The eukaryotic microbes called oomycetes include many important saprophytes and pathogens, with the latter exhibiting necrotrophy, biotrophy, or obligate biotrophy. Understanding oomycete metabolism is fundamental to understanding these lifestyles. Genome mining and biochemical studies have shown that oomycetes, which belong to the kingdom Stramenopila, secrete suites of carbohydrate- and protein-degrading enzymes adapted to their environmental niches and produce unusual lipids and energy storage compounds. Despite having limited secondary metabolism, many oomycetes make chemicals for communicating within their species or with their hosts. Horizontal and endosymbiotic gene transfer events have diversified oomycete metabolism, resulting in biochemical pathways that often depart from standard textbook descriptions by amalgamating enzymes from multiple sources. Gene fusions and duplications have further shaped the composition and expression of the enzymes. Current research is helping us learn how oomycetes interact with host and environment, understand eukaryotic diversity and evolution, and identify targets for drugs and crop protection chemicals.


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Literature Cited

  1. Abrahamian M, Ah-Fong AM, Davis C, Andreeva K, Judelson HS. 1.  2016. Gene expression and silencing studies in Phytophthora infestans reveal infection-specific nutrient transporters and a role for the nitrate reductase pathway in plant pathogenesis. PLOS Pathog 12:e1006097 [Google Scholar]
  2. Adhikari BN, Hamilton JP, Zerillo MM, Tisserat N, Levesque CA, Buell CR. 2.  2013. Comparative genomics reveals insight into virulence strategies of plant pathogenic oomycetes. PLOS ONE 8:e75072 [Google Scholar]
  3. Adl MS, Gupta VVSR. 3.  2006. Protists in soil ecology and forest nutrient cycling. Can. J. For. Res. 36:1805–17 [Google Scholar]
  4. Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR. 4.  et al. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52:399–451 [Google Scholar]
  5. Ah-Fong AMV, Kim KS, Judelson HS. 5.  2017. RNA-seq of life stages of the oomycete Phytophthora infestans reveals dynamic changes in metabolic, signal transduction, and pathogenesis genes and a major role for calcium signaling in development. BMC Genom 18:198 [Google Scholar]
  6. Ahn IP, Kim S, Lee YH. 6.  2005. Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol 138:1505–15 [Google Scholar]
  7. Bakthavatsalam D, Meijer HJG, Noegel AA, Govers F. 7.  2006. Novel phosphatidylinositol phosphate kinases with a G-protein coupled receptor signature are shared by Dictyostelium and Phytophthora. Trends Microbiol. 14:378–82 [Google Scholar]
  8. Ball S, Colleoni C, Cenci U, Raj JN, Tirtiaux C. 8.  2011. The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J. Exp. Bot. 62:1775–801 [Google Scholar]
  9. Bar-Even A, Flamholz A, Noor E, Milo R. 9.  2012. Rethinking glycolysis: on the biochemical logic of metabolic pathways. Nat. Chem. Biol. 8:509–17 [Google Scholar]
  10. Bartnicki-Garcia S, Wang MC. 10.  1983. Biochemical aspects of morphogenesis in Phytophthora. Phytophthora, Its Biology, Taxonomy, Ecology, and Pathology DC Erwin, S Bartnicki-Garcia, PH Tsao 121–37 St. Paul, MN: APS [Google Scholar]
  11. Baurain D, Brinkmann H, Petersen J, Rodriguez-Ezpeleta N, Stechmann A. 11.  et al. 2010. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol. Biol. Evol. 27:1698–709 [Google Scholar]
  12. Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A. 12.  et al. 2010. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330:1549–51 [Google Scholar]
