Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Impacts of endophyte infection of ryegrass on rhizosphere metabolome and microbial community

S. Wakelin A G , S. Harrison B C , C. Mander A , B. Dignam A D , S. Rasmussen B F , S. Monk E , K. Fraser B and M. O’Callaghan A
+ Author Affiliations
- Author Affiliations

A AgResearch Ltd, Innovative Farm Systems, Private Bag 4749, Christchurch 8140, New Zealand.

B AgResearch Ltd, Grasslands Research Centre, Private Bag 11008, Palmerston North 4442, New Zealand.

C Novo Nordisk Foundation, Center for Biosustainability, Hørsholm 2970, Denmark.

D Lincoln University, Faculty of Agriculture and Life Sciences, PO Box 85084, Lincoln 7647, New Zealand.

E Grasslanz Technology Ltd, Private Bag 4749, Christchurch 8140, New Zealand.

F Present address: Institute of Agriculture and Environment, Massey University, Palmerston North 4474, New Zealand.

G Corresponding author. Email: steve.wakelin@agresearch.co.nz

Crop and Pasture Science 66(10) 1049-1057 https://doi.org/10.1071/CP14321
Submitted: 19 November 2014  Accepted: 29 May 2015   Published: 30 September 2015

Abstract

The use of grasses such as ryegrass and fescues infected with endophytic fungi of the Epichloë genus is widespread in New Zealand’s pastoral systems. Each endophyte–cultivar combination represents a distinctive genome–genome association, resulting in unique biological outcomes. The wider influence of these interactions on rhizosphere microbiology are not well characterised. This is important, because there may be opportunities or risks associated with selective disruption of the rhizosphere microbiota. We explored the interaction of two commercially used endophyte fungi, E. festucae var. lolii strains AR1 and AR37, within a genetically uniform breeding line of perennial ryegrass (Lolium perenne cv. Samson 11104) on the rhizosphere metabolome and the composition of the fungal, bacterial, and Pseudomonas communities. There were strong differences in the rhizosphere metabolomes between infested and non-infested ryegrass strains (P = 0.06). These were attributed to shifts in various n-alkane hydrocarbon compounds. The endophyte-associated alteration in rhizosphere metabolome was linked to changes in the total bacterial (P < 0.01) and fungal (P < 0.05) rhizosphere communities. Furthermore, there was varying levels of support for endophyte-specific (AR1 v. AR37) impacts on the bacterial and fungal communities. Pseudomonas bacterial communities were not influenced by endophyte infection of ryegrass (P = 0.834).


References

Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.

Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253.
Distance-based tests for homogeneity of multivariate dispersions.Crossref | GoogleScholarGoogle Scholar | 16542252PubMed |

Anderson MJ, Gorley RN, Clarke KR (2008) ‘PERMANOVA+ for PRIMER: guide to software and statistical methods.’ (PRIMER-E: Plymouth, UK)

Baumann K, Marschner P, Smernik RJ, Baldock JA (2009) Residue chemistry and microbial community structure during decomposition of eucalypt, wheat and vetch residues. Soil Biology & Biochemistry 41, 1966–1975.
Residue chemistry and microbial community structure during decomposition of eucalypt, wheat and vetch residues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVenu7zK&md5=c0a80d3a6284e3f7d91eee73d5d9f88eCAS |

Bell NL, Rohan TC, James SM, Aalders LT, Burch G, Sarathchandra SU, Gerard E, O’Callaghan M (2009) An investigation on non-target impacts of ryegrass endophytes on nematodes and soil microorganisms. Proceedings of the New Zealand Grassland Association 71, 139–144.

