Molecular cloning, functional characterization and expression of potato (Solanum tuberosum) 1-deoxy-d-xylulose 5-phosphate synthase 1 (StDXS1) in response to Phytophthora infestans

Plant Science

Volumn 243, Issue , 2016, Pages 71-83

  Henriquez, Maria Antonia ^a,b   Soliman, Atta ^a,c   Li, Genyi ^a   Hannoufa, Abdelali ^b   Ayele, Belay T ^a   Daayf, Fouad ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^c TANTA UNIVERSITY   (Egypt)

Author keywords

Abscisic acid; Carotenoids; DOXP MEP; DXS; Functional analysis; Jasmonic acid; Phytophthora infestans; Salicylic acid; Solanum; Terpenoids

Indexed keywords

COMPLEMENTARY DNA; DEOXYXYLULOSE-5-PHOSPHATE SYNTHASE; GLUCAN; ICOSAPENTAENOIC ACID; PLANT DNA; PLANT PROTEIN; TRANSFERASE;

ARABIDOPSIS; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; PHYTOPHTHORA INFESTANS; PLANT DISEASE; TRANSGENIC PLANT;

ARABIDOPSIS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; DNA, PLANT; EICOSAPENTAENOIC ACID; GENE EXPRESSION REGULATION, PLANT; GLUCANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PHYTOPHTHORA INFESTANS; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SEQUENCE ANALYSIS, DNA; TRANSFERASES;

EID: 84959420244     PISSN: 01689452     EISSN: 18732259     Source Type: Journal    
DOI: 10.1016/j.plantsci.2015.12.001     Document Type: Article

References (66)

