Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution
Abstract
*Plants must rearrange the network of complex carbohydrates in their cell walls during normal growth and development. To accomplish this, all plants depend on proteins called expansins that non-enzymatically loosen noncovalent bonding between cellulose microfibrils. *Surprisingly, expansin genes have more recently been found in some bacteria and microbial eukaryotes, where their biological functions are largely unknown. *In this work, we reconstruct a comprehensive phylogeny of microbial expansin genes. We find these genes in all eukaryotic microorganisms that have structural cell wall cellulose, suggesting expansins evolved in ancient marine microorganisms long before the evolution of land plants. We also find expansins in an unexpectedly high diversity of bacteria and fungi that do not have cellulosic cell walls. These bacteria and fungi inhabit varied ecological contexts mirroring the diversity of terrestrial and aquatic niches where plant and/or algal cellulosic cell walls are present. *The microbial expansin phylogeny shows evidence of multiple horizontal gene transfer events within and between bacterial and eukaryotic microbial lineages, which may in part underlie their unusually broad phylogenetic distribution. Wholly, expansins are unexpectedly widespread in bacteria and eukaryotes, and the contribution of these genes to microbial ecological interactions with plants and algae has likely been underappreciated.
- Authors:
-
[3];
[3]
- Pennsylvania State Univ., University Park, PA (United States)
- Dartmouth College, Hanover, NH (United States)
- Harvard Medical School, Boston, MA (United States)
- Publication Date:
- Research Org.:
- Pennsylvania State Univ., University Park, PA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; Simons Foundation
- OSTI Identifier:
- 1598351
- Grant/Contract Number:
- FG02-84ER13179; ACI‐1548562; DBI‐1202736
- Resource Type:
- Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Volume: 226; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; expansin; cellulose; horizontal gene transfer; domain fusion; cell wall; plant-microbe interactions; glycoside hydrolase; carbohydrate binding module
Citation Formats
Chase, William R., Zhaxybayeva, Olga, Rocha, Jorge, Cosgrove, Daniel J., and Shapiro, Lori R. Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution. United States: N. p., 2020.
Web. doi:10.1111/nph.16428.
Chase, William R., Zhaxybayeva, Olga, Rocha, Jorge, Cosgrove, Daniel J., & Shapiro, Lori R. Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution. United States. https://doi.org/10.1111/nph.16428
Chase, William R., Zhaxybayeva, Olga, Rocha, Jorge, Cosgrove, Daniel J., and Shapiro, Lori R. Mon .
"Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution". United States. https://doi.org/10.1111/nph.16428. https://www.osti.gov/servlets/purl/1598351.
@article{osti_1598351,
title = {Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution},
author = {Chase, William R. and Zhaxybayeva, Olga and Rocha, Jorge and Cosgrove, Daniel J. and Shapiro, Lori R.},
abstractNote = {*Plants must rearrange the network of complex carbohydrates in their cell walls during normal growth and development. To accomplish this, all plants depend on proteins called expansins that non-enzymatically loosen noncovalent bonding between cellulose microfibrils. *Surprisingly, expansin genes have more recently been found in some bacteria and microbial eukaryotes, where their biological functions are largely unknown. *In this work, we reconstruct a comprehensive phylogeny of microbial expansin genes. We find these genes in all eukaryotic microorganisms that have structural cell wall cellulose, suggesting expansins evolved in ancient marine microorganisms long before the evolution of land plants. We also find expansins in an unexpectedly high diversity of bacteria and fungi that do not have cellulosic cell walls. These bacteria and fungi inhabit varied ecological contexts mirroring the diversity of terrestrial and aquatic niches where plant and/or algal cellulosic cell walls are present. *The microbial expansin phylogeny shows evidence of multiple horizontal gene transfer events within and between bacterial and eukaryotic microbial lineages, which may in part underlie their unusually broad phylogenetic distribution. Wholly, expansins are unexpectedly widespread in bacteria and eukaryotes, and the contribution of these genes to microbial ecological interactions with plants and algae has likely been underappreciated.},
doi = {10.1111/nph.16428},
journal = {New Phytologist},
number = ,
volume = 226,
place = {United States},
year = {2020},
month = {1}
}
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Works referenced in this record:
Bacterial expansins and related proteins from the world of microbes
journal, April 2015
- Georgelis, Nikolaos; Nikolaidis, Nikolas; Cosgrove, Daniel J.
