Carbohydrate-related enzymes of important Phytophthora plant pathogens

Fungal Genetics and Biology

Volumn 72, Issue , 2014, Pages 192-200

  Brouwer, Henk ^a,e   Coutinho, Pedro M ^b   Henrissat, Bernard ^b,c   de Vries, Ronald P ^a,d  

^a CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

^b AIX MARSEILLE UNIVERSITY   (France)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^d UTRECHT UNIVERSITY   (Netherlands)

^e CTGB ^*  (Netherlands)

Author keywords

Carbohydrate related enzymes; Carbon source utilization; Growth profiling; Phytophthora; Pythium

Indexed keywords

BETA 1,3 GLUCAN; CARBOHYDRATE ACTIVE ENZYME; CARBON; CELLULOSE; CUTINASE; FUNGAL ENZYME; GALACTURONIC ACID; GLUCAN GLUCOSIDASE; GLUCOSE; GUAR GUM; MANNOSE; PECTIN; STARCH; UNCLASSIFIED DRUG; XYLAN; XYLAN ENDO 1,3 BETA XYLOSIDASE; XYLOGLUCANASE; CULTURE MEDIUM; GLYCOSIDASE;

ARTICLE; CARBOHYDRATE METABOLISM; CARBON SOURCE; ENZYME ANALYSIS; ENZYME DEGRADATION; FUNGAL CELL WALL; FUNGAL GENOME; FUNGUS GROWTH; NONHUMAN; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS; PHYTOPHTHORA RAMORUM; PHYTOPHTHORA SOJAE; PLANT DISEASE; PREDICTION; PROTEIN FAMILY; PYTHIUM ULTIMUM; SACCHARIFICATION; BIOLOGY; CHEMISTRY; COMPARATIVE STUDY; CULTURE MEDIUM; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PYTHIUM;

CARBON; COMPUTATIONAL BIOLOGY; CULTURE MEDIA; GENOME, FUNGAL; GLYCOSIDE HYDROLASES; PHYTOPHTHORA; PYTHIUM;

EID: 84908509725     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2014.08.011     Document Type: Article

References (71)

