Saprophytic and pathogenic fungi in the Ceratocystidaceae differ in their ability to metabolize plant-derived sucrose

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dc.contributor.author Van der Nest, Magrieta Aletta
dc.contributor.author Steenkamp, Emma Theodora
dc.contributor.author McTaggart, Alistair R.
dc.contributor.author Trollip, C.
dc.contributor.author Godlonton, T.
dc.contributor.author Sauerman, E.
dc.contributor.author Roodt, Danielle
dc.contributor.author Naidoo, Kershney
dc.contributor.author Coetzee, Martin Petrus Albertus
dc.contributor.author Wilken, P. Markus
dc.contributor.author Wingfield, Michael J.
dc.contributor.author Wingfield, Brenda D.
dc.date.accessioned 2016-02-18T07:08:54Z
dc.date.available 2016-02-18T07:08:54Z
dc.date.issued 2015-12-07
dc.description Additional file 1: Table S1. Genomic location, Protein ID and GenBank accession numbers for the sequences used in the present study. (DOC 67 kb) en_ZA
dc.description Additional file 2: Figure S1. The chronogram was inferred using published calibration time points (see text for detail) and a Bayesian strict clock approach as implemented in BEAST (Bayesian evolutionary analysis by sampling trees) v.2 package v.2.2.1 [46]. Horizontal bars mark the lower and upper time boundaries of the indicated mean age (Million years ago) estimates of the nodes. The black arrows indicate the four calibration points, which include the Dothideomycetes crown group (mean 350 Million years ago [Mya] with 95 % credibility interval [CI] of 273–459) [50], the last common ancestor (LCA) of the Hypocreales (181 Mya with 95 % CI of 150–213) [51], the Clavicipitaceae crown group (117 Mya with 95 % CI of 95–144) [51], as well the Nectriaceae crown group (125 Mya with 95 % CI of 98–155) [52]. (PDF 227 kb) en_ZA
dc.description Additional file 3: Table S2. List of the putative Fot5 homologs identified in this study. (DOC 160 kb) en_ZA
dc.description Additional file 4: Figure S2. Maximum likelihood tree of the Fot5 DDD catalytic domain. This analysis was done using the WAG substitution model [49] and gamma correction to account for among site rate variation. Percentage bootstrap support (based on a 1000 repeats, with cut-off value of 50 %) is indicated at the internodes. Genomic coordinates of putative Ceratocystis Fot5 homologs are provided in Additional file 3: Table S2. GenBank accession numbers or sequence identifiers for previously identified Fot5 homologs are: Fot2 [Genbank:JN624854, F. oxysporum), Fot5 [Genbank:CAE55867, F. oxysporum], Fot1 [Genbank: X64799, F. oxysporum], Fot4 [Genbank:AF076632, F. oxysporum], Fot9 [JGI:2517, F. graminearum], Fotyl [Genbank:CAG33729.1 Yarrowia lipolytica], Molly [Genbank:CAD32687, Parastagonospora nodorum], Ophio [Genbank:ABG26269, Ophiostoma novo-ulmi], PABRA [Genbank:- ACY56713, Paracoccidioides brasiliensis], Pixie [Genbank:CAD32689, Parastagonospora nodorum], Pot2 [Genbank:CAA83918, Magnaporthe grisea], Pot3 [Genbank:AAC49418, M. grisea], SCSCL [Genbank: XP001592252, Sclerotinia sclerotiorum], Taf1 [Genbank:AAX83011, Aspergillus fumigatus], Tan1 [Genbank:U58946, Aspergillus awamori] USMA [Genbank:UM03882, Ustilago maydis), Flipper [Genbank: AAB63315, Botryotinia fuckeliana] and Cirt1 [Genbank:XP710204, Candida albicans]. For the Ceratocystis sequences JS = Ceratocystis albifundus (green dots), J = Ceratocystis manginecans (red dots) and A = Ceratocystis fimbriata (blue dots), followed by the genomic position. (PDF 59 kb) en_ZA
