ECOLOGICAL NETWORKS IN AGROECOSYSTEMS: APPROACHES AND APPLICATIONS

Highlights

● Agricultural intensification reduced the complexity and connectance of soil food webs.

● Agricultural intensification impaired the robustness of pollination networks.

● High connectance in co-occurrence networks indicates efficient nutrient utilization.

Abstract

Complex network theory has been increasingly used in various research areas, including agroecosystems. This paper summarizes the basic concepts and approaches commonly used in complex network theory, and then reviews recent studies on the applications in agroecosystems of three types of common ecological networks, i.e., food webs, pollination networks and microbial co-occurrence networks. In general, agricultural intensification is considered to be a key driver of the change of agroecosystems. It causes the simplification of landscape, leads to the loss of biocontrol through cascading effect in food webs, and also reduces the complexity and connectance of soil food webs. For pollination networks, agricultural intensification impaired the robustness by reducing specialization and enhancing generality. The microbial co-occurrence networks with high connectance and low modularity generally corresponded to high efficiency in utilization of nutrients, and high resistance to crop pathogens. This review aims to show the readers the advances of ecological networks in agroecosystems and inspire the researchers to conduct their studies in a new network perspective.

Graphical abstract

Keywords

bipartite network / co-occurrence network / food web / network theory

References

[1] BerthetE T, BretagnolleV, LavorelS, SabatierR, TichitM, SegrestinB. Applying ecological knowledge to the innovative design of sustainable agroecosystems. Journal of Applied Ecology, 2019, 56( 1): 44–51

[2] BarnesA D, JochumM, LefcheckJ S, EisenhauerN, ScherberC, O’ConnorM I, deRuiter P, BroseU. Energy flux: the link between multitrophic biodiversity and ecosystem functioning. Trends in Ecology & Evolution, 2018, 33( 3): 186–197

[3] PitteloudC, WalserJ C, DescombesP, deSantana N C, RasmannS, PellissierL. The structure of plant-herbivore interaction networks varies along elevational gradients in the European Alps. Journal of Biogeography, 2021, 48( 2): 465–476

[4] MaA, LuX, GrayC, RaybouldA, Tamaddoni-NezhadA, WoodwardG, BohanD A. Ecological networks reveal resilience of agro-ecosystems to changes in farming management. Nature Ecology & Evolution, 2019, 3( 2): 260–264

[5] PonisioL C, GaiarsaM P, KremenC. Opportunistic attachment assembles plant-pollinator networks. Ecology Letters, 2017, 20( 10): 1261–1272

[6] MaB, WangY, YeS, LiuS, StirlingE, GilbertJ A, FaustK, KnightR, JanssonJ K, CardonaC, RöttjersL, XuJ. Earth microbial co-occurrence network reveals interconnection pattern across microbiomes. Microbiome, 2020, 8( 1): 82

[7] MayR M. Will a large complex system be stable. Nature, 1972, 238( 5364): 413–414

[8] JordanoP. Patterns of mutualistic interactions in pollination and seed dispersal-connectance, dependence asymmetries, and coevolution. American Naturalist, 1987, 129( 5): 657–677

[9] CuiZ Y, KeR M, PuZ Y, MaX L, WangY H. Learning traffic as a graph: a gated graph wavelet recurrent neural network for network-scale traffic prediction. Transportation Research Part C, Emerging Technologies, 2020, 115 : 102620

[10] ChristakisN A, FowlerJ H. The spread of obesity in a large social network over 32 years. New England Journal of Medicine, 2007, 357( 4): 370–379

[11] FirthJ A, HellewellJ, KlepacP, KisslerS, CNMIDCOVID-19 Working Group, KucharskiA J, SpurginL G. Using a real-world network to model localized COVID-19 control strategies. Nature Medicine, 2020, 26( 10): 1616–1622

[12] JoppaL N, BascompteJ, MontoyaJ M, SoléR V, SandersonJ, PimmS L. Reciprocal specialization in ecological networks. Ecology Letters, 2009, 12( 9): 961–969

[13] MilnsI, BealeC M, SmithV A. Revealing ecological networks using Bayesian network inference algorithms. Ecology, 2010, 91( 7): 1892–1899

[14] ZhouJ, DengY, LuoF, HeZ, TuQ, ZhiX. Functional molecular ecological networks. mBio, 2010, 1( 4): e00169–10

[15] StaniczenkoP P A, KoppJ C, AllesinaS. The ghost of nestedness in ecological networks. Nature Communications, 2013, 4( 1): 1391