- Applied Microbiology and Biotechnology, Vol. 99, Issue 9
UFBoot2: Improving the Ultrafast Bootstrap Approximation
journal, October 2017
- Hoang, Diep Thi; Chernomor, Olga; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 35, Issue 2
Genome-wide identification, characterization and expression profile analysis of expansins gene family in sugarcane (Saccharum spp.)
journal, January 2018
- Santiago, Thaís R.; Pereira, Valquiria M.; de Souza, Wagner R.
- PLOS ONE, Vol. 13, Issue 1
Evolution and Diversity of Plant Cell Walls: From Algae to Flowering Plants
journal, June 2011
- Popper, Zoë A.; Michel, Gurvan; Hervé, Cécile
- Annual Review of Plant Biology, Vol. 62, Issue 1
A Population Genomics Perspective on the Emergence and Adaptation of New Plant Pathogens in Agro-Ecosystems
journal, September 2012
- Stukenbrock, Eva H.; Bataillon, Thomas
- PLoS Pathogens, Vol. 8, Issue 9
Pantoea stewartii subsp. stewartii: lessons learned from a xylem-dwelling pathogen of sweet corn: Pantoea stewartii subsp. stewartii
journal, February 2011
- Roper, M. Caroline
- Molecular Plant Pathology, Vol. 12, Issue 7
Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes
journal, September 2018
- Adl, Sina M.; Bass, David; Lane, Christopher E.
- Journal of Eukaryotic Microbiology
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010
- Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
- Systematic Biology, Vol. 59, Issue 3
Ecology drives a global network of gene exchange connecting the human microbiome
journal, October 2011
- Smillie, Chris S.; Smith, Mark B.; Friedman, Jonathan
- Nature, Vol. 480, Issue 7376
genoPlotR: comparative gene and genome visualization in R
journal, July 2010
- Guy, L.; Roat Kultima, J.; Andersson, S. G. E.
- Bioinformatics, Vol. 26, Issue 18
Myxobacterial Biodiversity in an Established Oak-Hickory Forest and a Savanna Restoration Site
journal, February 2005
- Neil, R. Brock; Hite, Dan; Kelrick, Michael I.
- Current Microbiology, Vol. 50, Issue 2
Growth of the plant cell wall
journal, November 2005
- Cosgrove, Daniel J.
- Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11, p. 850-861
The evolution of social behavior in microorganisms
journal, April 2001
- Crespi, Bernard J.
- Trends in Ecology & Evolution, Vol. 16, Issue 4
The Top 10 fungal pathogens in molecular plant pathology: Top 10 fungal pathogens
journal, April 2012
- Dean, Ralph; Van Kan, Jan A. L.; Pretorius, Zacharias A.
- Molecular Plant Pathology, Vol. 13, Issue 4
Dynamic metabolic exchange governs a marine algal-bacterial interaction
journal, November 2016
- Segev, Einat; Wyche, Thomas P.; Kim, Ki Hyun
- eLife, Vol. 5
Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security
journal, December 2016
- McDonald, Bruce A.; Stukenbrock, Eva H.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 371, Issue 1709
Pathogen effects on vegetative and floral odours mediate vector attraction and host exposure in a complex pathosystem
journal, September 2012
- Shapiro, Lori; De Moraes, Consuelo M.; Stephenson, Andrew G.