dc.description.abstract BACKGROUND : Proteins in the Glycoside Hydrolase family 32 (GH32) are carbohydrate-active enzymes known as invertases that hydrolyse the glycosidic bonds of complex saccharides. Fungi rely on these enzymes to gain access to and utilize plant-derived sucrose. In fungi, GH32 invertase genes are found in higher copy numbers in the genomes of pathogens when compared to closely related saprophytes, suggesting an association between invertases and ecological strategy. The aim of this study was to investigate the distribution and evolution of GH32 invertases in the Ceratocystidaceae using a comparative genomics approach. This fungal family provides an interesting model to study the evolution of these genes, because it includes economically important pathogenic species such as Ceratocystis fimbriata, C. manginecans and C. albifundus, as well as saprophytic species such as Huntiella moniliformis, H. omanensis and H. savannae. RESULTS : The publicly available Ceratocystidaceae genome sequences, as well as the H. savannae genome sequenced here, allowed for the identification of novel GH32-like sequences. The de novo assembly of the H. savannae draft genome consisted of 28.54 megabases that coded for 7 687 putative genes of which one represented a GH32 family member. The number of GH32 gene family members appeared to be related to the ecological adaptations of these fungi. The pathogenic Ceratocystis species all contained two GH32 family genes (a putative cell wall and a putative vacuolar invertase), while the saprophytic Huntiella species had only one of these genes (a putative cell wall invertase). Further analysis showed that the evolution of the GH32 gene family in the Ceratocystidaceae involved transposable element-based retro-transposition and translocation. As an example, the activity of a Fot5-like element likely facilitated the assembly of the genomic regions harbouring the GH32 family genes in Ceratocystis. CONCLUSIONS : This study provides insight into the evolutionary history of the GH32 gene family in Ceratocystidaceae. Our findings suggest that transposable elements shaped the evolution of the GH32 gene family, which in turn determines the sucrolytic activities and related ecological strategies of the Ceratocystidaceae species that harbour them. The study also provides insights into the role of carbohydrate-active enzymes in plant-fungal interactions and adds to our understanding of the evolution of these enzymes and their role in the life style of these fungi. en_ZA
dc.description.librarian am2015 en_ZA
dc.description.sponsorship Members of the Tree Protection Cooperative Program (TPCP), the Department of Science and Technology (DST)-National Research Foundation (NRF) Centre of Excellence in Tree Health Biotechnology and the Genomics Research Institute of the University of Pretoria. en_ZA
dc.description.uri http://www.biomedcentral.com/bmcevolbiol en_ZA
dc.identifier.citation Van der Nest, MA, Steenkamp, ET, McTaggart, AR, Trollip, C, Godlonton, T, Sauerman, E, Roodt, D, Naidoo, K, Coetzee, MPA, Wilken, PM, Wingfield, MJ & Wingfield, BD2015, ‘Saprophytic and pathogenic fungi in the Ceratocystidaceae differ in their ability to metabolize plant-derived sucrose', BMC Evolutionary Biology, vol. 15, art. no. 273, pp. 1-20. en_ZA
dc.identifier.issn 1471-2148
dc.identifier.other 10.1186/s12862-015-0550-7
dc.identifier.uri http://hdl.handle.net/2263/51435
dc.language.iso en en_ZA
dc.publisher BioMed Central en_ZA
dc.rights © 2015 Van der Nest et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License. en_ZA
dc.subject Ceratocystis en_ZA
dc.subject Huntiella en_ZA
dc.subject Vacuolar invertases en_ZA
dc.subject Cell wall invertases en_ZA
dc.subject Sucrolytic ability en_ZA
dc.subject Gene family evolution en_ZA
dc.subject Molecular dating en_ZA
dc.subject Transposable elements en_ZA
dc.subject Paralog en_ZA
dc.subject Glycoside Hydrolase family 32 (GH32) en_ZA
dc.title Saprophytic and pathogenic fungi in the Ceratocystidaceae differ in their ability to metabolize plant-derived sucrose en_ZA
dc.type Article en_ZA


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