[16] ZhaoL, ZhangH, O’GormanE J, TianW, MaA, MooreJ C, BorrettS R, WoodwardG. Weighting and indirect effects identify keystone species in food webs. Ecology Letters, 2016, 19( 9): 1032–1040

[17] NewmanM E J. Modularity and community structure in networks. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103( 23): 8577–8582

[18] MiloR, Shen-OrrS, ItzkovitzS, KashtanN, ChklovskiiD, AlonU. Network motifs: simple building blocks of complex networks. Science, 2002, 298( 5594): 824–827

[19] LuX K, GrayC, BrownL E, LedgerM E, MilnerA M, MondragonR J, WoodwardG, MaA. Drought rewires the cores of food webs. Nature Climate Change, 2016, 6( 9): 875–878

[20] StoufferD B, BascompteJ. Compartmentalization increases food-web persistence. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108( 9): 3648–3652

[21] ZhaoL, ZhangH, TianW, XuX. Identifying compartments in ecological networks based on energy channels. Ecology and Evolution, 2018, 8( 1): 309–318

[22] CsardiG, NepuszT. The igraph software package for complex network research. InterJournal, Complex Systems, 2005, 1695

[23] RCore Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2018

[24] GusevaK, DarcyS, SimonE, AlteioL V, Montesinos-NavarroA, KaiserC. From diversity to complexity: microbial networks in soils. Soil Biology & Biochemistry, 2022, 169 : 108604

[25] HudsonL N, EmersonR, JenkinsG B, LayerK, LedgerM E, PichlerD E, ThompsonM S A, O’GormanE J, WoodwardG, ReumanD C. Cheddar: analysis and visualisation of ecological communities in R. Methods in Ecology and Evolution, 2013, 4( 1): 99–104

[26] BorrettS R, LauM K. EnaR: an R package for ecosystem network analysis. Methods in Ecology and Evolution, 2014, 5( 11): 1206–1213

[27] deRuiter P C, NeutelA M, MooreJ C. Energetics, patterns of interaction strengths, and stability in real ecosystems. Science, 1995, 269( 5228): 1257–1260

[28] GuimarãesP R Jr. The structure of ecological networks across levels of organization. Annual Review of Ecology, Evolution, and Systematics, 2020, 51( 1): 433–460

[29] DormannC F, GruberB, FründJ. Introducing the bipartite package: analysing ecological networks. R News, 2008, 8 : 8–11

[30] PocockM J O, EvansD M, MemmottJ. The robustness and restoration of a network of ecological networks. Science, 2012, 335( 6071): 973–977

[31] BlüthgenN. Why network analysis is often disconnected from community ecology: a critique and an ecologist’s guide. Basic and Applied Ecology, 2010, 11( 3): 185–195

[32] VázquezD P, BlüthgenN, CagnoloL, ChacoffN P. Uniting pattern and process in plant-animal mutualistic networks: a review. Annals of Botany, 2009, 103( 9): 1445–1457

[33] FanK, WeisenhornP, GilbertJ A, ChuH. Wheat rhizosphere harbors a less complex and more stable microbial co-occurrence pattern than bulk soil. Soil Biology & Biochemistry, 2018, 125 : 251–260

[34] ChilloV, VázquezD P, TavellaJ, CagnoloL. Plant-plant co-occurrences under a complex land-use gradient in a temperate forest. Oecologia, 2021, 196( 3): 815–824

[35] ZhaoS, LiuJ, BanerjeeS, ZhouN, ZhaoZ, ZhangK, HuM, TianC. Biogeographical distribution of bacterial communities in saline agricultural soil. Geoderma, 2020, 361 : 114095

[36] GreenS, SerbanM, SchollR, JonesN, BrigandtI, BechtelW. Network analyses in systems biology: new strategies for dealing with biological complexity. Synthese, 2018, 195( 4): 1751–1777

[37] RöttjersL, FaustK. From hairballs to hypotheses-biological insights from microbial networks. FEMS Microbiology Reviews, 2018, 42( 6): 761–780

[38] WangS, BroseU. Biodiversity and ecosystem functioning in food webs: the vertical diversity hypothesis. Ecology Letters, 2018, 21( 1): 9–20

[39] FründJ, DormannC F, HolzschuhA, TscharntkeT. Bee diversity effects on pollination depend on functional complementarity and niche shifts. Ecology, 2013, 94( 9): 2042–2054

