First Cryo-Scanning Electron Microscopy Images and X-Ray Microanalyses of Mucoromycotinian Fine Root Endophytes in Vascular Plants
Arbuscule-producing fine root endophytes (FRE) (previously incorrectly ) were recently placed within subphylum Mucoromycotina; the first report of arbuscules outside subphylum Glomeromycotina. Here, we aimed to estimate nutrient concentrations in plant and fungal structures of FRE and to test the ut...
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Published in | Frontiers in microbiology Vol. 11; p. 2018 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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03.09.2020
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Abstract | Arbuscule-producing fine root endophytes (FRE) (previously incorrectly
) were recently placed within subphylum Mucoromycotina; the first report of arbuscules outside subphylum Glomeromycotina. Here, we aimed to estimate nutrient concentrations in plant and fungal structures of FRE and to test the utility of cryo-scanning electron microscopy (cryoSEM) for studying these fungi.
We used replicated cryoSEM and X-ray microanalysis of heavily colonized roots of
.
Intercellular hyphae and hyphae in developed arbuscules were consistently very thin; 1.35 ± 0.03 μm and 0.99 ± 0.03 μm in diameter, respectively (mean ± SE). Several intercellular hyphae were often adjacent to each other forming "hyphal ropes." Developed arbuscules showed higher phosphorus concentrations than senesced arbuscules and non-colonized structures. Senesced arbuscules showed greatly elevated concentrations of calcium and magnesium.
While uniformly thin hyphae and hyphal ropes are distinct features of FRE, the morphology of fully developed arbuscules, elevated phosphorus in fungal structures, and accumulation of calcium with loss of structural integrity in senesced arbuscules are similar to glomeromycotinian fungi. Thus, we provide evidence that FRE may respond to similar host-plant signals or that the host plant may employ a similar mechanism of association with FRE and AMF. |
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AbstractList | Arbuscule-producing fine root endophytes (FRE) (previously incorrectly Glomus tenue) were recently placed within subphylum Mucoromycotina; the first report of arbuscules outside subphylum Glomeromycotina. Here, we aimed to estimate nutrient concentrations in plant and fungal structures of FRE and to test the utility of cryo-scanning electron microscopy (cryoSEM) for studying these fungi.AIMSArbuscule-producing fine root endophytes (FRE) (previously incorrectly Glomus tenue) were recently placed within subphylum Mucoromycotina; the first report of arbuscules outside subphylum Glomeromycotina. Here, we aimed to estimate nutrient concentrations in plant and fungal structures of FRE and to test the utility of cryo-scanning electron microscopy (cryoSEM) for studying these fungi.We used replicated cryoSEM and X-ray microanalysis of heavily colonized roots of Trifolium subterraneum.METHODSWe used replicated cryoSEM and X-ray microanalysis of heavily colonized roots of Trifolium subterraneum.Intercellular hyphae and hyphae in developed arbuscules were consistently very thin; 1.35 ± 0.03 μm and 0.99 ± 0.03 μm in diameter, respectively (mean ± SE). Several intercellular hyphae were often adjacent to each other forming "hyphal ropes." Developed arbuscules showed higher phosphorus concentrations than senesced arbuscules and non-colonized structures. Senesced arbuscules showed greatly elevated concentrations of calcium and magnesium.RESULTSIntercellular hyphae and hyphae in developed