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Species-specific effects of polyploidisation and plant traits of Centaurea maculosa and Senecio inaequidens on rhizosphere microorganisms

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Abstract

Invasive plant species represent a threat to terrestrial ecosystems, but their effects on the soil biota and the mechanisms involved are not yet well understood. Many invasive species have undergone polyploidisation, leading to the coexistence of various cytotypes in the native range, whereas, in most cases, only one cytotype is present in the introduced range. Since genetic variation within a species can modify soil rhizosphere communities, we studied the effects of different cytotypes and ranges (native diploid, native tetraploid and introduced tetraploid) of Centaurea maculosa and Senecio inaequidens on microbial biomass carbon, rhizosphere total DNA content and bacterial communities of a standard soil in relation to plant functional traits. There was no overall significant difference in microbial biomass between cytotypes. The variation of rhizosphere total DNA content and bacterial community structure according to cytotype was species specific. The rhizosphere DNA content of S. inaequidens decreased with polyploidisation in the native range but did not vary for C. maculosa. In contrast, the bacterial community structure of C. maculosa was affected by polyploidisation and its diversity increased, whereas there was no significant change for S. inaequidens. Traits of S. inaequidens were correlated to the rhizosphere biota. Bacterial diversity and total DNA content were positively correlated with resource allocation to belowground growth and late flowering, whereas microbial biomass carbon was negatively correlated to investment in reproduction. There were no correlations between traits of the cytotypes of C. maculosa and corresponding rhizosphere soil biota. This study shows that polyploidisation may affect rhizosphere bacterial community composition, but that effects vary among plant species. Such changes may contribute to the success of invasive polyploid genotypes in the introduced range.

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References

  • Bais HP, Walker TS, Stermitz FR, Hufbauer RA, Vivanco JM (2002) Enantiomeric-dependent phytotoxic and antimicrobial activity of (±)-catechin. A rhizosecreted racemic mixture from spotted knapweed. Plant Physiol 128:1173–1179

    Article  CAS  PubMed  Google Scholar 

  • Batten KM, Scow KM, Davies KF, Harrison SP (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8:217–230

    Article  Google Scholar 

  • Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473

    Article  Google Scholar 

  • Blackwood CB, Marsh T, Kim SH, Paul EA (2003) Terminal restriction fragment length polymorphism data analysis for quantitative comparison of microbial communities. Appl Environ Microbiol 69:926–932

    Article  CAS  PubMed  Google Scholar 

  • Blair AC, Nissen SJ, Brunk GR, Hufbauer RA (2006) A lack of evidence for an ecological role of the putative allelochemical (±)-catechin in spotted knapweed invasion success. J Chem Ecol 32:2327–2331

    Article  CAS  PubMed  Google Scholar 

  • Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants—a hypothesis. J Ecol 83:887–889

    Article  Google Scholar 

  • Bornkamm R (2002) On the phytosociological affiliations of an invasive species Senecio inaequidens in Berlin. Preslia (Praha) 74:395–407

    Google Scholar 

  • Bossdorf O, Prati D, Auge H, Schmid B (2004) Reduced competitive ability in an invasive plant. Ecol Lett 7:346–353

    Article  Google Scholar 

  • Brodie E, Edwards S, Clipson N (2003) Soil fungal community structure in a temperate upland grassland soil. FEMS Microbiol Ecol 45:105–114

    Article  CAS  PubMed  Google Scholar 

  • Broennimann O, Treier UA, Muller-Scharer H, Thuiller W, Peterson AT, Guisan A (2007) Evidence of climatic niche shift during biological invasion. Ecol Lett 10:701–709

    Article  CAS  PubMed  Google Scholar 

  • Brookes PC (1985) Microbial biomass and activity measurements in soil. J Sci Food Agric 36:269–270

    Article  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  • Cano L, Escarre J, Vrieling K, Sans FX (2009) Palatability to a generalist herbivore, defence and growth of invasive and native Senecio species: testing the evolution of increased competitive ability hypothesis. Oecologia 159:95–106

    Article  CAS  PubMed  Google Scholar 

  • Chapin FS et al (2000) Consequences of changing biodiversity. Nature 405:234–242