Bowatte S, Barrett B, Luscombe C, Hume DE, Luo D, Theobald P, Newton PCD (2011) Effect of grass species and fungal endophyte on soil nitrification potential. New Zealand Journal of Agricultural Research 54, 275–284.
Effect of grass species and fungal endophyte on soil nitrification potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVKhsbrI&md5=ee89431025b20c6741131c120f80182dCAS |

Bünemann EK, Schwenke GD, Van Zwieten L (2006) Impact of agricultural inputs on soil organisms – a review. Australian Journal of Soil Research 44, 379–406.
Impact of agricultural inputs on soil organisms – a review.Crossref | GoogleScholarGoogle Scholar |

Casas C, Omacini M, Montecchia MS, Correa OS (2011) Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant and Soil 340, 347–355.
Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitFGksbk%3D&md5=1f07699e9135fce22cc81eb27de2cf91CAS |

Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genetics and Biology 45, 84–93.
Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves.Crossref | GoogleScholarGoogle Scholar | 17919950PubMed |

Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology 18, 117–143.

Clarke KR, Warwick RM (2001) ‘Change in marine communities: an approach to statistical analysis and interpretation.’ 2nd edn (PRIMER-E: Plymouth, UK)

Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. Journal of Experimental Marine Biology and Ecology 330, 55–80.
On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages.Crossref | GoogleScholarGoogle Scholar |

Fischer H, Meyer A, Fischer K, Kuzyakov Y (2007) Carbohydrate and amino acid composition of dissolved organic matter leached from soil. Soil Biology & Biochemistry 39, 2926–2935.
Carbohydrate and amino acid composition of dissolved organic matter leached from soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1Cgt70%3D&md5=94767c526167b9b76db005059fdb0a1fCAS |

Franzluebbers AJ, Nazih N, Stuedemann JA, Fuhrmann JJ, Schomberg HH, Hartel PG (1999) Soil carbon and nitrogen pools under low- and high-endophyte-infected tall fescue. Soil Science Society of America Journal 63, 1687–1694.
Soil carbon and nitrogen pools under low- and high-endophyte-infected tall fescue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsFyku7k%3D&md5=9970e570b7f38dc0f1e966cb507c29c5CAS |

Gallagher RT, White EP, Mortimer PH (1981) Ryegrass staggers: isolation of potent neurotoxins lolitrem A and lolitrem B from staggers producing pastures. New Zealand Veterinary Journal 29, 189–190.
Ryegrass staggers: isolation of potent neurotoxins lolitrem A and lolitrem B from staggers producing pastures.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL387kvFemtA%3D%3D&md5=6286463c87e32c67fa92dc6e67af11a0CAS | 6950333PubMed |

Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type. Annual Review of Phytopathology 42, 243–270.
Microbial diversity in soil: selection of microbial populations by plant and soil type.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotFyrtbk%3D&md5=df608251a2d4c57b0341b51036df58ddCAS | 15283667PubMed |

Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Molecular Ecology 2, 113–118.
ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslOmsro%3D&md5=8d06fe79e3108f1d7517272dafb2e4e1CAS | 8180733PubMed |

Germida J, Siciliano S (2001) Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biology and Fertility of Soils 33, 410–415.
Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars.Crossref | GoogleScholarGoogle Scholar |

Gillespie AW, Walley FL, Farrell RE, Leinweber P, Schlichting A, Eckhardt KU, Regier TZ, Blyth RIR (2009) Profiling rhizosphere chemistry: Evidence from carbon and nitrogen K-edge XANES and pyrolysis-FIMS. Soil Science Society of America Journal 73, 2002–2012.
Profiling rhizosphere chemistry: Evidence from carbon and nitrogen K-edge XANES and pyrolysis-FIMS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVSku7jP&md5=11ac286c0a90e8912fb097668ad86771CAS |

Heuer HK, Smalla K (1997) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) for studying soil microbial communities. In ‘Modern soil microbiology’. (Eds JD Elsas, EMH Wellington, JT Trevors) pp. 353–373. (Marcel Dekker: New York)

Hewitt AE (1998) ‘New Zealand Soil Classification.’ (Manaaki Whenua Press: Lincoln, New Zealand)

