Abstract
Pectin lyases (PNLs) are important enzymes that are involved in plant cell wall degradation during the infection process. Colletotrichum is a diverse genus of fungi, which allows the study of the evolution of PNLs and their possible role in pathogen–host interactions and lifestyle adaptations. The phylogenetic reconstruction of PNLs from Colletotrichum and analysis of selection pressures showed the formation of protein lineages by groups of species with different selection pressures and specific patterns. The analysis of positive selection at individual sites using different methods allowed for the identification of three codons with evidence of positive selection in the oligosaccharide-binding region and two codons on the antiparallel sheet, which may influence the interaction with the substrate. Seven codons on the surface of the protein, mainly in the peripheral helices of the PNLs, could have an important function in evasion of plant defenses, as has been proposed in other enzymes. According to our results, it is possible that events of genetic duplication occurred in ancestral lines, followed by episodes of genetic diversification and gene loss, probably influenced by differences in the composition of the host cell wall. Additionally, different patterns of evolution in Colletotrichum appear to be molded by a strong purifying selection and positive selection episodes that forged the observed evolutionary patterns, possibly influenced by host interaction or substrate specificity. This work represents a starting point for the study of sites that may be important for evasion of plant defenses and biotechnological purposes.
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References
Aguileta G, Refrégier G, Yockteng R et al (2009) Rapidly evolving genes in pathogens: methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Infect Genet Evol 9:656–670. doi:10.1016/j.meegid.2009.03.010
Aguileta G, Lengelle J, Chiapello H et al (2012) Genes under positive selection in a model plant pathogenic fungus, Botrytis. Infect Genet Evol 12:987–996. doi:10.1016/j.meegid.2012.02.012
Alaña A, Gabilondo A, Hernando F (1989) Pectin lyase production by a Penicillium italicum strain. Appl Environ Microbiol 55:1612–1616
Albersheim P, Anderson AJ (1971) Proteins from plant cell walls inhibit polygalacturonases secreted by plant pathogens. Proc Natl Acad Sci 68:1815–1819
Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2
Anisimova M, Nielsen R, Yang Z (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229–1236
Annis SL, Goodwin PH (1997) Recent advances in the molecular genetics of plant cell wall-degrading enzymes produced by plant pathogenic fungi. Eur J Plant Pathol 103:1–14. doi:10.1023/A:1008656013255
Arnold K, Bordoil L, Kopp J, Schwede T (2005) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201. doi:10.1093/bioinformatics/bti770
Balestrieri C, Castaldo D, Giovane A et al (1990) A glycoprotein inhibitor of pectin methylesterase in kiwi fruit (Actinidia chinensis). Eur J Biochem 193:183–187
Baroncelli R, Sanz-Martín JM, Rech GE et al (2014a) Draft genome sequence of Colletotrichum sublineola, a destructive pathogen of cultivated Sorghum. Genome Announc 2:e00540–e00514. doi:10.1128/genomeA.00540-14
Baroncelli R, Sreenivasaprasad S, Sukno SA et al (2014b) Draft genome sequence of Colletotrichum acutatum sensu lato (Colletotrichum fioriniae). Genome Announc 2:e00112–e00114. doi:10.1128/genomeA.00112-14
Barrus MF (1911) Variation of varieties of beans in their susceptibility to anthracnose. Phytopathology 1:190–195
Bateman A, Coin L, Durbin R et al (2004) The Pfam protein families database. Nucleic Acids Res 32:D138–D141. doi:10.1093/nar/gkh121
Bielawski JP, Yang Z (2003) Maximum likelihood methods for detecting adaptive evolution after gene duplication. J Struct Funct Genom 3:201–212
Bock H, Dongowski G, Gobel H, Krause M (1975) Nachweis der hemmung mikrobieller pektin und pektat lyase durch pftanzeneigene inhibitoren. Nahrung 19:411–416
Brunner PC, Keller N, McDonald BA (2009) Wheat domestication accelerated evolution and triggered positive selection in the beta-xylosidase enzyme of Mycosphaerella graminicola. PLoS ONE 4:e7884. doi:10.1371/journal.pone.0007884