- Ecology Letters, Vol. 15, Issue 12
Nonhost resistance to Phytophthora: novel prospects for a classical problem
journal, August 2001
- Kamoun, Sophien
- Current Opinion in Plant Biology, Vol. 4, Issue 4
Fungal Endophytes in Stems and Leaves: From Latent Pathogen to Mutualistic Symbiont
journal, February 1988
- Carroll, George
- Ecology, Vol. 69, Issue 1
Functional Characterization of Two Cellulase Genes in the Gram-Positive Pathogenic Bacterium Clavibacter michiganensis for Wilting in Tomato
journal, April 2019
- Hwang, In Sun; Oh, Eom-Ji; Lee, Han Beoyl
- Molecular Plant-Microbe Interactions, Vol. 32, Issue 4
Intensive fish farming and the evolution of pathogen virulence: the case of columnaris disease in Finland
journal, October 2009
- Pulkkinen, K.; Suomalainen, L. -R.; Read, A. F.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 277, Issue 1681
First multigene analysis of Archamoebae (Amoebozoa: Conosa) robustly reveals its phylogeny and shows that Entamoebidae represents a deep lineage of the group
journal, May 2016
- Pánek, Tomáš; Zadrobílková, Eliška; Walker, Giselle
- Molecular Phylogenetics and Evolution, Vol. 98
Draft Genome Sequence of Erwinia tracheiphila , an Economically Important Bacterial Pathogen of Cucurbits
journal, June 2015
- Shapiro, Lori R.; Scully, Erin D.; Roberts, Dana
- Genome Announcements, Vol. 3, Issue 3
Role of Swollenin, an Expansin-Like Protein from Trichoderma , in Plant Root Colonization
journal, April 2008
- Brotman, Yariv; Briff, Eden; Viterbo, Ada
- Plant Physiology, Vol. 147, Issue 2
Lateral Gene Transfer Dynamics in the Ancient Bacterial Genus Streptomyces
journal, June 2017
- McDonald, Bradon R.; Currie, Cameron R.
- mBio, Vol. 8, Issue 3
Associations with rhizosphere bacteria can confer an adaptive advantage to plants
journal, May 2015
- Haney, Cara H.; Samuel, Buck S.; Bush, Jenifer
- Nature Plants, Vol. 1, Issue 6
Gynuella sunshinyii gen. nov., sp. nov., an antifungal rhizobacterium isolated from a halophyte, Carex scabrifolia Steud
journal, January 2015
- Chung, E. J.; Park, J. A.; Jeon, C. O.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 65, Issue Pt 3
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
Modification of Expansin Protein Abundance in Tomato Fruit Alters Softening and Cell Wall Polymer Metabolism during Ripening
journal, November 1999
- Brummell, David A.; Harpster, Mark H.; Civello, Pedro M.
- The Plant Cell, Vol. 11, Issue 11
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana
journal, August 2000
- Cho, H. -T.; Cosgrove, D. J.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 17
Top 10 plant pathogenic bacteria in molecular plant pathology: Top 10 plant pathogenic bacteria
journal, June 2012
- Mansfield, John; Genin, Stephane; Magori, Shimpei
- Molecular Plant Pathology, Vol. 13, Issue 6
Role of an expansin-like molecule in Dictyostelium morphogenesis and regulation of its gene expression by the signal transducer and activator of transcription protein Dd-STATa: Novel expansin-like proteins in Dictyostelium
journal, February 2009
- Ogasawara, Shun; Shimada, Nao; Kawata, Takefumi
- Development, Growth & Differentiation, Vol. 51, Issue 2
CD-Search: protein domain annotations on the fly
journal, July 2004
- Marchler-Bauer, A.; Bryant, S. H.
