Can common mycorrhizal fungal networks be managed to enhance ecosystem functionality?

Mycorrhizal fungi are key components of soil biodiversity that offer potential to provide sustainable solutions for land management, notably in agriculture and forestry. Several studies conducted controlled environments show functional attributes common mycorrhizal networks (CMNs), which inter-link different plants, influenced by management practices. Here, we highlight the need consider how affects ubiquity function CMNs nature maximize role enhancing ecosystem services. We emphasize can sometimes negatively affect aspects plant performance, but there remain major gaps understanding before explicit consideration CMN be delivered. Most have capacity develop extensive extraradical mycelium, thus connect multiple plants form a ‘common network’. shown these influence establishment, nutrition, productivity defense, nutrient distribution storage, multitrophic interactions. However, many focused on importance ecological contexts has been less emphasis managed systems, including croplands, grassland, agroforestry forestry, humankind relies. Here review evidence insight into could effectively functions outputs from systems. also possible negative effects performance question popular views may panacea gain greater ubiquity, functioning, response interventions and, critically, determine extent add value promotion colonization. largely obligate biotrophs forming associations with majority terrestrial species (Brundrett & Tedersoo, 2018), often complex (usually) dense mycelium (ERM) (Miller et al., 1995). The ERM forages is not accessible root system granting increased access elements needed large amounts host phosphorus (P) nitrogen (N; Wipf 2019). A fascinating feature its interconnect numerous belonging same or (Rhodes, 2017; Simard, 2018; Simard 1997), coined ‘wood-wide web’(Rhodes, 2017). consequences such underground physical connections linking individual challenge our thinking resource capture interactions, as result spawned views, exaggerated, extolling virtues both natural systems (Simard, 2018). Such enthusiasm surprising given their capabilities. Indeed, formed arbuscular (AM) facilitate movement water (H2O; Egerton-Warburton 2007), significant P (Mikkelsen 2008) demonstrated through use radioisotopes. ectomycorrhizal (ECM) transfer carbon (C; Selosse 2006; Rog 2020), N (He 2005) H2O (Simard 2015). Furthermore, involvement limited exchange involve allelochemicals (Barto 2011) AM fungi, defence information (Gilbert Johnson, Oelmüller, 2019) ECM impact interactions Therefore, actively participate well-documented beneficial effect nutrition (Smith Read, well improving resistance tolerance abiotic (e.g. drought; (Plouznikoff 2016)) biotic (Whipps, 2004) stresses. Thus, growing multifunctional across ecosystems involving types fungi. burgeoning literature plethora commercial products organizations promoting fungal colonization interest (i.e. horticultural crop species), especially those mycorrhizas (Berruti 2016; Chen Yet, few attempts explicitly manage enhance valuable services, tackle globally important grand challenges related agriculture, production fuel fiber, conservation. new inform guidance best required. This particularly because Earth's some extent; recent consensus view estimates 51% area modified human purposes (Hooke 2012). estimate includes areas used croplands (13%) pasture grassland (23%), planted (2.1%) logged (1.8%) forest, urbanization. Additionally, humans unmanaged ‘natural’ indirectly due anthropogenic activities foraging, hunting, pollutant deposition). vast range specific land-uses potentially affected (Rillig they develop. Nevertheless, agroecosystems, crops forests, productive forest restoration creation, primary perspective CMNs. an overview reduced farming C cost. conventional high cost over fertilization pest tillage (C footprint, Figure 1; Hillier 2009). Crucially, ensure evidence-based, so effective strategies carefully developed. intrinsically linked produce this synthesis inevitably considers hyphal density alongside focus added (see 1) gained ecosystems. In order CMNs, reliable data extent, functionality distance. Alas, remains scarce, dominated despite previous calls collect (Babikova 2014), no doubt difficulty reliably estimating presence Notable exceptions include particular temperate forests US Durall, Canada (Beiler 2010). For example, Rhizopogon spp. Fr. extended 20 m × plot interconnected several trees far more kind broad statements about woodland relied upon. Heathland vegetation ericaceous supports ERM, fine roots adept at foraging mean generally confined close surface. Some ericoid occur localized scales (Kjøller Remarkably, simultaneously classic ectomycorrhizas shrubs, although restricted distances <4 cm (Grelet 