[40] GarcíaD, DonosoI, Rodriguez-PerezJ. Frugivore biodiversity and complementarity in interaction networks enhance landscape-scale seed dispersal function. Functional Ecology, 2018, 32( 12): 2742–2752

[41] Delgado-BaquerizoM, ReichP B, TrivediC, EldridgeD J, AbadesS, AlfaroF D, BastidaF, BerheA A, CutlerN A, GallardoA, García-VelázquezL, HartS C, HayesP E, HeJ Z, HseuZ Y, HuH W, KirchmairM, NeuhauserS, PérezC A, ReedS C, SantosF, SullivanB W, TrivediP, WangJ T, Weber-GrullonL, WilliamsM A, SinghB K. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nature Ecology & Evolution, 2020, 4( 2): 210–220

[42] JiaoS, LuY, WeiG. Soil multitrophic network complexity enhances the link between biodiversity and multifunctionality in agricultural systems. Global Change Biology, 2022, 28( 1): 140–153

[43] WuH, HuB, HanH, ChengX, KangF. Network analysis reveals the regulatory effect of mixed stands on ecosystem structure and functions in the Loess Plateau, China. Science of the Total Environment, 2022, 824 : 153588

[44] ThompsonR M, BroseU, DunneJ A, HallR O Jr, HladyzS, KitchingR L, MartinezN D, RantalaH, RomanukT N, StoufferD B, TylianakisJ M. Food webs: reconciling the structure and function of biodiversity. Trends in Ecology & Evolution, 2012, 27( 12): 689–697

[45] WardleD A, BardgettR D, KlironomosJ N, SetäläH, vander Putten W H, WallD H. Ecological linkages between aboveground and belowground biota. Science, 2004, 304( 5677): 1629–1633

[46] EvansD M, PocockM J O, BrooksJ, MemmottJ. Seeds in farmland food-webs: resource importance, distribution and the impacts of farm management. Biological Conservation, 2011, 144( 12): 2941–2950

[47] DamienM, LeLann C, DesneuxN, AlfordL, AlHassan D, GeorgesR, VanBaaren J. Flowering cover crops in winter increase pest control but not trophic link diversity. Agriculture, Ecosystems & Environment, 2017, 247 : 418–425

[48] ZhaoZ H, SandhuH S, GaoF, HeD H. Shifts in natural enemy assemblages resulting from landscape simplification account for biocontrol loss in wheat fields. Ecological Research, 2015, 30( 3): 493–498

[49] GagicV, TscharntkeT, DormannC F, GruberB, WilstermannA, ThiesC. Food web structure and biocontrol in a four-trophic level system across a landscape complexity gradient. Proceedings of the Royal Society B: Biological Sciences, 2011, 278( 1720): 2946–2953

[50] GagicV, HänkeS, ThiesC, ScherberC, TomanovićZ, TscharntkeT. Agricultural intensification and cereal aphid-parasitoid-hyperparasitoid food webs: network complexity, temporal variability and parasitism rates. Oecologia, 2012, 170( 4): 1099–1109

[51] YadavP, DuckworthK, GrewalP S. Habitat structure influences below ground biocontrol services: a comparison between urban gardens and vacant lots. Landscape and Urban Planning, 2012, 104( 2): 238–244

[52] SprungerC D, CulmanS W, PeraltaA L, DupontS T, LennonJ T, SnappS S. Perennial grain crop roots and nitrogen management shape soil food webs and soil carbon dynamics. Soil Biology & Biochemistry, 2019, 137 : 107573

[53] AdlS, LiuM, XuX. Mapping soil nitrogen fractionation. Rhizosphere, 2020, 16 : 100279

[54] KibblewhiteM G, RitzK, SwiftM J. Soil health in agricultural systems. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 2008, 363( 1492): 685–701

[55] deVries F T, WallensteinM D. Below-ground connections underlying above-ground food production: a framework for optimising ecological connections in the rhizosphere. Journal of Ecology, 2017, 105( 4): 913–920

[56] ContiE, DiMauro L S, PluchinoA, MulderC. Testing for top-down cascading effects in a biomass-driven ecological network of soil invertebrates. Ecology and Evolution, 2020, 10( 14): 7062–7072

[57] TsiafouliM A, ThébaultE, SgardelisS P, deRuiter P C, vander Putten W H, BirkhoferK, HemerikL, deVries F T, BardgettR D, BradyM V, BjornlundL, JørgensenH B, ChristensenS, HertefeldtT D, HotesS, GeraHol W H, FrouzJ, LiiriM, MortimerS R, SetäläH, TzanopoulosJ, UtesenyK, PižlV, StaryJ, WoltersV, HedlundK. Intensive agriculture reduces soil biodiversity across Europe. Global Change Biology, 2015, 21( 2): 973–985

