Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro
Abstract
Summary Serendipitaceae represents a diverse fungal group in the Basidiomycota that includes endophytes and lineages that repeatedly evolved ericoid, orchid and ectomycorrhizal lifestyle. Plants rely upon both nitrogen and phosphorous, for essential growth processes, and are often provided by mycorrhizal fungi. In this study, we investigated the cellular proteome of Serendipita vermifera MAFF305830 and closely related Serendipita vermifera subsp. bescii NFPB0129 grown in vitro under (N) ammonium and (P) phosphate starvation conditions. Mycelial growth pattern was documented under these conditions to correlate growth‐specific responses to nutrient starvation. We found that N‐starvation accelerated hyphal radial growth, whereas P‐starvation accelerated hyphal branching. Additionally, P‐starvation triggers an integrated starvation response leading to remodelling of lipid metabolism. Higher abundance of an ammonium transporter known to serve as both an ammonium sensor and stimulator of hyphal growth was detected under N‐starvation. Additionally, N‐starvation led to strong up‐regulation of nitrate, amino acid, peptide, and urea transporters, along with several proteins predicted to have peptidase activity. Taken together, our finding suggests S. bescii and S. vermifera have the metabolic capacity for nitrogen assimilation from organic forms of N compounds. We hypothesize that the nitrogen metabolite repression is a key regulator of such organic N assimilation.
- Authors:
-
[1];
[1]
- Noble Research Institute, LLC Ardmore OK 73401 USA
- Chemical Sciences Division, Oak Ridge National Laboratory Oak Ridge TN 37831 USA
- Biosciences Division, Oak Ridge National Laboratory Oak Ridge TN 37831 USA
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1510338
- Alternate Identifier(s):
- OSTI ID: 1510341; OSTI ID: 1545210
- Grant/Contract Number:
- AC05‐00OR22725; AC05-00OR22725
- Resource Type:
- Published Article
- Journal Name:
- Environmental Microbiology Reports
- Additional Journal Information:
- Journal Name: Environmental Microbiology Reports Journal Volume: 11 Journal Issue: 4; Journal ID: ISSN 1758-2229
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES
Citation Formats
Ray, Prasun, Abraham, Paul E., Guo, Yingqing, Giannone, Richard J., Engle, Nancy L., Yang, Zamin K., Jacobson, Daniel, Hettich, Robert L., Tschaplinski, Timothy J., and Craven, Kelly D. Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro. United States: N. p., 2019.
Web. doi:10.1111/1758-2229.12757.
Ray, Prasun, Abraham, Paul E., Guo, Yingqing, Giannone, Richard J., Engle, Nancy L., Yang, Zamin K., Jacobson, Daniel, Hettich, Robert L., Tschaplinski, Timothy J., & Craven, Kelly D. Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro. United States. https://doi.org/10.1111/1758-2229.12757
Ray, Prasun, Abraham, Paul E., Guo, Yingqing, Giannone, Richard J., Engle, Nancy L., Yang, Zamin K., Jacobson, Daniel, Hettich, Robert L., Tschaplinski, Timothy J., and Craven, Kelly D. Wed .
"Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro". United States. https://doi.org/10.1111/1758-2229.12757.
@article{osti_1510338,
title = {Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro},
author = {Ray, Prasun and Abraham, Paul E. and Guo, Yingqing and Giannone, Richard J. and Engle, Nancy L. and Yang, Zamin K. and Jacobson, Daniel and Hettich, Robert L. and Tschaplinski, Timothy J. and Craven, Kelly D.},
abstractNote = {Summary Serendipitaceae represents a diverse fungal group in the Basidiomycota that includes endophytes and lineages that repeatedly evolved ericoid, orchid and ectomycorrhizal lifestyle. Plants rely upon both nitrogen and phosphorous, for essential growth processes, and are often provided by mycorrhizal fungi. In this study, we investigated the cellular proteome of Serendipita vermifera MAFF305830 and closely related Serendipita vermifera subsp. bescii NFPB0129 grown in vitro under (N) ammonium and (P) phosphate starvation conditions. Mycelial growth pattern was documented under these conditions to correlate growth‐specific responses to nutrient starvation. We found that N‐starvation accelerated hyphal radial growth, whereas P‐starvation accelerated hyphal branching. Additionally, P‐starvation triggers an integrated starvation response leading to remodelling of lipid metabolism. Higher abundance of an ammonium transporter known to serve as both an ammonium sensor and stimulator of hyphal growth was detected under N‐starvation. Additionally, N‐starvation led to strong up‐regulation of nitrate, amino acid, peptide, and urea transporters, along with several proteins predicted to have peptidase activity. Taken together, our finding suggests S. bescii and S. vermifera have the metabolic capacity for nitrogen assimilation from organic forms of N compounds. We hypothesize that the nitrogen metabolite repression is a key regulator of such organic N assimilation.},
doi = {10.1111/1758-2229.12757},
journal = {Environmental Microbiology Reports},
number = 4,
volume = 11,
place = {United States},
year = {Wed May 01 00:00:00 EDT 2019},
month = {Wed May 01 00:00:00 EDT 2019}
}
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https://doi.org/10.1111/1758-2229.12757
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Works referenced in this record:
Mycorrhizas and tropical soil fertility
journal, August 2006
- Cardoso, I.; Kuyper, T.
