287
Views
1
CrossRef citations to date
0
Altmetric
Original Article

The presence of a foreign microbial community promotes plant growth and reduces filtering of root fungi in the arctic-alpine plant Silene acaulis

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 377-390 | Received 21 Jul 2020, Accepted 30 Nov 2020, Published online: 06 Jul 2021

References

  • Abarenkov K, Zirk A, Piirmann T, Pöhönen R, Ivanov F, Nilsson RH, Kõljalg U. 2020. UNITE general FASTA release for Fungi 2. Version. 04: 02.2020.
  • Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26:32–46.
  • Bagi B, Nagy C, Tóth A,Palkovics L, Petróczy M. 2020. Plenodomus biglobosus on oilseed rape in Hungary. Phytopathol Mediterr. 59:345–351. doi:10.14601/Phyto-11099
  • Berendsen RL, Pieterse CMJ, Bakker PAHM. 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17(8):478–486. doi:10.1016/j.tplants.2012.04.001.
  • Bernardet J-F, Bowman JP. 2006. The genus Flavobacterium. In: M D F, Rosenberg S, Schleifer EK, editors. The Prokaryotes, Third. New York (NY): Springer-Verlag; p. 481–531.
  • Bever JD, Platt TG, Morton ER. 2012. Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol. 66(1):265–283. doi:10.1146/annurev-micro-092611-150107.
  • Bouffaud M-L, Poirier M-A, Muller D, Moënne-Loccoz Y. 2014. Root microbiome relates to plant host evolution in maize and other Poaceae. Environ Microbiol. 16(9):2804–2814. doi:10.1111/1462-2920.12442.
  • Bueno de Mesquita CP, Sartwell SA, Ordemann E V., et al. 2018. Patterns of root colonization by arbuscular mycorrhizal fungi and dark septate endophytes across a mostly-unvegetated, high-elevation landscape. Fungal Ecol. 36:63–74. doi:10.1016/j.funeco.2018.07.009
  • Callahan BJ, McMurdie PJ, Rosen MJ,Han AW, Johnson AJA, Holmes SP. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 13:581–583. doi:10.1038/nmeth.3869
  • Callaway RM, Thelen GC, Rodriguez A, Holben WE. 2004. Soil biota and exotic plant invasion. Nature. 427:731–733. doi:10.1038/nature02322
  • Chaparro JM, Badri DV, Vivanco JM. 2014. Rhizosphere microbiome assemblage is affected by plant development. Isme J. 8:790–803. doi:10.1038/ismej.2013.196
  • Chater AO, Walters SM, Akeroyd JR, 1993. Flora Europaea, : psilotaceae to Platanaceae. Vol. 1. 209. 2nd edn. Cambridge University Press. Cambridge, England.
  • Chen I-C, Hill JK, Ohlemüller R, Roy DB, Thomas CD. 2011. Rapid range shifts of species associated with high levels of climate warming. Science (80-). 333:1024–1026. doi:10.1126/science.1206432
  • Core Team R. 2019. R: a language and environment for statistical computing
  • Diez JM, Dickie I, Edwards G,Hulme PE, Sullivan JJ, Duncan RP. 2010. Negative soil feedbacks accumulate over time for non-native plant species. Ecol Lett. 13:803–809. doi:10.1111/j.1461-0248.2010.01474.x
  • Doak DF, Morris WF. 2010. Demographic compensation and tipping points in climate-induced range shifts. Nature. 467:959–962.
  • Douglas AE. 1998. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria buchnera. Annu Rev Entomol. 43:17–37. doi:10.1146/annurev.ento.43.1.17
  • Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 10:996–998. doi:10.1038/nmeth.2604
  • Edwards JA, Johnson C, Santos-Medellín C,Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V, Jeffery LD. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci U S A. 112:E911–E920. doi:10.1073/pnas.1414592112
  • Edwards JA, Santos-Medellín CM, Liechty ZS, Nguyen B, Lurie E, Eason S, Phillips G, Sundaresan V. 2018. Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice. PLoS Biol. 16:1–28. doi:10.1371/journal.pbio.2003862
  • Fang K, Bao ZSN, Chen L,Zhou J, Yang ZP, Dong XF, Zhang HB. 2019. Growth-promoting characteristics of potential nitrogen-fixing bacteria in the root of an invasive plant Ageratina adenophora. PeerJ. 2019:e7099. doi:10.7717/peerj.7099
  • Fierer N, Jackson RB. 2006. The diversity and biogeography of soil bacterial communities. PNAS. 103:626–631.