[58] BloorJ M G, Si-MoussiS, TaberletP, CarrèreP, HeddeM. Analysis of complex trophic networks reveals the signature of land-use intensification on soil communities in agroecosystems. Scientific Reports, 2021, 11( 1): 18260

[59] PresslerY, FosterE J, MooreJ C, CotrufoM F. Coupled biochar amendment and limited irrigation strategies do not affect a degraded soil food web in a maize agroecosystem, compared to the native grassland. Global Change Biology. Bioenergy, 2017, 9( 8): 1344–1355

[60] Sánchez-MorenoS, CanoM, López-PérezA, ReyBenayas J M. Microfaunal soil food webs in Mediterranean semi-arid agroecosystems. Does organic management improve soil health. Applied Soil Ecology, 2018, 125 : 138–147

[61] LiY, ChenY, LiJ, SunQ, LiJ, XuJ, LiuB, LangQ, QiaoY. Organic management practices enhance soil food web biomass and complexity under greenhouse conditions. Applied Soil Ecology, 2021, 167 : 104010

[62] HenneronL, BernardL, HeddeM, PelosiC, VillenaveC, ChenuC, BertrandM, GirardinC, BlanchartE. Fourteen years of evidence for positive effects of conservation agriculture and organic farming on soil life. Agronomy for Sustainable Development, 2015, 35( 1): 169–181

[63] BongiornoG, BodenhausenN, BünemannE K, BrussaardL, GeisenS, MäderP, QuistC W, WalserJ C, deGoede R G M. Reduced tillage, but not organic matter input, increased nematode diversity and food web stability in European long-term field experiments. Molecular Ecology, 2019, 28( 22): 4987–5005

[64] EisenhauerN, HörschV, MoeserJ, ScheuS. Synergistic effects of microbial and animal decomposers on plant and herbivore performance. Basic and Applied Ecology, 2010, 11( 1): 23–34

[65] NeilsonR, RobinsonD, MarriottC A, ScrimgeourC M, HamiltonD, WishartJ, BoagB, HandleyL L. Above-ground grazing affects floristic composition and modifies soil trophic interactions. Soil Biology & Biochemistry, 2002, 34( 10): 1507–1512

[66] WangB, WuL, ChenD, WuY, HuS, LiL, BaiY. Grazing simplifies soil micro-food webs and decouples their relationships with ecosystem functions in grasslands. Global Change Biology, 2020, 26( 2): 960–970

[67] WangB, WuY, ChenD M, HuS J, BaiY F. Legacy effect of grazing intensity mediates the bottom-up controls of resource addition on soil food webs. Journal of Applied Ecology, 2021, 58( 5): 976–987

[68] WanB, MeiX, HuZ, GuoH, ChenX, GriffithsB S, LiuM. Moderate grazing increases the structural complexity of soil micro-food webs by promoting root quantity and quality in a Tibetan alpine meadow. Applied Soil Ecology, 2021, 168 : 104161

[69] RamirezK S, GeisenS, MorriënE, SnoekB L, vander Putten W H. Network analyses can advance above-belowground ecology. Trends in Plant Science, 2018, 23( 9): 759–768

[70] FerreiraP A, BoscoloD, VianaB F. What do we know about the effects of landscape changes on plant-pollinator interaction networks. Ecological Indicators, 2013, 31 : 35–40

[71] MorrisonB M L, BrosiB J, DirzoR. Agricultural intensification drives changes in hybrid network robustness by modifying network structure. Ecology Letters, 2020, 23( 2): 359–369

[72] MorrisonB M L, DirzoR. Distinct responses of antagonistic and mutualistic networks to agricultural intensification. Ecology, 2020, 101( 10): e03116

[73] Martínez-NúñezC, ReyP J. Hybrid networks reveal contrasting effects of agricultural intensification on antagonistic and mutualistic motifs. Functional Ecology, 2021, 35( 6): 1341–1352

[74] AdedojaO, KehindeT. Changes in interaction network topology and species composition of flower-visiting insects across three land use types. African Journal of Ecology, 2018, 56( 4): 964–971

[75] Kovács-HostyánszkiA, FoldesiR, BaldiA, EndrediA, JordanF. The vulnerability of plant-pollinator communities to honeybee decline: a comparative network analysis in different habitat types. Ecological Indicators, 2019, 97 : 35–50