- Agriculture, Ecosystems & Environment, Vol. 116, Issue 1-2
The Endophytic Fungus Piriformospora indica Stimulates the Expression of Nitrate Reductase and the Starch-degrading Enzyme Glucan-water Dikinase in Tobacco and Arabidopsis Roots through a Homeodomain Transcription Factor That Binds to a Conserved Motif in Their Promoters
journal, February 2005
- Sherameti, Irena; Shahollari, Bationa; Venus, Yvonne
- Journal of Biological Chemistry, Vol. 280, Issue 28
Molecular cloning and characterization of a negative-acting nitrogen regulatory gene of Neurospora crassa
journal, September 1988
- Fu, Ying-Hui; Young, James L.; Marzluf, George A.
- MGG Molecular & General Genetics, Vol. 214, Issue 1
Host-related metabolic cues affect colonization strategies of a root endophyte
journal, August 2013
- Lahrmann, Urs; Ding, Yi; Banhara, Aline
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 34
Sebacinales – one thousand and one interactions with land plants
journal, February 2016
- Weiß, Michael; Waller, Frank; Zuccaro, Alga
- New Phytologist, Vol. 211, Issue 1
The molecular components of the extracellular protein-degradation pathways of the ectomycorrhizal fungus Paxillus involutus
journal, July 2013
- Shah, Firoz; Rineau, Francois; Canbäck, Björn
- New Phytologist, Vol. 200, Issue 3
Detection of extracellular protease activity in different species and genera of ectomycorrhizal fungi
journal, January 2007
- Nygren, Cajsa M. R.; Edqvist, Johan; Elfstrand, Malin
- Mycorrhiza, Vol. 17, Issue 3
Fungal and plant gene expression in the Tulasnella calospora - Serapias vomeracea symbiosis provides clues about nitrogen pathways in orchid mycorrhizas
journal, November 2016
- Fochi, Valeria; Chitarra, Walter; Kohler, Annegret
- New Phytologist, Vol. 213, Issue 1
Mycorrhizal ecology and evolution: the past, the present, and the future
journal, February 2015
- van der Heijden, Marcel G. A.; Martin, Francis M.; Selosse, Marc-André
- New Phytologist, Vol. 205, Issue 4
Genome Sequence of the Plant Growth Promoting Fungus Serendipita vermifera subsp. bescii : The First Native Strain from North America
journal, January 2018
- Ray, Prasun; Chi, Myoung-Hwan; Guo, Yingqing
- Phytobiomes Journal, Vol. 2, Issue 2
2016 update of the PRIDE database and its related tools
journal, November 2015
- Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi
- Nucleic Acids Research, Vol. 44, Issue D1
ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks
journal, February 2009
- Bindea, Gabriela; Mlecnik, Bernhard; Hackl, Hubert
- Bioinformatics, Vol. 25, Issue 8
A Phosphate Transporter from the Root Endophytic Fungus Piriformospora indica Plays a Role in Phosphate Transport to the Host Plant
journal, May 2010
- Yadav, Vikas; Kumar, Manoj; Deep, Deepak Kumar
- Journal of Biological Chemistry, Vol. 285, Issue 34
Nitrogen regulation of fungal secondary metabolism in fungi
journal, November 2014
- Tudzynski, Bettina
- Frontiers in Microbiology, Vol. 5
Enigmatic Sebacinales
journal, January 2013
- Oberwinkler, Franz; Riess, Kai; Bauer, Robert
- Mycological Progress, Vol. 12, Issue 1
Responses of root architecture development to low phosphorus availability: a review
journal, December 2012
- Niu, Yao Fang; Chai, Ru Shan; Jin, Gu Lei
- Annals of Botany, Vol. 112, Issue 2
The control of filamentous differentiation and virulence in fungi
journal, September 1998
- Madhani, Hiten D.; Fink, Gerald R.