arbuscules were consistently very thin; 1.35 ± 0.03 μm and 0.99 ± 0.03 μm in diameter, respectively (mean ± SE). Several intercellular hyphae were often adjacent to each other forming "hyphal ropes." Developed arbuscules showed higher phosphorus concentrations than senesced arbuscules and non-colonized structures. Senesced arbuscules showed greatly elevated concentrations of calcium and magnesium.While uniformly thin hyphae and hyphal ropes are distinct features of FRE, the morphology of fully developed arbuscules, elevated phosphorus in fungal structures, and accumulation of calcium with loss of structural integrity in senesced arbuscules are similar to glomeromycotinian fungi. Thus, we provide evidence that FRE may respond to similar host-plant signals or that the host plant may employ a similar mechanism of association with FRE and AMF.CONCLUSIONWhile uniformly thin hyphae and hyphal ropes are distinct features of FRE, the morphology of fully developed arbuscules, elevated phosphorus in fungal structures, and accumulation of calcium with loss of structural integrity in senesced arbuscules are similar to glomeromycotinian fungi. Thus, we provide evidence that FRE may respond to similar host-plant signals or that the host plant may employ a similar mechanism of association with FRE and AMF. Arbuscule-producing fine root endophytes (FRE) (previously incorrectly ) were recently placed within subphylum Mucoromycotina; the first report of arbuscules outside subphylum Glomeromycotina. Here, we aimed to estimate nutrient concentrations in plant and fungal structures of FRE and to test the utility of cryo-scanning electron microscopy (cryoSEM) for studying these fungi. We used replicated cryoSEM and X-ray microanalysis of heavily colonized roots of . Intercellular hyphae and hyphae in developed arbuscules were consistently very thin; 1.35 ± 0.03 μm and 0.99 ± 0.03 μm in diameter, respectively (mean ± SE). Several intercellular hyphae were often adjacent to each other forming "hyphal ropes." Developed arbuscules showed higher phosphorus concentrations than senesced arbuscules and non-colonized structures. Senesced arbuscules showed greatly elevated concentrations of calcium and magnesium. While uniformly thin hyphae and hyphal ropes are distinct features of FRE, the morphology of fully developed arbuscules, elevated phosphorus in fungal structures, and accumulation of calcium with loss of structural integrity in senesced arbuscules are similar to glomeromycotinian fungi. Thus, we provide evidence that FRE may respond to similar host-plant signals or that the host plant may employ a similar mechanism of association with FRE and AMF. AimsArbuscule-producing fine root endophytes (FRE) (previously incorrectly Glomus tenue) were recently placed within subphylum Mucoromycotina; the first report of arbuscules outside subphylum Glomeromycotina. Here, we aimed to estimate nutrient concentrations in plant and fungal structures of FRE and to test the utility of cryo-scanning electron microscopy (cryoSEM) for studying these fungi.MethodsWe used replicated cryoSEM and X-ray microanalysis of heavily colonized roots of Trifolium subterraneum.ResultsIntercellular hyphae and hyphae in developed arbuscules were consistently very thin; 1.35 ± 0.03 μm and 0.99 ± 0.03 μm in diameter, respectively (mean ± SE). Several intercellular hyphae were often adjacent to each other forming “hyphal ropes.” Developed arbuscules showed higher phosphorus concentrations than senesced arbuscules and non-colonized structures. Senesced arbuscules showed greatly elevated concentrations of calcium and magnesium.ConclusionWhile uniformly thin hyphae and hyphal ropes are distinct features of FRE, the morphology of fully developed arbuscules, elevated phosphorus in fungal structures, and accumulation of calcium with loss of structural integrity in senesced arbuscules are similar to glomeromycotinian fungi. Thus, we provide evidence that FRE may respond to similar host-plant signals or that the host plant may employ a similar mechanism of association with FRE and AMF. |
