Nitrogen Type and Availability Drive Mycorrhizal Effects on Wheat Performance, Nitrogen Uptake and Recovery, and Production Sustainability

Plant performance is strongly dependent on nitrogen (N), and thus increasing N nutrition is of great relevance for the productivity of agroecosystems. The effects of arbuscular mycorrhizal (AM) fungi on plant N acquisition are debated because contradictory results have been reported. Using 15N-labeled fertilizers as a tracer, we evaluated the effects of AM fungi on N uptake and recovery from mineral or organic sources in durum wheat. Under sufficient N availability, AM fungi had no effects on plant biomass but increased N concentrations in plant tissue, plant N uptake, and total N recovered from the fertilizer. In N-deficient soil, AM fungi led to decreased aboveground biomass, which suggests that plants and AM fungi may have competed for N. When the organic source had a low C:N ratio, AM fungi favored both plant N uptake and N recovery. In contrast, when the organic source had a high C:N ratio, a clear reduction in N recovery from the fertilizer was observed. Overall, the results indicate an active role of arbuscular mycorrhizae in favoring plant N-related traits when N is not a limiting factor and show that these fungi help in N recovery from the fertilizer. These results hold great potential for increasing the sustainability of durum wheat production.

[1]  Hyungwon Choi,et al.  Moving beyond P values: data analysis with estimation graphics , 2019, Nature Methods.

[2]  M. Rillig,et al.  Subsoil Arbuscular Mycorrhizal Fungi for Sustainability and Climate-Smart Agriculture: A Solution Right Under Our Feet? , 2019, Front. Microbiol..

[3]  Dylan T. Simpson,et al.  Revisiting the ‘direct mineral cycling’ hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why? , 2019, The ISME Journal.

[4]  R. Betensky.  The p-Value Requires Context, Not a Threshold , 2019, The American Statistician.

[5]  N. Lazar,et al.  Moving to a World Beyond “p < 0.05” , 2019, The American Statistician.

[6]  Hyungwon Choi,et al.  Moving beyond P values: Everyday data analysis with estimation plots , 2018, bioRxiv.

[7]  M. Bonkowski,et al.  Utilization of organic nitrogen by arbuscular mycorrhizal fungi—is there a specific role for protists and ammonia oxidizers? , 2018, Mycorrhiza.

[8]  Xin-ping Chen,et al.  Arbuscular Mycorrhizal Fungi Negatively Affect Nitrogen Acquisition and Grain Yield of Maize in a N Deficient Soil , 2018, Front. Microbiol..

[9]  K. Treseder,et al.  Arbuscular mycorrhizal fungi as mediators of ecosystem responses to nitrogen deposition: A trait‐based predictive framework , 2018 .

[10]  M. Bonkowski,et al.  Utilization of organic nitrogen by arbuscular mycorrhizal fungi—is there a specific role for protists and ammonia oxidizers? , 2018, Mycorrhiza.

[11]  anonymous.  In Review , 2018 .

[12]  A. Plaia,et al.  Switching from conventional tillage to no-tillage: Soil N availability, N uptake,15N fertilizer recovery, and grain yield of durum wheat , 2018 .

[13]  A. Hodge,et al.  Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots , 2017, The New phytologist.

[14]  C. Rauh,et al.  Soil Biodiversity Effects from Field to Fork. , 2018, Trends in plant science.

[15]  L. Ercoli,et al.  Strong increase of durum wheat iron and zinc content by field-inoculation with arbuscular mycorrhizal fungi at different soil nitrogen availabilities , 2017, Plant and Soil.

[16]  M. Rillig,et al.  Towards an Integrated Mycorrhizal Technology: Harnessing Mycorrhiza for Sustainable Intensification in Agriculture , 2016, Front. Plant Sci..

[17]  M. Hujslová,et al.  Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply , 2016, Ecology and evolution.

[18]  E. Paterson,et al.  Arbuscular mycorrhizal hyphae promote priming of native soil organic matter mineralisation , 2016, Plant and Soil.

