Generic placeholder image

Current Topics in Medicinal Chemistry


ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Research Article

DISTATIS: A Promising Framework to Integrate Distance Matrices in Molecular Phylogenetics

Author(s): Guillermin Agüero-Chapin*, Yuliana Jiménez, Aminael Sánchez-Rodríguez*, Reinaldo Molina-Ruiz, Oscar Vivanco and Agostinho Antunes

Volume 21 , Issue 7 , 2021

Published on: 13 January, 2021

Page: [599 - 611] Pages: 13

DOI: 10.2174/1568026621666210113164605

Price: $65


Background: Molecular phylogenetic algorithms frequently disagree with the approaches considering reproductive compatibility and morphological criteria for species delimitation. The question stems if the resulting species boundaries from molecular, reproductive and/or morphological data are definitively not reconcilable; or if the existing phylogenetic methods are not sensitive enough to agree morphological and genetic variation in species delimitation.

Objective: We propose DISTATIS as an integrative framework to combine alignment-based (AB) and alignment-free (AF) distance matrices from ITS2 sequences/structures to shed light whether Gelasinospora and Neurospora are sister but independent genera.

Methods: We aimed at addressing this standing issue by harmonizing genus-specific classification based on their ascospore morphology and ITS2 molecular data. To validate our proposal, three phylogenetic approaches: i) traditional alignment-based, ii) alignment-free and iii) novel distance integrative (DI)-based were comparatively evaluated on a set of Gelasinospora and Neurospora species. All considered species have been extensively characterized at both the morphological and reproductive levels and there are known incongruences between their ascospore morphology and molecular data that hampers genus-specific delimitation.

Results: Traditional AB phylogenetic analyses fail at resolving the Gelasinospora and Neurospora genera into independent monophyletic clades following ascospore morphology criteria. In contrast, AF and DI approaches produced phylogenetic trees that could properly delimit the expected monophyletic clades.

Conclusion: The DI approach outperformed the AF one in the sense that it could also divide the Neurospora species according to their reproduction mode.

Keywords: Alignment-free, ITS2, DISTATIS, Ascospore morphology, Mating strategy, Phylogenetics.