Author | Bending, Gary D. Hayes, Patrick E. Orchard, Suzanne Ryan, Megan H. Clode, Peta L. Albornoz, Felipe E. Hilton, Sally Nazeri, Nazanin K. Standish, Rachel J. |
AuthorAffiliation | 1 School of Agriculture and Environment, Institute of Agriculture, The University of Western Australia , Perth, WA , Australia 3 School of Biological Sciences, The University of Western Australia , Perth, WA , Australia 4 Environmental and Conservation Sciences, College of Science, Health, Engineering and Education, Murdoch University , Murdoch, WA , Australia 2 Centre for Microscopy, Characterisation and Analysis, The University of Western Australia , Perth, WA , Australia 5 School of Life Sciences, University of Warwick , Coventry , United Kingdom |
AuthorAffiliation_xml | – name: 3 School of Biological Sciences, The University of Western Australia , Perth, WA , Australia – name: 1 School of Agriculture and Environment, Institute of Agriculture, The University of Western Australia , Perth, WA , Australia – name: 4 Environmental and Conservation Sciences, College of Science, Health, Engineering and Education, Murdoch University , Murdoch, WA , Australia – name: 5 School of Life Sciences, University of Warwick , Coventry , United Kingdom – name: 2 Centre for Microscopy, Characterisation and Analysis, The University of Western Australia , Perth, WA , Australia |
Author_xml | – sequence: 1 givenname: Felipe E. surname: Albornoz fullname: Albornoz, Felipe E. – sequence: 2 givenname: Patrick E. surname: Hayes fullname: Hayes, Patrick E. – sequence: 3 givenname: Suzanne surname: Orchard fullname: Orchard, Suzanne – sequence: 4 givenname: Peta L. surname: Clode fullname: Clode, Peta L. – sequence: 5 givenname: Nazanin K. surname: Nazeri fullname: Nazeri, Nazanin K. – sequence: 6 givenname: Rachel J. surname: Standish fullname: Standish, Rachel J. – sequence: 7 givenname: Gary D. surname: Bending fullname: Bending, Gary D. – sequence: 8 givenname: Sally surname: Hilton fullname: Hilton, Sally – sequence: 9 givenname: Megan H. surname: Ryan fullname: Ryan, Megan H. |
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Cites_doi | 10.1111/ppl.12732 10.1093/jxb/erz156 10.1111/j.1744-697X.2005.00023.x 10.1007/s00572-017-0815-7 10.1016/j.pbi.2017.12.004 10.1104/pp.19.00729 10.1111/j.1469-8137.1990.tb00476.x 10.1111/jmi.12531 10.1111/jmi.12466 10.1046/j.1365-2818.1998.00313.x 10.1098/rsbl.2010.1203 10.5598/imafungus.2017.08.02.03 10.1071/FP10095 10.1007/s11104-019-03980-8 10.1111/nph.15819 10.1139/m76-009 10.1007/s11104-016-2867-4 10.1111/j.1469-8137.1981.tb01739.x 10.1111/j.1469-8137.1974.tb01319.x 10.1093/jxb/erz241 10.1007/978-1-4419-0318-1 10.1071/BT9820485 10.1128/aem.64.12.5004-5007.1998 10.1038/nmeth.3869 10.3390/ijerph16030373 10.1007/s00374-015-1027-y 10.1007/978-0-387-87458-6 10.1071/CP12194 10.1093/nar/gks1219 10.1242/jeb.032177 10.3389/fpls.2014.00337 10.1080/0028825X.1963.10428694 10.1046/j.1469-8137.2003.00884.x 10.1007/978-3-319-24277-4 10.1007/s00572-011-0373-3 10.1016/S0953-7562(89)80092-9 10.3852/16-042 10.7287/peerj.preprints.27295v2 10.1038/ismej.2015.204 10.1111/nph.15043 10.1038/s41598-018-28920-x 10.1007/s11104-016-2804-6 10.1071/FP08304 10.1111/pce.13124 10.1017/S0953756299001094 10.1016/j.scienta.2014.07.016 10.1111/nph.13024 10.1002/jemt.1070280108 10.1139/m75-258 10.1093/jxb/44.3.587 10.1080/0028825X.1979.10425160 10.1016/S0007-1536(77)80186-1 10.14806/ej.17.1.200 10.1111/nph.14268 10.1111/j.1365-2818.2011.03539.x 10.1139/m75-280 10.1071/FP06242 10.1007/s00572-017-0782-z 10.1111/j.1469-8137.1973.tb02073.x 10.1023/A:1004727331860 10.1139/m75-146 10.1006/anbo.2001.1540 |