1. Friedman M., McDonald G.M. Potato glycoalkaloids: chemistry, analysis, safety, and plant physiology. Crit. Rev. Plant Sci. 1997, 16:55-132.
2. Daayf F., Platt H.W., Mahuku G., Peters R.D. Relationships between pathotypes and RAPDs, Gpi-allozyme patterns, mating types, and resistance to metalaxyl of Phytophthora infestans in Canada in 1997. Am. J. Potato Res. 2001, 78:129-139.
3. B. Hardy, B., Trognitz, G. Forbes, Late blight breeding at CIP. CIP Circular Lima, Peru, 21 (1995) 2-5.
4. Judelson H.S., Blanco F.A. The spores of Phytophthora: Weapons of the plant destroyer. Nat. Rev. Microbiol. 2005, 3:47-58.
5. Daayf F., Adam L., Fernando D. Comparative screening of bacteria for biological control of potato late blight (strain US-8), using in vitro, detached leaves, and whole plant-testing systems. Can. J. Plant Pathol. 2003, 25:276-284.
6. El Hassni M., J'Aiti F., Dihazi A., Ait Barka E., Daayf F., El Hadrami I. Enhancement of induced defense responses against Bayoud disease by treatment of date palm seedlings with a hypoaggressive Fusarium oxysporum isolate. J. Phytopathol. 2004, 152:182-189.
7. Fry W.E., Goodwin S.B. Re-emergence of potato and tomato late blight in the United States. Plant Dis. 1997, 81:1349-1357.
8. Daayf F., Platt H.W., Peters R.D. Changes in mating types, resistance to metalaxyl, and Gpi-allozyme genotypes of Phytophthora infestans in Canadian provinces from 1996 to 1998. Can. J. Plant Pathol. 2000, 22:110-116.
9. Wang X., El Hadrami A., Adam L., Daayf F. US-1 and US-8 genotypes of Phytophthora infestans differentially affect local, proximal and distal gene expression of phenylalanine ammonia-lyase and 3-hydroxy, 3-methylglutaryl CoA reductase in potato leaves. Physiol. Mol. Plant Pathol. 2004, 65:157-167.
10. Wang X., El Hadrami A., Adam L.R., Daayf F. Differential activation and suppression of potato defence responses by Phytophthora infestans isolates representing US-1 and US-8 genotypes. Plant Pathol. 2008, 57:1026-1037.
11. McGarvey D.J., Croteau R. Terpenoid metabolism. Plant Cell 1995, 7:1015-1026.
12. Chappell J. Biochemistry and molecular-biology of the isoprenoid biosynthetic-pathway in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1995, 46:521-547.
13. Flesch G., Rohmer M. Prokaryotic hopanoids - the biosynthesis of the bacteriohopane skeleton - formation of isoprenic units from 2 distinct acetate pools and a novel type of carbon carbon linkage between a triterpene and D-ribose. Eur. J. Biochem. 1988, 175:405-411.
14. 2 as main carbon source for isoprenoid biosynthesis via the mevalonate-independent methylerythritol 4-phosphate route in the marine diatoms Phaeodactylum tricornutum and Nitzschia ovalis. Phytochemistry 2000, 53:21-28.
15. Jomaa H., Wiesner J., Sanderbrand S., Altincicek B., Weidemeyer C., Hintz M., Turbachova I., Eberl M., Zeidler J., Lichtenthaler H.K., Soldati D., Beck E. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 1999, 285:1573-1576.
16. Lichtenthaler H.K., Schwender J., Disch A., Rohmer M. Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Lett. 1997, 400:271-274.
17. Hunter W.N., Bond C.S., Gabrielsen M., Kemp L.E. Structure and reactivity in the non-mevalonate pathway of isoprenoid biosynthesis. Biochem. Soc. Trans. 2003, 31:537-542.
18. Eisenreich W., Schwarz M., Cartayrade A., Arigoni D., Zenk M.H., Bacher A. The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. Chem. Biol. 1998, 5:R221-R233.
19. Rohmer M., Seemann M., Horbach S., Bringer-Meyer S., Sahm H. Glyceraldehyde 3-phosphate and pyruvate as precursors of isoprenic units in an alternative non-mevalonate pathway for terpenoid biosynthesis. J. Am. Chem. Soc. 1996, 118:2564-2566.
20. Lois L.M., Rodriguez-Concepcion M., Gallego F., Campos N., Boronat A. Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-d-xylulose 5-phosphate synthase. Plant J. 2000, 22:503-513.
21. Lange B.M., Rujan T., Martin W., Croteau R. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:13172-13177.
22. Eisenreich W., Bacher A., Arigoni D., Rohdich F. Biosynthesis of isoprenoids via the non-mevalonate pathway. Cell. Mol. Life Sci. 2004, 61:1401-1426.
23. Rodríguez-Concepción M., Forés O., Martínez-García J.F., González V., Phillips M.A., Ferrer A., Boronat A. Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. Plant Cell 2004, 16:144-156.
24. Cordoba E., Salmi M., León P. Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. J. Exp. Bot. 2009, 60:2933-2943.
25. Kim B.R., Kim S.U., Chang Y.J. Differential expression of three 1-deoxy-d-xylulose-5-phosphate synthase genes in rice. Biotechnol. Lett. 2005, 27:997-1001.
26. Walter M.H., Hans J., Strack D. Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J. 2002, 31:243-254.
27. Cordoba E., Porta H., Arroyo A., San Roman C., Medina L., Rodríguez-Concepción M., León P. Functional characterization of the three genes encoding 1-deoxy-d-xylulose 5-phosphate synthase in maize. J. Exp. Bot. 2011, 62:2023-2038.
28. Floß D.S., Hause B., Lange P.R., Küster H., Strack D., Walter M.H. Knock-down of the MEP pathway isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids, and abolishes normal expression of mycorrhiza-specific plant marker genes. Plant J. 2008, 56:86-100.
29. Okada A., Shimizu T., Okada K., Kuzuyama T., Koga J., Shibuya N., Nojiri H., Yamane H. Elicitor induced activation of the methylerythritol phosphate pathway toward phytoalexins biosynthesis in rice. Plant Mol. Biol. 2007, 65:177-187.
30. Hsieh M.H., Goodman H.M. The Arabidopsis IspH homolog is involved in the plastid nonmevalonate pathway of isoprenoid biosynthesis. Plant Physiol. 2005, 138:641-653.
31. Rodríguez-Villalón A., Gas E., Rodríguez-Concepción M. Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark-grown Arabidopsis seedlings. Plant J. 2009, 60:424-435.
32. Guevara-García A.A., San Roman C., Arroyo A., Cortés M.E., Gutiérrez-Nava M.L., León P. The characterization of the Arabidopsis clb6 mutant illustrates the importance of post-transcriptional regulation of the methyl-d-erythritol 4-phosphate pathway. Plant Cell 2005, 17:628-643.