  13. Beakes GW, Glockling SL, Sekimoto S. 13.  2012. The evolutionary phylogeny of the oomycete “fungi.”. Protoplasma 249:3–19 [Google Scholar]
  14. Belbahri L, Calmin G, Mauch F, Andersson JO. 14.  2008. Evolution of the cutinase gene family: evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene 408:1–8 [Google Scholar]
  15. Belmonte R, Wang TH, Duncan GJ, Skaar I, Melida H. 15.  et al. 2014. Role of pathogen-derived cell wall carbohydrates and prostaglandin E-2 in immune response and suppression of fish immunity by the oomycete Saprolegnia parasitica. Infect. Immun. 82:4518–29 [Google Scholar]
  16. Bimpong CE. 16.  1975. Changes in metabolic reserves activities during zoospore motility and cyst germination in Phytophthora palmivora. Can. J. Bot. 53:1411–16 [Google Scholar]
  17. Blackman LM, Cullerne DP, Torrena P, Taylor J, Hardham AR. 17.  2015. RNA-Seq analysis of the expression of genes encoding cell wall degrading enzymes during infection of lupin (Lupinus angustifolius) by Phytophthora parasitica. PLOS ONE 10:e0136899 [Google Scholar]
  18. Blein JP, Coutos-Thevenot P, Marion D, Ponchet M. 18.  2002. From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci 7:293–96 [Google Scholar]
  19. Bostock RM, Kuc JA, Laine RA. 19.  1981. Eicosapentaenoic and arachidonic acids from Phytophthora infestans elicit fungitoxic sesquiterpenes in the potato. Science 212:67–69 [Google Scholar]
  20. Brouwer H, Coutinho PM, Henrissat B, de Vries RP. 20.  2014. Carbohydrate-related enzymes of important Phytophthora plant pathogens. Fungal Genet. Biol. 72:192–200 [Google Scholar]
  21. Caballero JRI, Tisserat NA. 21.  2016. Transcriptome and secretome of two Pythium species during infection and saprophytic growth. Physiol. Mol. Plant Pathol. In press. https://doi.org/10.1016/j.pmpp.2016.09.001 [Crossref] [Google Scholar]
  22. Cardenas ML, Cornish-Bowden A, Ureta T. 22.  1998. Evolution and regulatory role of the hexokinases. Biochim. Biophys. Acta 1401:242–64 [Google Scholar]
  23. Carlile MJ. 23.  1996. The discovery of fungal sex hormones: II. Antheridiol. Mycologist 10:113–17 [Google Scholar]
  24. Carvalho-Santos Z, Azimzadeh J, Pereira-Leal JB, Bettencourt-Dias M. 24.  2011. Evolution: tracing the origins of centrioles, cilia, and flagella. J. Cell Biol. 194:165–75 [Google Scholar]
  25. Creamer JR, Bostock RM. 25.  1986. Characterization and biological-activity of Phytophthora infestans phospholipids in the hypersensitive response of potato-tuber. Physiol. Mol. Plant Pathol. 28:215–25 [Google Scholar]
  26. de Bruijn I, Belmonte R, Anderson VL, Saraiva M, Wang TH. 26.  et al. 2012. Immune gene expression in trout cell lines infected with the fish pathogenic oomycete Saprolegnia parasitica. Dev. Comp. Immun. 38:44–54 [Google Scholar]
  27. de Cock AWAM, Lodhi AM, Rintoul TL, Bala K, Robideau GP. 27.  et al. 2015. Phytopythium: molecular phylogeny and systematics. Persoonia 34:25–39 [Google Scholar]
  28. DeBary A. 28.  1876. Researches into the nature of the potato fungus Phytophthora infestans. J. R. Agr. Soc. Engl. 12:239 [Google Scholar]
  29. Denoeud F, Roussel M, Noel B, Wawrzyniak I, Da Silva C. 29.  et al. 2011. Genome sequence of the stramenopile Blastocystis, a human anaerobic parasite. Genome Biol 12:R29 [Google Scholar]
  30. Ellington WR. 30.  2001. Evolution and physiological roles of phosphagen systems. Annu. Rev. Physiol. 63:289–325 [Google Scholar]
  31. Erwin DC, Ribeiro OK. 31.  1996. Phytophthora Diseases Worldwide St. Paul, MN: APS [Google Scholar]
  32. Etalo DW, De Vos RCH, Joosten MHAJ, Hall RD. 32.  2015. Spatially resolved plant metabolomics: some potentials and limitations of laser-ablation electrospray ionization mass spectrometry metabolite imaging. Plant Physiol 169:1424–35 [Google Scholar]