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Copyright | Copyright © 2020 Albornoz, Hayes, Orchard, Clode, Nazeri, Standish, Bending, Hilton and Ryan. Copyright © 2020 Albornoz, Hayes, Orchard, Clode, Nazeri, Standish, Bending, Hilton and Ryan. 2020 Albornoz, Hayes, Orchard, Clode, Nazeri, Standish, Bending, Hilton and Ryan |
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Keywords | cryoSEM Glomus tenue Mucoromycotina arbuscules Planticonsortium |
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License | Copyright © 2020 Albornoz, Hayes, Orchard, Clode, Nazeri, Standish, Bending, Hilton and Ryan. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Sabine Dagmar Zimmermann, Délégation Languedoc Roussillon (CNRS), France; Bettina Hause, Leibniz-Institut für Pflanzenbiochemie (IPB), Germany; Catarina Cardoso, Technical University of Munich, Germany Edited by: Pierre-Emmanuel Courty, INRA Centre Dijon Bourgogne Franche-Comté, France This article was submitted to Microbe and Virus Interactions with Plants, a section of the journal Frontiers in Microbiology |
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References | Lee (B33) 1993; 44 Brundrett (B4) 1996 Field (B12) 2019; 223 Orchard (B45); 213 Hoysted (B24) 2018; 44 Nichols (B43) 2012; 63 Thippayarugs (B58) 1999; 103 Hayes (B22) 2018; 41 Zuur (B67) 2009 Hayes (B21) 2019; 70 Huang (B25) 1994; 28 McCully (B39) 2009; 36 Marshall (B35) 2009; 212 Ding (B8) 2018; 163 Jin (B27) 2017; 265 McCully (B40) 2010; 37 Bidartondo (B2) 2011; 7 Ryan (B54) 2007; 34 Marshall (B34) 2017; 266 Wickham (B64) 2016 Feijen (B11) 2018; 8 Kotula (B32) 2019; 70 Goldstein (B17) 2018 Taylor (B100) 2015; 51 Crush (B7) 1973; 72 Orchard (B46); 27 Kinden (B29); 21 Field (B13) 2015; 205 Walker (B62) 1979; 17 Kinden (B31) 1976; 22 Pinheiro (B49) 2016 McGee (B41) 1989; 92 White (B63) 2001; 88 Jentschke (B26) 2000; 220 Sato (B55) 2005; 51 Abbott (B1) 1982; 30 Bolyen (B3) 2018; 6 Martin (B38) 2011; 17 Ryan (B53) 2003; 160 Xiao (B65) 2014; 177 Smith (B56) 2008 Gianinazzi-Pearson (B16) 1981; 88 Callahan (B5) 2016; 13 Spatafora (B57) 2016; 108 Walker (B60) 2005; 56 Ding (B9) 2020; 447 Yamato (B66) 2011; 21 Walker (B61) 2018; 28 Hall (B20) 1977; 68 Greenall (B18) 1963; 1 Kinden (B28); 21 Orchard (B48); 403 Desirò (B10) 2017; 8 Garcia (B15) 2014; 5 Cox (B6) 1974; 73 Field (B14) 2016; 10 Marshall (B36) 2012; 245 Kinden (B30); 21 Orchard (B47); 412 (B52) 2016 Vierheilig (B59) 1998; 64 McGonigle (B42) 1990; 115 Marshall (B37) 1998; 190 Quast (B51) 2013; 41 Guilherme Pereira (B19) 2018; 218 Hoysted (B23) 2019; 181 Pinheiro (B50) 2000 Ondrasek (B44) 2019; 16 |
References_xml | – volume: 163 start-page: 386 year: 2018 ident: B8 article-title: Effects of calcium and its interaction with phosphorus on the nutrient status and growth of three Lupinus species. publication-title: Physiol. Plant. doi: 10.1111/ppl.12732 – volume: 70 start-page: 3995 year: 2019 ident: B21 article-title: Calcium modulates leaf cell-specific phosphorus allocation in Proteaceae from south-western Australia. publication-title: J. Exp. Bot. doi: 10.1093/jxb/erz156 – volume: 51 start-page: 179 year: 2005 ident: B55 article-title: A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. publication-title: Grassl. Sci. doi: 10.1111/j.1744-697X.2005.00023.x – volume: 28 start-page: 213 year: 2018 ident: B61 article-title: A new genus, Planticonsortium (Mucoromycotina), and new combination (P. tenue), for the fine root endophyte, Glomus tenue (basionym Rhizophagus tenuis). publication-title: Mycorrhiza doi: 10.1007/s00572-017-0815-7 – volume: 44 start-page: 1 year: 2018 ident: B24 article-title: A mycorrhizal revolution. publication-title: Curr. Opin. Plant Biol. doi: 10.1016/j.pbi.2017.12.004 – volume: 181 start-page: 565 year: 2019 ident: B23 article-title: Mucoromycotina fine root endophyte fungi form nutritional mutualisms with vascular plants. publication-title: Plant Physiol. doi: 10.1104/pp.19.00729 – volume: 115 start-page: 495 year: 1990 ident: B42 article-title: A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. publication-title: New Phytol. doi: 10.1111/j.1469-8137.1990.tb00476.x – volume: 266 start-page: 231 year: 2017 ident: B34 article-title: Quantitative x-ray microanalysis of model biological samples in the SEM using remote standards and the XPP analytical model. publication-title: J. Microsc. doi: 10.1111/jmi.12531 – volume: 265 start-page: 81 year: 2017 ident: B27 article-title: Preserving elemental content in adherent mammalian cells for analysis by synchrotron-based X-ray fluorescence microscopy. publication-title: J. Microsc. doi: 10.1111/jmi.12466 – volume: 190 start-page: 305 year: 1998 ident: B37 article-title: Quantitative elemental X-ray imaging of frozen-hydrated biological samples. publication-title: J. Microsc. doi: 10.1046/j.1365-2818.1998.00313.x – volume: 7 start-page: 574 year: 2011 ident: B2 article-title: The dawn of symbiosis between plants and fungi. publication-title: Biol. Lett. doi: 10.1098/rsbl.2010.1203 – year: 2018 ident: B17 article-title: Energy dispersive X-ray spectrometry: physical principles and user-selected parameters publication-title: Scanning Electron Microscopy and X-Ray Microanalysis – volume: 8 start-page: 245 year: 2017 ident: B10 article-title: Multigene phylogeny of Endogonales, an early diverging lineage of fungi associated with plants publication-title: IMA Fungus doi: 10.5598/imafungus.2017.08.02.03 – volume: 37 start-page: 1011 year: 2010 ident: B40 article-title: Cryo-scanning electron microscopy (CSEM) in the advancement of functional plant biology: energy dispersive X-ray microanalysis (CEDX) applications. publication-title: Funct. Plant Biol. doi: 10.1071/FP10095 – volume: 447 start-page: 9 year: 2020 ident: B9 article-title: Effects of pH and bicarbonate on the nutrient status and growth of three Lupinus species. publication-title: Plant Soil doi: 10.1007/s11104-019-03980-8 – volume: 223 start-page: 908 year: 2019 ident: B12 article-title: Functional complementarity of ancient plant–fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts. publication-title: New Phytol. doi: 10.1111/nph.15819 – volume: 22 start-page: 64 year: 1976 ident: B31 article-title: Electron-microscopy of vesicular-arbuscular mycorrhizae of yellow poplar. 4. Host-endophyte interactions during arbuscular deterioration. publication-title: Can. J. Microbiol. doi: 10.1139/m76-009 – volume: 412 start-page: 35 ident: B47 article-title: Sample storage conditions alter colonisation structures of arbuscular mycorrhizal fungi and, particularly, fine root endophyte. publication-title: Plant Soil doi: 10.1007/s11104-016-2867-4 – volume: 88 start-page: 633 year: 1981 ident: B16 article-title: Ultrastructural and ultracytochemical features of a Glomus tenuis mycorrhiza. publication-title: New Phytol. doi: 10.1111/j.1469-8137.1981.tb01739.x – volume: 56 