Hume DE, Popay AJ, Cooper BM, Eerens PJ, Lyons TB, Pennell CGL, Tapper BA, Latch GCM, Baird DB (2004) Effect of a novel endophyte on the productivity of perennial ryegrass (Lolium perenne) in New Zealand. In ‘Proceedings 5th International Symposium on Neotyphodium/Grass Interactions’. Fayetteville, Arkansas, USA. (Eds R Kallenbach, C Rosenkraus, Jr, TR Lock)

Hume DE, Ryan DL, Cooper BM, Popay AJ (2007) Agronomic performance of AR37-infected ryegrass in northern New Zealand. Proceedings of the New Zealand Grasslands Association 69, 201–206.

Hunt WF, Easton HS (1989) Fifty years of ryegrass research in New Zealand. Proceedings of the New Zealand Grasslands Association 50, 1–23.

Jandl G, Baum C, Leinweber P (2013) Crop-specific differences in the concentrations of lipids in leachates from the root zone. Archives of Agronomy and Soil Science 59, 119–125.
Crop-specific differences in the concentrations of lipids in leachates from the root zone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1yktr3P&md5=09099f1d6bf62d244d464ade76df10f5CAS |

Johnson RD, Bassett S, Christensen M, Gaborit C, Johnson L, Khan A, Koulman A, Rasmussen S, Voisey C, Bryan G (2007) Functional genomics of the Neotyphodium lolii/ryegrass symbiosis. In ‘Proceedings 6th International Symposium on Fungal Endophytes of Grasses’. Grassland Research and Practice Series No. 13. (Eds AJ Popay, ER Thom) pp. 433–450. (New Zealand Grassland Association: Dunedin, New Zealand)

Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols 1, 387–396.
Gas chromatography mass spectrometry-based metabolite profiling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFOitbnN&md5=7701cada7764f5873d550e5a76f6cf99CAS | 17406261PubMed |

Liu Q, Parsons AJ, Xue H, Fraser K, Ryan GD, Newman JA, Rasmussen S (2011) Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Functional Ecology 25, 910–920.
Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content.Crossref | GoogleScholarGoogle Scholar |

Mackay T (1887) ‘A manual of the grasses and forage-plants useful to New Zealand. Part 1.’ (George Didsbury, Government Printer: Wellington, New Zealand)

McNear DN, McCulley RL (2012) Influence of the Neotyphodium – Tall fescue symbiosis on belowground processes. In ‘Epichloae, endophytes of cool season grasses: implications, utilization and biology’. (Eds CA Young, GE Aiken, RL McCulley, JR Strickland, CL Schardl) pp. 137. (Samuel Roberts Noble Foundation: Ardmore, OK, USA)

Milling A, Smalla K, Maidl FX, Schloter M, Munch JC (2004) Effects of transgenic potatoes with an altered starch composition on the diversity of soil and rhizosphere bacteria and fungi. Plant and Soil 266, 23–39.

Monreal CM, Schnitzer M (2013) The chemistry and biochemistry of organic components in the soil solutions of wheat rhizospheres. Advances in Agronomy 121, 179–251.

Okubara PA, Bonsall RF (2008) Accumulation of Pseudomonas-derived 2,4-diacetylphloroglucinol on wheat seedlings roots is influenced by host cultivar. Biological Control 46, 322–331.
Accumulation of Pseudomonas-derived 2,4-diacetylphloroglucinol on wheat seedlings roots is influenced by host cultivar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVOju7Y%3D&md5=ef52d7eeb978f7e4fc02aceacef3293fCAS |

Omacini M, Chaneton EJ, Ghersa CM (2005) A hierarchical framework for understanding the ecosystem consequences of endophyte–grass symbioses. In ‘Neotyphodium in cool-season grasses’. (Eds CA Roberts, CP West, DE Spiers) pp. 131–162. (Blackwell Publishing: Oxford, UK)

Popay AJ, Hume DE, Baltus JG, Latch GCM, Tapper BA, Lyons TB, Cooper BM, Pennell C, Eerens JPJ, Marshall SL (1999) Field performance of perennial ryegrass (Lolium perenne) infected with toxin-free fungal endophytes (Neotyphodium spp.). Ryegrass endophyte: an essential New Zealand symbiosis. Grassland Research and Practice Series 7, 113–122.