    Article  CAS  PubMed  Google Scholar 

  • Cornelissen JHC (1996) An experimental comparison of leaf decomposition rates in a wide range of temperate plant species and types. J Ecol 84:573–582

    Article  Google Scholar 

  • Cornelissen JHC et al (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380

    Article  Google Scholar 

  • De Deyn GB, Cornelissen JHC, Bardgett RD (2008) Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol Lett 11:516–531

    Article  PubMed  Google Scholar 

  • De Jesus-Gonzalez L, Weathers PJ (2003) Tetraploid Artemisia annua hairy roots produce more artemisinin than diploids. Plant Cell Rep 21:809–813

    PubMed  Google Scholar 

  • Dhawan OP, Lavania UC (1996) Enhancing the productivity of secondary metabolites via induced polyploidy: a review. Euphytica 87:81–89

    Article  CAS  Google Scholar 

  • Duncan C (2001) Knapweed management: another decade of changes. In: Smith L (ed) Proc First Int Knapweed Symp 21st Century. United States Department of Agriculture, Agricultural Research Service, Albany, pp 1–7

  • Engelkes T et al (2008) Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456:946–948

    Article  CAS  PubMed  Google Scholar 

  • Eppinga MB, Rietkerk M, Dekker SC, De Ruiter PC, Van der Putten WH (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114:168–176

    Article  Google Scholar 

  • Frey B, Stemmer M, Widmer F, Luster J, Sperisen C (2006) Microbial activity and community structure of a soil after heavy metal contamination in a model forest ecosystem. Soil Biol Biochem 38:1745–1756

    Article  CAS  Google Scholar 

  • Frey B, Pesaro M, Rudt A, Widmer F (2008) Resilience of the rhizosphere Pseudomonas and ammonia-oxidizing bacterial populations during phytoextraction of heavy metal polluted soil with poplar. Environ Microbiol 10:1433–1449

    Article  CAS  PubMed  Google Scholar 

  • Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241

    CAS  PubMed  Google Scholar 

  • Hobbie SE (1992) Effects of plant-species on nutrient cycling. Trends Ecol Evol 7:336–339

    Article  Google Scholar 

  • Hol WHG, Van Veen JA (2002) Pyrrolizidine alkaloids from Senecio jacobaea affect fungal growth. J Chem Ecol 28:1763–1772

    Article  CAS  PubMed  Google Scholar 

  • Hook PB, Olson BE, Wraith JM (2004) Effects of the invasive Forb Centaurea maculosa on grassland carbon and nitrogen pools in Montana, USA. Ecosystems 7:686–694

    Article  CAS  Google Scholar 

  • Hull-Sanders HM, Johnson RH, Owen HA, Meyer GA (2009) Effects of polyploidy on secondary chemistry, physiology, and performance of native and invasive genotypes of Solidago gigantea (Asteraceae). Am J Bot 96:762–770

    Article  Google Scholar 

  • Kim YS, Hahn EJ, Murthy HN, Paek KY (2004) Effect of polyploidy induction on biomass and ginsenoside accumulations in adventitious roots of ginseng. J Plant Biol 47:356–360

    Article  Google Scholar 

  • Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70

    Article  CAS  PubMed  Google Scholar 

  • Kowalchuk GA, Hol WHG, Van Veen JA (2006) Rhizosphere fungal communities are influenced by S. jacobaea pyrrolizidine alkaloid content and composition. Soil Biol Biochem 38:2852–2859

    Article  CAS  Google Scholar 

  • Kubatova B, Travnicek P, Bastlova D, Curn V, Jarolimova V, Suda J (2008) DNA ploidy-level variation in native and invasive populations of Lythrum salicaria at a large geographical scale. J Biogeogr 35:167–176

    Google Scholar 

  • Lafuma L, Balkwill K, Imbert E, Verlaque R, Maurice S (2003) Ploidy level and origin of the European invasive weed S. inaequidens (Asteraceae). Plant Syst Evol 243:59–72

    Article  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, Amsterdam

  • Levine JM, Vila M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B Biol Sci 270:775–781

    Article  Google Scholar 

  • Loreau M et al (2001) Ecology—biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808

    Article  CAS  PubMed  Google Scholar 

  • Macel M, Vrieling K (2003) Pyrrolizidine alkaloids as oviposition stimulants for the cinnabar moth, Tyria jacobaeae. J Chem Ecol 29:1435–1446

