Outcome variation in maize interaction with arbuscular mycorrhizal fungi is correlated with extent of extra-radical mycelium

In light of the rising cost, and often limited availability, of agricultural fertilizers, arbuscular mycorrhizas are attracting ever greater interest for their potential to promote more efficient use of the world9s mineral resources. And yet, this potential remains largely unrealized, in part because of a lack of understanding of the factors determining the outcome of the symbiosis in any given context. In this work, we evaluated a panel of maize inbred lines, selected to maximize genetic diversity, under low phosphate availability, with or without inoculation with arbuscular mycorrhizal fungi. Concomitant with measurement of plant growth, we characterized fungal morphology, element profiles and accumulation of transcripts encoding the PHT1 family of phosphorus transporters. We identified the lines Oh43 and Mo18W to show similar performance when not inoculated, but outlying high and low performance, respectively, when inoculated with arbuscular mycorrhizal fungi. We observed a correlation between the high responsiveness of Oh43 and the extent of the extra-radical fungal mycelium, consistent with the interpretation that the phosphorus contribution from the mycorrhizal uptake pathway is determined largely by the abundance of hyphae in the soil.

[1]  A. Fernie,et al.  An integrated functional approach to dissect systemic responses in maize to arbuscular mycorrhizal symbiosis. , 2015, Plant, cell & environment.

[2]  M. J. Harrison,et al.  Suppression of Arbuscule Degeneration in Medicago truncatula phosphate transporter4 Mutants Is Dependent on the Ammonium Transporter 2 Family Protein AMT2;3 , 2015, Plant Cell.

[3]  I. Baxter Should we treat the ionome as a combination of individual elements, or should we be deriving novel combined traits? , 2015, Journal of experimental botany.

[4]  T. Boller,et al.  Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. , 2015, The New phytologist.

[5]  Benjamin L Turner,et al.  Leaf manganese accumulation and phosphorus-acquisition efficiency. , 2015, Trends in plant science.

[6]  S. Baldwin,et al.  Phosphate Concentration and Arbuscular Mycorrhizal Colonisation Influence the Growth, Yield and Expression of Twelve PHT1 Family Phosphate Transporters in Foxtail Millet (Setaria italica) , 2014, PloS one.

[7]  M. R. Espuny,et al.  Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. , 2014, Microbiological research.

[8]  B. Buer,et al.  Mycorrhizal phosphate uptake pathway in maize: vital for growth and cob development on nutrient poor agricultural and greenhouse soils , 2013, Front. Plant Sci..

[9]  H. Lambers,et al.  Do arbuscular mycorrhizas or heterotrophic soil microbes contribute toward plant acquisition of a pulse of mineral phosphate? , 2013, Plant and Soil.

[10]  P. Armstrong,et al.  Ionomic Screening of Field‐Grown Soybean Identifies Mutants with Altered Seed Elemental Composition , 2013 .

[11]  Fusuo Zhang,et al.  Mycorrhizal responsiveness of maize (Zea mays L.) genotypes as related to releasing date and available P content in soil , 2013, Mycorrhiza.

[12]  D. Wipf,et al.  The Medicago truncatula sucrose transporter family: characterization and implication of key members in carbon partitioning towards arbuscular mycorrhizal fungi. , 2012, Molecular plant.

[13]  U. Paszkowski,et al.  Nonredundant Regulation of Rice Arbuscular Mycorrhizal Symbiosis by Two Members of the PHOSPHATE TRANSPORTER1 Gene Family[W] , 2012, Plant Cell.

[14]  D. Wipf,et al.  Sugar transporters in plants and in their interactions with fungi. , 2012, Trends in plant science.

[15]  Jason G. Bragg,et al.  Opportunities for improving phosphorus-use efficiency in crop plants. , 2012, The New phytologist.

[16]  M. J. Harrison,et al.  Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon , 2012, Planta.

[17]  T. Boller,et al.  Mycorrhizal Networks: Common Goods of Plants Shared under Unequal Terms of Trade1[W][OA] , 2012, Plant Physiology.

[18]  Lin Mao,et al.  Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. , 2012, The New phytologist.

[19]  M. J. Harrison,et al.  Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion , 2012, Proceedings of the National Academy of Sciences.

[20]  David M. Goodstein,et al.  Phytozome: a comparative platform for green plant genomics , 2011, Nucleic Acids Res..

[21]  R. Sekhon,et al.  Utility of RNA Sequencing for Analysis of Maize Reproductive Transcriptomes , 2011 .

[22]  M. Rose,et al.  The Frustration with Utilization: Why Have Improvements in Internal Phosphorus Utilization Efficiency in Crops Remained so Elusive? , 2011, Front. Plant Sci..

[23]  T. Fester,et al.  Progress and Challenges in Agricultural Applications of Arbuscular Mycorrhizal Fungi , 2011 .

[24]  Jonathan P Lynch,et al.  Root Phenes for Enhanced Soil Exploration and Phosphorus Acquisition: Tools for Future Crops , 2011, Plant Physiology.

[25]  James C. Schnable,et al.  Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss , 2011, Proceedings of the National Academy of Sciences.

[26]  Robert Turgeon,et al.  The developmental dynamics of the maize leaf transcriptome , 2010, Nature Genetics.

[27]  C. Lévesque,et al.  Conspecificity of DAOM 197198, the model arbuscular mycorrhizal fungus, with Glomus irregulare: molecular evidence with three protein-encoding genes. , 2010 .

[28]  Lisa C. Harper,et al.  Choosing a genome browser for a Model Organism Database: surveying the Maize community , 2010, Database J. Biol. Databases Curation.