- Nucleic Acids Research, Vol. 32, Issue Web Server
The biomass distribution on Earth
journal, May 2018
- Bar-On, Yinon M.; Phillips, Rob; Milo, Ron
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 25
The seaweed holobiont: understanding seaweed–bacteria interactions
journal, May 2013
- Egan, Suhelen; Harder, Tilmann; Burke, Catherine
- FEMS Microbiology Reviews, Vol. 37, Issue 3
Biofilms: the matrix revisited
journal, January 2005
- Branda, Steven S.; Vik, Åshild; Friedman, Lisa
- Trends in Microbiology, Vol. 13, Issue 1
Nomenclature for members of the expansin superfamily of genes and proteins
journal, May 2004
- Kende, Hans; Bradford, Kent; Brummell, David
- Plant Molecular Biology, Vol. 55, Issue 3
ModelFinder: fast model selection for accurate phylogenetic estimates
journal, May 2017
- Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F.
- Nature Methods, Vol. 14, Issue 6
Cellulose Synthesis in Phytophthora infestans Is Required for Normal Appressorium Formation and Successful Infection of Potato
journal, March 2008
- Grenville-Briggs, Laura J.; Anderson, Victoria L.; Fugelstad, Johanna
- The Plant Cell, Vol. 20, Issue 3
Expression of an Expansin Gene Is Correlated with Root Elongation in Soybean
journal, January 2003
- Lee, Dong-Keun; Ahn, Ji Hoon; Song, Sang-Kee
- Plant Physiology, Vol. 131, Issue 3
Relative rates of gene fusion and fission in multi-domain proteins
journal, January 2005
- Kummerfeld, Sarah K.; Teichmann, Sarah A.
- Trends in Genetics, Vol. 21, Issue 1
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
Transcriptional analysis of cell growth and morphogenesis in the unicellular green alga Micrasterias (Streptophyta), with emphasis on the role of expansin
journal, January 2011
- Vannerum, Katrijn; Huysman, Marie JJ; De Rycke, Riet
- BMC Plant Biology, Vol. 11, Issue 1
Diversity and Temporal Dynamics of the Epiphytic Bacterial Communities Associated with the Canopy-Forming Seaweed Cystoseira compressa (Esper) Gerloff and Nizamuddin
journal, April 2016
- Mancuso, Francesco P.; D'Hondt, Sofie; Willems, Anne
- Frontiers in Microbiology, Vol. 7
Intensive Farming: Evolutionary Implications for Parasites and Pathogens
journal, July 2010
- Mennerat, Adèle; Nilsen, Frank; Ebert, Dieter
- Evolutionary Biology, Vol. 37, Issue 2-3
Transcriptional regulation of a horizontally transferred gene from bacterium to chordate
journal, December 2016
- Sasakura, Yasunori; Ogura, Yosuke; Treen, Nicholas
- Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1845
Expansins Abundant in Secondary Xylem Belong to Subgroup A of the α -Expansin Gene Family
journal, July 2004
- Gray-Mitsumune, Madoka; Mellerowicz, Ewa J.; Abe, Hisashi
- Plant Physiology, Vol. 135, Issue 3
A new view of the tree of life
journal, April 2016
- Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik
- Nature Microbiology, Vol. 1, Issue 5
Ultrafast Approximation for Phylogenetic Bootstrap
journal, February 2013
- Minh, B. Q.; Nguyen, M. A. T.; von Haeseler, A.
- Molecular Biology and Evolution, Vol. 30, Issue 5
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space
journal, February 2012
- Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul
- Systematic Biology, Vol. 61, Issue 3
Trichoderma species — opportunistic, avirulent plant symbionts
journal, January 2004
- Harman, Gary E.; Howell, Charles R.; Viterbo, Ada
- Nature Reviews Microbiology, Vol. 2, Issue 1
Peptidoglycan types of bacterial cell walls and their taxonomic implications.
journal, January 1972
- Schleifer, K. H.; Kandler, O.
- Bacteriological Reviews, Vol. 36, Issue 4
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data
journal, September 2016
- Yu, Guangchuang; Smith, David K.; Zhu, Huachen
- Methods in Ecology and Evolution, Vol. 8, Issue 1
The Endo-β-1,4-glucanase CelA of Clavibacter michiganensis subsp. michiganensis Is a Pathogenicity Determinant Required for Induction of Bacterial Wilt of Tomato
journal, July 2000
- Jahr, Holger; Dreier, Jens; Meletzus, Dietmar
- Molecular Plant-Microbe Interactions, Vol. 13, Issue 7
Evidence for the role of the glomerulocyte in cellulose synthesis in the tunicate,Metandrocarpa uedai
journal, March 1995
- Kimura, S.; Itoh, T.