  33. Gaastra W, Lipman LJA, De Cock AWAM, Exel TK, Pegge RBG. 33.  et al. 2010. Pythium insidiosum: an overview. Vet. Microbiol. 146:1–16 [Google Scholar]
  34. Galindo JA, Hohl HR. 34.  1985. Phytophthora mirabilis, a new species of Phytophthora. Sydowia 38:87–96 [Google Scholar]
  35. Garcia-Bayona L, Garavito MF, Lozano GL, Vasquez JJ, Myers K. 35.  et al. 2014. De novo pyrimidine biosynthesis in the oomycete plant pathogen Phytophthora infestans. Gene 537:312–21 [Google Scholar]
  36. Gardner MJ, Hall N, Fung E, White O, Berriman M. 36.  et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498–511 [Google Scholar]
  37. Gaulin E, Madoui MA, Bottin A, Jacquet C, Mathe C. 37.  et al. 2008. Transcriptome of Aphanomyces euteiches: new oomycete putative pathogenicity factors and metabolic pathways. PLOS ONE 3:e1723 [Google Scholar]
  38. Gleason FH, Rudolph CR, Price JS. 38.  1970. Growth of certain aquatic oomycetes on amino acids: I. Saprolegnia, Achlya, Leptolegnia, and Dicryuchus. Plant Pathol 23:513–16 [Google Scholar]
  39. Gotesson A, Marshall JS, Jones DA, Hardham AR. 39.  2002. Characterization and evolutionary analysis of a large polygalacturonase gene family in the oomycete plant pathogen Phytophthora cinnamomi. Mol. Plant Microbe Interact. 15:907–21 [Google Scholar]
  40. Graham JWA, Williams TCR, Morgan M, Fernie AR, Ratcliffe RG, Sweetlove LJ. 40.  2007. Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 19:3723–38 [Google Scholar]
  41. Griffiths RG, Dancer J, O'Neill E, Harwood JL. 41.  2003. A mandelamide pesticide alters lipid metabolism in Phytophthora infestans. New Phytol. 158:345–53 [Google Scholar]
  42. Griffiths RG, Dancer J, O'Neill E, Harwood JL. 42.  2003. Effect of culture conditions on the lipid composition of Phytophthora infestans. New Phytol. 158:337–44 [Google Scholar]
  43. Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE. 43.  et al. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–98 [Google Scholar]
  44. Hohl HR. 44.  1991. Nutrition. Adv. Plant Pathol. 7:53–83 [Google Scholar]
  45. Jiang RHY, de Bruijn I, Haas BJ, Belmonte R, Lobach L. 45.  et al. 2013. Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica. PLOS Genet. 9:e1003272 [Google Scholar]
  46. Judelson HS. 46.  2014. Phytophthora infestans. Genomics of Plant-Associated Fungi and Oomycetes: Dicot Pathogens RA Dean, A Lichens-Park, C Kole 175–208 Heidelberg, Germ.: Springer [Google Scholar]
  47. Judelson HS, Ah-Fong AM, Aux G, Avrova AO, Bruce C. 47.  et al. 2008. Gene expression profiling during asexual development of the late blight pathogen Phytophthora infestans reveals a highly dynamic transcriptome. Mol. Plant Microbe Interact. 21:433–47 [Google Scholar]
  48. Judelson HS, Ah-Fong AMV. 48.  2009. Progress and challenges in oomycete transformation. Oomycete Genetics and Genomics K Lamour, S Kamoun 435–54 Hoboken, NJ: Wiley [Google Scholar]
  49. Judelson HS, Shrivastava J, Manson J. 49.  2012. Decay of genes encoding the oomycete flagellar proteome in the downy mildew Hyaloperonospora arabidopsidis. PLOS ONE 7:e47624 [Google Scholar]
  50. Jupe J, Stam R, Howden AJM, Morris JA, Zhang RX. 50.  et al. 2013. Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biol 14:R63 [Google Scholar]
  51. Kagda M. 51.  2017. Insight into the dynamic metabolism of Phytophthora infestans PhD Thesis Univ. Calif., Riverside [Google Scholar]
  52. Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL. 52.  et al. 2011. Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLOS Biol. 9:e1001094 [Google Scholar]
