Physiological characterisation of coprophilous fungal isolates that behave as plant root associates
Victoria Miranda
A E , José Martin Scervino B , Johana Barros A , María Alejandra Rodríguez C and Sebastián Fracchia A D
+ Author Affiliations
- Author Affiliations
A Centro Regional de Investigaciones Científicas y Transferencia Tecnológica de La Rioja (CRILAR-CONICET, Provincia de La Rioja, UNLAR, SEGEMAR, UNCa), Entre Ríos y Mendoza s/n, 5301, Anillaco La Rioja, Argentina.
B Departamento de Botánica INIBIOMA (CONICET-UNC), Quintral 1250, 8400, San Carlos de Bariloche, Río Negro, Argentina.
C Laboratorio de Microbiología del Suelo, Departamento de Biodiversidad y Biología Experimental,Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IBBEA, CONICET, Argentina.
D Universidad Nacional de Chilecito, Chilecito, La Rioja, Argentina.
E Corresponding author. Email: victoriamiranda16@hotmail.com
Soil Research 58(8) 748-758 https://doi.org/10.1071/SR20141
Submitted: 19 May 2020 Accepted: 14 August 2020 Published: 18 September 2020
Abstract
Different fungal isolates closely related to Zopfiella erostrata and Cercophora caudata have been found to colonise plant root tissues in an asymptomatic way in the Monte Desert biome of La Rioja Province, Argentina. This interaction has been newly discovered, and the role of these fungi in their desert habitat has never been studied in detail. The objective of this study was to evaluate eight fungal isolates by means of specific physiological traits that could have implications for their interaction with the host plant. The selected isolates, four endophytic and four rhizospheric, were characterised for their ability to produce indole acetic acid, solubilise and mineralise phosphorus (P), and utilise different nitrogen sources. In addition, we evaluated organic acid production and phosphatase activities as mechanisms of P recycling. These analyses revealed that most isolates produced indole acetic acid, and that all isolates could solubilise and mineralise P, although to different degrees. Furthermore, the production of organic acids correlated with P solubilisation levels, which may enhance P availability in soils. Nitrogen utilisation was variable among the isolates, without specific patterns concerning the different sources and fungal isolates tested. Our results demonstrated that the fungal isolates had great variability, probably because they complete their teleomorphic phase in their habitats, generating viable meiotic spores, in addition to the active dispersion of these fungi by the underground rodent Ctenomys aff. knightii from which they were isolated. Although the isolates were variable, the endophytic isolates exhibited improvement in all the P parameters measured. This can be explained by the ability of these isolates to intimately colonise root tissues, while the colonisation by rhizospheric isolates is produced superficially in the rhizoplane. The high occurrence of this interaction, as well as the physiological traits detected, suggest that this kind of fungi could play an important ecological role in the Monte Desert environment, benefiting the establishment and growth of new seedlings in areas occupied by the rodents.
Keywords: coprophilous fungi, desert ecosystem, endophytes, indole, phosphorus solubilisation, rhizosphere.
References
Acevedo E, Galindo-Castaneda T, Prada F, Navia M, Romero HM (2014) Phosphate-solubilizing microorganisms associated with the rhizosphere of oil palm (Elaeis guineensis Jacq.) in Colombia. Applied Soil Ecology 80, 26–33.| Phosphate-solubilizing microorganisms associated with the rhizosphere of oil palm (Elaeis guineensis Jacq.) in Colombia.Crossref | GoogleScholarGoogle Scholar |
Alberton O, Kuyper TW, Summerbell RC (2010) Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant and Soil 328, 459–470.
| Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency.Crossref | GoogleScholarGoogle Scholar |
Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141, 221–235.
| Water pulses and biogeochemical cycles in arid and semiarid ecosystems.Crossref | GoogleScholarGoogle Scholar | 14986096PubMed |
Barrow J, Aaltonen R (2001) Evaluation of the internal colonization of Atriplex canescens (Pursh) Nutt. roots by dark septate fungi and the influence of host physiological activity. Mycorrhiza 11, 199–205.
| Evaluation of the internal colonization of Atriplex canescens (Pursh) Nutt. roots by dark septate fungi and the influence of host physiological activity.Crossref | GoogleScholarGoogle Scholar |
Barrow JR, Osuna P (2002) Phosphorus solubilization and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt. Journal of Arid Environments 51, 449–459.
| Phosphorus solubilization and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt.Crossref | GoogleScholarGoogle Scholar |
Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Applied Microbiology and Biotechnology 84, 11–18.
| Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture.Crossref | GoogleScholarGoogle Scholar | 19568745PubMed |
Berman T, Wynne D, Kaplan B (1990) Phosphatases revisited: analysis of particle-associated enzyme activities in aquatic systems. Hydrobiologia 207, 287–294.
| Phosphatases revisited: analysis of particle-associated enzyme activities in aquatic systems.Crossref | GoogleScholarGoogle Scholar |
Berthelot C, Leyval C, Foulon J, Chalot M, Blaudez D (2016) Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiology Ecology 92, fiw144
| Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites.Crossref | GoogleScholarGoogle Scholar | 27364359PubMed |
Della Monica IF, Saparrat MCN, Godeas AM, Scervino JM (2015) The co-existence between DSE and AMF symbionts affects plant P pools through P mineralization and solubilization processes. Fungal Ecology 17, 10–17.
| The co-existence between DSE and AMF symbionts affects plant P pools through P mineralization and solubilization processes.Crossref | GoogleScholarGoogle Scholar |
Dewan MM, Ghisalbertib EL, Rowland C, Sivasithamparam K (1994) Reduction of symptoms of take-all of wheat and rye-grass seedlings by the soil-borne fungus Sordaria fimicola. Applied Soil Ecology 1, 45–51.
| Reduction of symptoms of take-all of wheat and rye-grass seedlings by the soil-borne fungus Sordaria fimicola.Crossref | GoogleScholarGoogle Scholar |
Di Rienzo JA, Casanoves F, Balzarini M, Gonzalez L, Tablada M, Robledo C (2013) Infostat - Sofware estadístico. Universidad Nacional de Córdoba, Argentina. Available at http://www.infostat.com.ar/ [verified 3 September 2020].
Ehmann A (1977) The van URK-Salkowski reagent - a sensitive and specific chromogenic reagent for silica gel thin-layer chromatographic detection and identification of indole derivatives. Journal of Chromatography. A 132, 267–276.
| The van URK-Salkowski reagent - a sensitive and specific chromogenic reagent for silica gel thin-layer chromatographic detection and identification of indole derivatives.Crossref | GoogleScholarGoogle Scholar |
Fracchia S, Krapovickas L, Aranda-Rickert A, Valentinuzzi VS (2011) Dispersal of arbuscular mycorrhizal fungi and dark septate endophytes by Ctenomys cf. knighti (Rodentia) in the northern Monte Desert of Argentina. Journal of Arid Environments 75, 1016–1023.
| Dispersal of arbuscular mycorrhizal fungi and dark septate endophytes by Ctenomys cf. knighti (Rodentia) in the northern Monte Desert of Argentina.Crossref | GoogleScholarGoogle Scholar |
Fuentes-Ramirez LE, Jimenez-Salgado T, Abarca-Ocampo IR, Caballero-Mellado J (1993) Acetobacter diazotrophicus, an indoleacetic acid producing bacterium isolated from sugarcane cultivars of México. Plant and Soil 154, 145–150.
| Acetobacter diazotrophicus, an indoleacetic acid producing bacterium isolated from sugarcane cultivars of México.Crossref | GoogleScholarGoogle Scholar |
Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiology 26, 192–195.
| Colorimetric estimation of indoleacetic acid.Crossref | GoogleScholarGoogle Scholar | 16654351PubMed |
Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews 79, 293–320.
| The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes.Crossref | GoogleScholarGoogle Scholar | 26136581PubMed |
Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6, 58
| Microbial interactions within the plant holobiont.Crossref | GoogleScholarGoogle Scholar | 29587885PubMed |
Herrera J, Poudel R, Bokati D (2013) Assessment of root-associated fungal communities colonizing two species of tropical grasses reveals incongruence to fungal communities of North American native grasses. Fungal Ecology 6, 65–69.
| Assessment of root-associated fungal communities colonizing two species of tropical grasses reveals incongruence to fungal communities of North American native grasses.Crossref | GoogleScholarGoogle Scholar |
Hirose D, Matsuoka S, Osono T (2013) Assessment of the fungal diversity and succession of ligninolytic endophytes in Camellia japonica leaves using clone library analysis. Mycologia 105, 837–843.
| Assessment of the fungal diversity and succession of ligninolytic endophytes in Camellia japonica leaves using clone library analysis.Crossref | GoogleScholarGoogle Scholar | 23709486PubMed |
Huxman TE, Snyder KA, Tissue D, Leffler AJ, Ogle K, Pockman WT, Sandquist DR, Potts DL, Schwinning S (2004) Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141, 254–268.