  • Fitzpatrick CR, Copeland J, Wang PW,Guttman DS, Kotanen PM, Johnson MTJ. 2018. Assembly and ecological function of the root microbiome across angiosperm plant species. Proc Natl Acad Sci U S A. 115:E1157–E1165. doi:10.1073/pnas.1717617115
  • Franke-Whittle IH, Manici LM, Insam H, Stres B. 2015. Rhizosphere bacteria and fungi associated with plant growth in soils of three replanted apple orchards. Plant Soil. 395:317–333. doi:10.1007/s11104-015-2562-x
  • Gaiero JR, McCall CA, Thompson KA,Day NJ, Best AS, Dunfield KE. 2013. Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot. 100:1738–1750. doi:10.3732/ajb.1200572
  • Gray LK, Hamann A. 2013. Tracking suitable habitat for tree populations under climate change in western north america. Clim Change. 117:289–303. doi:10.1007/s10584-012-0548-8
  • Gussarova G, Allen GA, Mikhaylova Y,McCormick LJ, Mirré V, Marr KL, Hebda RJ, Brochmann C. 2015. Vicariance, long-distance dispersal, and regional extinction-recolonization dynamics explain the disjunct circumpolar distribution of the arctic-alpine plant Silene acaulis. Am J Bot. 102:1703–1720. doi:10.3732/ajb.1500072
  • Hewitt G. 2000. The genetic legacy of the quaternary ice ages. Nature. 405:907–913. doi:10.1038/35016000
  • Hirsch PR, Mauchline TH. 2012. Who’s who in the plant root microbiome? Nat Biotechnol. 30:961–962. doi:10.1038/nbt.2387
  • Hultén E 1971. The circumpolar plants. 2. Dicotyledons. Almqvist & Wiksell
  • Inderjit VDPWH. 2010. Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol. 25:512–519. doi:10.1016/j.tree.2010.06.006
  • IPCC. 2013. Climate Change 2013: The physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change
  • Jalas J, Suominen J 1986. Atlas florae Europaeae: distribution of vascular plants in europe, volume 7: caryophyllaceae (silenoideae); Silene acaulis (L.) Jacq. - Map 1167 - p.82. Committee for Mapping the Flora of Europe, Helsinki
  • Jump AS, Peñuelas J. 2005. Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett. 8:1010–1020. doi:10.1111/j.1461-0248.2005.00796.x
  • Keane RM, Crawley MJ 2002. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol.
  • King AJ, Farrer EC, Suding KN, Schmidt SK. 2012. Co-occurrence patterns of plants and soil bacteria in the high-alpine subnival zone track environmental harshness. Front Microbiol. 3:347. doi:10.3389/fmicb.2012.00347
  • Kittel TGF, Williams MW, Chowanski K,Hartman M, Ackerman T, Losleben M, Blanken PD. 2015. Contrasting long-term alpine and subalpine precipitation trends in a mid-latitude north american mountain system, colorado front range, USA. Plant Ecol Divers. 8:607–624. doi:10.1080/17550874.2016.1143536
  • Koske RE, Gemma JN. 1989. A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res. 92:486–488. doi:10.1016/S0953-7562(89)80195-9
  • Lakshmanan V. 2015. Root microbiome assemblage is modulated by plant host factors. Adv Bot Res. 75:57–79.doi:10.1016/bs.abr.2015.09.004
  • Lareen A, Burton F, Schäfer P. 2016. Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol. 90:575–587. doi:10.1007/s11103-015-0417-8
  • Lee KH, Koh RH, Song HG. 2008. Enhancement of growth and yield of tomato by Rhodopseudomonas spunder greenhouse conditions. J Microbiol. 46:641–646. doi:10.1007/s12275-008-0159-2
  • Losleben M 2017. Air temperature data for D1 chart recorder from 1952/10/1 - ongoing, daily. [Accessed 2018 May 31]. http://niwot.colorado.edu/index.php/data/data/air-temperature-data-for-d1-chart-recorder-1952-ongoing
  • Ma S, De Frenne P, Wasof S,Brunet J, Cousins SAO, Decocq G, Kolb A, Lemke I, Liira J, Naaf T, Orczewska A, Plue J, Wulf M, Verheyen K. 2019. Plant–soil feedbacks of forest understorey plants transplanted in nonlocal soils along a latitudinal gradient. Plant Biol. 21:677–687. doi:10.1111/plb.12960
  • McGonigle TP, Miller MH, Evans DG,Fairchild GL, Swan JA. 1990. A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol. 115:495–501. doi:10.1111/j.1469-8137.1990.tb00476.x
  • McLaren MR 2020. Silva SSU taxonomic training data formatted for DADA2 (silva version 138) (version 2) [data set]
  • Menzies JG, Ehret DL, Koch C, Bogdanoff C. 1998. Humicola fuscoatra infects tomato roots, but is not pathogenic. Eur J Plant Pathol. 104:769–775. doi:10.1023/A:1008680018677