  53. Lamour K, Mudge J, Gobena D, Hurtado-Gonzales OP, Schmutz J. 53.  et al. 2012. Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Mol. Plant Microbe Interact. 25:1350–60 [Google Scholar]
  54. Langcake P. 54.  1974. Sterols in potato leaves and their effects on growth and sporulation of Phytophthora infestans. Trans. Br. Mycol. Soc. 63:573–86 [Google Scholar]
  55. Lara E, Belbahri L. 55.  2011. SSU rRNA reveals major trends in oomycete evolution. Fungal Divers 49:93–100 [Google Scholar]
  56. Lee J, Mullins JT, Gander JE. 56.  1996. Water-soluble reserve polysaccharides from Achlya are 1,3-beta-glucans. Mycologia 88:264–70 [Google Scholar]
  57. Levesque CA, Brouwer H, Cano L, Hamilton JP, Holt C. 57.  et al. 2010. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 11:R73 [Google Scholar]
  58. Links MG, Holub E, Jiang RHY, Sharpe AG, Hegedus D. 58.  et al. 2011. De novo sequence assembly of Albugo candida reveals a small genome relative to other biotrophic oomycetes. BMC Genom 12:503 [Google Scholar]
  59. Losel DM. 59.  1988. Fungal lipids. Microbial Lipids C Rathledge, SG Wilkinson 699–794 San Diego, CA: Academic [Google Scholar]
  60. Luis P, Gauthier A, Trouvelot S, Poinssot B, Frettinger P. 60.  2013. Identification of Plasmopara viticola genes potentially involved in pathogenesis on grapevine suggests new similarities between oomycetes and true fungi. Phytopathology 103:1035–44 [Google Scholar]
  61. Madoui MA, Bertrand-Michel J, Gaulin E, Dumas B. 61.  2009. Sterol metabolism in the oomycete Aphanomyces euteiches, a legume root pathogen. New Phytol 183:291–300 [Google Scholar]
  62. Marshall JS, Ashton AR, Govers F, Hardham AR. 62.  2001. Isolation and characterization of four genes encoding pyruvate, phosphate dikinase in the oomycete plant pathogen Phytophthora cinnamomi. Curr. Genet. 40:73–81 [Google Scholar]
  63. Matari NH, Blair JE. 63.  2014. A multilocus timescale for oomycete evolution estimated under three distinct molecular clock models. BMC Evol. Biol. 14:101 [Google Scholar]
  64. McCarthy CG, Fitzpatrick DA. 64.  2016. Systematic search for evidence of interdomain horizontal gene transfer from prokaryotes to oomycete lineages. mSphere 1:e00195–16 [Google Scholar]
  65. Meijer HJ, Hassen HH, Govers F. 65.  2011. Phytophthora infestans has a plethora of phospholipase D enzymes including a subclass that has extracellular activity. PLOS ONE 6:e17767 [Google Scholar]
  66. Melida H, Sandoval-Sierra JV, Dieguez-Uribeondo J, Bulone V. 66.  2013. Analyses of extracellular carbohydrates in oomycetes unveil the existence of three different cell wall types. Eukaryot. Cell 12:194–203 [Google Scholar]
  67. Mertens E. 67.  1993. ATP versus pyrophosphate—glycolysis revisited in parasitic protists. Parasitol. Today 9:122–26 [Google Scholar]
  68. Michel G, Tonon T, Scornet D, Cock JM, Kloareg B. 68.  2010. Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus: insights into the origin and evolution of storage carbohydrates in Eukaryotes. New Phytol 188:67–81 [Google Scholar]
  69. Miles EW, Rhee S, Davies DR. 69.  1999. The molecular basis of substrate channeling. J. Biol. Chem. 274:12193–96 [Google Scholar]
  70. Misner I, Blouin N, Leonard G, Richards TA, Lane CE. 70.  2015. The secreted proteins of Achlya hypogyna and Thraustotheca clavata identify the ancestral oomycete secretome and reveal gene acquisitions by horizontal gene transfer. Genome Biol. Evol 7:120–35 [Google Scholar]
  71. Moktali V, Park J, Fedorova-Abrams ND, Park B, Choi J. 71.  et al. 2012. Systematic and searchable classification of cytochrome P450 proteins encoded by fungal and oomycete genomes. BMC Genom 13:525 [Google Scholar]