| Precipitation pulses and carbon fluxes in semiarid and arid ecosystems.Crossref | GoogleScholarGoogle Scholar | 15338414PubMed |
Huygens D, Díaz S, Urcelay C, Boeckx P (2016) Microbial recycling of dissolved organic matter confines plant nitrogen uptake to inorganic forms in a semi-arid ecosystem. Soil Biology & Biochemistry 101, 142–151.
| Microbial recycling of dissolved organic matter confines plant nitrogen uptake to inorganic forms in a semi-arid ecosystem.Crossref | GoogleScholarGoogle Scholar |
Illmer P, Schinner F (1995) Solubilization of inorganic calcium phosphates—solubilization mechanisms. Soil Biology & Biochemistry 27, 257–263.
| Solubilization of inorganic calcium phosphates—solubilization mechanisms.Crossref | GoogleScholarGoogle Scholar |
Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytologist 140, 295–310.
| Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi.Crossref | GoogleScholarGoogle Scholar |
Kariman K, Barker SJ, Jost R, Finnegan PM, Tibbett M (2012) Dual mycorrhizal associations of jarrah (Eucalyptus marginata) in a nurse-pot system. Australian Journal of Botany 60, 661–668.
| Dual mycorrhizal associations of jarrah (Eucalyptus marginata) in a nurse-pot system.Crossref | GoogleScholarGoogle Scholar |
Kariman K, Barker SJ, Jost R, Finnegan PM, Tibbett M (2014) A novel plant-fungus symbiosis benefits the host without forming mycorrhizal structures. New Phytologist 201, 1413–1422.
| A novel plant-fungus symbiosis benefits the host without forming mycorrhizal structures.Crossref | GoogleScholarGoogle Scholar | 24279681PubMed |
Khan AL, Hamayun M, Kang S-M, Kim Y-H, Jung H-Y, Lee J-H, Lee I-J (2012) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiology 12, 3
| Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10.Crossref | GoogleScholarGoogle Scholar | 22235902PubMed |
Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biology & Biochemistry 43, 2294–2303.
| Global diversity and distribution of arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Knapp DG, Kovács GM, Zajta E, Groenewald JZ, Crous PW (2015) Dark septate endophytic pleosporalean genera from semiarid areas. Persoonia 35, 87–100.
| Dark septate endophytic pleosporalean genera from semiarid areas.Crossref | GoogleScholarGoogle Scholar | 26823630PubMed |
Lahlali R, McGregor L, Song T, Gossen BD, Narisawa K, Peng G (2014) Heteroconium chaetospira induces resistance to clubroot via upregulation of host genes involved in jasmonic acid, ethylene, and auxin biosynthesis. PLoS One 9, e94144
| Heteroconium chaetospira induces resistance to clubroot via upregulation of host genes involved in jasmonic acid, ethylene, and auxin biosynthesis.Crossref | GoogleScholarGoogle Scholar | 24714177PubMed |
Mahmoud RS, Narisawa K (2013) A new fungal endophyte, Scolecobasidium humicola, promotes tomato growth under organic nitrogen. PLoS One 8, e78746
| A new fungal endophyte, Scolecobasidium humicola, promotes tomato growth under organic nitrogen.Crossref | GoogleScholarGoogle Scholar | 24223848PubMed |
Mandyam K, Loughin T, Jumpponen A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102, 813–821.
| Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie.Crossref | GoogleScholarGoogle Scholar | 20648749PubMed |
Mayerhofer MS, Kernaghan G, Harper KA (2013) The effects of fungal root endophytes on plant growth: A meta-analysis. Mycorrhiza 23, 119–128.
| The effects of fungal root endophytes on plant growth: A meta-analysis.Crossref | GoogleScholarGoogle Scholar | 22983627PubMed |
Miranda V, Rothen C, Yela N, Aranda-Rickert A, Barros J, Calcagno J, Fracchia S (2019) Subterranean desert rodents (Genus Ctenomys) create soil patches enriched in root endophytic fungal propagules. Microbial Ecology 77, 451–459.
| Subterranean desert rodents (Genus Ctenomys) create soil patches enriched in root endophytic fungal propagules.Crossref | GoogleScholarGoogle Scholar | 30003276PubMed |
Miranda V, Sede S, Aranda-Rickert A, Rothen C, Scervino JM, Barros J, Fracchia S (2020) Taxonomy, life cycle and endophytism of coprophilous fungi from an underground desert rodent. Fungal Ecology 43,
| Taxonomy, life cycle and endophytism of coprophilous fungi from an underground desert rodent.Crossref | GoogleScholarGoogle Scholar |
Nahas E, Centurion JF, Assis LC (1994) Microrganismos solubilizadores de fosfato e produtores de fosfatases de vários solos. Revista Brasileira de Ciência do Solo 18, 43–48.
