in

Acquisition and evolution of enhanced mutualism—an underappreciated mechanism for invasive success?

  • Pimentel D, McNair S, Janecka J, Wightman J, Simmonds C, O’Connell C, et al. Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ. 2001;84:1–20.

    Article 

    Google Scholar 

  • Diagne C, Leroy B, Vaissière AC, Gozlan RE, Roiz D, Jarić I, et al. High and rising economic costs of biological invasions worldwide. Nature. 2021;592:571–6.

    Article 
    CAS 

    Google Scholar 

  • Catford JA, Jansson R, Nilsson C. Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib. 2009;15:22–40.

    Article 

    Google Scholar 

  • Pearson DE, Ortega YK, Eren Ö, Hierro JL. Community assembly theory as a framework for biological invasions. Trends Ecol Evol. 2018;33:313–25.

    PubMed 
    Article 

    Google Scholar 

  • Inderjit, van der Putten WH. Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol. 2010;25:512–9.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Keane RM, Crawley MJ. Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol. 2002;17:164–70.

    Article 

    Google Scholar 

  • Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, et al. Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol. 2006;4:e140.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Hierro JL, Callaway RM. Allelopathy and exotic plant invasion. Plant Soil. 2003;256:29–39.

    Article 
    CAS 

    Google Scholar 

  • Reinhart KO, Callaway RM. Soil biota and invasive plants. N Phytol. 2006;170:445–57.

    Article 

    Google Scholar 

  • Waller LP, Allen WJ, Barratt BIP, Condron LM, França FM, Hunt JE, et al. Biotic interactions drive ecosystem responses to exotic plant invaders. Science. 2020;368:967–72.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • McLeod ML, Cleveland CC, Lekberg Y, Maron JL, Philippot L, Bru D, et al. Exotic invasive plants increase productivity, abundance of ammonia-oxidizing bacteria and nitrogen availability in intermountain grasslands. J Ecol. 2016;104:994–1002.

    Article 
    CAS 

    Google Scholar 

  • Saul WC, Jeschke JM. Eco-evolutionary experience in novel species interactions. Ecol Lett. 2015;18:236–45.

    PubMed 
    Article 

    Google Scholar 

  • Desprez-Loustau M, Robin C, Buee M, Courtecuisse R, Garbaye J, Suffert F, et al. The fungal dimension of biological invasions. Trends Ecol Evol. 2007;22:472–80.

    PubMed 
    Article 

    Google Scholar 

  • Hierro JL, Maron JL, Callaway RM. A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol. 2005;93:5–15.

    Article 

    Google Scholar 

  • Callaway RM, Thelen GC, Rodriguez A, Holben WE. Soil biota and exotic plant invasion. Nature. 2004;427:731–3.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Maron JL, Klironomos J, Waller L, Callaway RM. Invasive plants escape from suppressive soil biota at regional scales. J Ecol. 2014;102:19–27.

    Article 

    Google Scholar 

  • Brundrett MC. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil. 2009;320:37–77.

    Article 
    CAS 

    Google Scholar 

  • Smith SE, Read DJ. Mycorrhizal symbiosis. London: Academic Press; 2008.

  • O’Neill EG, O’Neill RV, Norby RJ. Hierarchy theory as a guide to mycorrhizal research on large-scale problems. Environ Pollut. 1991;73:271–84.

    PubMed 
    Article 

    Google Scholar 

  • Johnson NC, Wilson GWTT, Wilson JA, Miller RM, Bowker MA. Mycorrhizal phenotypes and the Law of the Minimum. N Phytol. 2015;205:1473–84.

    Article 
    CAS 

    Google Scholar 

  • Lekberg Y, Arnillas CA, Borer ET, Bullington LS, Fierer N, Kennedy PG, et al. Nitrogen and phosphorus fertilization consistently favor pathogenic over mutualistic fungi in grassland soils. Nat Commun. 2021;12:3484.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton S, Rejmanek M. Plant invasions – the role of mutualisms. Biol Rev. 2000;75:65–93.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Marler MJ, Zabinski CA, Callaway RM. Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology. 1999;80:1180–6.

    Article 

    Google Scholar 

  • Soti PG, Jayachandran K, Purcell M, Volin JC, Kitajima K. Mycorrhizal symbiosis and Lygodium microphyllum invasion in South Florida—a biogeographic comparison. Symbiosis. 2014;62:81–90.

