The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting Microbe

Serendipita indica (former Piriformospora indica) is a non-obligate endophytic fungus and generally a plant growth and defence promoter with high potential to be used in agriculture. However, S. indica may switch from biotrophy to saprotrophy losing its plant growth promoting traits. Our aim was to...

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Main Authors: Teresa Dias, Vívian Pimentel, Antônio Jesus Dorighetto Cogo, Raquel Costa, Amanda Azevedo Bertolazi, Camila Miranda, Sávio Bastos de Souza, Juliana Melo, Manuela Carolino, Ajit Varma, Frederico Eutrópio, Fábio Lopes Olivares, Alessandro Coutinho Ramos, Cristina Cruz
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.562238/full
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author Teresa Dias
Vívian Pimentel
Antônio Jesus Dorighetto Cogo
Raquel Costa
Amanda Azevedo Bertolazi
Camila Miranda
Sávio Bastos de Souza
Juliana Melo
Manuela Carolino
Ajit Varma
Frederico Eutrópio
Fábio Lopes Olivares
Alessandro Coutinho Ramos
Cristina Cruz
author_facet Teresa Dias
Vívian Pimentel
Antônio Jesus Dorighetto Cogo
Raquel Costa
Amanda Azevedo Bertolazi
Camila Miranda
Sávio Bastos de Souza
Juliana Melo
Manuela Carolino
Ajit Varma
Frederico Eutrópio
Fábio Lopes Olivares
Alessandro Coutinho Ramos
Cristina Cruz
author_sort Teresa Dias
collection DOAJ
description Serendipita indica (former Piriformospora indica) is a non-obligate endophytic fungus and generally a plant growth and defence promoter with high potential to be used in agriculture. However, S. indica may switch from biotrophy to saprotrophy losing its plant growth promoting traits. Our aim was to understand if the free-living stage growth conditions (namely C availability) regulate S. indica’s phenotype, and its potential as plant-growth-promoting-microbe (PGPM). We grew S. indica in its free-living stage under increasing C availabilities (2–20 g L–1 of glucose or sucrose). We first characterised the effect of C availability during free-living stage growth on fungal phenotype: colonies growth and physiology (plasma membrane proton pumps, stable isotopic signatures, and potential extracellular decomposing enzymes). The effect of the C availability during the free-living stage of the PGPM was evaluated on wheat. We observed that C availability during the free-living stage regulated S. indica’s growth, ultrastructure and physiology, resulting in two distinct colony phenotypes: compact and explorer. The compact phenotype developed at low C, used peptone as the major C and N source, and displayed higher decomposing potential for C providing substrates; while the explorer phenotype developed at high C, used glucose and sucrose as major C sources and casein and yeast extract as major N sources, and displayed higher decomposing potential for N and P providing substrates. The C availability, or the C/N ratio, during the free-living stage left a legacy to the symbiosis stage, regulating S. indica’s potential to promote plant growth: wheat growth promotion by the explorer phenotype was ± 40% higher than that by the compact phenotype. Our study highlights the importance of considering microbial ecology in designing PGPM/biofertilizers. Further studies are needed to test the phenotypes under more extreme conditions, and to understand if the in vitro acquired characteristics persist under field conditions.
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spelling doaj.art-8240e73e7f28445fb3ada5c88936c9e92022-12-21T22:25:24ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-09-011110.3389/fmicb.2020.562238562238The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting MicrobeTeresa Dias0Vívian Pimentel1Antônio Jesus Dorighetto Cogo2Raquel Costa3Amanda Azevedo Bertolazi4Camila Miranda5Sávio Bastos de Souza6Juliana Melo7Manuela Carolino8Ajit Varma9Frederico Eutrópio10Fábio Lopes Olivares11Alessandro Coutinho Ramos12Cristina Cruz13Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalLaboratory of Physiology and Biochemistry of Microorganisms, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, BrazilLaboratory of Environmental Microbiology and Biotechnology, Universidade Vila Velha, Vila Velha, BrazilCentre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalLaboratory of Environmental Microbiology and Biotechnology, Universidade Vila Velha, Vila Velha, BrazilLaboratory of Environmental Microbiology and Biotechnology, Universidade Vila Velha, Vila Velha, BrazilPlant Physiology Lab, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, BrazilCentre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalCentre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalAmity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, IndiaFaesa Centro Universitário – Campus Vitória, Vitória, BrazilCell Tissue and Biology Lab, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, BrazilLaboratory of Environmental Microbiology and Biotechnology, Universidade Vila Velha, Vila Velha, BrazilCentre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalSerendipita indica (former Piriformospora indica) is a non-obligate endophytic fungus and generally a plant growth and defence promoter with high potential to be used in agriculture. However, S. indica may switch from biotrophy to saprotrophy losing its plant growth promoting traits. Our aim was to understand if the free-living stage growth conditions (namely C availability) regulate S. indica’s phenotype, and its potential as plant-growth-promoting-microbe (PGPM). We grew S. indica in its free-living stage under increasing C availabilities (2–20 g L–1 of glucose or sucrose). We first characterised the effect of C availability during free-living stage growth on fungal phenotype: colonies growth and physiology (plasma membrane proton pumps, stable isotopic signatures, and potential extracellular decomposing enzymes). The effect of the C availability during the free-living stage of the PGPM was evaluated on wheat. We observed that C availability during the free-living stage regulated S. indica’s growth, ultrastructure and physiology, resulting in two distinct colony phenotypes: compact and explorer. The compact phenotype developed at low C, used peptone as the major C and N source, and displayed higher decomposing potential for C providing substrates; while the explorer phenotype developed at high C, used glucose and sucrose as major C sources and casein and yeast extract as major N sources, and displayed higher decomposing potential for N and P providing substrates. The C availability, or the C/N ratio, during the free-living stage left a legacy to the symbiosis stage, regulating S. indica’s potential to promote plant growth: wheat growth promotion by the explorer phenotype was ± 40% higher than that by the compact phenotype. Our study highlights the importance of considering microbial ecology in designing PGPM/biofertilizers. Further studies are needed to test the phenotypes under more extreme conditions, and to understand if the in vitro acquired characteristics persist under field conditions.https://www.frontiersin.org/article/10.3389/fmicb.2020.562238/fullfree-living stagefungal phenotypemorphologyphysiologyplant-growth-promoting-microbessymbiosis stage
spellingShingle Teresa Dias
Vívian Pimentel
Antônio Jesus Dorighetto Cogo
Raquel Costa
Amanda Azevedo Bertolazi
Camila Miranda
Sávio Bastos de Souza
Juliana Melo
Manuela Carolino
Ajit Varma
Frederico Eutrópio
Fábio Lopes Olivares
Alessandro Coutinho Ramos
Cristina Cruz
The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting Microbe
Frontiers in Microbiology
free-living stage
fungal phenotype
morphology
physiology
plant-growth-promoting-microbes
symbiosis stage
title The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting Microbe
title_full The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting Microbe
title_fullStr The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting Microbe
title_full_unstemmed The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting Microbe
title_short The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting Microbe
title_sort free living stage growth conditions of the endophytic fungus serendipita indica may regulate its potential as plant growth promoting microbe
topic free-living stage
fungal phenotype
morphology
physiology
plant-growth-promoting-microbes
symbiosis stage
url https://www.frontiersin.org/article/10.3389/fmicb.2020.562238/full
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