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The invasion of semiarid Mediterranean sites by Nicotiana glauca mediates temporary changes in mycorrhizal associations and a permanent decrease in rhizosphere activity

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Abstract

Background and aims

Exotic invasive plants may have adverse effects on native plant communities and ecosystem functions by altering communities of belowground mutualistic mycorrhizal fungi. However, little is known about how such alterations change over time. The aim of this work was to determine the arbuscular mycorrhizal fungi (AMF) communities colonizing the roots of Nicotiana glauca populations of distinct ages (1 and 20 years old), and of co-occurring native plants, growing at four different Mediterranean semiarid locations. The short-term and long-term effects of the invader on rhizosphere activity and nutrient pools were also determined.

Methods

Illumina MiSeq technology was used for high-throughput sequencing of AMF communities and basal respiration and enzymatic activities were determined for assessing rhizosphere activity.

Results

The composition and structure of AMF communities differed according to the invasive character of plant and the invaded site. The AMF community belonging to the young invasive plants had a significantly different structure and composition in comparison to the native plants and the adult invasive plants. However, the native plants and the adult invasive plants harboured a similar AMF community. In general, basal respiration, enzymatic activities and nutrients of the rhizospheres of two populations of N. glauca of distinct ages were significantly different from those of the rhizosphere of native plants, but these differences were independent of the time after the invasion.

Conclusions

The invasion of semiarid Mediterranean sites by N. glauca mediated temporary changes in mycorrhizal associations, whereas the early effect of this invasive plant decreasing rhizosphere activity remained across time.

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References

  • Alguacil MM, Torres MP, Montesinos-Navarro A, Roldán A (2016) Soil characteristics driving arbuscular mycorrhizal fungal communities in semiarid Mediterranean soils. Appl Environ Microb 82:3348–3356

    CAS  Google Scholar 

  • Álvarez-Rogel J, Ortiz Silla R, Alcaraz Ariza F (2001) Edaphic characterization and soil ionic composition influencing plant zonation in a semiarid Mediterranean salt marsh. Geoderma 99:81–98

    Google Scholar 

  • Andrade SAL, Malik S, Sawaya ACHF, Bottcher A, Mazzafera P (2013) Association with arbuscular mycorrhizal fungi influences alkaloid synthesis and accumulation in Catharanthus roseus and Nicotiana tabacum plants. Acta Physiol Plant 35:867–880

    CAS  Google Scholar 

  • Aslani F, Juraimi AS, Ahmad-Hamdani MS, Alam MA, Hasan MM, Hashemi FSG, Bahram M (2019) The role of arbuscular mycorrhizal fungi in plant invasion trajectory. Plant Soil 441:1–14. https://doi.org/10.1007/s11104-019-04127-5

    Article  CAS  Google Scholar 

  • Brink RH, Dubach P, Lynch DL (1960) Measurement of carbohydrates in soil hydrolyzates with anthrone. Soil Sci 89:157–166

    CAS  Google Scholar 

  • Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115

    PubMed  Google Scholar 

  • Bunn RA, Ramsey PW, Lekberg Y (2015) Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. J Ecol 103:1547–1556

    CAS  Google Scholar 

  • Bunsupa S, Komastsu K, Nakabayashi R, Saito K, Yamazaki M (2014) Revisiting anabasine biosynthesis in tobacco hairy roots expressing plant lysine decarboxylase gene by using 15N-labeled lysine. Plant Biotechnol 31:511–518

    CAS  Google Scholar 

  • CABI (2019) Invasive species compendium. CAB International, Wallingford, UK www.cabi.org/isc

    Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caravaca F, Azcón-Aguilar C, Figueroa D, Roldán A (2003) Alteration in the rhizosphere soil properties of afforested Rhamnus lycioides seedlings in short-term response to inoculation with Glomus intraradices and organic amendment. Environ Manag 31:412–420

    Google Scholar 

  • Cipollini K, Titus K, Wagner C (2012) Allelopathic effects of invasive species (Alliaria petiolata, Lonicera maackii, Ranunculus ficaria) in the Midwestern United States. Allelopathy J 29:63–76

    Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  • El-Kenany ET, El-Darier SM, Abdellatif AA, Shaklol SM (2017) Allelopathic potential of invasive species: Nicotiana glauca Graham on some ecological and physiological aspects of Medicago sativa L. and Triticum aestivum L. Rend Lincei 28:159–167

    Google Scholar 

  • Florentine SK, Westbrooke ME (2005) Invasion of the noxious weed Nicotiana glauca R. Graham after an episodic flooding event in the arid zone of Australia. J Arid Environ 60:531–545

