Genome sequence of the plant growth promoting endophytic yeast Rhodotorula graminis WP1

Firrincieli, Andrea; Otillar, Robert; Salamov, Asaf; Schmutz, Jeremy; Khan, Zareen; Redman, Regina S.; Fleck, Neil D.; Lindquist, Erika; Grigoriev, Igor V.; Doty, Sharon L.

doi:10.3389/fmicb.2015.00978

Title: Genome sequence of the plant growth promoting endophytic yeast Rhodotorula graminis WP1

Journal Article · Thu Sep 17 00:00:00 EDT 2015 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2015.00978· OSTI ID:1615256

Firrincieli, Andrea ^[1]; Otillar, Robert ^[2]; Salamov, Asaf ^[2]; Schmutz, Jeremy ^[3]; Khan, Zareen ^[4]; Redman, Regina S. ^[5]; Fleck, Neil D. ^[4]; Lindquist, Erika ^[2]; Grigoriev, Igor V. ^[2]; Doty, Sharon L. ^[4]

Univ. of Tuscia, Tuscia (Italy)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
Univ. of Washington, Seattle, WA (United States)
Adaptive Symbiotic Technologies, Seattle, WA (United States)

Here we present the genome sequence of Rhodotorula graminis WP1, a pink-pigmented, encapsulated yeast strain belonging to the Basidiomycota phylum that was isolated from within stems of Populus trichocarpa growing in its native riparian environment alongside the Snoqualmie River in Western Washington state(Xin et al., 2009). Although numerous bacterial endophytes, the microorganisms living fully within plants, have been characterized, relatively few endophytic yeast strains have been studied (Doty, 2011). The genome of strain WP1 was the first endophytic yeast to be sequenced, and has been included in several genomic analyses (Spatafora et al., 2013; Nagy et al., 2014; Pendleton et al., 2014). Although originally isolated from poplar, WP1 has a broad host range, providing growth benefits not only to poplar (Knoth et al., 2014; Khan et al. in review) but also to grasses and agricultural crop species (Khan et al., 2012; Knoth et al., 2013). Strain WP1 improves plant vigor and has useful biochemical properties (Doty, 2014) including the ability to ferment both pentoses and hexoses and to degrade fermentation inhibitors (Xu et al., 2011). Genomic analysis of bacterial endophytes has revealed certain features in common including genes for phytohormone synthesis, adhesion, colonization, stress reduction, and iron and phosphate acquisition (Fouts et al., 2008; Taghavi et al., 2010; Sessitsch et al., 2012; Witzel et al., 2012). We analyzed the genome of WP1 with a focus on genes potentially involved in plant-microbe interactions.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1615256

Journal Information:: Frontiers in Microbiology, Vol. 6, Issue SEP; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 58 works

Citation information provided by
Web of Science

References (62)

Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites Nielsen, H.; Engelbrecht, J.; Brunak, S. Protein Engineering Design and Selection, Vol. 10, Issue 1, p. 1-6 https://doi.org/10.1093/protein/10.1.1	journal	January 1997
The Mutualist Laccaria bicolor Expresses a Core Gene Regulon During the Colonization of Diverse Host Plants and a Variable Regulon to Counteract Host-Specific Defenses Plett, Jonathan M.; Tisserant, Emilie; Brun, Annick Molecular Plant-Microbe Interactions, Vol. 28, Issue 3 https://doi.org/10.1094/MPMI-05-14-0129-FI	journal	March 2015
Complete Genome Sequence of the N2-Fixing Broad Host Range Endophyte Klebsiella pneumoniae 342 and Virulence Predictions Verified in Mice Fouts, Derrick E.; Tyler, Heather L.; DeBoy, Robert T. PLoS Genetics, Vol. 4, Issue 7 https://doi.org/10.1371/journal.pgen.1000141	journal	July 2008
The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis Martin, F.; Aerts, A.; Ahrén, D. Nature, Vol. 452, Issue 7183 https://doi.org/10.1038/nature06556	journal	March 2008
Cryptococcosis in the era of AIDS--100 years after the discovery of Cryptococcus neoformans. Mitchell, T. G.; Perfect, J. R. Clinical Microbiology Reviews, Vol. 8, Issue 4 https://doi.org/10.1128/CMR.8.4.515	journal	October 1995
Growth-Promoting Endophytic Fungi of Forest Trees Doty, Sharon Lafferty Endophytes of Forest Trees https://doi.org/10.1007/978-94-007-1599-8_9	book	January 2011
The iron(II) and 2-oxoacid-dependent dioxygenases and their role in metabolism (1967 to 1999) Prescott, Andy G.; Lloyd, Matthew D. Natural Product Reports, Vol. 17, Issue 4 https://doi.org/10.1039/a902197c	journal	January 2000
Properties of bacterial endophytes and their proposed role in plant growth Hardoim, Pablo R.; van Overbeek, Leo S.; Elsas, Jan Dirk van Trends in Microbiology, Vol. 16, Issue 10 https://doi.org/10.1016/j.tim.2008.07.008	journal	October 2008
InterProScan: protein domains identifier Quevillon, E.; Silventoinen, V.; Pillai, S. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki442	journal	July 2005
Ab initio Gene Finding in Drosophila Genomic DNA Salamov, Asaf A.; Solovyev, Victor V. Genome Research, Vol. 10, Issue 4, p. 516-522 https://doi.org/10.1101/gr.10.4.516	journal	April 2000
Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions: Bacterial volatiles and multitrophic interactions D'Alessandro, Marco; Erb, Matthias; Ton, Jurriaan Plant, Cell & Environment, Vol. 37, Issue 4 https://doi.org/10.1111/pce.12220	journal	December 2013
Genome Sequence of the Plant Growth Promoting Endophytic Bacterium Enterobacter sp. 638 Taghavi, Safiyh; van der Lelie, Daniel; Hoffman, Adam PLoS Genetics, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pgen.1000943	journal	May 2010
Complete genome sequence of the sugarcane nitrogen-fixing endophyte Gluconacetobacter diazotrophicus Pal5 Bertalan, Marcelo; Albano, Rodolpho; de Pádua, Vânia BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-450	journal	January 2009
Our Current Understanding of Fungal Biofilms Ramage, Gordon; Mowat, Eilidh; Jones, Brian Critical Reviews in Microbiology, Vol. 35, Issue 4 https://doi.org/10.3109/10408410903241436	journal	October 2009
Horizontal Gene Exchange in Environmental Microbiota Aminov, Rustam I. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00158	journal	January 2011
Populus Rhizosphere and the Ectomycorrhizal Interactome Podila, Gopi K.; Sreedasyam, Avinash; Muratet, Michael A. Critical Reviews in Plant Sciences, Vol. 28, Issue 5 https://doi.org/10.1080/07352680903241220	journal	October 2009
Insights into Auxin Signaling in Plant?Pathogen Interactions Fu, Jing; Wang, Shiping Frontiers in Plant Science, Vol. 2 https://doi.org/10.3389/fpls.2011.00074	journal	January 2011
Conservation and Diversity of Seed Associated Endophytes in Zea across Boundaries of Evolution, Ethnography and Ecology Johnston-Monje, David; Raizada, Manish N. PLoS ONE, Vol. 6, Issue 6 https://doi.org/10.1371/journal.pone.0020396	journal	June 2011
Nitrilase enzymes and their role in plant-microbe interactions Howden, Andrew J. M.; Preston, Gail M. Microbial Biotechnology, Vol. 2, Issue 4 https://doi.org/10.1111/j.1751-7915.2009.00111.x	journal	July 2009
Genome Sequence of Enterobacter radicincitans DSM16656T, a Plant Growth-Promoting Endophyte Witzel, K.; Gwinn-Giglio, M.; Nadendla, S. Journal of Bacteriology, Vol. 194, Issue 19 https://doi.org/10.1128/JB.01193-12	journal	September 2012