Naik SK, Maurya S, Kumar R, Sadhna K, Gagrai S, Das B, Kumar S, Bhatt BP (2013) Inorganic phosphate solubilization by phosphate solubilizing fungi isolated from acidic soils. African Journal of Microbiological Research 7, 4310–4316.
Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiology Letters 170, 265–270.
| An efficient microbiological growth medium for screening phosphate solubilizing microorganisms.Crossref | GoogleScholarGoogle Scholar | 9919677PubMed |
Pandey A, Das N, Kumar B, Rinu K, Trivedi P (2008) Phosphate solubilization by Penicillium spp. isolated from soil samples of Indian Himalayan region. World Journal of Microbiology & Biotechnology 24, 97–102.
| Phosphate solubilization by Penicillium spp. isolated from soil samples of Indian Himalayan region.Crossref | GoogleScholarGoogle Scholar |
Pawar VC, Thaker VS (2009) Acid phosphatase and invertase activities of Aspergillus niger. Mycoscience 50, 323–330.
| Acid phosphatase and invertase activities of Aspergillus niger.Crossref | GoogleScholarGoogle Scholar |
Peterson RL, Wagg C, Pautler M (2008) Associations between microfungal endophytes and roots: do structural features indicate function? Botany 86, 445–456.
| Associations between microfungal endophytes and roots: do structural features indicate function?Crossref | GoogleScholarGoogle Scholar |
Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annual Review of Phytopathology 49, 291–315.
| Hidden fungi, emergent properties: endophytes and microbiomes.Crossref | GoogleScholarGoogle Scholar | 19400639PubMed |
Porras-Alfaro A, Herrera J, Sinsabaugh RL, Odenbach KJ, Lowrey T, Natvig DO (2008) Novel root fungal consortium associated with a dominant desert grass. Applied and Environmental Microbiology 74, 2805–2813.
| Novel root fungal consortium associated with a dominant desert grass.Crossref | GoogleScholarGoogle Scholar | 18344349PubMed |
Priyadharsini P, Muthukumar T (2017) The root endophytic fungus Curvularia geniculata from Parthenium hysterophorus roots improves plant growth through phosphate solubilization and phytohormone production. Fungal Ecology 27, 69–77.
| The root endophytic fungus Curvularia geniculata from Parthenium hysterophorus roots improves plant growth through phosphate solubilization and phytohormone production.Crossref | GoogleScholarGoogle Scholar |
Qin Y, Pan X, Kubicek C, Druzhinina I, Chenthamara K, Labbé J, Yuan Z (2017) Diverse plant-associated pleosporalean fungi from saline areas: ecological tolerance and nitrogen-status dependent effects on plant growth. Frontiers in Microbiology 8, 1–14.
| Diverse plant-associated pleosporalean fungi from saline areas: ecological tolerance and nitrogen-status dependent effects on plant growth.Crossref | GoogleScholarGoogle Scholar |
Radhakrishnan R, Khan AL, Kang SM, Lee IJ (2015) A comparative study of phosphate solubilization and the host plant growth promotion ability of Fusarium verticillioides RK01 and Humicola sp. KNU01 under salt stress. Annals of Microbiology 65, 585–593.
| A comparative study of phosphate solubilization and the host plant growth promotion ability of Fusarium verticillioides RK01 and Humicola sp. KNU01 under salt stress.Crossref | GoogleScholarGoogle Scholar |
Rashid M, Khalil S, Ayub N, Alam S, Latif F (2004) Organic acids production and phosphate solubilization by phosphate solubilizing microorganisms (PSM) under in vitro conditions. Pakistan Journal of Biological Sciences 7, 187–196.
| Organic acids production and phosphate solubilization by phosphate solubilizing microorganisms (PSM) under in vitro conditions.Crossref | GoogleScholarGoogle Scholar |
Redman RS, Dunigan DD, Rodriguez RJ, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytologist 151, 705–716.
| Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader?Crossref | GoogleScholarGoogle Scholar |
Richardson AE, Hadobas PA, Hayes JE (2000) Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture. Plant, Cell & Environment 23, 397–405.
| Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture.Crossref | GoogleScholarGoogle Scholar |
Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytologist 182, 314–330.
| Fungal endophytes: diversity and functional roles.Crossref | GoogleScholarGoogle Scholar | 19236579PubMed |
Rosling A, Lindahl BD, Taylor AFS, Finlay RD (2004) Mycelial growth and substrate acidification of ectomycorrhizal fungi in response to different minerals. FEMS Microbiology Ecology 47, 31–37.
| Mycelial growth and substrate acidification of ectomycorrhizal fungi in response to different minerals.Crossref | GoogleScholarGoogle Scholar | 19712344PubMed |
Rothen C, Miranda V, Fracchia S, Godeas A, Rodríguez A (2018) Microdochium bolleyi (Ascomycota: xylariales): physiological characterization and structural features of its association with wheat. Boletín de la Sociedad Argentina de Botánica 53, 169–182.
| Microdochium bolleyi (Ascomycota: xylariales): physiological characterization and structural features of its association with wheat.Crossref | GoogleScholarGoogle Scholar |
Rudgers JA, Koslow JM, Clay K (2004) Endophytic fungi alter relationships between diversity and ecosystem properties. Ecology Letters 7, 42–51.
| Endophytic fungi alter relationships between diversity and ecosystem properties.Crossref | GoogleScholarGoogle Scholar |
Scervino JM, Mesa MP, Della Mónica I, Recchi M, Moreno NS, Godeas A (2010) Soil fungal isolates produce different organic acid patterns involved in phosphate salts solubilization. Biology and fertility of soils 46, 755–763.
| Soil fungal isolates produce different organic acid patterns involved in phosphate salts solubilization.Crossref | GoogleScholarGoogle Scholar |
Scervino JM, Papinutti VL, Godoy MS, Rodriguez MA, Della Monica I, Recchi M, Pettinari MJ, Godeas AM (2011) Medium pH, carbon and nitrogen concentrations modulate the phosphate solubilization efficiency of Penicillium purpurogenum through organic acid production. Journal of Applied Microbiology 110, 1215–1223.
| Medium pH, carbon and nitrogen concentrations modulate the phosphate solubilization efficiency of Penicillium purpurogenum through organic acid production.Crossref | GoogleScholarGoogle Scholar | 21324053PubMed |
Schlaeppi K, Bulgarelli D (2015) The plant microbiome at work. Molecular Plant-Microbe Interactions 28, 212–217.
| The plant microbiome at work.Crossref | GoogleScholarGoogle Scholar | 25514681PubMed |
Sirrenberg A, Göbel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, Santos P, Feussner I, Pawlowski K (2007) Piriformospora indica affects plant growth by auxin production. Physiologia Plantarum 131, 581–589.
| Piriformospora indica affects plant growth by auxin production.Crossref | GoogleScholarGoogle Scholar | 18251849PubMed |
Šnajdr J, Cajthaml T, Valášková V, Merhautová V, Petránková M, Spetz P, Leppänen K, Baldrian P (2011) Transformation of Quercus petraea litter: Successive changes in litter chemistry are reflected in differential enzyme activity and changes in the microbial community composition. FEMS Microbiology Ecology 75, 291–303.
| Transformation of Quercus petraea litter: Successive changes in litter chemistry are reflected in differential enzyme activity and changes in the microbial community composition.Crossref | GoogleScholarGoogle Scholar | 21114504PubMed |
Surono , Narisawa K (2017) The dark septate endophytic fungus Phialocephala fortinii is a potential decomposer of soil organic compounds and a promoter of Asparagus officinalis growth. Fungal Ecology 28, 1–10.
| The dark septate endophytic fungus Phialocephala fortinii is a potential decomposer of soil organic compounds and a promoter of Asparagus officinalis growth.Crossref | GoogleScholarGoogle Scholar |
Tanney JB, Douglas B, Seifert KA (2016) Sexual and asexual states of some endophytic Phialocephala species of Picea. Mycologia 108, 255–280.
| Sexual and asexual states of some endophytic Phialocephala species of Picea.Crossref | GoogleScholarGoogle Scholar | 26740545PubMed |
Titus JH, Tsuyuzaki S (2003) Distribution of plants in relation to microsites on recent volcanic substrates on Mount Koma, Hokkaido, Japan. Mycorrhiza 18, 91–98.