    Google Scholar 

  • Gao C, Montoya L, Xu L, Madera M, Hollingsworth J, Purdom E, Hutmacher RB, Dahlberg JA, Coleman-Derr D, Lemaux PG, Taylor JW (2019) Strong succession in arbuscular mycorrhizal fungal communities. ISME J 13:214–226

    PubMed  Google Scholar 

  • García C, Hernandez T, Costa F (1997) Potential use of dehydrogenase activity as an index of microbial activity in degraded soils. Commun Soil Sci Plant Anal 28:123–134

    Google Scholar 

  • Gibbons SM, Lekberg Y, Mummey DL, Sangwan N, Ramsey PW, Gilbert JA (2017) Invasive plants rapidly reshape soil properties in a grassland ecosystem. mSystems 2:e00178–e00116

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grove S, Haubensak KA, Gehring C, Parker IM (2017) Mycorrhizae, invasions, and the temporal dynamics of mutualism disruption. J Ecol 105:1496–1508

    Google Scholar 

  • Hart MM, Reader RJ, Klironomos JN (2001) Life-history strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics. Mycologia 93:1186–1194

    Google Scholar 

  • Husband R, Herre EA, Young JPW (2002) Temporal variation in the arbuscular mycorrhizal communities colonising seedlings in a tropical forest. FEMS Microbiol Ecol 42:131–136

    CAS  PubMed  Google Scholar 

  • IUSS Working Group WRB (2015) World Reference Base for soil resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome

  • Johnson NC, Angelard C, Sanders IR, Kiers ET (2013) Predicting community and ecosystem outcomes of mycorrhizal responses to global change. Ecol Lett 16:140–153

    PubMed  Google Scholar 

  • Joner EJ, van Aarle IM, Vosatka M (2000) Phosphatase activity of extra-radical arbuscular mycorrhizal hyphae: a review. Plant Soil 226:199–210

    CAS  Google Scholar 

  • Jordan NR, Aldrich-Wolfe L, Huerd SC, Larson DL, Muehlbauer G (2012) Soil–occupancy effects of invasive and native grassland plant species on composition and diversity of mycorrhizal associations. Invas Plant Sci Mana 5:494–505

    Google Scholar 

  • Kandeler E, Stemmer M, Klimanek EM (1999) Response of soil microbial biomass, urease and xylanase within particle size fractions to long-term soil management. Soil Biol Biochem 31:261–273

    CAS  Google Scholar 

  • Ladd JN, Butler JHA (1972) Short term assays of soil proteolytic enzymes-using proteins and dipeptide derivatives as substrates. Soil Biol Biochem 4:19–30

    CAS  Google Scholar 

  • Lekberg Y, Gibbons SM, Rosendahl S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7:1424–1433

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu W, Jiang S, Zhang Y, Yue S, Christie P, Murray PJ, Li X, Zhang J (2014) Spatiotemporal changes in arbuscular mycorrhizal fungal communities under different nitrogen inputs over a 5-year period in intensive agricultural ecosystems on the North China plain. FEMS Microbiol Ecol 90:436–453

    CAS  PubMed  Google Scholar 

  • Magoč T, Salzberg SL (2011) Flash: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    PubMed  PubMed Central  Google Scholar 

  • Marchante E, Kjøller A, Struwe S, Freitas H (2008) Short- and long-term impacts of Acacia longifolia invasion on the belowground processes of a Mediterranean coastal dune ecosystem. Appl Soil Ecol 40:210–217

    Google Scholar 

  • Martinez Arbizu P (2017) Pairwiseadonis: Pairwisemultilevel comparison using Adonis. R Package Version 0.0.1

  • Mota JF, Sola AJ, Jiménez-Sánchez ML, Pérez-García F, Merlo ME (2004) Gypsicolous flora, conservation and restoration of quarries in the southeast of the Iberian Peninsula. Biodivers Conserv 13:1797–1808

    Google Scholar 

  • Mummey DL, Rillig MC (2006) The invasive plant species Centaurea maculosa alters arbuscular mycorrhizal fungal communities in the field. Plant Soil 288:81–90

    CAS  Google Scholar 

  • Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology and applications. Marcel Dekker, New York, pp 1–33

    Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Google Scholar 

  • Naseby DC, Lynch JM (1997) Rhizosphere soil enzymes as indicators of perturbations caused by enzyme substrate addition and inoculation of a genetically modified strain of Pseudomonas fluorescens on wheat seed. Soil Biol Biochem 29:1353–1362

    CAS  Google Scholar 

  • Nattero J, Sérsic AN, Cocucci AA (2011) Geographic variation of floral traits in Nicotiana glauca: relationships with biotic and abiotic factors. Acta Oecol 37:503–511

    Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) Vegan: community ecology package. R package version 2:5–6 http://CRAN.R-project.org/package=vegan

    Google Scholar 

  • Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241

    PubMed  Google Scholar 

  • Paudel S, Baer SG, Battaglia LL (2012) Arbuscular mycorrhizal fungi (AMF) and success of Triadica sebifera invasion in coastal transition ecosystems along the northern Gulf of Mexico. Plant Soil 378:337–349

    Google Scholar 

  • Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715

    Google Scholar 

  • Qin F, Yu S (2019) Arbuscular mycorrhizal fungi protect native woody species from novel weapons. Plant Soil 440:39–52. https://doi.org/10.1007/s11104-019-04063-4

    Article  CAS  Google Scholar 

  • Querejeta JI, Allen MF, Caravaca F, Roldán A (2006) Differential modulation of host plant δ13C and δ18O by native and nonnative arbuscular mycorrhizal fungi in a semiarid environment. New Phytol 169:379–387

    CAS  PubMed  Google Scholar 

  • Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531

    PubMed  Google Scholar 

  • Rodríguez-Caballero G, Caravaca F, Alguacil MM, Fernández-López M, Fernández-González AJ, Roldán A (2017) Striking alterations in the soil bacterial community structure and functioning of the biological N cycle induced by Pennisetum setaceum invasion in a semiarid environment. Soil Biol Biochem 109:176–187

    Google Scholar 

  • Rodríguez-Caballero G, Caravaca F, Roldán A (2018) The unspecificity of the relationships between the invasive Pennisetum setaceum and mycorrhizal fungi may provide advantages during its establishment at semiarid Mediterranean sites. Sci Total Environ 630:1464–1471

    PubMed  Google Scholar 

  • Roldán A, García-Orenes F, Lax A (1994) An incubation experiment to determine factors involving aggregation changes in an arid soil receiving urban refuse. Soil Biol Biochem 26:1699–1707

    Google Scholar 

  • Ruckli R, Rusterholz H-P, Baur B (2014) Invasion of an annual exotic plant into deciduous forests suppresses arbuscular mycorrhiza symbiosis and reduces performance of sycamore maple saplings. For Ecol Manag 318:285–293

    Google Scholar 

  • Smith SE, Read DJ (2010) Mycorrhizal symbiosis, 3rd edn. London, Academic Press

    Google Scholar 

  • Smith FA, Smith SE (2013) How useful is the mutualism-parasitism continuum of arbuscular mycorrhizal functioning? Plant Soil 363:7–18

    CAS  Google Scholar 

  • Souza-Alonso P, Guisande-Collazo A, González L (2015) Gradualism in Acacia dealbata link invasion: impact on soil chemistry and microbial community over a chronological sequence. Soil Biol Biochem 80:315–323

    CAS  Google Scholar 

  • Tabatabai MA (1982) Soil enzymes. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. Chemical and microbiological properties. American Society of Agronomy, Soil Science Society of America, Inc., Madison, WI, pp 903-947

  • Teste FP, Kardol P, Turner BL, Wardle DA, Zemunik G, Renton M, Laliberte E (2017) Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355:173–176

    CAS  PubMed  Google Scholar 

  • Traveset A, Richardson DM (2014) Mutualistic interactions and biological invasions. Annu Rev Ecol Evol Syst 45:89–113

    Google Scholar 

  • Vierheilig H, Lerat S, Piché Y (2003) Systematic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae. Mycorrhiza 13:167–170

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was supported by the Spanish Plan Nacional-FEDER Project RTI2018-094731-B-I00. The authors wish to thank Dr. D.J. Walker for kindly correcting the English language.

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Authors and Affiliations

  1. CSIC-Centro de Edafología y Biología Aplicada del Segura, Department of Soil and Water Conservation, P.O. Box 164, Campus de Espinardo, 30100, Murcia, Spain

    F. Caravaca, G. Rodríguez-Caballero, M. Campoy & A. Roldán

  2. Department of Agricultural Chemistry, Geology and Edaphology, University of Murcia, Campus de Espinardo, 30071, Murcia, Spain

    P. Marín Sanleandro

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  1. F. Caravaca
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  2. G. Rodríguez-Caballero
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Correspondence to F. Caravaca.

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Caravaca, F., Rodríguez-Caballero, G., Campoy, M. et al. The invasion of semiarid Mediterranean sites by Nicotiana glauca mediates temporary changes in mycorrhizal associations and a permanent decrease in rhizosphere activity. Plant Soil 450, 217–229 (2020). https://doi.org/10.1007/s11104-020-04497-1

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