  72. Morris PF, Schlosser LR, Onasch KD, Wittenschlaeger T, Austin R, Provart N. 72.  2009. Multiple horizontal gene transfer events and domain fusions have created novel regulatory and metabolic networks in the oomycete genome. PLOS ONE 4:e6133 [Google Scholar]
  73. Munnik T. 73.  2010. Lipid Signaling in Plants Plant Cell Monogr. , Vol. 16 Berlin: Springer-Verlag [Google Scholar]
  74. Nakayama T, Ishida K, Archibald JM. 74.  2012. Broad distribution of TPI-GAPDH fusion proteins among eukaryotes: evidence for glycolytic reactions in the mitochondrion?. PLOS ONE 7:e52340 [Google Scholar]
  75. Nes WD. 75.  1988. Phytophthorols—novel lipids produced by Phytophthora cactorum. Lipids 23:9–16 [Google Scholar]
  76. Ojika M, Molli SD, Kanazawa H, Yajima A, Toda K. 76.  et al. 2011. The second Phytophthora mating hormone defines interspecies biosynthetic crosstalk. Nat. Chem. Biol. 7:591–93 [Google Scholar]
  77. Palmer A, Begres BN, Van Houten JM, Snider MJ, Fraga D. 77.  2013. Characterization of a putative oomycete taurocyamine kinase: implications for the evolution of the phosphagen kinase family. Comp. Biochem. Physiol. B 166:173–81 [Google Scholar]
  78. Patron NJ, Durnford DG, Kopriva S. 78.  2008. Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evol. Biol. 8:39 [Google Scholar]
  79. Pfyffer GE, Rast DM. 79.  1980. The polyol pattern of some fungi not hitherto investigated for sugar alcohols. Exp. Mycol. 4:160–70 [Google Scholar]
  80. Phillips DI, Beech PL. 80.  2014. Phytophthora phospholipase C. US Patent Appl. US 20140329787 A1
  81. Qi J, Asano T, Jinno M, Matsui K, Atsumi K. 81.  et al. 2005. Characterization of a Phytophthora mating hormone. Science 309:1828 [Google Scholar]
  82. Raffaele S, Win J, Cano LM, Kamoun S. 82.  2010. Analyses of genome architecture and gene expression reveal novel candidate virulence factors in the secretome of Phytophthora infestans. BMC Genom. 11:637 [Google Scholar]
  83. Riyahi TY, Frese F, Steinert M, Omosigho NN, Glockner G. 83.  et al. 2011. RpkA, a highly conserved GPCR with a lipid kinase domain, has a role in phagocytosis and anti-bacterial defense. PLOS ONE 6:e27311 [Google Scholar]
  84. Roy S, Kagda M, Judelson HS. 84.  2013. Genome-wide prediction and functional validation of promoter motifs regulating gene expression in spore and infection stages of Phytophthora infestans. PLOS Pathog. 9:e1003182 [Google Scholar]
  85. Ruiz-Lopez N, Sayanova O, Napier JA, Haslam RP. 85.  2012. Metabolic engineering of the omega-3 long chain polyunsaturated fatty acid biosynthetic pathway into transgenic plants. J. Exp. Bot. 63:2397–410 [Google Scholar]
  86. Sandrock RW, Van Etten HD. 86.  1998. Fungal sensitivity to and enzymatic degradation of the phytoanticipin alpha-tomatine. Phytopathology 88:137–43 [Google Scholar]
  87. Saraiva M, De Bruijn I, Grenville-Briggs L, McLaggan D, Willems A. 87.  et al. 2014. Functional characterization of a tyrosinase gene from the oomycete Saprolegnia parasitica by RNAi silencing. Fungal Biol 118:621–29 [Google Scholar]
  88. Savory F, Leonard G, Richards TA. 88.  2015. The role of horizontal gene transfer in the evolution of the oomycetes. PLOS Pathog 11:e1004805 [Google Scholar]
  89. Schell JC, Rutter J. 89.  2013. The long and winding road to the mitochondrial pyruvate carrier. Cancer Metab 1:6 [Google Scholar]
  90. Schumacher J. 90.  2016. DHN melanin biosynthesis in the plant pathogenic fungus Botrytis cinerea is based on two developmentally regulated key enzyme (PKS)-encoding genes. Mol. Microbiol. 99:729–48 [Google Scholar]