Brunner PC, Torriani SFF, Croll D et al (2013) Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen. Mol Biol Evol 30:1337–1347. doi:10.1093/molbev/mst041
Bugbee WM (1993) A pectin lyase inhibitor protein from cell walls of sugar beet. Phytopathology 83:63–68
Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum - current status and future directions. Stud Mycol 73:181–213. doi:10.3114/sim0014
Cettul E, Rekab D, Locci R, Firrao G (2008) Evolutionary analysis of endopolygalacturonase-encoding genes of Botrytis cinerea. Mol Plant Pathol 9:675–685. doi:10.1111/j.1364-3703.2008.00492.x
Cooper JA (1983) The mechanisms and significance of enzymic degradation of host cell walls by parasites. In: Callow JA (ed) Biochemical plant pathology. Wiley, Chichester, pp 101–137
Cornell MJ, Alam I, Soanes DM et al (2007) Comparative genome analysis across a kingdom of eukaryotic organisms: specialization and diversification in the fungi. Genome Res 17:1809–1822. doi:10.1101/gr.6531807
Crouch J, O’Connell R, Gan P et al (2014) The genomics of Colletotrichum. In: Genomics of plant-associated fungi: monocot pathogens. Springer, Berlin, pp 69–102
D’Ovidio R, Raiola A, Capodicasa C et al (2004) Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects. Plant Physiol 135:2424–2435. doi:10.1104/pp.104.044644
Damm U, Woudenberg JHC, Cannon PF, Crous PW (2009) Colletotrichum species with curved conidia from herbaceous hosts. Fungal Divers 39:45–87
De Lorenzo G, D’Ovidio R, Cervone F (2001) The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi. Annu Rev Phytopathol 39:313–335. doi:10.1146/annurev.phyto.39.1.313
Dean R, van Kan JAL, Pretorius ZA et al (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. doi:10.1111/j.1364-3703.2011.00783.x
Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455–2457. doi:10.1093/bioinformatics/btq429
Demuth JP, Hahn MW (2009) The life and death of gene families. Bioessays 31:29–39. doi:10.1002/bies.080085
DePristo MA, Weinreich DM, Hartl DL (2005) Missense meanderings in sequence space: a biophysical view of protein evolution. Nat Rev Genet 6:678–687. doi:10.1038/nrg1672
Dornez E, Croes E, Gebruers K et al (2010) Accumulated evidence substantiates a role for three classes of wheat xylanase inhibitors in plant defense. Crit Rev Plant Sci 29:244–264. doi:10.1080/07352689.2010.487780
Federici L, Caprari C, Mattei B et al (2001) Structural requirements of endopolygalacturonase for the interaction with PGIP (polygalacturonase-inhibiting protein). Proc Natl Acad Sci 98:13425–13430. doi:10.1073/pnas.231473698
Federici L, Di Matteo A, Fernandez-Recio J et al (2006) Polygalacturonase inhibiting proteins: players in plant innate immunity? Trends Plant Sci 11:65–70. doi:10.1016/j.tplants.2005.12.005
Fierens E, Rombouts S, Gebruers K et al (2007) TLXI, a novel type of xylanase inhibitor from wheat (Triticum aestivum) belonging to the thaumatin family. Biochem J 403:583–591. doi:10.1042/BJ20061291
Gan P, Ikeda K, Irieda H et al (2013) Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytol 197:1236–1249. doi:10.1111/nph.12085
Gan P, Kumakura N, Narusaka M et al (2016) Genus-wide comparative genome analyses of Colletotrichum species reveal specific gene family losses and gains during adaptation to specific infection lifestyles. Genome Biol Evol 8:1467–1481. doi:10.1093/gbe/evw089
Gebruers K, Debyser W, Goesaert H et al (2001) Triticum aestivum L. endoxylanase inhibitor (TAXI) consists of two inhibitors, TAXI I and TAXI II, with different specificities. Biochem J 353:239–244
Helder P, Uma M, Martin U et al (2016) PhytoPath: an integrative resource for plant pathogen genomics. Nucleic Acids Res 44:D688–D693. doi:10.1093/nar/gkv1052
Herron SR, Benen J, Scavetta RD et al (2000) Structure and function of pectic enzymes: virulence factors of plant pathogens. Proc Natl Acad Sci 97:8762–8769
Herron SR, Scavetta RD, Garrett M et al (2003) Characterization and implications of Ca2+ binding to pectate lyase C. J Biol Chem 278:12271–12277. doi:10.1074/jbc.M209306200
Hiruma K, Gerlach N, Sacristán S et al (2016) Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165:464–474. doi:10.1016/j.cell.2016.02.028
Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14:33-8-27–33-8-28
Isshiki A, Akimitsu K, Yamamoto M, Yamamoto H (2001) Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata. Mol Plant Microbe Interact 14:749–757. doi:10.1094/MPMI.2001.14.6.749
Kim H, Ahn J-H, Görlach JM et al (2001) Mutational analysis of β-glucanase genes from the plant-pathogenic fungus Cochliobolus carbonum. Mol Plant Microbe Interact 14:1436–1443. doi:10.1094/MPMI.2001.14.12.1436
Lamb B (2003) Meiotic recombination in fungi: mechanisms and controls of crossing-over and gene conversion. In: Arora DK, Khachatourians GG (eds) Fungal genomics. Elsevier, Amsterdam, pp 15–41
Leckie F, Mattei B, Capodicasa C et al (1999) The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed β-strand/β-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J 18:2352–2363. doi:10.1093/emboj/18.9.2352
Lenné JM (2001) Some major plant diseases. In: Plant pathologist’s pocketbook, 3rd edn. CABI, Wallingford, pp 4–18
Lo Presti L, Lanver D, Schweizer G et al (2015) Fungal effectors and plant susceptibility. Annu Rev Plant Biol 66:513–545. doi:10.1146/annurev-arplant-043014-114623
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155
MacColl ADC (2011) The ecological causes of evolution. Trends Ecol Evol 26:514–522. doi:10.1016/j.tree.2011.06.009
Marcelino J, Giordano R, Gouli S et al (2008) Colletotrichum acutatum var. fioriniae (teleomorph: Glomerella acutata var. fioriniae var. nov.) infection of a scale insect. Mycologia 100:353–374
Martin U, Alayne C, Rutherford K et al (2017) PHI-base: a new interface and further additions for the multi-species pathogen–host interactions database. Nucl Acids Res 45:D604–D610. doi:10.1093/nar/gkw1089
Mayans O, Scott M, Connerton I et al (1997) Two crystal structures of pectin lyase a from Aspergillus reveal a pH driven conformational change and striking divergence in the substrate-binding clefts of pectin and pectate lyases. Structure 5:677–689
Murrell B, Wertheim JO, Moola S et al (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764. doi:10.1371/journal.pgen.1002764
Murrell B, Weaver S, Smith MD et al (2015) Gene-wide identification of episodic selection. Mol Biol Evol 32:1365–1371. doi:10.1093/molbev/msv035
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Nuss L, Mahé A, Clark AJ et al (1996) Differential accumulation of PGIP (polygalacturonase-inhibiting protein) mRNA in two near-isogenic lines of Phaseolus vulgaris L. upon infection with Colletotrichum lindemuthianum. Physiol Mol Plant Pathol 48:83–89. doi:10.1006/pmpp.1996.0008
O’Connell RJ, Thon MR, Hacquard S et al (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44:1060–1065. doi:10.1038/ng.2372
Perfect SE, Hughes HB, O’Connell RJ, Green JR (1999) Colletotrichum: a model genus for studies on pathology and fungal-plant interactions. Fungal Genet Biol 27:186–198. doi:10.1006/fgbi.1999.1143
Pollet A, Sansen S, Raedschelders G et al (2009) Identification of structural determinants for inhibition strength and specificity of wheat xylanase inhibitors TAXI-IA and TAXI-IIA. FEBS J 276:3916–3927. doi:10.1111/j.1742-4658.2009.07105.x
Pond SK, Pond SK, Muse SV (2005a) Site-to-site variation of synonymous substitution rates. Mol Biol Evol 22:2375–2385. doi:10.1093/molbev/msi232
Pond SLK, Pond SLK, Frost SDW, Frost SDW (2005b) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208–1222. doi:10.1093/molbev/msi105
Pond SLK, Pond SLK, Frost SDW, Frost SDW (2005c) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533. doi:10.1093/bioinformatics/bti320
Pond SLK, Frost SDW, Grossman Z et al (2006a) Adaptation to different human populations by HIV-1 revealed by codon-based analyses. PLoS Comp Biol 2:e62. doi:10.1371/journal.pcbi.0020062
Pond SLK, Posada D, Gravenor MB et al (2006b) GARD: a genetic algorithm for recombination detection. Bioinformatics 22:3096–3098. doi:10.1093/bioinformatics/btl474
Pond SLK, Posada D, Gravenor MB et al (2006c) Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23:1891–1901. doi:10.1093/molbev/msl051
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. doi:10.1093/molbev/msn083
Powell AJ, Conant GC, Brown DE et al (2008) Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens. BMC Genom 9:147. doi:10.1186/1471-2164-9-147