2010; Kjøller It assumed (especially science press) cover areas, field scales. enormous unlikely nature, objectively interpret contexts, AM-forming plants. work Chiariello al. (1982) measured 32P up 9 intact turfs, unequivocal was possible. laboratory, Mikkelsen (2008) cm, indicating dynamics relatively depending type. Increasing numbers quantified (Kim 2013) even turnover (Hagenbo 2017) (Table 1). densities hyphae itself provides strong perhaps adequate infer perspective, without undertake expensive, technically challenging, time-consuming molecular analyses. argue quantify land-management practices ability stable networks, rigorous test hypothesis proxy formation. Moreover, simple experiments undertaken confirm under conditions. assumption all capacity, systematic done. indeed functionally trait adds number using traits shed light significance microbial diversity (de Bello Fry 2019; Wang soil, represent between 20% 30% total biomass (Leake frequently accounts tens, hundred per cm3 Growth rates (calculated dividing length days growth) fast: vivo model estimated growth 738–1,067 mm day?1 (Giovannetti 2001), great roots. Anastomosis observed (Novais frequency fusions coming contact (67%–77%), along (0.46–0.51 mm?1; Novais speed formation varies environmental conditions, medium distance latter stages potato variety Bintje obtained after 12 vitro (Gallou 2010), whereas it 35 inoculation tomato pot experiment (Song Direct exploration network topology arrangement various communication nodes links; 2018) belowground difficult explore nature. analyses beginning alter showing clades host-specific generalist (Toju Generalist ranges working interaction hubs plant–fungus thereby connecting otherwise isolated groups (Olesen 2007). were associated narrower partners than expected models random hosts symbionts, compartmentalized modules closely 48 other trees, distinct inter-connected clearly offers opportunities exploitation services forestry restoration. outline most or, conversely, detrimentally (Figure simplified experimental settings much done findings realistic field-based illustrate managers 1); notably, no-till, diverse make seedlings become established critical survival becoming rapidly colonized facilitates process. From when creating woodland, establishment conservation concern, food crops) ensuring focal therefore important. Laboratory consistently promote fast homogenous seedling recruits Marquez Voets Demonstrating rely mesh cores Johnson 2001) manipulate supported surrounding adult approach perfect because, first, rarely unequivocally whether connected wider second, mechanism benefits (or not) integration neighbouring plant; resources volumes unavailable seedling; pathogen protection). Despite limitations, method manipulation presence, (Van der Heijden Horton, 2009) Booth, 2004; Liang 2020; Nara, 2006). Booth Hoeksema (2010) trenching connection had positive benefited water. stressful saline soils) uptake development highlighting application degraded soils (Yu 2020). addition colonize efficiently hosts, inoculum source reduce induced during early stage development. absence differences e.g. content fresh weight leaves plantlets newly incorporated versus non-mycorrhizal measured, suggesting probably smaller mostly taken donor (Alaux Gallou Seedlings establish easily within existing direct pool nutrients CMN, situations directly Heijden, 2008). is: do integrated solely community fungi? tackled inconsistent reporting leads compared controls (Francis 1995) others 1995; Janoušková 2011; Merrild 2013). While cases designs prevented clear analysis elegant 2013 showed led size inequality larger cucumber Inequality small big bluestem (Andropogon gerardii V.) emphasizing temporal responses fitness, grazed (Weremijewicz 2016). short-term grazers favor stature cost, while longer term, benefit acquisition if net nutrients, leading uniform amongst populations communities, retention (Hamel 1991) pollution fertilization. Arbuscular regulate inequalities (Welte, 2009; Whiteside seems increase trading (Whiteside origins translocated fungus directions, P-poor P-rich vice versa, rich poor Walder (2012) found two (Linum usitatissimum L. Sorghum bicolor L.) grown monocultures As result, trade only changing amount trades 2019), altering location (Fellbaum 2014; Jakobsen Hammer, 2015; Noë Kiers, These mechanisms help maintain mutualistic balance having control either flow (Kiers 2011). Below-ground signaling infected pests non-infested neighbors via (Babikova, Gilbert, 2013; Song 2010, endophyte (Vahabi elicit against biological stressors insect herbivores 2013), herbivory-elicitors foliar necrotrophic hemibiotrophs, Oomycota acting conduit interplant (Johnson Many relevant horticulture bean, tomato, tobacco, potato, reflecting agroecosystems. concept sentinel