    Article 

    Google Scholar 

  • Fumanal B, Plenchette C, Chauvel B, Bretagnolle F. Which role can arbuscular mycorrhizal fungi play in the facilitation of Ambrosia artemisiifolia L. invasion in France? Mycorrhiza. 2006;17:25–35.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Hart MM, Reader RJ. Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. N Phytol. 2002;153:335–44.

    Article 

    Google Scholar 

  • Maherali H, Klironomos JN. Influence of phylogeny on fungal community assembly and ecosystem functioning. Science. 2007;316:1746–8.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Kivlin SN, Hawkes CV, Treseder KK. Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem. 2011;43:2294–303.

    Article 
    CAS 

    Google Scholar 

  • Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A, et al. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science. 2015;349:970–3.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, et al. Biotic interactions and plant invasions. Ecol Lett. 2006;9:726–40.

    PubMed 
    Article 

    Google Scholar 

  • Ehrenfeld JG. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems. 2003;6:503–23.

    Article 
    CAS 

    Google Scholar 

  • Rout ME, Chrzanowski TH. The invasive Sorghum halepense harbors endophytic N2-fixing bacteria and alters soil biogeochemistry. Plant Soil. 2009;315:163–72.

    Article 
    CAS 

    Google Scholar 

  • Sardans J, Bartrons M, Margalef O, Gargallo-Garriga A, Janssens IA, Ciais P, et al. Plant invasion is associated with higher plant-soil nutrient concentrations in nutrient-poor environments. Glob Change Biol. 2017;23:1282–91.

    Article 

    Google Scholar 

  • Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D. Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia. 2005;144:1–11.

    PubMed 
    Article 

    Google Scholar 

  • Lankau RA. Resistance and recovery of soil microbial communities in the face of Alliaria petiolata invasions. N Phytol. 2011;189:536–48.

    Article 

    Google Scholar 

  • Blossey B, Nötzold R. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol. 1995;83:887–9.

    Article 

    Google Scholar 

  • van Kleunen M, Bossdorf O, Dawson W. The ecology and evolution of alien plants. Annu Rev Ecol Evol Syst. 2018;49:25–47.

    Article 

    Google Scholar 

  • Rosche C, Hensen I, Schaar A, Zehra U, Jasieniuk M, Callaway RM, et al. Climate outweighs native vs. nonnative range‐effects for genetics and common garden performance of a cosmopolitan weed. Ecol Monogr. 2019;89:e01386.

    Article 

    Google Scholar 

  • Weaver SE. The biology of Canadian weeds. 115. Conyza canadensis. Can J Plant Sci. 2001;81:867–75.

    Article 

    Google Scholar 

  • Gange AC, Ayres RL. On the relation between arbuscular mycorrhizal colonization and plant ’ benefit. Oikos. 1999;87:615–21.

    Article 

    Google Scholar 

  • Řezáčová V, Konvalinková T, Řezáč M. Decreased mycorrhizal colonization of Conyza canadensis (L.) Cronquist in invaded range does not affect fungal abundance in native plants. Biologia. 2020;75:693–9.

    Article 

    Google Scholar 

  • Zhang Q, Sun Q, Koide RT, Peng Z, Zhou J, Gu X, et al. Arbuscular mycorrhizal fungal mediation of plant-plant onteractions in a marshland plant community. Sci World J. 2014;2014:1–10.

    Google Scholar 

  • Zhang HY, Goncalves P, Copeland E, Qi SS, Dai ZC, Li GL, et al. Invasion by the weed Conyza canadensis alters soil nutrient supply and shifts microbiota structure. Soil Biol Biochem. 2020;143:107739.

    Article 
    CAS 

    Google Scholar 

  • Shah MA, Callaway RM, Shah T, Houseman GR, Pal RW, Xiao S, et al. Conyza canadensis suppresses plant diversity in its nonnative ranges but not at home: a transcontinental comparison. N Phytol. 2014;202:1286–96.

    Article 

    Google Scholar 

  • Colautti RI, Lau JA. Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol Ecol. 2015;24:1999–2017.

    PubMed 
    Article 

    Google Scholar 

  • Rosche C, Hensen I, Lachmuth S. Local pre-adaptation to disturbance and inbreeding-environment interactions affect colonisation abilities of diploid and tetraploid Centaurea stoebe. Plant Biol. 2018;20:75–84.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Hart SC, Start JM, Davidson EA, Firestone MK. Nitrogen mineralization, immobilization, and nitrification. In: Weaver RW, Angle J., Bottomley P., editors. Methods of soil analysis, part 2 microbiological and biochemical properties. Madison, WI: Soil Science Society of America; 1994. p. 985–1018.

  • Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N. Working with mycorrhizas in forestry and agriculture. ACIAR Monogr. 1996;32:1–374.

    Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA. A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. N Phytol. 1990;115:495–501.

    Article 
    CAS 

    Google Scholar 

  • Fick SE, Hijmans RJ. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol. 2017;4315:4302–15.

    Article 

    Google Scholar 

  • Hijmans RJ. raster: Geographic data analysis and modeling. R package version 3.3-13. 2020. https://cran.r-project.org/package=raster.

  • R Core Team. R: A language and environment for statistical computing [https://www.r-project.org/]. Vienna, Austria: R Foundation for Statistical Computing; 2019.

  • Oksanen J, Guillaume BF, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. R package. 2019. https://cran.r-project.org/package=vegan.

  • Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, et al. Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. N Phytol. 2011;190:794–804.

    Article 
    CAS 

    Google Scholar 

  • Lee J, Lee S, Young JPW. Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol. 2008;65:339–49.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Bullington LS, Lekberg Y, Larkin BG. Insufficient sampling constrains our characterization of plant microbiomes. Sci Rep. 2021;11:3645.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.

    PubMed 
    PubMed Central 
    CAS 

    Google Scholar 

  • Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, et al. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). N Phytol. 2010;188:223–41.

    Article 
    CAS 

    Google Scholar 

  • Chen J. GUniFrac: generalized UniFrac distances. R package version 1.1. 2018. https://cran.r-project.org/package=GUniFrac.

  • Webb CO. Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat. 2000;156:145–55.

    PubMed 
    Article 

    Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics. 2010;26:1463–4.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Price MN, Dehal PS, Arkin AP. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5:e9490.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Yu G, Smith DK, Zhu H, Guan Y, Lam TT. GGTREE: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol. 2017;8:28–36.

    Article 

    Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2014;67.

  • Borcard D, Gillet F, Legendre P. Numerical ecology with R. New York: Springer; 2011.

  • Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 1995;57:289–300.

    Google Scholar 

  • Anderson MJ, Walsh DCI. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr. 2013;83:557–74.

    Article 

    Google Scholar 

  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Felker-Quinn E, Schweitzer JA, Bailey JK. Meta-analysis reveals evolution in invasive plant species but little support for Evolution of Increased Competitive Ability (EICA). Ecol Evol. 2013;3:739–51.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Pal RW, Maron JL, Nagy DU, Waller LP, Tosto A, Liao H, et al. What happens in Europe stays in Europe: apparent evolution by an invader does not help at home. Ecology 2020;101:e03072.

    PubMed 
    Article 

    Google Scholar 

  • Matesanz S, Sultan SE. High-performance genotypes in an introduced plant: insights to future invasiveness. Ecology. 2013;94:2464–74.

    PubMed 
    Article 

    Google Scholar 

  • Hart M, Reader R. Host plant benefit from association with arbuscular mycorrhizal fungi: variation due to differences in size of mycelium. Biol Fertil Soils. 2002;36:357–66.

    Article 

    Google Scholar 

  • Yang H, Zhang Q, Koide RT, Hoeksema JD, Tang J, Bian X, et al. Taxonomic resolution is a determinant of biodiversity effects in arbuscular mycorrhizal fungal communities. J Ecol. 2017;105:219–28.

    Article 
    CAS 

    Google Scholar 

  • Moora M, Berger S, Davison J, Öpik M, Bommarco R, Bruelheide H, et al. Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. J Biogeogr. 2011;38:1305–17.

    Article 

    Google Scholar 

  • Policelli N, Bruns TD, Vilgalys R, Nuñez MA. Suilloid fungi as global drivers of pine invasions. N Phytol. 2019;222:714–25.

    Article 

    Google Scholar 

  • Jia Y, Heijden MGA, Wagg C, Feng G, Walder F. Symbiotic soil fungi enhance resistance and resilience of an experimental grassland to drought and nitrogen deposition. J Ecol. 2021;109:3171–81.

    Article 
    CAS 

    Google Scholar 

  • Van Der Heijden MGAA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature. 1998;396:69–72.