[19]  N. Lazar,et al.  The ASA Statement on p-Values: Context, Process, and Purpose , 2016 .

[20]  S. Saia,et al.  Long-term effects of no tillage treatment on soil N availability, N uptake, and 15N-fertilizer recovery of durum wheat differ in relation to crop sequence , 2016 .

[21]  M. V. D. Heijden,et al.  Arbuscular mycorrhizal fungal species differ in their effect on nutrient leaching , 2016 .

[22]  A. Hodge,et al.  Resolving the ‘nitrogen paradox’ of arbuscular mycorrhizas: fertilization with organic matter brings considerable benefits for plant nutrition and growth , 2016, Plant, cell & environment.

[23]  S. Saia,et al.  Soil inoculation with symbiotic microorganisms promotes plant growth and nutrient transporter genes expression in durum wheat , 2015, Front. Plant Sci..

[24]  D. Shan,et al.  Effects of Arbuscular Mycorrhizal Fungi on N2O Emissions from Rice Paddies , 2015, Water, Air, & Soil Pollution.

[25]  T. Cavagnaro,et al.  The role of arbuscular mycorrhizas in reducing soil nutrient loss. , 2015, Trends in plant science.

[26]  S. Saia,et al.  Nitrogen uptake and nitrogen fertilizer recovery in old and modern wheat genotypes grown in the presence or absence of interspecific competition , 2015, Front. Plant Sci..

[27]  C. Cruz,et al.  Nitrogen and carbon/nitrogen dynamics in arbuscular mycorrhiza: the great unknown , 2015, Mycorrhiza.

[28]  E. Kiers,et al.  Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. , 2014, The New phytologist.

[29]  A. Hodge,et al.  Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems , 2014, Plant and Soil.

[30]  C. Cruz,et al.  Shedding light onto nutrient responses of arbuscular mycorrhizal plants: nutrient interactions may lead to unpredicted outcomes of the symbiosis. , 2014, Plant science : an international journal of experimental plant biology.

[31]  A. Neftel,et al.  Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil , 2013, The ISME Journal.

[32]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[33]  M. Rillig,et al.  Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation—a meta-analysis , 2013, Plant and Soil.

[34]  R. Drijber,et al.  Diversity and vertical distribution of indigenous arbuscular mycorrhizal fungi under two soybean rotational systems , 2013, Biology and Fertility of Soils.

[35]  S. Saia,et al.  The effect of arbuscular mycorrhizal fungi on total plant nitrogen uptake and nitrogen recovery from soil organic material , 2013, The Journal of Agricultural Science.

[36]  R. Ceulemans,et al.  Effects of arbuscular mycorrhizal fungi on grassland productivity are altered by future climate and below-ground resource availability , 2012 .

[37]  Pariva Dobriyal,et al.  A review of the methods available for estimating soil moisture and its implications for water resource management , 2012 .

[38]  S. Saia,et al.  Faba bean grain yield, N2 fixation, and weed infestation in a long-term tillage experiment under rainfed Mediterranean conditions , 2012, Plant and Soil.

[39]  D. Herman,et al.  Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition. , 2012, FEMS microbiology ecology.

[40]  M. Rillig,et al.  Arbuscular mycorrhiza and soil nitrogen cycling , 2012 .

[41]  T. Cavagnaro,et al.  Arbuscular Mycorrhizas Reduce Nitrogen Loss via Leaching , 2012, PloS one.

[42]  V. Fiorilli,et al.  GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. , 2011, Fungal genetics and biology : FG & B.

[43]  Sally E. Smith,et al.  Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. , 2011, Annual review of plant biology.

[44]  Angela Hodge,et al.  Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling , 2010, Proceedings of the National Academy of Sciences.

[45]  Matthew Hannah,et al.  Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. , 2009, The New phytologist.

[46]  Marek Dynowski,et al.  A Mycorrhizal-Specific Ammonium Transporter from Lotus japonicus Acquires Nitrogen Released by Arbuscular Mycorrhizal Fungi1 , 2009, Plant Physiology.