plant, whereby susceptible inspected regular intervals signs symptoms attack, developed further warn unclear, regarding signal 2020) overall fitness Signals travel least detected terms measurable receiver defence: genes compounds) 24 hr 6 being exposed stressor peak 100 duration signals unknown appeared transitory, priming phase Plant jasmonic acid (JA), ethylene (Eth; Alaux 2014, salicylic (SA; Zhang Interestingly, defence) activate JA limit transfer. To pest-related losses additional investigated situations, putative relay among links (Wipf Manipulation composition tractable abundance functioning feedbacks positively performance. likely greatest relevance mixed genotype – see section below) i.e. where richness relative planting seeding. grasslands, targeting subordinate dominant promising hypothesized contrasting (Urcelay Díaz, 2003). Experimental (Veresoglou lead growth. dominance hierarchy (Mariotte Promotion formation: global databases suggest propensity ‘out-source’ dominates economic spectrum (Bergmann issue remains, communities function, reciprocal structure poorly studied unclear. Weremijewicz Janos, amplified competing genotypes C4 grass A. gerardii, eastern United States prairie. More works competition differential Elymus canadensis unaffected not, Common shaping comprising hosts. subtropical survival, (Liang Possible behind observations relate protection pathogens conferred forms, organic molecules phytate (Liu Few though (mostly) suggests Zhang, still lack clarity addition, scenarios should ignored, creation 1), political societal agenda (Bastin Furthermore sequestration above already no-till (around 115kg /ha/year Kingdom; 2009), contribute provided know sensitive physical, chemical, disturbances caused agricultural (Verzeaux agronomic monoculture cropping (Daniell 2001; Oehl 2003), ploughing (Helgason 1998; 2005; Ryan Graham, (Bhadalung 1993), pesticide applications (Buysens Calonne 2012; Channabasava 2015), herbicide (Druille Zaller long fallow periods present population density, diversity, efficacy (Avio 2004), Sustainable requires techniques short no-till/direct drilling. Greater intra co-culture (Derelle 2012), similar arise (Battie-Laclau intercropping Intercropping widely consists combination achieve yielding complementary partner species. mixtures typically comprise combinations cereals legumes (Inal C3 photosynthetic pathways, maize chili pepper (Hu reducing loss 1991), improve efficiency recovery excreted co-occurring soybeans 1991). intercropped supplying part increasing propagules fruit yield pepper. Amongst competitive strategy differed each higher careful selection season. Cover reported maintenance (Verbruggen winter allows subsequent cultivated By providing sustained perennial rapid herbaceous beneath active wheat roots, surface top 10 layer Currently underway UK assess hedgerows ley strips sources inocula reservoirs intensively arable (Holden Analysis walnut (Juglans nigra hardwood understorey recolonization subjected disruption Similar processes operate exploited productivity. leaving occasional mature following clear-cutting mother saplings, sapling (Teste put weeds; suppress weeds non-hosts (Daisog 2012) co-cultivated removal grazing tested. ambiguous Rillig, 2010) partly edaphic climatic variables (Faghihinia Ba feedback relationship light-to moderate-grazing, heavy-grazing. One aspect received varieties rather monocultures, years. Often perceived generalists, genotype-specific (Cosme Although lacking, Plouznikoff (2019) quantitative loci (QTLs) (from 15% 92%). There crops, wheat, vary considerably susceptibility Hetrick 1992), ecologically traits. expect dependent identity, seasons promise (Barot Finally, molecules, microbes, negatively. bacterial translocation simultaneous bacteria observation pave way delivery biofertilizers “super spreader”, biostimulants biocontrol agents (du Jardin, Velivelli infection. Colonization tends viruses mycorrhiza (MIS); (Miozzi research accelerating MIS. mRNA move parasitic 2014) raises questions genomic information. Humans step-change society's goals set out Nations. Capitalizing much-needed ‘holistic’ ecosystems, supporting limited, cases. basic concerns (positive negative) arising simply mycorrhizas. Just added-value bring? driving matter farmers better CMN. vital knowledge filled, characterize conditions involved consistent experimentation, collection, type would beneficial; studied. applied policy guidance. Notably, circumstances really land-managers? And ever considered separate management? Answering just fundamental context. funding Natural Environment Research Council (NE/P001823/1). DJ receives partial support N8 AgriFood program. P-LA, YZ, wrote manuscript. YZ collected table made summary figure. LG contributed manuscript editing central feedback. secured funding.