Graphical Abstract
Duminil, J.; Di Michele, M. Plant species delimitation: a comparison of morphological and molecular markers. Plant Biosyst., 2009, 143(3), 528-542.
Woese, C.R.; Fox, G.E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. USA, 1977, 74(11), 5088-5090.
[] [PMID: 270744]
Taylor, J.W.; Jacobson, D.J.; Kroken, S.; Kasuga, T.; Geiser, D.M.; Hibbett, D.S.; Fisher, M.C. Phylogenetic species recognition and species concepts in fungi. Fungal Genet. Biol., 2000, 31(1), 21-32.
[] [PMID: 11118132]
Hebert, P.D.; Cywinska, A.; Ball, S.L.; deWaard, J.R. Biological identifications through DNA barcodes. Proc. Biol. Sci., 2003, 270(1512), 313-321.
[] [PMID: 12614582]
Fišer Pečnikar, Ž.; Buzan, E.V. 20 years since the introduction of DNA barcoding: from theory to application. J. Appl. Genet., 2014, 55(1), 43-52.
[] [PMID: 24203863]
Mishler, B. D. The phylogenetic species concept (sensu Mishler and Theriot): monophyly, apomorphy, and phylogenetic species concepts. Species concepts and phylogenetic theory, a debate, 2000, 1, 119-132.
Flot, J-F.; Blanchot, J.; Charpy, L.; Cruaud, C.; Licuanan, W.Y.; Nakano, Y.; Payri, C.; Tillier, S. Incongruence between morphotypes and genetically delimited species in the coral genus Stylophora: phenotypic plasticity, morphological convergence, morphological stasis or interspecific hybridization? BMC Ecol., 2011, 11(1), 22.
[] [PMID: 21970706]
Dettman, J.R.; Harbinski, F.M.; Taylor, J.W. Ascospore morphology is a poor predictor of the phylogenetic relationships of Neurospora and Gelasinospora. Fungal Genet. Biol., 2001, 34(1), 49-61.
[] [PMID: 11567551]
Rokas, A.; Williams, B.L.; King, N.; Carroll, S.B. Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature, 2003, 425(6960), 798-804.
[] [PMID: 14574403]
de Queiroz, A.; Gatesy, J. The supermatrix approach to systematics. Trends Ecol. Evol., 2007, 22(1), 34-41.
[] [PMID: 17046100]
Bryant, D. A classification of consensus methods for phylogenetics. DIMACS, 2003, 61, 163-184.
Darling, A.E.; Miklós, I.; Ragan, M.A. Dynamics of genome rearrangement in bacterial populations. PLoS Genet., 2008, 4(7), e1000128.
[] [PMID: 18650965]
Zhaxybayeva, O.; Doolittle, W.F. Lateral gene transfer. Curr. Biol., 2011, 21(7), R242-R246.
[] [PMID: 21481756]
Chan, C.X.; Bernard, G.; Poirion, O.; Hogan, J.M.; Ragan, M.A. Inferring phylogenies of evolving sequences without multiple sequence alignment. Sci. Rep., 2014, 4, 6504.
[] [PMID: 25266120]
Bonham-Carter, O.; Steele, J.; Bastola, D. Alignment-free genetic sequence comparisons: a review of recent approaches by word analysis. Brief. Bioinform., 2014, 15(6), 890-905.
[] [PMID: 23904502]
Schultz, J.; Wolf, M. ITS2 sequence-structure analysis in phylogenetics: a how-to manual for molecular systematics. Mol. Phylogenet. Evol., 2009, 52(2), 520-523.
[] [PMID: 19489124]
Koetschan, C.; Förster, F.; Keller, A.; Schleicher, T.; Ruderisch, B.; Schwarz, R.; Müller, T.; Wolf, M.; Schultz, J. The ITS2 Database III-sequences and structures for phylogeny. Nucleic Acids Res., 2010, 38(Database issue)(Suppl. 1), D275-D279.
[] [PMID: 19920122]
Agüero-Chapin, G.; Sánchez-Rodríguez, A.; Hidalgo-Yanes, P.I.; Pérez-Castillo, Y.; Molina-Ruiz, R.; Marchal, K.; Vasconcelos, V.; Antunes, A. An alignment-free approach for eukaryotic ITS2 annotation and phylogenetic inference. PLoS One, 2011, 6(10), e26638.
[] [PMID: 22046320]
Shen, H-B.; Chou, K-C. Ensemble classifier for protein fold pattern recognition. Bioinformatics, 2006, 22(14), 1717-1722.
[] [PMID: 16672258]