| Distribution of plants in relation to microsites on recent volcanic substrates on Mount Koma, Hokkaido, Japan.Crossref | GoogleScholarGoogle Scholar |
Upson R, Read DJ, Newsham KK (2009) Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza 20, 1–11.
| Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes.Crossref | GoogleScholarGoogle Scholar | 19495811PubMed |
Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99, 175–184.
| A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage.Crossref | GoogleScholarGoogle Scholar | 17682770PubMed |
Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytologist 206, 1196–1206.
| The importance of the microbiome of the plant holobiont.Crossref | GoogleScholarGoogle Scholar | 25655016PubMed |
Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P-solubilizing and biocontrol activity of microorganisms: Potentials and future trends. Applied Microbiology and Biotechnology 71, 137–144.
| Simultaneous P-solubilizing and biocontrol activity of microorganisms: Potentials and future trends.Crossref | GoogleScholarGoogle Scholar | 16544140PubMed |
Vergara C, Araujo KEC, Urquiaga S, Schultz N, Balieiro F de C, Medeiros PS, Santos LA, Xavier GR, Zilli JE (2017) Dark septate endophytic fungi help tomato to acquire nutrients from ground plant material. Frontiers in Microbiology 8, 2437
| Dark septate endophytic fungi help tomato to acquire nutrients from ground plant material.Crossref | GoogleScholarGoogle Scholar | 29312163PubMed |
Vyas P, Gulati A (2009) Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiology 9, 174
| Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas.Crossref | GoogleScholarGoogle Scholar | 19698133PubMed |
Waqas M, Khan AL, Kamran M, Hamayun M, Kang S, Kim Y, Lee I (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules (Basel, Switzerland) 17, 10754–10773.
| Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress.Crossref | GoogleScholarGoogle Scholar |
Whitelaw MA, Harden TJ, Helyar KR (1999) Phosphate solubilisation in solution culture by the soil fungus Penicillium radicum. Soil Biology & Biochemistry 31, 655–665.
| Phosphate solubilisation in solution culture by the soil fungus Penicillium radicum.Crossref | GoogleScholarGoogle Scholar |
Yakti W, Kovács GM, Vági P, Franken P (2018) Impact of dark septate endophytes on tomato growth and nutrient uptake. Plant Ecology & Diversity 11, 637–648.
| Impact of dark septate endophytes on tomato growth and nutrient uptake.Crossref | GoogleScholarGoogle Scholar |
Yamanaka T (1999) Utilization of inorganic and organic nitrogen in pure cultures by saprotrophic and ectomycorrhizal fungi producing sporophores on urea-treated forest floor. Mycological Research 103, 811–816.
| Utilization of inorganic and organic nitrogen in pure cultures by saprotrophic and ectomycorrhizal fungi producing sporophores on urea-treated forest floor.Crossref | GoogleScholarGoogle Scholar |
Yin Z, Shi F, Jiang H, Roberts DP, Chen S, Fan B (2015) Phosphate solubilization and promotion of maize growth by Penicillium oxalicum P4 and Aspergillus niger P85 in a calcareous soil. Canadian Journal of Microbiology 61, 913–923.
| Phosphate solubilization and promotion of maize growth by Penicillium oxalicum P4 and Aspergillus niger P85 in a calcareous soil.Crossref | GoogleScholarGoogle Scholar | 26469739PubMed |
Yonezawa M, Usuki F, Narisawa K (2004) Anatomical study on the interaction between the root endophytic fungus Heteroconium chaetospira and Chinese cabbage. Mycoscience 45, 367–371.
| Anatomical study on the interaction between the root endophytic fungus Heteroconium chaetospira and Chinese cabbage.Crossref | GoogleScholarGoogle Scholar |
Zhao L, Zhang Y (2015) Effects of phosphate solubilization and phytohormone production of Trichoderma asperellum Q1 on promoting cucumber growth under salt stress. Journal of Integrative Agriculture 14, 1588–1597.
| Effects of phosphate solubilization and phytohormone production of Trichoderma asperellum Q1 on promoting cucumber growth under salt stress.Crossref | GoogleScholarGoogle Scholar |
Zheng Y-K, Qiao X-G, Miao C-P, Liu K, Chen Y-W, Xu L-H, Zhao L-X (2016) Diversity, distribution and biotechnological potential of endophytic fungi. Annals of Microbiology 66, 529–542.
| Diversity, distribution and biotechnological potential of endophytic fungi.Crossref | GoogleScholarGoogle Scholar |