[76] Bustamante-CastilloM, Hernández-BañosB E, ArizmendiM D C. Hummingbird-plant visitation networks in agricultural and forested areas in a tropical dry forest region of Guatemala. Journal of Ornithology, 2020, 161( 1): 189–201

[77] LaBarT, CampbellC, YangS, AlbertR, SheaK. Restoration of plant-pollinator interaction networks via species translocation. Theoretical Ecology, 2014, 7( 2): 209–220

[78] MalenaS, MeliP, RovereA. Criteria to select vegetal species for restoration of plant-pollinator interactions in agricultural landscapes of the Pampa grassland (Argentina). Acta Oecologica, 2021, 111 : 103710

[79] Parra-TablaV, Campos-NavarreteM J, Arceo-GomezG. Plant-floral visitor network structure in a smallholder Cucurbitaceae agricultural system in the tropics: implications for the extinction of main floral visitors. Arthropod-Plant Interactions, 2017, 11( 5): 731–740

[80] PonisioL C, deValpine P, M’GonigleL K, KremenC. Proximity of restored hedgerows interacts with local floral diversity and species’ traits to shape long-term pollinator metacommunity dynamics. Ecology Letters, 2019, 22( 7): 1048–1060

[81] MoreiraE F, BoscoloD, VianaB F. Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PLoS One, 2015, 10( 4): e0123628

[82] RedheadJ W, WoodcockB A, PocockM J O, PywellR F, VanbergenA J, OliverT H. Potential landscape-scale pollinator networks across Great Britain: structure, stability and influence of agricultural land cover. Ecology Letters, 2018, 21( 12): 1821–1832

[83] RussoL, DebarrosN, YangS, SheaK, MortensenD. Supporting crop pollinators with floral resources: network-based phenological matching. Ecology and Evolution, 2013, 3( 9): 3125–3140

[84] VilhenaA M G F, RabeloL S, BastosE M A F, AugustoS C. Acerola pollinators in the savanna of Central Brazil: temporal variations in oil-collecting bee richness and a mutualistic network. Apidologie, 2012, 43( 1): 51–62

[85] SauveA M C, ThebaultE, PocockM J O, FontaineC. How plants connect pollination and herbivory networks and their contribution to community stability. Ecology, 2016, 97( 4): 908–917

[86] TheodorouP, AlbigK, RadzeviciuteR, SetteleJ, SchweigerO, MurrayT E, PaxtonR J. The structure of flower visitor networks in relation to pollination across an agricultural to urban gradient. Functional Ecology, 2017, 31( 4): 838–847

[87] CopleyJ. Ecology goes underground. Nature, 2000, 406( 6795): 452–454

[88] ShahK K, TripathiS, TiwariI, ShresthaJ, ModiB, PaudelN, DasB D. Role of soil microbes in sustainable crop production and soil health: a review. Agricultural Science and Technology, 2021, 13( 2): 109–118

[89] Lima-MendezG, FaustK, HenryN, DecelleJ, ColinS, CarcilloF, ChaffronS, Ignacio-EspinosaJ C, RouxS, VincentF, BittnerL, DarziY, WangJ, AudicS, BerlineL, BontempiG, CabelloA M, CoppolaL, Cornejo-CastilloF M, d’OvidioF, DeMeester L, FerreraI, Garet-DelmasM J, GuidiL, LaraE, PesantS, Royo-LlonchM, SalazarG, SánchezP, SebastianM, SouffreauC, DimierC, PicheralM, SearsonS, Kandels-LewisS, GorskyG, NotF, OgataH, SpeichS, StemmannL, WeissenbachJ, WinckerP, AcinasS G, SunagawaS, BorkP, SullivanM B, KarsentiE, BowlerC, deVargas C, RaesJ. Ocean plankton. Determinants of community structure in the global plankton interactome. Science, 2015, 348( 6237): 1262073

[90] BerryD, WidderS. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Frontiers in Microbiology, 2014, 5 : 219

[91] WaniF, AhmadD, AliT, MushtaqA. Role of microorganisms in nutrient mobilization and soil health—a review. Journal of Pure & Applied Microbiology, 2015, 9( 2): 1401–1410

[92] SelosseM A, BaudoinE, VandenkoornhuyseP. Symbiotic microorganisms, a key for ecological success and protection of plants. Comptes Rendus Biologies, 2004, 327( 7): 639–648