  • MGA VDH, Bardgett RD, van Straalen NM. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett. 11:296–310. doi:10.1111/j.1461-0248.2007.01139.x
  • Mitchell CE, Power AO. 2003. Release of invasive plants from fungal and viral pathogens. Nature. 421:625–627. doi:10.1038/nature01317
  • Morriën E, van der Putten WH. 2013. Soil microbial community structure of range-expanding plant species differs from co-occurring natives. J Ecol. 101:1093–1102. doi:10.1111/1365-2745.12117
  • Morris WF, Doak DF. 1998. Life history of the long-lived gynodioecious cushion plant Silene acaulis (Caryophyllaceae), inferred from size-based population projection matrices. Am J Bot. 85:784–793. doi:10.2307/2446413
  • Nguyen NH, Song Z, Bates ST,Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG. 2016. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 20:241–248. doi:10.1016/j.funeco.2015.06.006
  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, et al. 2019. vegan: community ecology package. R Package Version. 2:5–6.
  • Osman M, Stigloher C, Mueller MJ, Waller F. 2020. An improved growth medium for enhanced inoculum production of the plant growth-promoting fungus serendipita indica. Plant Methods. 16:39. doi:10.1186/s13007-020-00584-7
  • Pauli H, Gottfried M, Reiter K, Klettner C, Grabherr G. 2007. Signals of range expansions and contractions of vascular plants in the high alps: observations (1994-2004) at the gloria *master site schrankogel, tyrol, austria. Glob Chang Biol. 13:147–156. doi:10.1111/j.1365-2486.2006.01282.x
  • Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH. 2013. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol. 11:789.
  • Porazinska DL, Farrer EC, Spasojevic MJ, Bueno de Mesquita CP, Sartwell SA, Smith JG, White CT, King AJ, Suding KN, Schmidt SK. 2018. Plant diversity and density predict belowground diversity and function in an early successional alpine ecosystem. Ecology. 99:1942–1952. doi:10.1002/ecy.2420
  • Prober SM, Leff JW, Bates ST, Borer ET, Firn J, Harpole WS, Lind EM, Seabloom EW, Adler PB, Bakker JD,et al. 2015. Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett. 18:85–95. doi:10.1111/ele.12381
  • Qiu W, Su H, Yan L,Ji K, Liu Q, Jian H. 2020. Organic fertilization assembles fungal communities of wheat rhizosphere soil and suppresses the population growth of Heterodera avenae in the field. Front Plant Sci. 11:1225. doi:10.3389/fpls.2020.01225
  • Richardson DM, Pyšek P. 2006. Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geogr Earth Environ. 30:409–431. doi:10.1191/0309133306pp490pr
  • Rodríguez-Caballero G, Caravaca F, Díaz G, Torres P, Roldán A. 2020. The invader Carpobrotus edulis promotes a specific rhizosphere microbiome across globally distributed coastal ecosystems. Sci Total Environ. 719. doi:10.1016/j.scitotenv.2020.137347.
  • Roy J, Bonneville J-M, Saccone P, Ibanez S, Albert CH, Boleda M, Gueguen M, Ohlmann M, Rioux D, Clément J-C, et al. 2018. Differences in the fungal communities nursed by two genetic groups of the alpine cushion plant, Silene acaulis. Ecol Evol. 8:11568–11581. doi:10.1002/ece3.4606
  • Sasse J, Martinoia E, Northen T. 2018. Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci. 23:25–41. doi:10.1016/j.tplants.2017.09.003
  • Schmidt SK, Sobieniak-Wiseman LC, Kageyama SA, Halloy SRP, Schadt CW. 2008. Mycorrhizal and dark-septate fungi in plant roots above 4270 meters elevation in the andes and rocky mountains. Arctic, Antarct Alp Res. 40:576–583. doi:10.1657/1523-0430(07-068)
  • Sen D, Paul K, Saha C,Mukherjee G, Nag M, Ghosh S, Das A, Seal A, Tripathy S. 2019. A unique life-strategy of an endophytic yeast Rhodotorula mucilaginosa JGTA-S1—a comparative genomics viewpoint. DNA Res. 26:131–146. doi:10.1093/dnares/dsy044
  • Settele J, Scholes R, Betts R, Bunn S, Leadley PW, Nepstad D, Overpeck JT, Taboada MA. 2014. Terrestrial and inland water systems. Field CB, Barros VR, Dokken DJ, Mach KJ, MacCracken S, Mastandrea PR, White LL editors Climate Change 2014: impacts, Adaptation, and Vulnerability. Part A: global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge. UK and New York (USA):271–359.