- Protoplasma, Vol. 186, Issue 1-2
Local expression of expansin induces the entire process of leaf development and modifies leaf shape
journal, September 2001
- Pien, S.; Wyrzykowska, J.; McQueen-Mason, S.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 20
Transposon-mediated insertional mutagenesis revealed the functions of animal cellulose synthase in the ascidian Ciona intestinalis
journal, October 2005
- Sasakura, Y.; Nakashima, K.; Awazu, S.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 42
Expression of a family of expansin-like proteins during the development of Dictyostelium discoideum
journal, June 2003
- Darley, Catherine P.; Li, Yi; Schaap, Pauline
- FEBS Letters, Vol. 546, Issue 2-3
EXPANSIN A1-mediated radial swelling of pericycle cells positions anticlinal cell divisions during lateral root initiation
journal, April 2019
- Ramakrishna, Priya; Ruiz Duarte, Paola; Rance, Graham A.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 17
Infection processes of xylem-colonizing pathogenic bacteria: possible explanations for the scarcity of qualitative disease resistance genes against them in crops
journal, April 2015
- Bae, Chungyun; Han, Sang Wook; Song, Yu-Rim
- Theoretical and Applied Genetics, Vol. 128, Issue 7
CDD/SPARCLE: functional classification of proteins via subfamily domain architectures
journal, November 2016
- Marchler-Bauer, Aron; Bo, Yu; Han, Lianyi
- Nucleic Acids Research, Vol. 45, Issue D1
Bacteraemia with Cedecea neteri in a patient with systemic lupus erythematosus
journal, March 1995
- Aguilera, A.; Pascual, J.; Loza, E.
- Postgraduate Medical Journal, Vol. 71, Issue 833
Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials: A fungal expansin homologue
journal, August 2002
- Saloheimo, Markku; Paloheimo, Marja; Hakola, Satu
- European Journal of Biochemistry, Vol. 269, Issue 17
Plant biomass degradation by gut microbiomes: more of the same or something new?
journal, June 2009
- Morrison, Mark; Pope, Phillip B.; Denman, Stuart E.
- Current Opinion in Biotechnology, Vol. 20, Issue 3
PcExl1 a Novel Acid Expansin-Like Protein from the Plant Pathogen Pectobacterium carotovorum, Binds Cell Walls Differently to BsEXLX1
journal, April 2014
- Olarte-Lozano, Miguel; Mendoza-Nuñez, Mario A.; Pastor, Nina
- PLoS ONE, Vol. 9, Issue 4
Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis
journal, November 2010
- Burke, Catherine; Thomas, Torsten; Lewis, Matt
- The ISME Journal, Vol. 5, Issue 4
Expansins: ever-expanding numbers and functions
journal, December 2001
- Lee, Yi; Choi, Dongsu; Kende, Hans
- Current Opinion in Plant Biology, Vol. 4, Issue 6
Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls
journal, September 2013
- Wang, T.; Park, Y. B.; Caporini, M. A.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 41
Expansins and cell growth
journal, December 2003
- Li, Yi; Jones, Louise; McQueen-Mason, Simon
- Current Opinion in Plant Biology, Vol. 6, Issue 6
Ecological Genomics of Marine Roseobacters
journal, May 2007
- Moran, M. A.; Belas, R.; Schell, M. A.
- Applied and Environmental Microbiology, Vol. 73, Issue 14
The Vibrio cholerae chitin utilization program
journal, February 2004
- Meibom, K. L.; Li, X. B.; Nielsen, A. T.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 8
Fusarium graminearum: pathogen or endophyte of North American grasses?
journal, November 2017
- Lofgren, Lotus A.; LeBlanc, Nicholas R.; Certano, Amanda K.