    Article  CAS  PubMed  Google Scholar 

  • Mangla S, Inderjit, Callaway RM (2008) Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J Ecol 96:58–67

    Google Scholar 

  • Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution of invasive plants: implications for biological control. Trends Ecol Evol 19:417–422

    Article  PubMed  Google Scholar 

  • Noble JW et al (1994) Pyrrolizidine alkaloidosis of cattle associated with S. lautus. Aust Vet J 71:196–200

    Article  CAS  PubMed  Google Scholar 

  • Pandit MK, Tan HTW, Bisht MS (2006) Polyploidy in invasive plant species of Singapore. Bot J Linn Soc 151:395–403

    Article  Google Scholar 

  • Perry LG, Thelen GC, Ridenour WM, Callaway RM, Paschke MW, Vivanco JM (2007) Concentrations of the allelochemical (±)-catechin in Centaurea maculosa soils. J Chem Ecol 33:2337–2344

    Article  CAS  PubMed  Google Scholar 

  • Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • Prieur-Richard AH, Lavorel S (2000) Invasions: the perspective of diverse plant communities. Austral Ecol 25:1–7

    Google Scholar 

  • Richardson DM, Pysek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geogr 30:409–431

    Article  Google Scholar 

  • Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126:444–450

    Article  Google Scholar 

  • Scherer-Lorenzen M (2008) Functional diversity affects decomposition processes in experimental grasslands. Funct Ecol 22:547–555

    Article  Google Scholar 

  • Schlaepfer DR, Edwards PJ, Semple JC, Billeter R (2008) Cytogeography of Solidago gigantea (Asteraceae) and its invasive ploidy level. J Biogeogr 35:2119–2127

    Article  Google Scholar 

  • Schweitzer JA et al (2008) Plant-soil-microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89:773–781

    Google Scholar 

  • Skinner K, Smith L, Rice P (2000) Using noxious weed lists to prioritize targets for developing weed management strategies. Weed Sci 48:640–644

    Article  CAS  Google Scholar 

  • Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360

    Article  PubMed  Google Scholar 

  • Treier UA et al (2009) Shift in cytotype frequency and niche space in the invasive plant C. maculosa. Ecology 90:1366–1377

    Article  PubMed  Google Scholar 

  • van der Heijden MGA et al (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  CAS  Google Scholar 

  • Van Der Putten WH (2003) Plant defense belowground and spatiotemporal processes in natural vegetation. Ecology 84:2269–2280

    Article  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Google Scholar 

  • Verlaque R, Aboucaya A, Fridlender A (2002) Invasive alien flora of France: ecology, life-forms and polyploidy. Bot Helv 112:121–136

    Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  CAS  PubMed  Google Scholar 

  • Watson AK, Renney AJ (1974) The biology of Canadian weeds: Centaurea diffusa and Centaurea maculosa. Can J Plant Sci 54:687–701

    Article  Google Scholar 

  • Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C by fumigation extraction—an automated procedure. Soil Biol Biochem 22:1167–1169

    Article  CAS  Google Scholar 

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Acknowledgments

This project was funded by the National Centre of Competence in Research (NCCR) Plant Survival, a research program of the Swiss National Science Foundation. We thank Joanne Félix, Elena Rossel, Daniela Steiner and Damien Pasche for technical assistance. We are grateful to Olivier Broennimann, Signe Normand, and Urs Treier for collecting seeds of C. maculosa, and to Daniel Prati for supplying seeds of S. inaequidens. We also thank the University of Lausanne for providing greenhouse facilities and material. We are grateful to Wim van der Putten and two anonymous reviewers whose comments greatly improved the manuscript. This experiment complies with the Swiss regulation for invasive plant experimentation, as stated by the Federal Office for the Environment (FOEN).

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Correspondence to Aurélie Thébault.

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Communicated by Tim Seastedt.

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Thébault, A., Frey, B., Mitchell, E.A.D. et al. Species-specific effects of polyploidisation and plant traits of Centaurea maculosa and Senecio inaequidens on rhizosphere microorganisms. Oecologia 163, 1011–1020 (2010). https://doi.org/10.1007/s00442-010-1598-0

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