[29]  S. Hata,et al.  Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. , 2010, Plant & cell physiology.

[30]  U. Paszkowski,et al.  Characterizing variation in mycorrhiza effect among diverse plant varieties , 2010, Theoretical and Applied Genetics.

[31]  Dawn H. Nagel,et al.  The B73 Maize Genome: Complexity, Diversity, and Dynamics , 2009, Science.

[32]  M. McMullen,et al.  Genetic Properties of the Maize Nested Association Mapping Population , 2009, Science.

[33]  X. Liu,et al.  Genome-Wide and Organ-Specific Landscapes of Epigenetic Modifications and Their Relationships to mRNA and Small RNA Transcriptomes in Maize[W] , 2009, The Plant Cell Online.

[34]  M. Tester,et al.  Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. , 2009, The New phytologist.

[35]  U. Paszkowski,et al.  Arbuscular Mycorrhiza–Specific Signaling in Rice Transcends the Common Symbiosis Signaling Pathway[W] , 2008, The Plant Cell Online.

[36]  Martin Parniske,et al.  Arbuscular mycorrhiza: the mother of plant root endosymbioses , 2008, Nature Reviews Microbiology.

[37]  T. Roose,et al.  Impact of growth and uptake patterns of arbuscular mycorrhizal fungi on plant phosphorus uptake—a modelling study , 2008, Plant and Soil.

[38]  Olga Vitek,et al.  The leaf ionome as a multivariable system to detect a plant's physiological status , 2008, Proceedings of the National Academy of Sciences.

[39]  Caroline Gutjahr,et al.  Cereal mycorrhiza: an ancient symbiosis in modern agriculture. , 2008, Trends in plant science.

[40]  J. Syers,et al.  Efficiency of soil and fertilizer phosphorus use. Reconciling changing concepts of soil phosphorus behaviour with agronomic information , 2008 .

[41]  M. J. Harrison,et al.  A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis , 2007, Proceedings of the National Academy of Sciences.

[42]  M. Bucher Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. , 2007, The New phytologist.

[43]  D. Janos Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas , 2007, Mycorrhiza.

[44]  U. Paszkowski,et al.  Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis. , 2006, The Plant journal : for cell and molecular biology.

[45]  K. Izui,et al.  Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. , 2006, Plant & cell physiology.

[46]  N. Amrhein,et al.  Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). , 2006, Plant biology.

[47]  D. Read,et al.  European and African maize cultivars differ in their physiological and molecular responses to mycorrhizal infection. , 2005, The New phytologist.

[48]  F. W. Smith,et al.  Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots , 2005, Planta.

[49]  A. Osbourn,et al.  Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Guohua Xu,et al.  The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. , 2005, The Plant journal : for cell and molecular biology.

[51]  M. Bucher,et al.  Symbiotic phosphate transport in arbuscular mycorrhizas. , 2005, Trends in plant science.

[52]  M. Vestberg,et al.  High functional diversity within species of arbuscular mycorrhizal fungi. , 2004, The New phytologist.

[53]  I. Jakobsen,et al.  Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake , 2004 .

[54]  Steven G. Schroeder,et al.  Anchoring 9,371 Maize Expressed Sequence Tagged Unigenes to the Bacterial Artificial Chromosome Contig Map by Two-Dimensional Overgo Hybridization1 , 2004, Plant Physiology.

[55]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[56]  V. Römheld,et al.  Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize , 1994, Mycorrhiza.

[57]  R. Koide,et al.  Role of mycorrhizal infection in the growth and reproduction of wild vs. cultivated plants , 1988, Oecologia.

[58]  I. Jakobsen,et al.  Mycorrhizal Fungi Can Dominate Phosphate Supply to Plants Irrespective of Growth Responses1 , 2003, Plant Physiology.

[59]  M. J. Harrison,et al.  A Phosphate Transporter from Medicago truncatula Involved in the Acquisition of Phosphate Released by Arbuscular Mycorrhizal Fungi Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004861. , 2002, The Plant Cell Online.

[60]  U. Paszkowski,et al.  Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[61]  G. Feng,et al.  Influence of extramatrical hyphae on mycorrhizal dependency of wheat genotypes , 2001 .

[62]  J. Jansa,et al.  A phosphate transporter expressed in arbuscule-containing cells in potato , 2001, Nature.

[63]  C. Vance,et al.  Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. , 2001, Plant physiology.

[64]  I. Jakobsen,et al.  Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores. , 2001, The New phytologist.

[65]  S. Kaeppler,et al.  Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi , 2000 .

[66]  P. Schweiger,et al.  Comparison of two test systems for measuring plant phosphorus uptake via arbuscular mycorrhizal fungi , 1999, Mycorrhiza.

[67]  B. Hetrick,et al.  Mycorrhizal response in wheat cultivars: relationship to phosphorus , 1996 .

[68]  I. Jakobsen,et al.  The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labelling with 32P and 33P , 1993 .

[69]  B. Hetrick,et al.  Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors , 1992 .

[70]  I. Jakobsen,et al.  External hyphae of vesicular–arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. , 1992 .

[71]  S. Harashima,et al.  The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter , 1991, Molecular and cellular biology.

[72]  V. Römheld,et al.  Effect of a vesicular–arbuscular mycorrhizal fungus and rhizosphere micro-organisms on manganese reduction in the rhizosphere and manganese concentrations in maize (Zea mays L.) , 1991 .

[73]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[74]  P. Kormanik,et al.  Quantification of vesicular-arbuscular mycorrhizae in plant roots. , 1982 .

[75]  S. R. Olsen,et al.  Estimation of available phosphorus in soils by extraction with sodium bicarbonate , 1954 .