- New Phytologist, Vol. 217, Issue 3
Simplified and representative bacterial community of maize roots
journal, March 2017
- Niu, Ben; Paulson, Joseph Nathaniel; Zheng, Xiaoqi
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 12
Isolation and Characterization of Anaerobic Bacteria for Symbiotic Recycling of Uric Acid Nitrogen in the Gut of Various Termites
journal, January 2012
- Thong-On, Arunee; Suzuki, Katsuyuki; Noda, Satoko
- Microbes and Environments, Vol. 27, Issue 2
Portrait of the Expansin Superfamily in Physcomitrella patens: Comparisons with Angiosperm Expansins
journal, April 2007
- Carey, Robert E.; Cosgrove, Daniel J.
- Annals of Botany, Vol. 99, Issue 6
Plant Expansins in Bacteria and Fungi: Evolution by Horizontal Gene Transfer and Independent Domain Fusion
journal, October 2013
- Nikolaidis, Nikolas; Doran, Nicole; Cosgrove, Daniel J.
- Molecular Biology and Evolution, Vol. 31, Issue 2
INVITED REVIEW: Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea
journal, May 2006
- Johannesson, Kerstin; AndrÉ, Carl
- Molecular Ecology, Vol. 15, Issue 8
Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants
journal, May 2016
- Shabat, Sheerli Kruger Ben; Sasson, Goor; Doron-Faigenboim, Adi
- The ISME Journal, Vol. 10, Issue 12
Plant-like bacterial expansins play contrasting roles in two tomato vascular pathogens: Bacterial expansins modify plant interactions
journal, December 2017
- Tancos, Matthew A.; Lowe-Power, Tiffany M.; Peritore-Galve, F. Christopher
- Molecular Plant Pathology, Vol. 19, Issue 5
Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes
journal, September 2010
- Danchin, Etienne G. J.; Rosso, Marie-Noëlle; Vieira, Paulo
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 41
Evolution of Plant Pathogenicity in Streptomyces
journal, September 2006
- Loria, Rosemary; Kers, Johan; Joshi, Madhumita
- Annual Review of Phytopathology, Vol. 44, Issue 1
Structural basis for entropy-driven cellulose binding by a type-A cellulose-binding module (CBM) and bacterial expansin
journal, August 2012
- Georgelis, N.; Yennawar, N. H.; Cosgrove, D. J.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 37
Plant expansins: diversity and interactions with plant cell walls
journal, June 2015
- Cosgrove, Daniel J.
- Current Opinion in Plant Biology, Vol. 25
XSEDE: Accelerating Scientific Discovery
journal, September 2014
- Towns, John; Cockerill, Timothy; Dahan, Maytal
- Computing in Science & Engineering, Vol. 16, Issue 5
Catalysts of plant cell wall loosening
journal, January 2016
- Cosgrove, Daniel J.
- F1000Research, Vol. 5
The evolutionary origin of animal cellulose synthase
journal, February 2004
- Nakashima, Keisuke; Yamada, Lixy; Satou, Yutaka
- Development Genes and Evolution, Vol. 214, Issue 2
Horizontal Gene Acquisitions, Mobile Element Proliferation, and Genome Decay in the Host-Restricted Plant Pathogen Erwinia Tracheiphila
journal, March 2016
- Shapiro, Lori R.; Scully, Erin D.; Straub, Timothy J.
- Genome Biology and Evolution, Vol. 8, Issue 3
dbCAN: a web resource for automated carbohydrate-active enzyme annotation
journal, May 2012
- Yin, Yanbin; Mao, Xizeng; Yang, Jincai
- Nucleic Acids Research, Vol. 40, Issue W1
Fungi in the Marine Environment: Open Questions and Unsolved Problems
journal, March 2019
- Amend, Anthony; Burgaud, Gaetan; Cunliffe, Michael
- mBio, Vol. 10, Issue 2
Subcellular Localization of Expansin mRNA in Xylem Cells
journal, June 2000
- Im, Kyung-Hoan; Cosgrove, Daniel J.; Jones, Alan M.