1. Adhikari B.N., Hamilton J.P., Zerillo M.M., Tisserat N., Lévesque C.A., Buell C.R. Comparative genomics reveals insight into virulence strategies of plant pathogenic oomycetes. PLoS One 2013, 8:e75072.
2. Aspeborg H., Coutinho P.M., Wang Y., Brumer H., Henrissat B. Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol. Biol. 2012, 12:186.
3. Bartnicki-Garcia S. Cell wall chemistry, morphogenesis, and taxonomy of fungi. Ann. Rev. Microbiol. 1968, 22:87-108.
4. Baxter L., Tripathy S., Ishaque N., Boot N., Cabral A., Kemen E., Thines M., Ah-Fong A., Anderson R., Badejoko W., Bittner-Eddy P., Boore J.L., Chibucos M.C., Coates M., Dehal P., Delehaunty K., Dong S., Downton P., Dumas B., Fabro G., Fronick C., Fuerstenberg S.I., Fulton L., Gaulin E., Govers F., Hughes L., Humphray S., Jiang R.H.Y., Judelson H., Kamoun S., Kyung K., Meijer H., Minx P., Morris P., Nelson J., Phuntumart V., Qutob D., Rehmany A., Rougon-Cardoso A., Ryden P., Torto-Alalibo T., Studholme D., Wang Y., Win J., Wood J., Clifton S.W., Rogers J., den Ackerveken G.V., Jones J.D.G., McDowell J.M., Beynon J., Tyler B.M. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 2010, 330:1549-1551.
5. Beakes G.W., Glockling S.L., Sekimoto S. The evolutionary phylogeny of the oomycete "fungi". Protoplasma 2012, 249:3-19.
6. Belbahri L., Calmin G., Mauch F., Andersson J.O. Evolution of the cutinase gene family: evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene 2008, 408:1-8.
7. Berka R.M., Grigoriev I.V., Otillar R., Salamov A., Grimwood J., Reid I., Ishmael N., John T., Darmond C., Moisan M.-C., Henrissat B., Coutinho P.M., Lombard V., Natvig D.O., Lindquist E., Schmutz J., Lucas S., Harris P., Powlowski J., Bellemare A., Taylor D., Butler G., de Vries R.P., Allijn I.E., van den Brink J., Ushinsky S., Storms R., Powell A.J., Paulsen I.T., Elbourne L.D.H., Baker S.E., Magnuson J., Laboissiere S., Clutterbuck A.J., Martinez D., Wogulis M., de Leon A.L., Rey M.W., Tsang A. Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Nat. Biotechnol. 2011, 29:922-927.
8. Bernards M.A. Demystifying suberin. Can. J. Bot. 2002, 80:227-240.
9. Brasier, C.M., Kirk, S., Rose, J., 2006. Differences in phenotypic stability and adaptive variation between the main European and American lineages of Phytophthora ramorum. In: Progress in Research on Phytophthora Diseases of Forest Trees. Proceedings of the Third International IU-FRO Working Party, Forest Research, Farnham UK, pp. 166-173.
10. Brunner F., Wirtz W., Rose J.K.C., Darvill A.G., Govers F., Scheel D., Nürnberger T. A beta-glucosidase/xylosidase from the phytopathogenic oomycete, Phytophthora infestans. Phytochemistry 2002, 59:689-696.
11. Caffall K.H., Mohnen D. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr. Res. 2009, 344:1879-1900.
12. Cantarel B.L., Coutinho P.M., Rancurel C., Bernard T., Lombard V., Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucl. Acids Res. 2009, 37:D233-D238.
13. Cantu D., Vicente A.R., Labavitch J.M., Bennett A.B., Powell A.L.T. Strangers in the matrix: plant cell walls and pathogen susceptibility. Trends Plant Sci. 2008, 13:610-617.
14. Cavalier-Smith T., Chao E.E.-Y. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). J. Mol. Evol. 2006, 62:388-420.
15. Chérif M., Benhamou N., Bélanger R.R. Occurrence of cellulose and chitin in the hyphal walls of Pythium ultimum: a comparative study with other plant pathogenic fungi. Can. J. Microbiol. 1993, 39:213-222.
16. Costanzo S., Ospina-Giraldo M.D., Deahl K.L., Baker C.J., Jones R.W. Gene duplication event in family 12 glycosyl hydrolase from Phytophthora spp. Fung. Genet. Biol. 2006, 43:707-714.
17. Costanzo S., Ospina-Giraldo M.D., Deahl K.L., Baker C.J., Jones R.W. Alternate intron processing of family 5 endoglucanase transcripts from the genus Phytophthora. Curr. Genet. 2007, 52:115-123.
18. Culleton H., McKie V., de Vries R.P. Physiological and molecular aspects of degradation of plant polysaccharides by fungi: what have we learned from Aspergillus?. Biotechnol. J. 2013, 8:884-894.
19. Dantzig A.H., Zuckerman S.H., Andonov-Roland M.M. Isolation of a Fusarium solani mutant reduced in cutinase activity and virulence. J. Bact. 1986, 168:911-916.
