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Fungal root endophytes of the carnivorous plant Drosera rotundifolia

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Abstract

As carnivorous plants acquire substantial amounts of nutrients from the digestion of their prey, mycorrhizal associations are considered to be redundant; however, fungal root endophytes have rarely been examined. As endophytic fungi can have profound impacts on plant communities, we aim to determine the extent of fungal root colonisation of the carnivorous plant Drosera rotundifolia at two points in the growing season (spring and summer). We have used a culture-dependent method to isolate fungal endophytes and diagnostic polymerase chain reaction methods to determine arbuscular mycorrhizal fungi colonisation. All of the roots sampled contained culturable fungal root endophytes; additionally, we have provided molecular evidence that they also host arbuscular mycorrhizal fungi. Colonisation showed seasonal differences: Roots in the spring were colonised by Articulospora tetracladia, two isolates of uncultured ectomycorrhizal fungi, an unidentified species of fungal endophyte and Trichoderma viride, which was present in every plant sampled. In contrast, roots in the summer were colonised by Alatospora acuminata, an uncultured ectomycorrhizal fungus, Penicillium pinophilum and an uncultured fungal clone. Although the functional roles of fungal endophytes of D. rotundifolia are unknown, colonisation may (a) confer abiotic stress tolerance, (b) facilitate the acquisition of scarce nutrients particularly at the beginning of the growing season or (c) play a role in nutrient signalling between root and shoot.

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References

  • Adamec L (1997) Mineral nutrition of carnivorous plants: a review. Bot Rev 63:273–299

    Article  Google Scholar 

  • Adamec L (2002) Leaf absorption of mineral nutrients in carnivorous plants stimulates root nutrient uptake. New Phytol 155:89–100

    Article  CAS  Google Scholar 

  • Adamec L (2005) Ecophysiological characterization of carnivorous plant roots: oxygen fluxes, respiration, and water exudation. Biologia Plant 49:247–255

    Article  Google Scholar 

  • Adlassnig W, Peroutka M, Lambers H, Lichtscheidl IK (2005) The roots of carnivorous plants. Plant Soil 274:127–140

    Article  CAS  Google Scholar 

  • Albino U, Saridakis DP, Ferreira MC, Hungria M, Vinuesa P, Andrade G (2006) High diversity of diazotrophic bacteria associated with the carnivorous plant Drosera villosa var. villosa growing in oligotrophic habitats in Brazil. Plant Soil 287:199–207

    Article  CAS  Google Scholar 

  • Auge RM (2001) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Babula P, Adam V, Havel L, Kizek R (2009) Noteworthy secondary metabolites naphthoquinones—their occurrence, pharmacological properties and analysis. Curr Pharm Anal 5:47–68

    Article  CAS  Google Scholar 

  • Brundrett MC (2009) 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 320:37–77

    Article  CAS  Google Scholar 

  • Chambers SM, Curlevski NJA, Cairney JWG (2008) Ericoid mycorrhizal fungi are common root inhabitants of non-Ericaceae plants in a south-eastern Australian sclerophyll forest. FEMS Microbiol Ecol 65:263–270

    Article  CAS  PubMed  Google Scholar 

  • Conran JG (2008) Aestivation organ structure in Drosera subgen. Ergaleium (Droseraceae): corms or tubers; roots or shoots? Aust J Bot 56:144–152

    Article  Google Scholar 

  • Crowder AA, Pearson MC, Grubb PJ, Langlois PH (1990) Biological flora of the British Isles: Drosera L. J Ecol 78:233–267

    Article  Google Scholar 

  • Davis EC, Shaw AJ (2008) Biogeographic and phylogenetic patterns in diversity of liverwort-associated endophytes. Am J Bot 95:914–924

    Article  Google Scholar 

  • Ellison AM, Gotelli NJ (2009) Energetics and the evolution of carnivorous plants—Darwin’s ‘most wonderful plants in the world’. J Exp Bot 60:19–42

    Article  CAS  PubMed  Google Scholar 

  • Fan YQ, Luan YS, An LJ, Yu K (2008) Arbuscular mycorrhizae formed by Penicillium pinophilum improve the growth, nutrient uptake and photosynthesis of strawberry with two inoculum-types. Biotechnol Lett 30:1489–1494

    Article  CAS  PubMed  Google Scholar 

  • Fisher PJ, Petrini O, Webster J (1991) Aquatic hyphomycetes and other fungi in living aquatic and terrestrial roots of Alnus glutinosa. Mycol Res 95:543–547

    Article  Google Scholar 

  • Fuchs B, Haselwandter K (2004) Red list plants: colonization by arbuscular mycorrhizal fungi and dark septate endophytes. Mycorrhiza 14:277–281