Prusky D (1996) Pathogen quiescence in postharvest diseases. Annu Rev Phytopathol 34:413–434. doi:10.1146/annurev.phyto.34.1.413
Raiola A, Lionetti V, Elmaghraby I et al (2011) Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant Microbe Interact 24:432–440. doi:10.1094/MPMI-07-10-0157
Robinson O, Dylus D, Dessimoz C (2016) Phylo.io: interactive viewing and comparison of large phylogenetic trees on the web. Mol Biol Evol 33:2163–2166. doi:10.1093/molbev/msw080
Romero PA, Arnold FH (2009) Exploring protein fitness landscapes by directed evolution. Nat Rev Mol Cell Biol 10:866–876. doi:10.1038/nrm2805
Ronquist F, Teslenko M, van der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029
Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5:725–738. doi:10.1038/nprot.2010.5
Sánchez-Torres P, Visser J, Benen JAE (2003) Identification of amino acid residues critical for catalysis and stability in Aspergillus niger family 1 pectin lyase A. Biochem J 370:331–337. doi:10.1042/BJ20021071
Shriner D, Nickle DC, Jensen MA, Mullins JI (2003) Potential impact of recombination on sitewise approaches for detecting positive natural selection. Genet Res 81:115–121
Silvestro D, Michalak I (2011) raxmlGUI: a graphical front-end for RAxML. Org Diver Evol 12:335–337. doi:10.1007/s13127-011-0056-0
Soanes DM, Alam I, Cornell M et al (2008) Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS ONE 3:e2300. doi:10.1371/journal.pone.0002300
Solovyev V, Kosarev P, Seledsov I, Vorobyev D (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol. doi:10.1186/gb-2006-7-s1-s10
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. doi:10.1093/bioinformatics/btu033
Stanke M, Morgenstern B (2005) AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucl Acids Res 33:W465–W467. doi:10.1093/nar/gki458
Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197
Tokuriki N, Stricher F, Serrano L, Tawfik DS (2008) How protein stability and new functions trade off. PLoS Comp Biol 4:e1000002. doi:10.1371/journal.pcbi.1000002
Vitali J, Schick B, Kester HC et al (1998) The tree-dimensional structure of Aspergillus niger pectin lyase B at 1.7-A resolution. Plant Physiol 116:69–80
Walton J (1994) Deconstructing the cell wall. Plant Physiol 104:1113–1118
Wang Y-T, Lo H-S, Wang P-H (2008) Endophytic fungi from taxus mairei in Taiwan: first report of Colletotrichum gloeosporioides as an endophyte of Taxus mairei. Bot Stud 39:39–43
Wapinski I, Pfeffer A, Friedman N, Regev A (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449:54–61. doi:10.1038/nature06107
Xu B, Yang Z (2013) PAMLX: a graphical user interface for PAML. Mol Biol Evol 30:2723–2724. doi:10.1093/molbev/mst179
Xu D, Zhang Y (2011) Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophys J 101:2525–2534. doi:10.1016/j.bpj.2011.10.024
Yang Z, Nielsen R, Goldman N, Pedersen A-MK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449. doi:10.1016/S0378-1119(99)00294-2
Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118. doi:10.1093/molbev/msi097
Zhao Z, Liu H, Wang C, Xu J-R (2013) Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genom 14:274. doi:10.1186/1471-2164-14-274
Acknowledgements
The authors thank the financial support provided by Secretaría de Educación Pública-Consejo Nacional de Ciencia y Tecnología (SEP-CONACyT), México (project 2012-01-182755 to María G. Zavala-Páramo); Coordinación de la Investigación, Universidad Michoacana de San Nicolás de Hidalgo (project 2014–2015 to Horacio Cano-Camacho); Universidad Nacional Autónoma de México (for post-doctoral fellowship program 2012–14 granted to Alicia Lara-Márquez); and Consejo Nacional de Ciencia y Tecnología, México (for scholarship number 209148 granted to Ulises Conejo-Saucedo and scholarship number 233565 granted to Maria G. Villa-Rivera).
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Lara-Márquez, A., Oyama, K., Zavala-Páramo, M.G. et al. Evolutionary Analysis of Pectin Lyases of the Genus Colletotrichum . J Mol Evol 85, 120–136 (2017). https://doi.org/10.1007/s00239-017-9812-x
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DOI: https://doi.org/10.1007/s00239-017-9812-x