20. de Vries R.P., Visser J. Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol. Mol. Biol. Rev. 2001, 65:497-522.
21. Dybdahl M.F., Storfer A. Parasite local adaptation: Red Queen versus Suicide King. Trends Ecol. Evol. 2003, 18:523-530.
22. Erwin D., Ribeiro O.K. Phytophthora Diseases Worldwide 1996, APS Press, St. Paul Minn.
23. Feng B., Li P., Wang H., Zhang X. Functional analysis of pcpme6 from oomycete plant pathogen Phytophthora capsici. Microb. Pathogenesis 2010, 49:23-31.
24. Gams K.W., Hoekstra E.S., Aptroot A. CBS Course of Mycology 1998, Centraalbureau voor Schimmelcultures, Baarn, The Netherlands.
25. Geldner N. The endodermis. Ann. Rev. Plant Biol. 2013, 64:531-558.
26. Goss E.M., Carbone I., Grünwald N.J. Ancient isolation and independent evolution of the three clonal lineages of the exotic sudden oak death pathogen Phytophthora ramorum. Mol. Ecol. 2009, 18:1161-1174.
27. Götesson A., Marshall J.S., Jones D.A., Hardham A.R. Characterization and evolutionary analysis of a large polygalacturonase gene family in the oomycete plant pathogen Phytophthora cinnamomi. Mol. Plant Microbe Interact. 2002, 15:907-921.
28. Grenville-Briggs L.J., Anderson V.L., Fugelstad J., Avrova A.O., Bouzenzana J., Williams A., Wawra S., Whisson S.C., Birch P.R.J., Bulone V., van West P. Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato. Plant Cell Online 2008, 20:720-738.
29. Haas B.J., Kamoun S., Zody M.C., Jiang R.H.Y., Handsaker R.E., Cano L.M., Grabherr M., Kodira C.D., Raffaele S., Torto-Alalibo T., Bozkurt T.O., Ah-Fong A.M.V., Alvarado L., Anderson V.L., Armstrong M.R., Avrova A., Baxter L., Beynon J., Boevink P.C., Bollmann S.R., Bos J.I.B., Bulone V., Cai G., Cakir C., Carrington J.C., Chawner M., Conti L., Costanzo S., Ewan R., Fahlgren N., Fischbach M.A., Fugelstad J., Gilroy E.M., Gnerre S., Green P.J., Grenville-Briggs L.J., Griffith J., Grünwald N.J., Horn K., Horner N.R., Hu C.-H., Huitema E., Jeong D.-H., Jones A.M.E., Jones J.D.G., Jones R.W., Karlsson E.K., Kunjeti S.G., Lamour K., Liu Z., Ma L., MacLean D., Chibucos M.C., McDonald H., McWalters J., Meijer H.J.G., Morgan W., Morris P.F., Munro C.A., O'Neill K., Ospina-Giraldo M., Pinzón A., Pritchard L., Ramsahoye B., Ren Q., Restrepo S., Roy S., Sadanandom A., Savidor A., Schornack S., Schwartz D.C., Schumann U.D., Schwessinger B., Seyer L., Sharpe T., Silvar C., Song J., Studholme D.J., Sykes S., Thines M., van de Vondervoort P.J.I., Phuntumart V., Wawra S., Weide R., Win J., Young C., Zhou S., Fry W., Meyers B.C., van West P., Ristaino J., Govers F., Birch P.R.J., Whisson S.C., Judelson H.S., Nusbaum C. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 2009, 461:393-398.
30. Haldar K., Kamoun S., Hiller N.L., Bhattacharje S., van Ooij C. Common infection strategies of pathogenic eukaryotes. Nat. Rev. Microbiol. 2006, 4:922-931.
31. Hansen E.M. Alien forest pathogens; Phytophthora species are changing world forests. Boreal Environ. Res. 2008, 13:33-41.
32. Jiang R.H.Y., Tyler B.M., Govers F. Comparative analysis of Phytophthora genes encoding secreted proteins reveals conserved synteny and lineage-specific gene duplications and deletions. Mol. Plant Microbe Interact. 2006, 19:1311-1321.
33. Jiang R.H.Y., de Bruijn I., Haas B.J., Belmonte R., Lobach L., Christie J., van den Ackerveken G., Bottin A., Bulone V., Diaz-Moreno S.M., Dumas B., Fan L., Gaulin E., Govers F., Grenville-Briggs L.J., Horner N.R., Levin J.Z., Mammella M., Meijer H.J.G., Morris P., Nusbaum C., Oome S., Phillips A.J., van Rooyen D., Rzeszutek E., Saraiva M., Secombes C.J., Seidl M.F., Snel B., Stassen J.H.M., Sykes S., Tripathy S., van den Berg H., Vega-Arreguin J.C., Wawra S., Young S.K., Zeng Q., Dieguez-Uribeondo J., Russ C., Tyler B.M., van West P. Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica. PLoS Genet. 2013, 9.
34. Judelson H.S., Tani S., Narayan R.D. Metabolic adaptation of Phytophthora infestans during growth on leaves, tubers and artificial media. Mol. Plant Pathol. 2009, 10:843-855.
35. Kamoun S. A catalogue of the effector secretome of plant pathogenic oomycetes. Ann. Rev. Phytopathol. 2006, 44:41-60.
