This paper describes research on interactions between grassland plant species and soil microorganisms. Both parasitic and symbiotic microorganisms modify nutrient transfers between plants and soil. Experiments are described in which nematode infection of clover increased nitrogen transfer to companion ryegrass plants. Infection of clover enhanced activity of soil bacterial and fungal communities. Legume genotypes differing only in responses to symbionts (rhizobium and arbuscular mycorrhizal fungi) and pathogens are being developed for studies of gene expression during establishing and functional symbioses. Such plants can be used in experiments as defined perturbations that will provide information on the interactions and functions of symbiotic and pathogenic microorganisms. Such studies, related to field observations, may have value for defining biological attributes of sustainable grassland soil systems

Bardgett, R. D.

Cook, R.

Eason, W. R.

Skøt, L.

Webb, K. J.

English

University of Kentucky

University of Kentucky UKnowledge International Grassland Congress Proceedings XIX International Grassland Congress Biological Interactions in Grassland Soils and Productivity R. Cook Institute of Grassland and Environmental Research, UK R. D. Bardgett Institute of Environmental and Natural Sciences, UK W. R. Eason Institute of Grassland and Environmental Research, UK L. Skøt Institute of Grassland and Environmental Research, UK K. J. Webb Institute of Grassland and Environmental Research, UK Follow this and additional works at: https://uknowledge.uky.edu/igc  Part of the Plant Sciences Commons, and the Soil Science Commons This document is available at https://uknowledge.uky.edu/igc/19/4/5 This collection is currently under construction. The XIX International Grassland Congress took place in São Pedro, São Paulo, Brazil from February 11 through February 21, 2001. Proceedings published by Fundacao de Estudos Agrarios Luiz de Queiroz This Event is brought to you for free and open access by the Plant and Soil Sciences at UKnowledge. It has been accepted for inclusion in International Grassland Congress Proceedings by an authorized administrator of UKnowledge. For more information, please contact UKnowledge@lsv.uky.edu. ID # 04-05BIOLOGICAL INTERACTIONS IN GRASSLAND SOILS AND PRODUCTIVITYR. Cook1, R. D. Bardgett2, W. R. Eason1, L. Skøt1 and K. J. Webb11Institute of Grassland and Environmental Research, Aberystwyth, SY23 3EB, UK2Institute of Environmental and Natural Sciences, Lancaster University, Lancaster, LA1 4YQ,UKAbstractThis paper describes research on interactions between grassland plant species and soilmicroorganisms.  Both parasitic and symbiotic microorganisms modify nutrient transfersbetween plants and soil.  Experiments are described in which nematode infection of cloverincreased nitrogen transfer to companion ryegrass plants.  Infection of clover enhancedactivity of soil bacterial and fungal communities.  Legume genotypes differing only inresponses to symbionts (rhizobium and arbuscular mycorrhizal fungi) and pathogens are beingdeveloped for studies of gene expression during establishing and functional symbioses.  Suchplants can be used in experiments as defined perturbations that will provide information onthe interactions and functions of symbiotic and pathogenic microorganisms.  Such studies,related to field observations, may have value for defining biological attributes of sustainablegrassland soil systems.Keywords: Gene expression, nematodes, nutrient cycling, mycorrhizae, rhizobia, whiteclover.IntroductionSoils under temperate grasslands develop rich biological communities of micro-floraand fauna (Bardgett and Cook, 1998) that determine soil fertility and hence productivity ofgrassland systems.  The roles of some of the soil biota are well known particularly as directinteractions with single crop plant species.  For example, root-feeding nematode speciesreduce plant growth and crop yield.  In contrast, symbioses with arbuscular mycorhizal fungi(AMF) and with rhizobia contribute directly to plant phosphorus and nitrogen nutrition.There are also indirect effects of these interactions.  For example, nematodes impact onmicrobial activities, affecting decomposition and plant growth, and AMF promote planthealth, through alleviation of stress.  