- Trends in Cell Biology, Vol. 8, Issue 9
The fungal vacuole: composition, function, and biogenesis.
journal, January 1990
- Klionsky, D. J.; Herman, P. K.; Emr, S. D.
- Microbiological Reviews, Vol. 54, Issue 3
The Perseus computational platform for comprehensive analysis of (prote)omics data
journal, June 2016
- Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel
- Nature Methods, Vol. 13, Issue 9
The structure and function of the vegetative mycelium of ectomycorrhizal plants. VI. Activities of nutrient mobilizing enzymes in birch litter colonized by Paxillus involutus (Fr.) Fr.
journal, July 1995
- Bending, Gary D.; Read, David J.
- New Phytologist, Vol. 130, Issue 3
Enhancement of Switchgrass (Panicum virgatum L.) Biomass Production under Drought Conditions by the Ectomycorrhizal Fungus Sebacina vermifera
journal, August 2011
- Ghimire, Sita R.; Craven, Kelly D.
- Applied and Environmental Microbiology, Vol. 77, Issue 19
Detecting the heavy metal tolerance level in ectomycorrhizal fungi in vitro
journal, April 2005
- Ray, Prasun; Tiwari, Richa; Reddy, U. Gangi
- World Journal of Microbiology and Biotechnology, Vol. 21, Issue 3
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research
journal, August 2005
- Conesa, A.; Gotz, S.; Garcia-Gomez, J. M.
- Bioinformatics, Vol. 21, Issue 18
Mycorrhizal associations of isolates of Sebacina vermifera
journal, October 1988
- Warcup, J. H.
- New Phytologist, Vol. 110, Issue 2
Morphology and molecules: the Sebacinales, a case study
journal, April 2014
- Oberwinkler, Franz; Riess, Kai; Bauer, Robert
- Mycological Progress, Vol. 13, Issue 3
A Novel Delivery System for the Root Symbiotic Fungus, Sebacina vermifera, and Consequent Biomass Enhancement of Low Lignin COMT Switchgrass Lines
journal, June 2015
- Ray, Prasun; Ishiga, Takako; Decker, Stephen R.
- BioEnergy Research, Vol. 8, Issue 3
Phosphate utilization by the fungal root endophyte Piriformospora indica
journal, December 2015
- Ngwene, B.; Boukail, S.; Söllner, L.
- Plant and Soil, Vol. 405, Issue 1-2
Vacuolar Function in the Phosphate Homeostasis of the Yeast Saccharomyces cerevisiae
journal, December 1996
- Shirahama, K.; Yazaki, Y.; Sakano, K.
- Plant and Cell Physiology, Vol. 37, Issue 8
Subtle hydrophobic interactions between the seventh residue of the zinc finger loop and the first base of an HGATAR sequence determine promoter-specific recognition by the Aspergillus nidulans GATA factor AreA
journal, July 1997
- Ravagnani, Adriana; Gorfinkiel, Lisette; Langdon, Timothy
- The EMBO Journal, Vol. 16, Issue 13
Sebacina vermifera: a unique root symbiont with vast agronomic potential
journal, December 2015
- Ray, Prasun; Craven, Kelly D.
- World Journal of Microbiology and Biotechnology, Vol. 32, Issue 1
Molecular characterization, function and regulation of ammonium transporters (Amt) and ammonium-metabolizing enzymes (GS, NADP-GDH) in the ectomycorrhizal fungus Hebeloma cylindrosporum: Ammonium assimilation in Hebeloma cylindrosporum
journal, January 2003
- Javelle, Arnaud; Morel, Mélanie; Rodríguez-Pastrana, Blanca-Rosa
- Molecular Microbiology, Vol. 47, Issue 2
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis
journal, July 2010
- Bonfante, Paola; Genre, Andrea
- Nature Communications, Vol. 1, Issue 1
Endophytic Life Strategies Decoded by Genome and Transcriptome Analyses of the Mutualistic Root Symbiont Piriformospora indica
journal, October 2011
- Zuccaro, Alga; Lahrmann, Urs; Güldener, Ulrich
- PLoS Pathogens, Vol. 7, Issue 10
Variation in nutrient-acquisition patterns by mycorrhizal fungi of rare and common orchids explains diversification in a global biodiversity hotspot
journal, March 2013
- Nurfadilah, Siti; Swarts, Nigel D.; Dixon, Kingsley W.
- Annals of Botany, Vol. 111, Issue 6