Porter JK (1995) Analysis of endophyte toxins: fescue and other grasses toxic to livestock. Journal of Animal Science 73, 871–880.

Rasmussen S, Parsons AJ, Fraser K, Xue H, Newman JA (2008) Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiology 146, 1440–1453.
Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVKgur8%3D&md5=aba8451211dcc2e7c6ffe696a8ad12ddCAS | 18218971PubMed |

Rasmussen S, Parsons AJ, Newman JA (2009) Metabolomics analysis of the Lolium perenneNeotyphodium lolii symbiosis: more than just alkaloids? Phytochemistry Reviews 8, 535–550.
Metabolomics analysis of the Lolium perenneNeotyphodium lolii symbiosis: more than just alkaloids?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Cqur3K&md5=a5031404ea39e70d62d42aee3d8c29e0CAS |

Rasmussen S, Parsons AJ, Jones CS (2012) Review: Part of a highlight on breeding strategies for forage and grass improvement. Annals of Botany 110, 1281–1290.
Review: Part of a highlight on breeding strategies for forage and grass improvement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Sru77N&md5=94ad421ea386aceeac5d4d344ea8d951CAS | 22351485PubMed |

Rengel Z (2002) Genetic control of root exudation. Plant and Soil 245, 59–70.
Genetic control of root exudation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVCitrw%3D&md5=7f0a74febc0f6ed8b9158962cbea6421CAS |

Rudgers JA, Clay K (2007) Community and ecosystem consequences of endophyte symbiosis with tall fescue. In ‘Proceedings 6th International Symposium on Fungal Endophytes of Grasses’. Grasslands Research and Practice Series No. 13. (Eds AJ Popay, ER Thom) pp. 19–35. (New Zealand Grasslands Association: Dunedin, New Zealand)

Sayer ST, Burch G, Sarathchandra SU (2004) The impact of tall fescue (Festuca arundinacea) endophypte (Neotyphodium spp.) on non-target soil micro-organisms. New Zealand Plant Protection 57, 329–336.

Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, Panaccione DG, Schweri KK, Voisey CR, Farman ML, Jaromczyk JW, Roe BA, O’Sullivan DM, Scott B, Tudzynski P, An Z, Arnaoudova EG, Bullock CT, Charlton ND, Chen L, Cox M, Dinkins RD, Florea S, Glenn AE, Gordon A, Güldener U, Harris DR, Hollin W, Jaromczyk J, Johnson RD, Khan AK, Leistner E, Leuchtmann A, Li C, Liu J, Liu J, Liu M, Mace W, Machado C, Nagabhyru P, Pan J, Schmid J, Sugawara K, Steiner U, Takach JE, Tanaka E, Webb JS, Wilson EV, Wiseman JL, Yoshida R, Zeng Z (2013) Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLOS Genetics 9, e1003323
Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktlSksr0%3D&md5=cd340bc7ad7435eb52d70a6b1d5f3367CAS | 23468653PubMed |

Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56.
Persistence of soil organic matter as an ecosystem property.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1yltrnF&md5=189199c9486fa2fb2c34645259ddc558CAS |

Schreiter S, Ding G-C, Heuer H, Neumann G, Sandmann M, Grosch R, Kropf S, Smalla K (2014) Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Frontiers in Microbiology 5, 144
Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce.Crossref | GoogleScholarGoogle Scholar | 24782839PubMed |

Simpson WR, Schmid J, Singh J, Faville MJ, Johnson RD (2012) A morphological change in the fungal symbiont Neotyphodium lolii induces dwarfing in its host plant Lolium perenne. Fungal Biology 116, 234–240.
A morphological change in the fungal symbiont Neotyphodium lolii induces dwarfing in its host plant Lolium perenne.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC387ptVSisA%3D%3D&md5=b8d1adecb335b4d55693e980f784e6d7CAS | 22289769PubMed |

Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Ruskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant derived enrichment and seasonal shifts revealed. Applied and Environmental Microbiology 67, 4742–4751.
Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant derived enrichment and seasonal shifts revealed.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXns1Wit74%3D&md5=7e30ce6ffea271072d9cd89de513afdfCAS | 11571180PubMed |

Wakelin SA, Colloff MJ, Harvey PR, Marschner P, Gregg AL, Rogers SL (2007) The effects of stubble retention and nitrogen application on soil microbial community structure and functional gene abundance under irrigated maize. FEMS Microbiology Ecology 59, 661–670.
The effects of stubble retention and nitrogen application on soil microbial community structure and functional gene abundance under irrigated maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsVyqu7k%3D&md5=ec32cf6a72646d46eef21d1599fae00fCAS | 17116166PubMed |

Wakelin SA, Gregg AL, Simpson RJ, Li GD, Riley IT, McKay AC (2009) Pasture management clearly affects soil microbial community structure and N-cycling bacteria. Pedobiologia 52, 237–251.
Pasture management clearly affects soil microbial community structure and N-cycling bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlKqsLY%3D&md5=ac7c7f02c6e66fc1b043122d82ec468cCAS |

Wakelin S, Mander C, Gerard E, Jansa J, Erb A, Young S, Condron L, O’Callaghan M (2012) Response of soil microbial communities to contrasted histories of phosphorus fertilisation in pastures. Applied Soil Ecology 61, 40–48.
Response of soil microbial communities to contrasted histories of phosphorus fertilisation in pastures.Crossref | GoogleScholarGoogle Scholar |

Wakelin SA, Barratt BIP, Gerard E, Gregg AL, Brodie EL, Andersen GL, DeSantis TZ, Zhou J, He Z, Kowalchuk GA, O’Callaghan M (2013) Shifts in the phylogenetic structure and functional capacity of soil microbial communities follow alteration of native tussock grassland ecosystems. Soil Biology & Biochemistry 83, 568–584.

Wardle DA, Bonner KI, Barker GM, Yeates GW, Nicholson KS, Bardgett RD, Watson RN, Ghani A (1999) Plant removals in perennial grassland: Vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecological Monographs 69, 535–568.
Plant removals in perennial grassland: Vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties.Crossref | GoogleScholarGoogle Scholar |

Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633.
Ecological linkages between aboveground and belowground biota.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks1Cgsrs%3D&md5=62fc1820c53224a6604e34052c1f3839CAS | 15192218PubMed |

Watt M, McCully ME, Kirkegaard JA (2003) Soil strength and rate of root elongation alter the accumulation of Pseudomonas spp. and other bacteria in the rhizosphere of wheat. Functional Plant Biology 30, 483–491.
Soil strength and rate of root elongation alter the accumulation of Pseudomonas spp. and other bacteria in the rhizosphere of wheat.Crossref | GoogleScholarGoogle Scholar |

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 Microbiology Ecology 75, 497–506.
PhyloChip hybridization uncovered an enormous bacterial diversity in the rhizosphere of different potato cultivars: many common and few cultivar-dependent taxa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXit1Oju7c%3D&md5=290b02727abc7cccbb4836e44d8da8c1CAS | 21204872PubMed |

Wiesenberg GLB, Gocke M, Kuzyakov Y (2010) Fast incorporation of root-derived lipids and fatty acids into soil – Evidence from a short term multiple 14CO2 pulse labelling experiment. Organic Geochemistry 41, 1049–1055.
Fast incorporation of root-derived lipids and fatty acids into soil – Evidence from a short term multiple 14CO2 pulse labelling experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFWntL%2FE&md5=4e91f922e8ed607ea35a0254b84da459CAS |