  • Shen Z, Ruan Y, Xue C, Zhong S, Li R, Shen Q. 2015. Soils naturally suppressive to banana Fusarium wilt disease harbor unique bacterial communities. Plant Soil. 393:21–33. doi:10.1007/s11104-015-2474-9
  • Smith DS, Schweitzer JA, Turk P, Bailey JK, Hart SC, Shuster SM, Whitham TG. 2012. Soil-mediated local adaptation alters seedling survival and performance. Plant Soil. 352:243–251. doi:10.1007/s11104-011-0992-7
  • Tedersoo L, Bahram M, Polme S,Koljalg U, Yorou N, Wijesundera R, Villarreal Ruiz L, Vasco-Palacios AM, Thu PQ, Suija A, et al. 2014. Global diversity and geography of soil fungi. Science (80-). 346: 10.1126/science.aaa1185 10.1126/science.aaa1185
  • Thuiller W, Albert C, Araújo MB, Berry PM, Cabeza M, Guisan A, Hickler T, Midgley GF, Paterson J, Schurr FM, et al. 2008. Predicting global change impacts on plant species’ distributions: future challenges. Perspect Plant Ecol Evol Syst. 9:137–152. doi:10.1016/j.ppees.2007.09.004
  • van der Putten WH. 2012. Climate change, aboveground-belowground interactions, and species’ range shifts. Annu Rev Ecol Evol Syst. 43:365–383. doi:10.1146/annurev-ecolsys-110411-160423
  • van der Putten WH, Macel M, Visser ME. 2010. Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos Trans R Soc Lond B Biol Sci. 365:2025–2034. doi:10.1098/rstb.2010.0037
  • Wallander H, Johansson U, Sterkenburg E, Brandström Durling M, Lindahl BD. 2010. Production of ectomycorrhizal mycelium peaks during canopy closure in Norway spruce forests. New Phytol. 187:1124–1134. doi:10.1111/j.1469-8137.2010.03324.x
  • Walsh S. 2012. A Summary Of Climate Averages For Ireland 1981-2010, Climatological Note No. 14. Met Éireann: Dublin
  • Weinert N, Piceno Y, Ding G-C, Meincke R, Heuer H, Berg G, Schloter M, Andersen G, Smalla K. 2011. PhyloChip hybridization uncovered an enormous bacterial diversity in the rhizosphere of different potato cultivars: many common and few cultivar-dependent taxa. FEMS Microbiol Ecol. 75:497–506.
  • White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T, editors. PCR Protocols. Academic Press: New York; p. 315–322.
  • Wirth F, Goldani LZ. 2012. Epidemiology of Rhodotorula: An emerging pathogen. Interdiscip. Perspect. Infect. Dis.2012:465717.
  • Wong W-T, Tseng C-H, Hsu S-H,Lur H-S, Mo C-W, Huang C-N, Hsu S-C, Lee K-T, Liu C-T. 2014. Promoting effects of a single Rhodopseudomonas palustris inoculant on plant growth by brassica rapa chinensis under low fertilizer input. Microbes Environ. 29:303–313. doi:10.1264/jsme2.ME14056
  • Yang Q, Carrillo J, Jin H,Shang L, Hovick SM, Nijjer S, Gabler CA, Li B, Siemann E. 2013. Plant–soil biota interactions of an invasive species in its native and introduced ranges: implications for invasion success. Soil Biol Biochem. 65:78–85. doi:10.1016/j.soilbio.2013.05.004
  • Zhang FJ, Li Q, Chen FX, Xu HY, Inderjit, Wan FH. 2017. Arbuscular mycorrhizal fungi facilitate growth and competitive ability of an exotic species Flaveria bidentis. Soil Biol Biochem. 115:275–284. doi:10.1016/j.soilbio.2017.08.019

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.