36. Kemen E., Gardiner A., Schultz-Larsen T., Kemen A.C., Balmuth A.L., Robert-Seilaniantz A., Bailey K., Holub E., Studholme D.J., MacLean D., Jones J.D.G. Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol. 2011, 9:e1001094.
37. Kombrink A., Thomma B.P.H.J. LysM effectors: secreted proteins supporting fungal life. PLoS Pathog. 2013, 9:e1003769.
38. Kroon L., Brouwer H., De Cock A.W.A.M., Govers F. The Phytophthora genus anno 2012. Phytopathology 2012, 102:348-364.
39. Lacey J. The infectivity of soils containing Phytophthora infestans. Ann. Appl. Biol. 1965, 56:363-380.
40. Lafond M., Navarro D., Haon M., Couturier M., Berrin J.-G. Characterization of a broad-specificity β-glucanase acting on β-(1,3)-, β-(1,4)-, and β-(1,6)-glucans that defines a new glycoside hydrolase family. Appl. Environ. Microbiol. 2012, 78:8540-8546.
41. Lamour K.H., Mudge J., Gobena D., Hurtado-Gonzales O.P., Schmutz J., Kuo A., Miller N.A., Rice B.J., Raffaele S., Cano L.M., Bharti A.K., Donahoo R.S., Finley S., Huitema E., Hulvey J., Platt D., Salamov A., Savidor A., Sharma R., Stam R., Storey D., Thines M., Win J., Haas B.J., Dinwiddie D.L., Jenkins J., Knight J.R., Affourtit J.P., Han C.S., Chertkov O., Lindquist E.A., Detter C., Grigoriev I.V., Kamoun S., Kingsmore S.F. Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Mol. Plant Microbe Interact. 2012, 25:1350-1360.
42. Lévesque C.A., Brouwer H., Cano L., Hamilton J.P., Holt C., Huitema E., Raffaele S., Robideau G.P., Thines M., Win J., Zerillo M.M., Beakes G.W., Boore J.L., Busam D., Dumas B., Ferriera S., Fuerstenberg S.I., Gachon C.M., Gaulin E., Govers F., Grenville-Briggs L., Horner N., Hostetler J., Jiang R.H., Johnson J., Krajaejun T., Lin H., Meijer H.J., Moore B., Morris P., Phuntmart V., Puiu D., Shetty J., Stajich J.E., Tripathy S., Wawra S., van West P., Whitty B.R., Coutinho P.M., Henrissat B., Martin F., Thomas P.D., Tyler B.M., de Vries R.P., Kamoun S., Yandell M., Tisserat N., Buell C.R. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol. 2010, 11:R73.
43. Li P., Feng B., Wang H., Tooley P.W., Zhang X. Isolation of nine Phytophthora capsici pectin methylesterase genes which are differentially expressed in various plant species. J. Basic Microbiol. 2011, 51:61-70.
44. Links M.G., Holub E., Jiang R.H., Sharpe A.G., Hegedus D., Beynon E., Sillito D., Clarke W.E., Uzuhashi S., Borhan M.H. De novo sequence assembly of Albugo candida reveals a small genome relative to other biotrophic oomycetes. BMC Genom. 2011, 12:503.
45. Lombard V., Golaconda Ramulu H., Drula E., Coutinho P.M., Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucl. Acids Res. 2014, 42:D490-D495.
46. McLeod A., Smart C.D., Fry W.E. Characterization of 1,3-β-glucanase and 1,3;1,4-β-glucanase genes from Phytophthora infestans. Fung. Genet. Biol. 2003, 38:250-263.
47. McNeil M., Darvill A.G., Fry S.C., Albersheim P. Structure and function of the primary cell walls of plants. Ann. Rev. Biochem. 1984, 53:625-663.
48. Ospina-Giraldo M.D., Griffith J.G., Laird E.W., Mingora C. The CAZyome of Phytophthora spp.: a comprehensive analysis of the gene complement coding for carbohydrate-active enzymes in species of the genus Phytophthora. BMC Genom. 2010, 11:525.
49. Ospina-Giraldo M.D., McWalters J., Seyer L. Structural and functional profile of the carbohydrate esterase gene complement in Phytophthora infestans. Curr. Genet. 2010, 56:495-506.
50. Quinn L., O'Neill P.A., Harrison J., Paskiewicz K.H., McCracken A.R., Cooke L.R., Grant M.R., Studholme D.J. Genome-wide sequencing of Phytophthora lateralis reveals genetic variation among isolates from Lawson cypress (Chamaecyparis lawsoniana) in Northern Ireland. FEMS Microbiol. Lett. 2013, 344:179-185.
51. Ridings W.H., Gallegly M.E., Lilly V.G. Thiamine requirements helpful in distinguishing isolates of Pythium from those of Phytophthora. Phytopathology 1969, 59:737-742.
52. Ristaino J.B. Tracking historic migrations of the Irish potato famine pathogen, Phytophthora infestans. Microbes Infect. 2002, 4:1369-1377.
53. Robideau G.P., de Cock A.W.A.M., Coffey M.D., Voglmayr H., Brouwer H., Bala K., Chitty D.W., Desaulniers N., Eggertson Q.A., Gachon C.M.M., Hu C.-H., Kupper F.C., Rintoul T.L., Sarhan E., Verstappen E.C.P., Zhang Y., Bonants P.J.M., Ristaino J.B., Levesque C.A. DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Mol. Ecol. Resour. 2011, 11:1002-1011.