Gene Ontology: tool for the unification of biology Ashburner, Michael; Ball, Catherine A.; Blake, Judith A. Nature Genetics, Vol. 25, Issue 1 https://doi.org/10.1038/75556	journal	May 2000
Promotion of plant growth by an auxin-producing isolate of the yeast Williopsis saturnus endophytic in maize (Zea mays L.) roots Nassar, Amr H.; El-Tarabily, Khaled A.; Sivasithamparam, Krishnapillai Biology and Fertility of Soils, Vol. 42, Issue 2 https://doi.org/10.1007/s00374-005-0008-y	journal	July 2005
Effector candidates in the secretome of Piriformospora indica, a ubiquitous plant-associated fungus Rafiqi, Maryam; Jelonek, Lukas; Akum, Ndifor F. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00228	journal	January 2013
Whole-Genome Sequence Assembly for Mammalian Genomes: Arachne 2 Jaffe, D. B. Genome Research, Vol. 13, Issue 1 https://doi.org/10.1101/gr.828403	journal	January 2003
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence Lowe, Todd M.; Eddy, Sean R. Nucleic Acids Research, Vol. 25, Issue 5 https://doi.org/10.1093/nar/25.5.0955	journal	March 1997
Role of Pseudomonas putida Indoleacetic Acid in Development of the Host Plant Root System Patten, C. L.; Glick, B. R. Applied and Environmental Microbiology, Vol. 68, Issue 8 https://doi.org/10.1128/AEM.68.8.3795-3801.2002	journal	August 2002
Biological nitrogen fixation and biomass accumulation within poplar clones as a result of inoculations with diazotrophic endophyte consortia Knoth, Jenny L.; Kim, Soo-Hyung; Ettl, Gregory J. New Phytologist, Vol. 201, Issue 2 https://doi.org/10.1111/nph.12536	journal	October 2013
Functional diversity of 2-oxoglutarate/Fe(II)-dependent dioxygenases in plant metabolism Farrow, Scott C.; Facchini, Peter J. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00524	journal	October 2014
Transcriptional Responses to Sucrose Mimic the Plant-Associated Life Style of the Plant Growth Promoting Endophyte Enterobacter sp. 638 Taghavi, Safiyh; Wu, Xiao; Ouyang, Liming PLOS ONE, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pone.0115455	journal	January 2015
Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions: Auxin, plant roots and plant-microbe interaction Sukumar, Poornima; LeguÉ, ValÉRie; VayssiÈRes, Alice Plant, Cell & Environment, Vol. 36, Issue 5 https://doi.org/10.1111/pce.12036	journal	December 2012
Characterization of three endophytic, indole-3-acetic acid-producing yeasts occurring in Populus trees Xin, Gang; Glawe, Dean; Doty, Sharon L. Mycological Research, Vol. 113, Issue 9 https://doi.org/10.1016/j.mycres.2009.06.001	journal	September 2009
Studies on the Sexuality of Rhodotorula Banno, Isao The Journal of General and Applied Microbiology, Vol. 13, Issue 2 https://doi.org/10.2323/jgam.13.167	journal	January 1967
Bacterial and Yeast Endophytes from Poplar and Willow Promote Growth in Crop Plants and Grasses Khan, Zareen; Guelich, Grant; Phan, Ha ISRN Agronomy, Vol. 2012 https://doi.org/10.5402/2012/890280	journal	January 2012
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) Tuskan, G. A.; DiFazio, S.; Jansson, S. Science, Vol. 313, Issue 5793, p. 1596-1604 https://doi.org/10.1126/science.1128691	journal	September 2006
Functional Characteristics of an Endophyte Community Colonizing Rice Roots as Revealed by Metagenomic Analysis Sessitsch, A.; Hardoim, P.; Döring, J. Molecular Plant-Microbe Interactions, Vol. 25, Issue 1 https://doi.org/10.1094/MPMI-08-11-0204	journal	January 2012
Horizontal Gene Transfer to Endogenous Endophytic Bacteria from Poplar Improves Phytoremediation of Toluene Taghavi, S.; Barac, T.; Greenberg, B. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8500-8505.2005	journal	December 2005
Acquisition of prokaryotic genes by fungal genomes Marcet-Houben, Marina; Gabaldón, Toni Trends in Genetics, Vol. 26, Issue 1 https://doi.org/10.1016/j.tig.2009.11.007	journal	January 2010
Duplications and losses in gene families of rust pathogens highlight putative effectors Pendleton, Amanda L.; Smith, Katherine E.; Feau, Nicolas Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00299	journal	June 2014
Effects of cross host species inoculation of nitrogen-fixing endophytes on growth and leaf physiology of maize Knoth, Jenny L.; Kim, Soo-Hyung; Ettl, Gregory J. GCB Bioenergy, Vol. 5, Issue 4 https://doi.org/10.1111/gcbb.12006	journal	September 2012
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures Murashige, Toshio; Skoog, Folke Physiologia Plantarum, Vol. 15, Issue 3, p. 473-497 https://doi.org/10.1111/j.1399-3054.1962.tb08052.x	journal	July 1962
Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts Nagy, László G.; Ohm, Robin A.; Kovács, Gábor M. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5471	journal	July 2014
De novo identification of repeat families in large genomes Price, A. L.; Jones, N. C.; Pevzner, P. A. Bioinformatics, Vol. 21, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/bti1018	journal	June 2005
Using GeneWise in the Drosophila Annotation Experiment Birney, E. Genome Research, Vol. 10, Issue 4 https://doi.org/10.1101/gr.10.4.547	journal	April 2000
Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren Journal of Molecular Biology, Vol. 300, Issue 4 https://doi.org/10.1006/jmbi.2000.3903	journal	July 2000
A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonum Pitkin, J. W.; Panaccione, D. G.; Walton, J. D. Microbiology, Vol. 142, Issue 6 https://doi.org/10.1099/13500872-142-6-1557	journal	June 1996
The KEGG resource for deciphering the genome Kanehisa, M. Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh063	journal	January 2004
The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003 Boeckmann, B. Nucleic Acids Research, Vol. 31, Issue 1 https://doi.org/10.1093/nar/gkg095	journal	January 2003
Indole-3-acetic acid in plant–microbe interactions Duca, Daiana; Lorv, Janet; Patten, Cheryl L. Antonie van Leeuwenhoek, Vol. 106, Issue 1 https://doi.org/10.1007/s10482-013-0095-y	journal	January 2014
Acetolactate Synthase from Bacillus subtilis Serves as a 2-Ketoisovalerate Decarboxylase for Isobutanol Biosynthesis in Escherichia coli Atsumi, S.; Li, Z.; Liao, J. C. Applied and Environmental Microbiology, Vol. 75, Issue 19 https://doi.org/10.1128/AEM.01160-09	journal	August 2009
A conserved mechanism for nitrile metabolism in bacteria and plants Howden, Andrew J. M.; Jill Harrison, C.; Preston, Gail M. The Plant Journal, Vol. 57, Issue 2 https://doi.org/10.1111/j.1365-313X.2008.03682.x	journal	January 2009
Analysis of donor splice sites in different eukaryotic organisms Rogozin, Igor B.; Milanesi, Luciano Journal of Molecular Evolution, Vol. 45, Issue 1 https://doi.org/10.1007/PL00006200	journal	July 1997
Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training Ter-Hovhannisyan, V.; Lomsadze, A.; Chernoff, Y. O. Genome Research, Vol. 18, Issue 12 https://doi.org/10.1101/gr.081612.108	journal	October 2008
Reliability Measures for Membrane Protein Topology Prediction Algorithms Melén, Karin; Krogh, Anders; von Heijne, Gunnar Journal of Molecular Biology, Vol. 327, Issue 3 https://doi.org/10.1016/S0022-2836(03)00182-7	journal	March 2003
Cryptococcus neoformans CAP59 (or Cap59p) Is Involved in the Extracellular Trafficking of Capsular Glucuronoxylomannan García-Rivera, Javier; Chang, Yun C.; Kwon-Chung, K. J. Eukaryotic Cell, Vol. 3, Issue 2 https://doi.org/10.1128/EC.3.2.385-392.2004	journal	April 2004
Towards a holistic understanding of the beneficial interactions across the Populus microbiome Hacquard, Stéphane; Schadt, Christopher W. New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13133	journal	November 2014
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
EuSplice: a unified resource for the analysis of splice signals and alternative splicing in eukaryotic genes Bhasi, Ashwini; Pandey, Ram Vinay; Utharasamy, Suriya Prabha Bioinformatics, Vol. 23, Issue 14 https://doi.org/10.1093/bioinformatics/btm084	journal	March 2007
Using next generation transcriptome sequencing to predict an ectomycorrhizal metabolome Larsen, Peter E.; Sreedasyam, Avinash; Trivedi, Geetika BMC Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1186/1752-0509-5-70	journal	January 2011
A Role for a Dioxygenase in Auxin Metabolism and Reproductive Development in Rice Zhao, Zhigang; Zhang, Yunhui; Liu, Xi Developmental Cell, Vol. 27, Issue 1 https://doi.org/10.1016/j.devcel.2013.09.005	journal	October 2013
Repbase Update, a database of eukaryotic repetitive elements Jurka, J.; Kapitonov, V. V.; Pavlicek, A. Cytogenetic and Genome Research, Vol. 110, Issue 1-4 https://doi.org/10.1159/000084979	journal	January 2005
Structure and Functions of the Bacterial Microbiota of Plants Bulgarelli, Davide; Schlaeppi, Klaus; Spaepen, Stijn Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120106	journal	April 2013
Genetic analysis of D-xylose metabolism by endophytic yeast strains of Rhodotorula graminis and Rhodotorula mucilaginosa Xu, Ping; Bura, Renata; Doty, Sharon L. Genetics and Molecular Biology, Vol. 34, Issue 3 https://doi.org/10.1590/S1415-47572011000300018	journal	January 2011