start-page: 68 year: 2005 ident: B60 article-title: A simple blue staining technique for arbuscular mycorrhizal and other root-inhabiting fungi. publication-title: Inoculum – volume: 73 start-page: 901 year: 1974 ident: B6 article-title: Ultrastructure of host-fungus interface in a vesicular-arbuscular mycorrhiza. publication-title: New Phytol. doi: 10.1111/j.1469-8137.1974.tb01319.x – volume: 70 start-page: 4991 year: 2019 ident: B32 article-title: Salinity tolerance in chickpea is associated with the ability to ‘exclude’ Na from leaf mesophyll cells. publication-title: J. Exp. Bot. doi: 10.1093/jxb/erz241 – year: 2000 ident: B50 publication-title: Mixed-Effects Models in S and S-PLUS. doi: 10.1007/978-1-4419-0318-1 – volume: 30 start-page: 485 year: 1982 ident: B1 article-title: Comparative anatomy of vesicular-arbuscular mycorrhizas formed on subterranean clover. publication-title: Aust. J. Bot. doi: 10.1071/BT9820485 – volume: 64 start-page: 5004 year: 1998 ident: B59 article-title: Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. publication-title: Appl. Environ. Microbiol. doi: 10.1128/aem.64.12.5004-5007.1998 – volume: 13 start-page: 581 year: 2016 ident: B5 article-title: DADA2: high resolution sample inference from amplicon data. publication-title: Nat. Methods doi: 10.1038/nmeth.3869 – volume: 16 year: 2019 ident: B44 article-title: Zinc and cadmium mapping in the apical shoot and hypocotyl tissues of radish by high-resolution secondary ion mass spectrometry (NanoSIMS) after short-term exposure to metal contamination. publication-title: Int. J. Environ. Res. Public Health doi: 10.3390/ijerph16030373 – volume: 51 start-page: 801 year: 2015 ident: B100 article-title: Growth and nutritional responses to arbuscular mycorrhizal fungi are dependent on onion genotype and fungal species. publication-title: Biol. Fertil. Soils doi: 10.1007/s00374-015-1027-y – year: 2009 ident: B67 publication-title: Mixed Effects Models and Extensions in Ecology With R. doi: 10.1007/978-0-387-87458-6 – volume: 63 start-page: 691 year: 2012 ident: B43 article-title: Temperate pasture legumes in Australia—their history, current use, and future prospects. publication-title: Crop Past. Sci. doi: 10.1071/CP12194 – volume: 41 start-page: D590 year: 2013 ident: B51 article-title: The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. publication-title: Nucleic Acids Res. doi: 10.1093/nar/gks1219 – volume: 212 start-page: 2977 year: 2009 ident: B35 article-title: X-ray microanalysis of Rb+ entry into cricket Malpighian tubule cells via putative K+ channels. publication-title: J. Exp. Biol. doi: 10.1242/jeb.032177 – volume: 5 year: 2014 ident: B15 article-title: The role of mycorrhizal associations in plant potassium nutrition. publication-title: Front. Plant Sci. doi: 10.3389/fpls.2014.00337 – volume: 1 start-page: 389 year: 1963 ident: B18 article-title: The mycorrhizal endophytes of Griselinia littoralis (Cornaceae). publication-title: New Zeal. J. Bot. doi: 10.1080/0028825X.1963.10428694 – volume: 160 start-page: 429 year: 2003 ident: B53 article-title: Location and quantification of phosphorus and other elements in fully hydrated, soil-grown arbuscular mycorrhizas: a cryo-analytical scanning electron microscopy study. publication-title: New Phytol. doi: 10.1046/j.1469-8137.2003.00884.x – year: 2016 ident: B64 publication-title: ggplot2: Elegant Graphics for Data Analysis. doi: 10.1007/978-3-319-24277-4 – volume: 21 start-page: 631 year: 2011 ident: B66 article-title: Specific arbuscular mycorrhizal fungi associated with non-photosynthetic Petrosavia sakuraii (Petrosaviaceae). publication-title: Mycorrhiza