Analysis of biological communities and study of theirinteractions with each other and with plants is important to increase understanding of soilfunctions.We describe our current approaches to the study of 1) how nutrient cycling is affectedby grassland nematodes and 2) plant microbial interactions with legumes to identify thegenetic basis of effective symbioses.Materials and methodsRoot nematodes and nitrogen transfer.  Experiments to assess nematode impacts onnutrient cycling used white clover infected by clover cyst nematode, Heterodera trifolii.Clover and perennial ryegrass, Lolium perenne, were grown in field soil microcosms incontrolled environments.  In half the microcosms, soil was infested by addition of infectivejuvenile nematodes.  In one experiment, expanded leaves of clover plants were immersed in asolution of K15NO3 for 72h and the distribution of 15N to the companion ryegrass wasmeasured.  After 12 weeks, when second generation nematodes were feeding on the cloverroots, root biomass was determined and active soil microbial biomass estimated bychloroform fumigation-extraction and by analyses of phospholipid fatty acids (PLFA)(Bardgett et al., 1999a, b).Genetic basis of effective symbioses.  Two legumes are used to study geneexpression in symbiotic interactions: a model legume, Lotus japonicus, and the agriculturallyimportant, white clover.  One genetically tagged transformant of L. japonicus (line T90)responds to the presence of the nitrogen-fixing bacterium, Mesorhizobium loti, by expressingthe reporter gene, â-glucuronidase (GUS), in roots and nodules.  This tagged gene hashomology to genes encoding calcium-binding proteins (Webb, Skøt et al., 2000).Homozygous seedlings from T90 were challenged with two AMF species, Glomusintraradices and G. mossae and with pathogenic, root-knot nematode, Meloidogyne hapla.We monitored expression of the rhizobium-induced promoter by histochemically staining forGUS expression in inoculated roots.Traits of agronomic importance are fixed in near-isogenic lines (NILs) of white cloverthat have been uniquely developed by IGER (Michaelson-Yeates et al, 1997).  43 NILs wereinfected with G. mossae and plant growth responses and AMF root infection monitored.Results and DiscussionRoot nematodes and nitrogen transfer. Root biomass of nematode-infected whiteclover plants was 140% more than that of uninfected controls.  There were 37% moreRhizobium-nodules on these roots and enhanced nitrogen fixation capacity and nitrogensupply to the plant may account for the heavier roots of infected plants.  Nematode infectionof white clover roots also led to a significant increase (217%) in root biomass of thecompanion ryegrass, not itself infected by the nematodes, and to a 322% increase in grassuptake of white clover-derived 15N.  Total abundance of PLFA, a measure of the 'active'microbial biomass, in the rhizosphere soil from lightly infested plants was twice that in soilfrom uninfected controls.  Increases in the size of the active rhizosphere microbial biomasswere associated with increases in the abundance of fatty acids synthesised by gram-negativeand gram-positive bacteria, and fatty acids specific to fungi.These experiments suggest that non-damaging infection of white clover rootsenhances N flux into the soil, where it is recycled by the microbial community and taken upby neighbouring ryegrass.  This is evidence of a linkage between nematode-induced increasesin soil microbial metabolism and below ground performance of companion plants.  Insect rootherbivory also increases loss of nitrogen from clover roots (Murray and Hatch, 1994).  It hasalso been shown that low densities root infection of white clover by cyst nematode increasedrhizodeposition of carbon (Yeates et al., 1998).  The overall effect of such interactions is toincrease root growth of both the host plant (white clover) and also the uninfectedneighbouring grass, presumably influencing productivity and competitive interactionsbetween these plant species (Bardgett et al., 1999b).These experiments emphasise the importance of microorganisms in nutrient transferswithin grassland soils.  It seems likely that rhizodepositions of carbon will be importantenergy sources for nutrient transfers facilitated by microorganisms.  