    Article  CAS  PubMed  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Gryndler M, Vosatka M, Hrselova H, Chvatalova I, Jansa J (2002) Interaction between arbuscular mycorrhizal fungi and cellulose in growth substrate. Appl Soil Ecol 19:279–288

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hempel S (2009) The formation of arbuscular mycorrhizae by an Ascomycete? Biotechnol Lett 31:155–156

    Article  CAS  PubMed  Google Scholar 

  • Jaklitsch WM, Samuels GJ, Dodd SL, Lu BS, Druzhinina IS (2006) Hypocrea rufa/Trichoderma viride: a reassessment, and description of five closely related species with and without warted conidia. Stud Mycol 56:135–177

    Article  PubMed  Google Scholar 

  • Juniper BE, Robins RJ, Joel DM (1989) Carnivorous plants. Academic, London

    Google Scholar 

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    Article  CAS  PubMed  Google Scholar 

  • MacDougal DT (1899) Symbiotic saprophytism. Ann Bot 13:1–46

    Google Scholar 

  • Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53: 173–189

    Article  Google Scholar 

  • Meazza G, Dayan FE, Wedge DE (2003) Activity of quinones on Colletotrichum species. J Agric Food Chem 51:3824–3828

    Article  CAS  PubMed  Google Scholar 

  • Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide-Biol & Chem 5:62–71

    Article  CAS  Google Scholar 

  • Mulvaney RL (1996) Nitrogen-inorganic forms. In: Sparks DL et al (eds) Methods of soil analysis. Part 3. SSSA book Ser. 5. SSSA, Madison, pp 1123–1184

    Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2:10–20

    Article  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin in Pl Biol 10:393–398

    Article  CAS  Google Scholar 

  • Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME 2:404–416

    Article  Google Scholar 

  • Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  CAS  PubMed  Google Scholar 

  • Rudresh DL, Shivaprakash MK, Prasad RD (2005) Tricalcium phosphate solubilizing abilities of Trichoderma spp. in relation to P uptake and growth and yield parameters of chickpea (Cicer arietinum L.). Can J Microbiol 51:217–222

    Article  CAS  PubMed  Google Scholar 

  • Sati SC, Belwal M (2005) Aquatic hyphomycetes as endophytes of riparian plant roots. Mycologia 97:45–49

    Article  CAS  PubMed  Google Scholar 

  • Selosse MA, Vohnik M, Chauvet E (2008) Out of the rivers: are some aquatic hyphomycetes plant endophytes? New Phytol 178:3–7

    Article  PubMed  Google Scholar 

  • Sokolski S, Piche Y, Chauvet E, Berube JA (2006) A fungal endophyte of black spruce (Picea mariana) needles is also an aquatic hyphomycete. Mol Ecol 15:1955–1962

    Article  CAS  PubMed  Google Scholar 

  • Sridhar KR, Barlocher F (1992) Endophytic aquatic hyphomycetes of roots of Spruce, Birch and Maple. Mycol Res 96:305–308

    Article  Google Scholar 

  • Taylor DL, Herriott IC, Long J, O’Neill K (2007) TOPO TA is A-OK: a test of phylogenetic bias in fungal environmental clone library construction. Environ Microbiol 9:1329–1334

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence-weighting position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Venugopal N, Raseshowri Devi K (2007) An interesting observation on the mycorrhizal symbiosis in the insectivorous plant, Drosera peltata Sm., in Meghalaya, north-east India. Carniv Plant Newsl 36:9–13

    Google Scholar 

  • Weishampel PA, Bedford BL (2006) Wetland dicots and monocots differ in colonization by arbuscular mycorrhizal fungi and dark septate endophytes. Mycorrhiza 16:495–502

    Article  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Shinsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315–322

    Google Scholar 

  • Wilberforce EM, Boddy L, Griffiths R, Griffith GW (2003) Agricultural management affects communities of culturable root-endophytic fungi in temperate grasslands. Soil Biol Biochem 35:1143–1154

    Article  CAS  Google Scholar 

  • Ziaratnia SM, Kunert KJ, Lall N (2009) Elicitation of 7-methyljuglone in Drosera capensis. S Afri J Bot 75:97–103

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This project was funded by a Botanical Society of the British Isles research grant awarded to RSQ. We thank Philip Swarbrick for advice on DNA sequence analysis.

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  1. School of Environment, Natural Resources & Geography, Bangor University, Bangor, Gwynedd, LL57 2UW, UK

    Richard S. Quilliam & David L. Jones

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  1. Richard S. Quilliam
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  2. David L. Jones
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Correspondence to Richard S. Quilliam.

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Quilliam, R.S., Jones, D.L. Fungal root endophytes of the carnivorous plant Drosera rotundifolia . Mycorrhiza 20, 341–348 (2010). https://doi.org/10.1007/s00572-009-0288-4

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  • DOI: https://doi.org/10.1007/s00572-009-0288-4

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