa had fewer commercial successes for SCN (Tranier reported in the literature, associated with SCN, as et al., 2014; Musil, 2016). Filamentous fungi could well as anti-nemic metabolites from fungi that have overwinter, produce spores and remain in the soil been studied for their potential against SCN and for longer periods of time than their non-sporulating other cyst nematodes. This review also discusses counterparts (Jung et al., 2014); and thus, may various soil amendments that have been shown reduce reapplication rates and associated costs. to reduce SCN levels in the soil, which may have Given that the major soybean producing states (Iowa, indirect effects on fungal communities in the soil Illinois, Minnesota, the Dakotas and Ohio) (USDA, affecting SCN. 2016) have harsh winters with fallow fields and conditions unfavorable for any growth, filamentous and sporulating fungi could be the most viable option Common culturable fungi for biocontrol, yet few have been commercially (mycobiome) associated with SCN developed. Furthermore, desiccated spores enable cysts and eggs easy storage and transport of the organism without losing viability for long periods compared to live The diversity of fungi and fungal-like organisms is vegetative cells. Desiccated fungal spores could also vast, and soil is a very complex habitat that hosts all be easily formulated to be applied as soil drenches kinds of fungi with varying modes of nutrition. Obligate like in the case of Melocon WG or coated on seeds parasites of SCN are highly virulent and effective as in the case of Poncho/Votivo (BAYER, 2012, 2015). nematode parasites, but they have limitations as There are several reviews that discuss biological viable biocontrol options as they cannot be cultured control of several plant-parasitic nematodes using easily on artificial media and other fungi usually fungi. This review aims to specifically summarize outcompete them in soil. On the other end of the 2 JOURNAL OF NEMATOLOGY continuum, true saprophytes can be easily cultured Family Nectriaceae: Fusarium, on artificial media, but generally may not colonize the Cylindrocarpon and other genera SCN as pathogens. Thus, facultative saprophytes that are both effective parasites of nematodes, but Assessment of fungal genera associated with SCN can also be cultured on artificial media have promise cysts and eggs as potential biocontrol agents have as potential biocontrol agents. been reported for more than three decades. These Several studies have investigated the fungi studies have reported Fusarium spp., to be highly associated with the SCN from several locations of associated with SCN cysts,