54. Rogers L.M., Kim Y.K., Guo W., González-Candelas L., Li D., Kolattukudy P.E. Requirement for either a host- or pectin-induced pectate lyase for infection of Pisum sativum by Nectria hematococca. Proc. Natl. Acad. Sci. USA 2000, 97:9813-9818.
55. Schmoll M., Kubicek C.P. Regulation of Trichoderma cellulase formation: lessons in molecular biology from an industrial fungus. A review. Acta Microbiol. Immunol. Hungarica 2003, 50:125-145.
56. St.John F.J., González J.M., Pozharski E. Consolidation of glycosyl hydrolase family 30: a dual domain 4/7 hydrolase family consisting of two structurally distinct groups. FEBS Lett. 2010, 584:4435-4441.
57. Sulzenbacher G., Shareck F., Morosoli R., Dupont C., Davies G.J. The Streptomyces lividans family 12 endoglucanase: construction of the catalytic cre, expression, and X-ray structure at 1.75 A resolution. Biochemistry 1997, 36:16032-16039.
58. Thomas R., Fang X., Ranathunge K., Anderson T.R., Peterson C.A., Bernards M.A. Soybean root suberin: anatomical distribution, chemical composition, and relationship to partial resistance to Phytophthora sojae. Plant Physiol. 2007, 144:299-311.
59. Torto T.A., Rauser L., Kamoun S. The pipg1 gene of the oomycete Phytophthora infestans encodes a fungal-like endopolygalacturonase. Curr. Genet. 2002, 40:385-390.
60. Tyler B.M. Phytophthora sojae: root rot pathogen of soybean and model oomycete. Mol. Plant Pathol. 2007, 8:1-8.
61. Tyler B.M., Tripathy S., Zhang X., Dehal P., Jiang R.H.Y., Aerts A., Arredondo F.D., Baxter L., Bensasson D., Beynon J.L., Chapman J., Damasceno C.M.B., Dorrance A.E., Dou D., Dickerman A.W., Dubchak I.L., Garbelotto M., Gijzen M., Gordon S.G., Govers F., Grunwald N.J., Huang W., Ivors K.L., Jones R.W., Kamoun S., Krampis K., Lamour K.H., Lee M.-K., McDonald W.H., Medina M., Meijer H.J.G., Nordberg E.K., Maclean D.J., Ospina-Giraldo M.D., Morris P.F., Phuntumart V., Putnam N.H., Rash S., Rose J.K.C., Sakihama Y., Salamov A.A., Savidor A., Scheuring C.F., Smith B.M., Sobral B.W.S., Terry A., Torto-Alalibo T.A., Win J., Xu Z., Zhang H., Grigoriev I.V., Rokhsar D.S., Boore J.L. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 2006, 313:1261-1266.
62. Van den Brink J., de Vries R.P. Fungal enzyme sets for plant polysaccharide degradation. Appl. Microbiol. Biotechnol. 2011, 91:1477-1492.
63. Van Poucke K., Franceschini S., Webber J.F., Vercauteren A., Turner J.A., McCracken A.R., Heungens K., Brasier C.M. Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2. Fung. Biol. 2012, 116:1178-1191.
64. Wahl R., Wippel K., Goos S., Kämper J., Sauer N. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol. 2010, 8:e1000303.
65. Wang M.C., Bartnicki-Garcia S. Mycolaminarans: storage (1→3)-β-d-glucans from the cytoplasm of the fungus Phytophthora palmivora. Carbohydr. Res. 1974, 37:331-338.
66. Wang H., Fu L., Zhang X. Comparison of expression, purification and characterization of a new pectate lyase from Phytophthora capsici using two different methods. BMC Biotechnol. 2011, 11:32.
67. Werres S., Marwitz R., Man In't Veld W.A., De Cock A.W.A.M., Bonants P.J.M., De Weerdt M., Themann K., Ilieva E., Baayen R.P. Phytophthora ramorum sp. nov., a new pathogen on Rhododendron and Viburnum. Mycol. Res. 2001, 105:1155-1165.
68. Wu C.-H., Yan H.-Z., Liu L.-F., Liou R.-F. Functional characterization of a gene family encoding polygalacturonases in Phytophthora parasitica. Mol. Plant Microbe Interact. 2008, 21:480-489.
69. Yan H.-Z., Liou R.-F. Cloning and analysis of pppg1, an inducible endopolygalacturonase gene from the oomycete plant pathogen Phytophthora parasitica. Fung. Genet. Biol. 2005, 42:339-350.
70. Zerillo M.M., Adhikari B.N., Hamilton J.P., Buell C.R., Lévesque C.A., Tisserat N. Carbohydrate-active enzymes in Pythium and their role in plant cell wall and storage polysaccharide degradation. PLoS One 2013, 8:e72572.
71. Zevenhuizen L.P.T.M., Bartnicki-Garcia S. Structure and role of a soluble cytoplasmic glucan from Phytophthora cinnamomi. J. Gen. Microbiol. 1970, 61:183-188.