doi: 10.1007/s00572-011-0373-3 – volume: 92 start-page: 28 year: 1989 ident: B41 article-title: Variation in propagule numbers of vesicular-arbuscular mycorrhizal fungi in a semi-arid soil. publication-title: Mycol. Res. doi: 10.1016/S0953-7562(89)80092-9 – volume: 108 start-page: 1028 year: 2016 ident: B57 article-title: A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. publication-title: Mycologia doi: 10.3852/16-042 – volume: 6 year: 2018 ident: B3 article-title: QIIME 2: reproducible, interactive, scalable, and extensible microbiome data science. publication-title: PeerJ Prepr. doi: 10.7287/peerj.preprints.27295v2 – volume: 10 start-page: 1514 year: 2016 ident: B14 article-title: Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline. publication-title: ISME J. doi: 10.1038/ismej.2015.204 – volume: 218 start-page: 959 year: 2018 ident: B19 article-title: Eudicots from severely phosphorus-impoverished environments preferentially allocate phosphorus to their mesophyll. publication-title: New Phytol. doi: 10.1111/nph.15043 – volume: 8 year: 2018 ident: B11 article-title: Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification. publication-title: Sci. Rep. doi: 10.1038/s41598-018-28920-x – volume: 403 start-page: 305 ident: B48 article-title: The response of fine root endophyte (Glomus tenue) to waterlogging is dependent on host plant species and soil type. publication-title: Plant Soil doi: 10.1007/s11104-016-2804-6 – volume: 36 start-page: 97 year: 2009 ident: B39 article-title: Cryo-scanning electron microscopy (CSEM) in the advancement of functional plant biology. publication-title: Funct. Plant Biol. doi: 10.1071/FP08304 – year: 2008 ident: B56 publication-title: Mycorrhizal Symbiosis – volume: 41 start-page: 605 year: 2018 ident: B22 article-title: Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: an adaptation improving phosphorus-use efficiency. publication-title: Plant Cell Environ. doi: 10.1111/pce.13124 – volume: 103 start-page: 1369 year: 1999 ident: B58 article-title: Morphology and infectivity of fine endophyte in a Mediterranean environment. publication-title: Mycol. Res. doi: 10.1017/S0953756299001094 – volume: 177 start-page: 14 year: 2014 ident: B65 article-title: Effects of low magnesium and an arbuscular mycorrhizal fungus on the growth, magnesium distribution and photosynthesis of two citrus cultivars. publication-title: Scientia Horticult. doi: 10.1016/j.scienta.2014.07.016 – volume: 205 start-page: 743 year: 2015 ident: B13 article-title: First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2. publication-title: New Phytol. doi: 10.1111/nph.13024 – volume: 28 start-page: 67 year: 1994 ident: B25 article-title: Planing frozen hydrated plant specimens for SEM observation and EDX microanalysis. publication-title: Microsc. Res. Tech. doi: 10.1002/jemt.1070280108 – volume: 21 start-page: 1768 ident: B29 article-title: Electron-microscopy of vesicular-arbuscular mycorrhizae of yellow poplar. 2. Intracellular hyphae and vesicles. publication-title: Can. J. Microbiol. doi: 10.1139/m75-258 – volume: 44 start-page: 587 year: 1993 ident: B33 article-title: Subcellular distribution of inorganic phosphate, and levels of nucleoside triphosphate, in mature maize roots at low external phosphate concentrations: measurements with 31P-NMR. publication-title: J. Exp. Bot. doi: 10.1093/jxb/44.3.587 – volume: 17 start-page: 55 year: 1979 ident: B62 article-title: Vesicular-arbuscular mycorrhizas in white clover – scanning electron-microscope and X-ray microanalytical study. publication-title: New Zeal. J. Bot. doi: 10.1080/0028825X.1979.10425160 – volume: 68 start-page: 