[93] ZhangG, WeiG, WeiF, ChenZ, HeM, JiaoS, WangY, DongL, ChenS. Dispersal limitation plays stronger role in the community assembly of fungi relative to bacteria in rhizosphere across the arable area of medicinal plant. Frontiers in Microbiology, 2021, 12 : 713523

[94] CardinaleM, GrubeM, ErlacherA, QuehenbergerJ, BergG. Bacterial networks and co-occurrence relationships in the lettuce root microbiota. Environmental Microbiology, 2015, 17( 1): 239–252

[95] MaW, YangZ, LiangL, MaQ, WangG, ZhaoT. Characteristics of the fungal communities and co-occurrence networks in hazelnut tree root endospheres and rhizosphere soil. Frontiers in Plant Science, 2021, 12 : 749871

[96] MarascoR, RolliE, FusiM, MichoudG, DaffonchioD. Grapevine rootstocks shape underground bacterial microbiome and networking but not potential functionality. Microbiome, 2018, 6( 1): 3

[97] BrissonV L, SchmidtJ E, NorthenT R, VogelJ P, GaudinA C M. Impacts of maize domestication and breeding on rhizosphere microbial community recruitment from a nutrient depleted agricultural soil. Scientific Reports, 2019, 9( 1): 15611

[98] SchmidtJ E, KentA D, BrissonV L, GaudinA C M. Agricultural management and plant selection interactively affect rhizosphere microbial community structure and nitrogen cycling. Microbiome, 2019, 7( 1): 146

[99] YanL, ZhangW, DuanW, ZhangY, ZhengW, LaiX. Temporal bacterial community diversity in the Nicotiana tabacum rhizosphere over years of continuous monocropping. Frontiers in Microbiology, 2021, 12 : 641643

[100] PivatoB, SemblatA, GuéganT, JacquiodS, MartinJ, DeauF, MoutierN, LecomteC, BurstinJ, LemanceauP. Rhizosphere bacterial networks, but not diversity, are impacted by pea-wheat intercropping. Frontiers in Microbiology, 2021, 12 : 674556

[101] ChenY, BonkowskiM, ShenY, GriffithsB S, JiangY, WangX, SunB. Root ethylene mediates rhizosphere microbial community reconstruction when chemically detecting cyanide produced by neighbouring plants. Microbiome, 2020, 8( 1): 4

[102] ShangJ Y, WuY, HuoB, ChenL, WangE T, SuiY, ChenW F, TianC F, ChenW X, SuiX H. Potential of Bradyrhizobia inoculation to promote peanut growth and beneficial Rhizobacteria abundance. Journal of Applied Microbiology, 2021, 131( 5): 2500–2515

[103] TangM J, ZhuQ, ZhangF M, ZhangW, YuanJ, SunK, XuF J, DaiC C. Enhanced nitrogen and phosphorus activation with an optimized bacterial community by endophytic fungus Phomopsis liquidambari in paddy soil. Microbiological Research, 2019, 221 : 50–59

[104] SchmidC A O, SchröderP, ArmbrusterM, SchloterM. Organic amendments in a long-term field trial— consequences for the bulk soil bacterial community as revealed by network analysis. Microbial Ecology, 2018, 76( 1): 226–239

[105] WuX, LiuY, ShangY, LiuD, LiesackW, CuiZ, PengJ, ZhangF. Peat-vermiculite alters microbiota composition towards increased soil fertility and crop productivity. Plant and Soil, 2022, 470( 1−2): 21–34

[106] WenT, ZhaoM, LiuT, HuangQ, YuanJ, ShenQ. High abundance of Ralstonia solanacearum changed tomato rhizosphere microbiome and metabolome. BMC Plant Biology, 2020, 20( 1): 166

[107] Fernández-GonzálezA J, CardoniM, Gómez-LamaCabanás C, Valverde-Corredor A, VilladasP J, Fernández-López M, Mercado-BlancoJ. Linking belowground microbial network changes to different tolerance level towards Verticillium wilt of olive. Microbiome, 2020, 8( 1): 11

[108] MaY, WeisenhornP, GuoX, WangD, YangT, ShiY, ZhangH, ChuH. Effect of long-term fertilization on bacterial communities in wheat endosphere. Pedosphere, 2021, 31( 4): 538–548

Acknowledgements

This work was funded by the National Key Research and Development Program of China (2021YFD190090307), the National Natural Science Foundation of China (31901108), the Beijing Natural Science Foundation (5222014), and the 2115 Talent Development Program of China Agricultural University.

Compliance with ethics guidelines

Ying Gong, Langqin Yu, and Lei Zhao declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2022. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)