[47]  Yun Li,et al.  Effects of mulch, N fertilizer, and plant density on wheat yield, wheat nitrogen uptake, and residual soil nitrate in a dryland area of China , 2009, Nutrient Cycling in Agroecosystems.

[48]  S. Allison,et al.  Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change , 2008 .

[49]  A. Schüßler,et al.  Arbuscular Mycorrhiza , 2007, Plant signaling & behavior.

[50]  B. Ney,et al.  The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. , 2007, Journal of experimental botany.

[51]  M. V. D. van der Heijden,et al.  The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. , 2006, The New phytologist.

[52]  J. Bever,et al.  Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. , 2005, The New phytologist.

[53]  I. Jakobsen,et al.  Nitrogen input mediates the effect of free‐air CO2 enrichment on mycorrhizal fungal abundance , 2004 .

[54]  A. Lüscher,et al.  Arbuscular mycorrhizal fungi benefit from 7 years of free air CO2 enrichment in well‐fertilized grass and legume monocultures , 2004 .

[55]  A. Johansen,et al.  Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi , 2000, Plant and Soil.

[56]  Jean-Marc Meynard,et al.  Relationship between rate of crop growth at date of fertiliser N application and fate of fertiliser N applied to winter wheat , 1999, Plant and Soil.

[57]  A. Johansen,et al.  Hyphal N transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at three nitrogen levels , 1994, Plant and Soil.

[58]  H. Vierheilig,et al.  Variable carbon-sink strength of different Glomus mosseae strains colonizing barley roots , 2003 .

[59]  K. Treseder,et al.  Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. , 2002, The New phytologist.

[60]  Hans-Werner Olfs,et al.  Strategies to Improve the Use Efficiency of Mineral Fertilizer Nitrogen Applied to Winter Wheat , 2002 .

[61]  A. Hodge,et al.  An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material , 2001, Nature.

[62]  Y. Shachar-Hill,et al.  Carbon metabolism and transport in arbuscular mycorrhizas. , 2000, Plant physiology.

[63]  A. Hodge,et al.  Are microorganisms more effective than plants at competing for nitrogen? , 2000, Trends in plant science.

[64]  William R. Raun,et al.  Improving Nitrogen Use Efficiency for Cereal Production , 1999 .

[65]  L. Drinkwater,et al.  Legume-based cropping systems have reduced carbon and nitrogen losses , 1998, Nature.

[66]  R. K. Scott,et al.  Evidence for differences between winter wheat cultivars in acquisition of soil mineral nitrogen and uptake and utilization of applied fertilizer nitrogen , 1998, The Journal of Agricultural Science.

[67]  M. Quemada,et al.  Carbon and Nitrogen Mineralized from Leaves and Stems of Four Cover Crops , 1995 .

[68]  J. Visser,et al.  Carbon metabolism. , 1994, Progress in industrial microbiology.

[69]  L. Brussaard,et al.  Biological effects of plant residues with contrasting chemical compositions under humid tropical conditions-decomposition and nutrient release , 1992 .

[70]  G. Fairchild,et al.  A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. , 1990, The New phytologist.

[71]  Christopher B. Field,et al.  Plant Responses to Multiple Environmental FactorsPhysiological ecology provides tools for studying how interacting environmental resources control plant growth , 1987 .

[72]  M. Gardner,et al.  Confidence intervals rather than P values: estimation rather than hypothesis testing. , 1986, British medical journal.

[73]  J. M. Bremner,et al.  Use of Tracers For Soil And Fertilizer Nitrogen Research , 1976 .

[74]  D. Tennant,et al.  A test of a modified line intersect method of estimating root length , 1975 .

[75]  J. M. Phillips,et al.  Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. , 1970 .

[76]  Haddon Ac.  PROFESSOR FLINDERS PETRIE'S SCHEME OF AN ETHNOLOGICAL STORE-HOUSE. , 1897 .