Agüero-Chapin, G.; Molina-Ruiz, R.; Maldonado, E.; de la Riva, G.; Sánchez-Rodríguez, A.; Vasconcelos, V.; Antunes, A. Exploring the adenylation domain repertoire of nonribosomal peptide synthetases using an ensemble of sequence-search methods. PLoS One, 2013, 8(7), e65926.
[] [PMID: 23874386]
Abeysundera, M.; Field, C.; Gu, H. Phylogenetic analysis based on spectral methods. Mol. Biol. Evol., 2012, 29(2), 579-597.
[] [PMID: 21880577]
Abeysundera, M.; Kenney, T.; Field, C.; Gu, H. Combining distance matrices on identical taxon sets for multi-gene analysis with singular value decomposition. PLoS One, 2014, 9(4), e94279.
[] [PMID: 24732341]
Abdi, H.; O’Toole, A.J.; Valentin, D.; Edelman, B. In DISTATIS: The analysis of multiple distance matrices. Proceeding of 2005 IEEE Computer Society Conference on Computer Vision and Pattern Recognition (CVPR’05)-Workshops, 2005, pp. 42-42.
Bengtsson-Palme, J.; Ryberg, M.; Hartmann, M.; Branco, S.; Wang, Z.; Godhe, A.; Wit, P.; Sánchez-García, M.; Ebersberger, I.; Sousa, F. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol., 2013, 4(10), 914-919.
Cai, L.; Jeewon, R.; Hyde, K.D. Phylogenetic investigations of Sordariaceae based on multiple gene sequences and morphology. Mycol. Res., 2006, 110(Pt 2), 137-150.
[] [PMID: 16378718]
Pöggeler, S. Phylogenetic relationships between mating-type sequences from homothallic and heterothallic ascomycetes. Curr. Genet., 1999, 36(4), 222-231.
[] [PMID: 10541860]
Fujisawa, T.; Barraclough, T.G. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Syst. Biol., 2013, 62(5), 707-724.
[] [PMID: 23681854]
Tamura, K.; Stecher, G.; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol., 2013, 30(12), 2725-2729.
[] [PMID: 24132122]
Larkin, M.A.; Blackshields, G.; Brown, N.P.; Chenna, R.; McGettigan, P.A.; McWilliam, H.; Valentin, F.; Wallace, I.M.; Wilm, A.; Lopez, R.; Thompson, J.D.; Gibson, T.J.; Higgins, D.G. Clustal W and Clustal X version 2.0. Bioinformatics, 2007, 23(21), 2947-2948.
[] [PMID: 17846036]
Swofford, D. PAUP 4.0: phylogenetic analysis using parsimony; In: Smithsonian Institution USA; , 1998.
Boc, A.; Diallo, A.B.; Makarenkov, V. T-REX T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Res., 2012, 40(Web Server issue), W573-W579.
Zuker, M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 2003, 31(13), 3406-3415.
[] [PMID: 12824337]
Hofacker, I. L.; Fontana, W.; Stadler, P. F.; Bonhoeffer, L. S.; Tacker, M.; Schuster, P. Fast folding and comparison of RNA secondary structures. Monatshefte für Chemie/Chemical Monthly, 1994, 125(2), 167-188.
Lorenz, R.; Bernhart, S.H.; Höner Zu Siederdissen, C.; Tafer, H.; Flamm, C.; Stadler, P.F.; Hofacker, I.L. ViennaRNA Package 2.0. Algorithms Mol. Biol., 2011, 6(1), 26.
[] [PMID: 22115189]
Suzuki, R.; Shimodaira, H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics, 2006, 22(12), 1540-1542.
[] [PMID: 16595560]
Abdi, H. Multivariate analysis. In: Encyclopedia for research methods for the social sciences; Sage: Thousand Oaks, 2003, 699-702.
Abdi, H.; Williams, L.J.; Valentin, D.; Bennani-Dosse, M. STATIS and DISTATIS: optimum multitable principal component analysis and three way metric multidimensional scaling. Wiley Interdiscip. Rev. Comput. Stat., 2012, 4(2), 124-167.
Abdi, H.; Dunlop, J.P.; Williams, L.J. How to compute reliability estimates and display confidence and tolerance intervals for pattern classifiers using the Bootstrap and 3-way multidimensional scaling (DISTATIS). Neuroimage, 2009, 45(1), 89-95.
[] [PMID: 19084072]
Perkins, D.D.; Raju, N.B. Neurospora discreta, a new heterothallic species defined by its crossing behavior. Exp. Mycol., 1986, 10(4), 323-338.
Furuya, K.; Udagawa, S. New species of Gelasinospora and Anixiella. Nippon Kingakkai Kaiho, 1976, 81(2), 226-233.