Cited By (13)

An analysis of codon bias in six red yeast species Camiolo, Salvatore; Toome-Heller, Merje; Aime, M. Catherine Yeast, Vol. 36, Issue 1 https://doi.org/10.1002/yea.3359	journal	October 2018
Endophytes: The Unmapped Repository for Natural Products Sarethy, Indira P.; Srivastava, Nidhi; Pan, Sharadwata Natural Bio-active Compounds https://doi.org/10.1007/978-981-13-7154-7_2	book	January 2019
Phosphorus Input Alters the Assembly of Rice (Oryza sativa L.) Root-Associated Communities Long, Xi-En; Yao, Huaiying Microbial Ecology https://doi.org/10.1007/s00248-019-01407-6	journal	July 2019
Biology, dynamics, and applications of transposable elements in basidiomycete fungi Castanera, Raúl; Borgognone, Alessandra; Pisabarro, Antonio G. Applied Microbiology and Biotechnology, Vol. 101, Issue 4 https://doi.org/10.1007/s00253-017-8097-8	journal	January 2017
Identification of Novel Endophytic Yeast Strains from Tangerine Peel Ling, Lijun; Li, Zibin; Jiao, Zhenglong Current Microbiology, Vol. 76, Issue 9 https://doi.org/10.1007/s00284-019-01721-9	journal	June 2019
AYbRAH: a curated ortholog database for yeasts and fungi spanning 600 million years of evolution Correia, Kevin; Yu, Shi M.; Mahadevan, Radhakrishnan Database, Vol. 2019 https://doi.org/10.1093/database/baz022	journal	January 2019
Fungal evolution: major ecological adaptations and evolutionary transitions Naranjo‐Ortiz, Miguel A.; Gabaldón, Toni Biological Reviews https://doi.org/10.1111/brv.12510	journal	April 2019
Torulene and torularhodin: “new” fungal carotenoids for industry? Kot, Anna M.; Błażejak, Stanisław; Gientka, Iwona Microbial Cell Factories, Vol. 17, Issue 1 https://doi.org/10.1186/s12934-018-0893-z	journal	March 2018
Genome-enhanced detection and identification of fungal pathogens responsible for pine and poplar rust diseases Bergeron, Marie-Josée; Feau, Nicolas; Stewart, Don PLOS ONE, Vol. 14, Issue 2 https://doi.org/10.1371/journal.pone.0210952	journal	February 2019
Genomic Data Quality Impacts Automated Detection of Lateral Gene Transfer in Fungi Dupont, Pierre-Yves; Cox, Murray P. G3: Genes\|Genomes\|Genetics, Vol. 7, Issue 4 https://doi.org/10.1534/g3.116.038448	journal	February 2017
The Effect of Microbial Endophyte Consortia on Pseudotsuga menziesii and Thuja plicata Survival, Growth, and Physiology Across Edaphic Gradients Aghai, Matthew M.; Khan, Zareen; Joseph, Matthew R. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01353	journal	June 2019
“Omics” Tools for Better Understanding the Plant–Endophyte Interactions Kaul, Sanjana; Sharma, Tanwi; K. Dhar, Manoj Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00955	journal	June 2016
A draft genome and transcriptome of common milkweed ( Asclepias syriaca ) as resources for evolutionary, ecological, and molecular studies in milkweeds and Apocynaceae Weitemier, Kevin; Straub, Shannon C. K.; Fishbein, Mark PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7649	journal	January 2019