- Plant Physiology, Vol. 123, Issue 2
Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization
journal, October 2008
- Kerff, F.; Amoroso, A.; Herman, R.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 44
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014
- Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 32, Issue 1
Loosening of plant cell walls by expansins
journal, September 2000
- Cosgrove, Daniel J.
- Nature, Vol. 407, Issue 6802
Transcriptome Profiling of the Green Alga Spirogyra pratensis (Charophyta) Suggests an Ancestral Role for Ethylene in Cell Wall Metabolism, Photosynthesis, and Abiotic Stress Responses
journal, August 2016
- Van de Poel, Bram; Cooper, Endymion D.; Van Der Straeten, Dominique
- Plant Physiology, Vol. 172, Issue 1
Characterization of native crystalline cellulose in the cell walls of Oomycota
journal, September 1997
- Helbert, William; Sugiyama, Junji; Ishihara, Masaru
- Journal of Biotechnology, Vol. 57, Issue 1-3
Cellulose digestion by common Japanese freshwater clam Corbicula japonica
journal, June 2007
- Sakamoto, Kentaro; Touhata, Ken; Yamashita, Michiaki
- Fisheries Science, Vol. 73, Issue 3
Microbial Expansins
journal, September 2017
- Cosgrove, Daniel J.
- Annual Review of Microbiology, Vol. 71, Issue 1
Oomycete Interactions with Plants: Infection Strategies and Resistance Principles
journal, June 2015
- Fawke, Stuart; Doumane, Mehdi; Schornack, Sebastian
- Microbiology and Molecular Biology Reviews, Vol. 79, Issue 3
Xanthomonas campestris expansin-like X domain is a structurally disordered beta-sheet macromolecule capable of synergistically enhancing enzymatic efficiency of cellulose hydrolysis
journal, August 2015
- Junior, Atílio Tomazini; Dolce, Luciano Graciani; de Oliveira Neto, Mario
- Biotechnology Letters, Vol. 37, Issue 12
Cell biology of plant?oomycete interactions
journal, January 2007
- Hardham, Adrienne R.
- Cellular Microbiology, Vol. 9, Issue 1
Cyanophora paradoxa Genome Elucidates Origin of Photosynthesis in Algae and Plants
journal, February 2012
- Price, D. C.; Chan, C. X.; Yoon, H. S.
- Science, Vol. 335, Issue 6070
Crystal structure and activities of EXPB1 (Zea m 1), a beta-expansin and group-1 pollen allergen from maize
journal, September 2006
- Yennawar, N. H.; Li, L. -C.; Dudzinski, D. M.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 40
The Neolithic revolution of bacterial genomes
journal, May 2006
- Mira, Alex; Pushker, Ravindra; Rodríguez-Valera, Francisco
- Trends in Microbiology, Vol. 14, Issue 5
Selaginella moellendorffii has a reduced and highly conserved expansin superfamily with genes more closely related to angiosperms than to bryophytes
journal, January 2013
- Carey, Robert E.; Hepler, Nathan K.; Cosgrove, Daniel J.
- BMC Plant Biology, Vol. 13, Issue 1
Carbohydrate-binding modules: fine-tuning polysaccharide recognition
journal, September 2004
- Boraston, Alisdair B.; Bolam, David N.; Gilbert, Harry J.