    Article 
    CAS 

    Google Scholar 

  • Zhang Q, Yang R, Tang J, Yang H, Hu S, Chen X. Positive feedback between mycorrhizal fungi and plants influences plant invasion success and resistance to invasion. PLoS ONE. 2010;5:e12380.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Shah MA, Reshi ZA, Khasa DP. Arbuscular mycorrhizas: drivers or passengers of alien plant invasion. Bot Rev. 2009;75:397–417.

    Article 

    Google Scholar 

  • Valverde-Barrantes OJ, Horning AL, Smemo KA, Blackwood CB. Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms. Plant Soil. 2016;404:1–12.

    Article 
    CAS 

    Google Scholar 

  • Wilson GWT, Hartnett DC. Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot. 1998;85:1732–8.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Seifert EK, Bever JD, Maron JL. Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 2009;90:1055–62.

    PubMed 
    Article 

    Google Scholar 

  • Deveautour C, Donn S, Power SA, Bennett AE, Powell JR. Experimentally altered rainfall regimes and host root traits affect grassland arbuscular mycorrhizal fungal communities. Mol Ecol. 2018;27:2152–63.

    PubMed 
    Article 

    Google Scholar 

  • Osborne OG, De-Kayne R, Bidartondo MI, Hutton I, Baker WJ, Turnbull CGN, et al. Arbuscular mycorrhizal fungi promote coexistence and niche divergence of sympatric palm species on a remote oceanic island. N Phytol. 2018;217:1254–66.

    Article 
    CAS 

    Google Scholar 

  • Tian B, Pei Y, Huang W, Ding J, Siemann E. Increasing flavonoid concentrations in root exudates enhance associations between arbuscular mycorrhizal fungi and an invasive plant. ISME J. 2021;15:1919–30.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Pimprikar P, Gutjahr C. Transcriptional regulation of arbuscular mycorrhiza development. Plant Cell Physiol. 2018;59:673–90.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Wendlandt CE, Helliwell E, Roberts M, Nguyen KT, Friesen ML, Wettberg E, et al. Decreased coevolutionary potential and increased symbiont fecundity during the biological invasion of a legume‐rhizobium mutualism. Evolution. 2021;75:731–47.

    PubMed 
    Article 

    Google Scholar 

  • Callaway RM, Bedmar EJ, Reinhart KO, Silvan CG, Klironomos J. Effects of soil biota from different ranges on Robinia invasion: acquiring mutualists and escaping pathogens. Ecology. 2011;92:1027–35.

    PubMed 
    Article 

    Google Scholar 

  • Shelby N, Duncan RP, Putten WH, McGinn KJ, Weser C, Hulme PE. Plant mutualisms with rhizosphere microbiota in introduced versus native ranges. J Ecol. 2016;104:1259–70.

    Article 
    CAS 

    Google Scholar 

  • Yang Q, Carrillo J, Jin H, Shang L, Hovick SM, Nijjer S, et al. Plant–soil biota interactions of an invasive species in its native and introduced ranges: Implications for invasion success. Soil Biol Biochem. 2013;65:78–85.

    Article 
    CAS 

    Google Scholar 

  • Bronstein JL. The exploitation of mutualisms. Ecol Lett. 2001;4:277–87.

    Article 

    Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science. 2011;333:880–2.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Koziol L, Bever JD. Mycorrhizal feedbacks generate positive frequency dependence accelerating grassland succession. J Ecol. 2019;107:622–32.

    Article 

    Google Scholar 

  • Yang H, Yuan Y, Zhang Q, Tang J, Liu Y, Chen X. Changes in soil organic carbon, total nitrogen, and abundance of arbuscular mycorrhizal fungi along a large-scale aridity gradient. Catena. 2011;87:70–7.

    Article 
    CAS 

    Google Scholar 

  • Zhang J, Wang F, Che R, Wang P, Liu H, Ji B, et al. Precipitation shapes communities of arbuscular mycorrhizal fungi in Tibetan alpine steppe. Sci Rep. 2016;6:23488.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Read DJ. Mycorrhizas in ecosystems. Experientia. 1991;47:376–91.

    Article 

    Google Scholar 

  • Delavaux CS, Smith-Ramesh LM, Kuebbing SE. Beyond nutrients: a meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology. 2017;98:2111–9.

    PubMed 
    Article 

    Google Scholar 


  • Source: Ecology - nature.com

    Root exudate composition reflects drought severity gradient in blue grama (Bouteloua gracilis)

    Helping cassava farmers by extending crop life