33. Henriquez M.A., Wolski E.A., Molina O.I., Adam L.R., Andreu A.B., Daayf F. Effects of glucans and eicosapentanoic acid on differential regulation of phenylpropanoid and mevalonic pathways during potato response to Phytophthora infestans. Plant Physiol. Biochem. 2012, 60:119-128.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
35. Clough S.J., Bent A.F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998, 16:735-743.
36. Yoo S.D., Cho Y.H., Sheen J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protocols 2007, 2:1565-1572.
37. Inskeep W.P., Bloom P.R. Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiol. 1985, 77:483-485.
38. Kanno Y., Jikumaru Y., Hanada A., Nambara E., Abrams S., et al. Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiol. 2010, 51:1988-2001.
39. Liu A., Kanno Y., Jordan M.C., Kamiya Y., Mitsunori S., Ayele B.T. Regulation of wheat seed dormancy by after-ripening is mediated by specific transcriptional switches that induce changes in seed hormone metabolism and signaling. PLoS One 2013, 8:e56570.
40. Yu Z., Gao X., Zhao Y., Bi K. HPLC determination of safflor yellow A and three active isoflavones from TCM Naodesheng in rat plasma and tissues and its application to pharmacokinetic studies. Biomed. Chromatogr. 2007, 21:577-584.
41. Pan X., Welti R., Wang X. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat. Protocols 2010, 5:986.
42. Nawrath C., Métraux J.P. Salicylic acid induction-deficient mutants of arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 1999, 11:1393-1404.
43. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
44. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
45. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
46. Estevez J.M., Cantero A., Romero C., Kawaide H., Jimenez L.F., Kuzuyama T., Seto H., Kamiya Y., Leon P. Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-d-erythritol-4-phosphate pathway in Arabidopsis. Plant Physiol. 2000, 124:95-104.
47. Paetzold H., Garms S., Bartram S., Wieczorek J., Urós-Gracia E.M., Rodríguez-Concepción M., Boland W., Strack D., Hause B., Walter M.H. The isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 controls isoprenoid profiles, precursor pathway allocation, and density of tomato trichomes. Mol. Plant 2010, 3:904-916.
48. Lichtenthaler H.K. Non-mevalonate isoprenoid biosynthesis: enzymes, genes and inhibitors. Biochem. Soc. Trans. 2000, 28:785-789.
49. Walter M.H., Fester T., Strack D. Arbuscular mycorrhizal fungi induce the non-mevalonate methylerythritol phosphate pathway of isoprenoid biosynthesis correlated with accumulation of the 'yellow pigment' and other apocarotenoids. Plant J. 2000, 21:571-578.
50. Gil M.J., Coego A., Mauch-Mani B., Jordá P.L., Vera The Arabidopsis csb3 mutant reveals a regulatory link between salicylic acid-mediated disease resistance and the methyl-erythritol 4-phosphate pathway. Plant J. 2005, 44:155-166.
51. Rodriguez-Concepcion M., Boronat A. Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 2002, 130:1079-1089.
52. Vallabhaneni R., Wurtzel E.T. Timing and biosynthetic potential for carotenoid accumulation in genetically diverse germplasm of maize. Plant Physiol. 2009, 150:562-572.
53. Henriquez M.A., Adam L.R., Daayf F. Alteration of secondary metabolites' profiles in potato leaves in response to weakly and highly aggressive isolates of Phytophthora infestans. Plant Physiol. Biochem. 2012, 57:8-14.
54. Veneault-Fourrey C., Laugé R., Langin T. Nonpathogenic strains of Colletotrichum lindemuthianum trigger progressive bean defense responses during appressorium-mediated penetration. Appl. Environ. Microbiol. 2005, 71:4761-4770.
55. Rose J.K.C., Ham K.S., Darvill A.G., Albersheim P. Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counterdefense mechanism by by plant pathogens. Plant Cell Online 2002, 14:1329-1345.
56. Engstrom K., Widmark A.K., Brishammar S., Helmersson S. Antifungal activity to Phytophthora infestans of sesquiterpenoids from infected potato tubers. Potato Res. 1999, 42:43-50.
57. Dixon R.A. Natural products and plant disease resistance. Nature 2001, 411:843-847.
58. Estévez J.M., Cantero A., Reindl A., Reichler S., León P. 1-Deoxy-d-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J. Biol. Chem. 2001, 276:22901-22909.
59. Enfissi E.M., Fraser P.D., Lois L.M., Boronat A., Schuch W., Bramley P. Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnol. J. 2005, 3:17-27.
60. Engprasert S., Taura F., Kawamukai M., Shoyama Y. Molecular cloning and functional expression of geranylgeranyl pyrophosphate synthase from Coleus forskohlii Briq. BMC Plant Biol. 2004, 4:18-23.
61. Morris W.L., Ducreux L.J., Hedden P., Millam S., Taylor M.A. Overexpression of a bacterial 1-deoxy-d-xylulose 5-phosphate synthase gene in potato tubers perturbs the isoprenoid metabolic network: implications for the control of the tuber life cycle. J. Exp. Bot. 2006, 57:3007-3018.
62. Lindgren L.O., Stålberg K.G., Höglund A.S. Seed-specific overexpression of an endogenous Arabidopsis phytoene synthase gene results in delayed germination and increased levels of carotenoids, chlorophyll, and abscisic acid. Plant physiol. 2003, 132:779-785.
63. Yu B., Gruber M.Y., Khachatourians G.G., Zhou R., Epp D.J., Hegedus D.D., Parkin I.A.P., Welsch R., Hannoufa A. Arabidopsis cpSRP54 regulates carotenoid accumulation in Arabidopsis and Brassica napus. J. Exp. Bot. 2012, 63:5189-5202.
64. McCarty D.R. Genetic control and integration of maturation and germination pathways in seed development. Ann. Rev. Plant Physiol. Plant Mol. Biol. 1995, 46:71-93.
65. Botella-Pavia P., Rodriguez-Concepcion M. Carotenoid biotechnology in plants for nutritionally improved foods. Physiol. Plant 2006, 126:369-381.
66. Mandel M.A., Feldmann K.A., Herrera-Estrella L., Rocha-Sosa M., León P. CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J. 1996, 9:649-658.