341 year: 1977 ident: B20 article-title: Species and mycorrhizal infections of New Zealand Endogonaceae. publication-title: Trans. Brit. Mycol. Soc. doi: 10.1016/S0007-1536(77)80186-1 – volume: 17 start-page: 10 year: 2011 ident: B38 article-title: Cutadapt removes adapter sequences from high-throughput sequencing reads. publication-title: EMBnet J. doi: 10.14806/ej.17.1.200 – volume: 213 start-page: 481 ident: B45 article-title: Fine endophytes (Glomus tenue) are related to Mucoromycotina not Glomeromycota. publication-title: New Phytol. doi: 10.1111/nph.14268 – year: 1996 ident: B4 publication-title: Working With Mycorrhizas in Forestry and Agriculture. – year: 2016 ident: B52 publication-title: R: A Language and Environment for Statistical Computing. – volume: 245 start-page: 17 year: 2012 ident: B36 article-title: Sequential quantitative X-ray elemental imaging of frozen-hydrated and freeze-dried biological bulk samples in the SEM. publication-title: J. Microsc. doi: 10.1111/j.1365-2818.2011.03539.x – year: 2016 ident: B49 publication-title: nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3.1–128. – volume: 21 start-page: 1930 ident: B30 article-title: Electron-microscopy of vesicular-arbuscular mycorrhizae of yellow poplar. 3. Host-endophyte interactions during arbuscular development. publication-title: Can. J. Microbiol. doi: 10.1139/m75-280 – volume: 34 start-page: 457 year: 2007 ident: B54 article-title: Relative amounts of soluble and insoluble forms of phosphorus and other elements in intraradical hyphae and arbuscules of arbuscular mycorrhizas. publication-title: Funct. Plant Biol. doi: 10.1071/FP06242 – volume: 27 start-page: 619 ident: B46 article-title: Fine root endophytes under scrutiny: a review of the literature on arbuscule-producing fungi recently suggested to belong to the Mucoromycotina. publication-title: Mycorrhiza doi: 10.1007/s00572-017-0782-z – volume: 72 start-page: 965 year: 1973 ident: B7 article-title: The effect of Rhizophagus tenuis mycorrhizas on ryegrass, cocksfoot and sweet vernal. publication-title: New Phytol. doi: 10.1111/j.1469-8137.1973.tb02073.x – volume: 220 start-page: 243 year: 2000 ident: B26 article-title: The mycorrhizal fungus Paxillus involutus transports magnesium to Norway spruce seedlings. Evidence from stable isotope labeling. publication-title: Plant and Soil doi: 10.1023/A:1004727331860 – volume: 21 start-page: 989 ident: B28 article-title: Electron-microscopy of vesicular-arbuscular mycorrhizae of yellow poplar. 1. Characterization of endophytic structures by scanning electron stereoscopy. publication-title: Can. J. Microbiol. doi: 10.1139/m75-146 – volume: 88 start-page: 967 year: 2001 ident: B63 article-title: Chloride in soils and its uptake and movement within the plant: a review. publication-title: Ann. Bot. doi: 10.1006/anbo.2001.1540 |
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Snippet | Arbuscule-producing fine root endophytes (FRE) (previously incorrectly
) were recently placed within subphylum Mucoromycotina; the first report of arbuscules... Arbuscule-producing fine root endophytes (FRE) (previously incorrectly Glomus tenue) were recently placed within subphylum Mucoromycotina; the first report of... AimsArbuscule-producing fine root endophytes (FRE) (previously incorrectly Glomus tenue) were recently placed within subphylum Mucoromycotina; the first report... |
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Title | First Cryo-Scanning Electron Microscopy Images and X-Ray Microanalyses of Mucoromycotinian Fine Root Endophytes in Vascular Plants |
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