Dettman, J.R.; Jacobson, D.J.; Taylor, J.W. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution, 2003, 57(12), 2703-2720.
[] [PMID: 14761051]
García, D.; Stchigel, A.M.; Cano, J.; Guarro, J.; Hawksworth, D.L. A synopsis and re-circumscription of Neurospora (syn. Gelasinospora) based on ultrastructural and 28S rDNA sequence data. Mycol. Res., 2004, 108(Pt 10), 1119-1142.
[] [PMID: 15535064]
Schwarz, R.F.; Fletcher, W.; Förster, F.; Merget, B.; Wolf, M.; Schultz, J.; Markowetz, F. Evolutionary distances in the twilight zone a rational kernel approach. PLoS One, 2010, 5(12), e15788.
[] [PMID: 21209825]
Li, W.; Fang, W.; Ling, L.; Wang, J.; Xuan, Z.; Chen, R. Phylogeny based on whole genome as inferred from complete information set analysis. J. Biol. Phys., 2002, 28(3), 439-447.
[] [PMID: 23345787]
Jun, S-R.; Sims, G.E.; Wu, G.A.; Kim, S-H. Whole-proteome phylogeny of prokaryotes by feature frequency profiles: an alignment-free method with optimal feature resolution. Proc. Natl. Acad. Sci. USA, 2010, 107(1), 133-138.
[] [PMID: 20018669]
Qi, J.; Luo, H.; Hao, B. CVTree: A phylogenetic tree reconstruction tool based on whole genomes. Nucleic Acids Res., 2004, 32(Web Server issue), W45-7.
Miller, A.N.; Huhndorf, S.M. Multi-gene phylogenies indicate ascomal wall morphology is a better predictor of phylogenetic relationships than ascospore morphology in the Sordariales (Ascomycota, Fungi). Mol. Phylogenet. Evol., 2005, 35(1), 60-75.
[] [PMID: 15737582]
Nygren, K.; Strandberg, R.; Wallberg, A.; Nabholz, B.; Gustafsson, T.; García, D.; Cano, J.; Guarro, J.; Johannesson, H. A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Mol. Phylogenet. Evol., 2011, 59(3), 649-663.
[] [PMID: 21439389]
Thioulouse, J.; Simier, M.; Chessel, D. Simultaneous analysis of a sequence of paired ecological tables. Ecology, 2004, 85(1), 272-283.
Thioulouse, J. Simultaneous analysis of a sequence of paired ecological tables: A comparison of several methods. Ann. Appl. Stat., 2011, 2011(4), 2300-2325.
Shinkareva, S.V.; Ombao, H.C.; Sutton, B.P.; Mohanty, A.; Miller, G.A. Classification of functional brain images with a spatio-temporal dissimilarity map. Neuroimage, 2006, 33(1), 63-71.
[] [PMID: 16908198]
Shinkareva, S.V.; Mason, R.A.; Malave, V.L.; Wang, W.; Mitchell, T.M.; Just, M.A. Using FMRI brain activation to identify cognitive states associated with perception of tools and dwellings. PLoS One, 2008, 3(1), e1394.
[] [PMID: 18167553]
Arcidiacono, C.; Sarnacchiaro, P.; Velleman, R. Testing fidelity to a new psychological intervention for family members of substance misusers during implementation in Italy. J. Subst. Use, 2008, 13(6), 361-381.
Guebel, D.V.; Cánovas, M.; Torres, N.V. Model identification in presence of incomplete information by generalized principal component analysis: application to the common and differential responses of Escherichia coli to multiple pulse perturbations in continuous, high-biomass density culture. Biotechnol. Bioeng., 2009, 104(4), 785-795.
[] [PMID: 19603428]
Márquez, E.J.; Knowles, L.L. Correlated evolution of multivariate traits: detecting co-divergence across multiple dimensions. J. Evol. Biol., 2007, 20(6), 2334-2348.
[] [PMID: 17956395]
Perkins, D.D.; Turner, B.C. Neurospora from natural populations: toward the population biology of a haploid eukaryote. Exp. Mycol., 1988, 12(2), 91-131.
Turner, B.C.; Perkins, D.D.; Fairfield, A. Neurospora from natural populations: a global study. Fungal Genet. Biol., 2001, 32(2), 67-92.
[] [PMID: 11352529]

Rights & Permissions Print Export Cite as
© 2022 Bentham Science Publishers | Privacy Policy