Observations on thechanges in, for example, nematode and fungal communities in response to changes inmanagement practices (mainly quantity and quality of nitrogen supply) indicate that fungalactivity is more prominent in lower input systems (Yeates et al., 1997).Genetic basis of effective symbioses.  In L. japonicus line T90, the GUS-taggedpromoter was induced by symbionts - M. loti and both species of AMF - but not by root-knotnematodes (Tuck et al., 2000).  Further tests of the specificity of this tagged gene includechallenge by a range of other pathogens, such as root-rot fungus, Fusarium sp. andRhizoctonia sp. and chemicals, such as Nod factor signals.Clover genotype influenced both plant response to AMF as well as AMF infectionrates, supporting previous findings (Manske, 1990).  Infection rates ranged from 0 to 37%,with shoot weight increasing with infection of some plants but decreasing for others.  Linesthat were closely related (i.e. derived from the same original parent line) but that differed inresponses to infection were selected for more detailed study.  Nutrient flowing culturemicrocosm systems are being used to relate key physiological markers (such as phosphateuptake) to plant gene expression using differential display analysis.  Other white clover NILshave been identified that differ in response to rhizobium and to a nematode pest, Ditylenchusdipsaci.Plants, such as the single gene transformed Lotus plants and clover NILs that havebeen characterised genetically and phenotypically, are valuable for making controlledperturbations in realistic grassland soil systems.  Growing such contrasting plants andcomparing the responses of the soil biota and consequences for plant nutrition and soilfunction will contribute to understanding how complex nutrient cycles may be regulated byinteractions between heterotrophic micro-organisms.  Such understanding will be of value indesigning and managing sustainable grassland systems.ReferencesBardgett, R.D. and Cook, R.  (1998).  Functional aspects of soil animal diversity inagricultural grasslands.  Applied Soil Ecology 10: 263-276.Bardgett, R.D., Cook, R., Yeates, G.W. and Denton, C.S.  (1999a).  The influence ofnematodes on belowground processes in grassland ecosystems.  Plant and Soil 212: 23-33.Bardgett, R.D., Denton, C.S. and Cook, R.  (1999b).  Belowground herbivory promotes soilnutrient transfer and root growth in grassland.  Ecology Letters 2: 357-360.Manske, G.G.B.  (1990).  Genetical analysis of the efficiency of vesicular-arbuscularmycorrhiza in spring wheat.  Agriculture, Ecosystems and Environment 29: 273-280.Michaelson-Yeates, T.P.T., Marshall, A., Abberton, M.T. and Rhodes, I.  (1997).  Self-compatibility and heterosis in white clover (Trifolium repens).  Euphytica 94: 341-348.Murray, P.J. and Hatch, D.J.  (1994).  Sitona weevils (Coleoptera; Curculionidae) as agentsfor rapid transfer of nitrogen from white clover (Trifolium repens L.) to perennial ryegrass.Annals of Applied Biology 125: 29-33.Tuck, E., Skot, L. Cook, R., Parniske, M.  and Webb, K.J.  (2000).  Early gene expressionduring plant-microbe interactions.  Second International Conference on the Model LegumeLotus japonicus. Norwich, U.K. 24-28th June 2000. [Abstract].Webb, K.J., Skøt, L., Nicholson, M.N., Jørgensen, B. and Mizen, S.  (2000).  Mesorhizobiumloti increases root-specific expression of a calcium-binding protein homologue identified bypromoter tagging in Lotus japonicus.  Molecular Plant-Microbe Interactions (in press).Yeates, G.W., Bardgett, R.D., Cook, R., Hobbs, P.J., Bowling, P.J. and Potter, J.F.(1997).  Faunal and microbial diversity in three Welsh grassland soils under conventional andorganic management regimes.  Journal of Applied Ecology 34: 453-470.Yeates, G.W., Saggar, S., Denton, C.S. and Mercer, C.F.  (1998).  Impact of clover cystnematodes (Heterodera trifolii) infection on soil microbial activity in the rhizosphere of whiteclover (Trifolium repens): a pulse labelling experiment.  Nematologica 44: 81-90.

Biological Interactions in Grassland Soils and Productivity

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Biological Interactions in Grassland Soils and Productivity

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