  91. Seidl MF, Van den Ackerveken G, Govers F, Snel B. 91.  2011. A domain-centric analysis of oomycete plant pathogen genomes reveals unique protein organization. Plant Physiol 155:628–44 [Google Scholar]
  92. Sello MM, Jafta N, Nelson DR, Chen WP, Yu JH. 92.  et al. 2015. Diversity and evolution of cytochrome P450 monooxygenases in oomycetes. Sci. Rep. 5:11572 [Google Scholar]
  93. Sharma R, Xia XJ, Cano LM, Evangelisti E, Kemen E. 93.  et al. 2015. Genome analyses of the sunflower pathogen Plasmopara halstedii provide insights into effector evolution in downy mildews and Phytophthora. BMC Genom 16:741 [Google Scholar]
  94. Shirasaka N, Yokochi T, Shimizu S. 94.  1995. Formation of a novel odd chain polyunsaturated fatty-acid, 5,8,11,14,17-cis-nonadecapentaenoic acid, by an EPA-producing aquatic fungus, Saprolegnia sp. 28YTF-1. Biosci. Biotechnol. Biochem 59:1963–65 [Google Scholar]
  95. Slot JC, Hibbett DS. 95.  2007. Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLOS ONE 2:e1097 [Google Scholar]
  96. Stiller JW, Huang J, Ding Q, Tian J, Goodwillie C. 96.  2009. Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses?. BMC Genom 10:484 [Google Scholar]
  97. Stossel P. 97.  1983. In vitro effects of glyceollin on Phytophthora megasperma f. sp. glycinea. Phytopathology 73:1603–7 [Google Scholar]
  98. Stredansky M, Conti E, Salaris A. 98.  2000. Production of polyunsaturated fatty acids by Pythium ultimum in solid-state cultivation. Enzym. Microb. Technol. 26:304–07 [Google Scholar]
  99. Tani S, Yatzkan E, Judelson HS. 99.  2004. Multiple pathways regulate the induction of genes during zoosporogenesis in Phytophthora infestans. Mol. Plant Microbe Interact. 17:330–37 [Google Scholar]
  100. Torto TA, Rauser L, Kamoun S. 100.  2002. The pipg1 gene of the oomycete Phytophthora infestans encodes a fungal-like endopolygalacturonase. Curr. Genet. 40:385–90 [Google Scholar]
  101. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH. 101.  et al. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–66 [Google Scholar]
  102. Uda K, Hoshijima M, Suzuki T. 102.  2013. A novel taurocyamine kinase found in the protist Phytophthora infestans. Comp. Biochem. Phys. B 165:42–48 [Google Scholar]
  103. van West P. 103.  2006. Saprolegnia parasitica, an oomycete pathogen with a fishy appetite: new challenges for an old problem. Mycologist 20:99–104 [Google Scholar]
  104. Vogel HJ. 104.  1964. Distribution of lysine pathways among fungi: evolutionary implications. Am. Nat. 48:435–46 [Google Scholar]
  105. Wang RB, Zhang MX, Liu H, Xu J, Yu J. 105.  et al. 2016. PsAAT3, an oomycete-specific aspartate aminotransferase, is required for full pathogenicity of the oomycete pathogen Phytophthora sojae. Fungal Biol. 120:620–30 [Google Scholar]
  106. Warrilow AGS, Hull CM, Rolley NJ, Parker JE, Nes WD. 106.  et al. 2014. Clotrimazole as a potent agent for treating the oomycete fish pathogen Saprolegnia parasitica through inhibition of sterol 14α-demethylase (CYP51). Appl. Env. Microbiol. 80:6154–66 [Google Scholar]
  107. Yousef LF, Wojno M, Dick WA, Dick RP. 107.  2012. Lipid profiling of the soybean pathogen Phytophthora sojae using fatty acid methyl esters (FAMEs). Fungal Biol 116:613–19 [Google Scholar]
  108. Zamboni N, Saghatelian A, Patti GJ. 108.  2015. Defining the metabolome: size, flux, and regulation. Mol. Cell 58:699–706 [Google Scholar]
  109. Zerillo MM, Adhikari BN, Hamilton JP, Buell CR, Levesque CA, Tisserat N. 109.  2013. Carbohydrate-active enzymes in Pythium and their role in plant cell wall and storage polysaccharide degradation. PLOS ONE 8:e72572 [Google Scholar]

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