- Biochemical Journal, Vol. 382, Issue 3
The timescale of early land plant evolution
journal, February 2018
- Morris, Jennifer L.; Puttick, Mark N.; Clark, James W.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 10
The cellulase encoded by the native plasmid of Clavibacter michiganensis ssp. sepedonicus plays a role in virulence and contains an expansin-like domain
journal, November 2000
- Laine, Marko J.; Haapalainen, Minna; Wahlroos, Tony
- Physiological and Molecular Plant Pathology, Vol. 57, Issue 5
Plant Expansins Are a Complex Multigene Family with an Ancient Evolutionary Origin
journal, February 2002
- Li, Yi; Darley, Catherine P.; Ongaro, Verónica
- Plant Physiology, Vol. 128, Issue 3
The Revised Classification of Eukaryotes
journal, September 2012
- Adl, Sina M.; Simpson, Alastair G. B.; Lane, Christopher E.
- Journal of Eukaryotic Microbiology, Vol. 59, Issue 5
Expression of an Expansin Is Associated with Endosperm Weakening during Tomato Seed Germination
journal, November 2000
- Chen, Feng; Bradford, Kent J.
- Plant Physiology, Vol. 124, Issue 3
Control of the negative IRES trans -acting factor KHSRP by ubiquitination
journal, November 2016
- Kung, Yu-An; Hung, Chuan-Tien; Chien, Kun-Yi
- Nucleic Acids Research, Vol. 45, Issue 1
Bacteremia Due to Cedecea neteri sp. nov
journal, January 1982
- Farmer, J. J.; Sheth, Neela K.; Hudzinski, June A.
- Journal of Clinical Microbiology, Vol. 16, Issue 4
Genome-wide identification of the expansin gene family in tobacco (Nicotiana tabacum)
journal, June 2016
- Ding, Anming; Marowa, Prince; Kong, Yingzhen
- Molecular Genetics and Genomics, Vol. 291, Issue 5
Beyond the Green: Understanding the Evolutionary Puzzle of Plant and Algal Cell Walls
journal, April 2010
- Popper, Zoë A.; Tuohy, Maria G.
- Plant Physiology, Vol. 153, Issue 2
The end of microbiology
journal, June 2018
- Kolter, Roberto; Chimileski, Scott
- Environmental Microbiology, Vol. 20, Issue 6
Rheological Properties and Molecular Structure of Tunicate Cellulose in LiCl/1,3-Dimethyl-2-imidazolidinone
journal, March 2004
- Tamai, Nobutake; Tatsumi, Daisuke; Matsumoto, Takayoshi
- Biomacromolecules, Vol. 5, Issue 2
Host–pathogen warfare at the plant cell wall
journal, August 2009
- Hématy, Kian; Cherk, Candice; Somerville, Shauna
- Current Opinion in Plant Biology, Vol. 12, Issue 4
Mechanisms Employed by Trichoderma Species in the Biological Control of Plant Diseases: The History and Evolution of Current Concepts
journal, January 2003
- Howell, C. R.
- Plant Disease, Vol. 87, Issue 1
Time to re-think fungal ecology? Fungal ecological niches are often prejudged
journal, January 2018
- Selosse, Marc-André; Schneider-Maunoury, Laure; Martos, Florent
- New Phytologist, Vol. 217, Issue 3
Ecology of Actinomycetes
journal, October 1983
- Goodfellow, M.; Williams, S. T.
- Annual Review of Microbiology, Vol. 37, Issue 1
A Drought Resistance-Promoting Microbiome Is Selected by Root System under Desert Farming
journal, October 2012
- Marasco, Ramona; Rolli, Eleonora; Ettoumi, Besma
- PLoS ONE, Vol. 7, Issue 10
Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera
journal, August 2009
- Sgroy, Verónica; Cassán, Fabricio; Masciarelli, Oscar
- Applied Microbiology and Biotechnology, Vol. 85, Issue 2
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
Complete Genome Sequence of Cedecea neteri Strain SSMD04, a Bacterium Isolated from Pickled Mackerel Sashimi
journal, November 2014
- Chan, K. -G.; Tan, K. -H.; Yin, W. -F.
- Genome Announcements, Vol. 2, Issue 6
The NCBI Taxonomy database
journal, December 2011
- Federhen, S.
- Nucleic Acids Research, Vol. 40, Issue D1