The polyphenol oxidase gene family in poplar: Phylogeny, differential expression and identification of a novel, vacuolar isoform

Planta

Volumn 234, Issue 4, 2011, Pages 799-813

  Tran, Lan T ^a   Constabel, C Peter ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

Author keywords

Genome analysis; Phenolic metabolism; Vacuolar targeting

Indexed keywords

ACETIC ACID DERIVATIVE; CATECHOL OXIDASE; CYCLOPENTANE DERIVATIVE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; ISOPROTEIN; JASMONIC ACID METHYL ESTER; OXYLIPIN; PHYTOHORMONE; POLYPHENOL; SIGNAL PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; CELL VACUOLE; DNA SEQUENCE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT GENOME; POPULUS; SEQUENCE ALIGNMENT; TRANSGENIC PLANT;

ACETATES; AMINO ACID SEQUENCE; BASE SEQUENCE; CATECHOL OXIDASE; CLONING, MOLECULAR; CYCLOPENTANES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; GENOMICS; GREEN FLUORESCENT PROTEINS; MOLECULAR SEQUENCE DATA; OXYLIPINS; PHYLOGENY; PLANT GROWTH REGULATORS; PLANTS, GENETICALLY MODIFIED; POLYPHENOLS; POPULUS; PROTEIN ISOFORMS; PROTEIN SORTING SIGNALS; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; VACUOLES;

POPULUS TRICHOCARPA;

EID: 80053133338     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-011-1441-9     Document Type: Article

References (77)

1. Barbehenn RV, Jones CP, Yip L, Tran LT, Constabel CP (2007) Limited impact of elevated levels of polyphenol oxidase on tree-feeding caterpillars? Assessing individual plant defenses with transgenic poplar. Oecologia 154: 129-140.
2. Bhonwong A, Stout MJ, Attajarusit J, Tantasawat P (2009) Defensive role of tomato polyphenol oxidases against cotton bollworm (Helicoverpa armigera) and beet armyworm (Spodoptera exigua). J Chem Ecol 35: 28-38.
3. Bittner S (2006) When quinones meet amino acids: chemical, physical and biological consequences. Amino Acids 30: 205-224.
4. Boss PK, Gardner RC, Janssen BJ, Ross GS (1995) An apple polyphenol oxidase is up-regulated in wounded tissues. Plant Mol Biol 27: 429-433.
5. Bucheli CS, Dry IB, Robinson SP (1996) Purification of polyphenol oxidase and isolation of a full length cDNA from sugarcane, a C4 grass. Plant Mol Biol 31: 1233-1238.
6. Cho M, Moinuddin SGA, Helms GL, Hishiyama S, Eichinger D, Davin LB, Lewis ND (2003) (+)-Larreatricin hydroxylase, an enantio-specific polyphenol oxidase from the creosote bush (Larrea tridentata. Proc Natl Acad Sci USA 100: 10641-10646.
7. Constabel CP, Barbehenn RV (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, New York, pp 253-269.
8. Constabel CP, Lindroth R (2010) The impact of genomics on advances in herbivore defense and secondary metabolism in poplar. In: Jansson S, Bhalerao RP, Groover AT (eds) Genetics and Genomics of Populus. Springer, New York, pp 279-305.
9. Constabel CP, Bergey DR, Ryan CA (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci USA 92: 407-411.
10. Constabel CP, Yip L, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol 124: 285-295.
11. Doyle J, Doyle JL (1990) Isolation of plant DNA from fresh tissue. BRL Focus 12: 13-15.
12. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8: 978-984.
13. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP, and related tools. Nat Protoc 2: 953-971.
14. Gandía-Herrero F, Escribano J, García-Carmona F (2005) Betaxanthins as substrates for tyrosinase. An approach to the role of tyrosinase in the biosynthetic pathway of betalains. Plant Physiol 138: 421-432.
15. Goldman MH, Seurinck J, Marins M, Goldman GH, Mariani C (1998) A tobacco flower-specific gene encodes a polyphenol oxidase. Plant Mol Biol 36: 479-485.
16. Gooding PS, Bird C, Robinson SP (2001) Molecular cloning and characterization of banana fruit polyphenol oxidase. Planta 213: 748-757.
17. Görlich D, Mattaj IW (1996) Nucleocytoplasmic transport. Science 271: 1513-1518.
18. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
19. Haruta M, Murata M, Kadokura H, Homma S (1999) Immunological and molecular comparison of polyphenol oxidase in Rosaceae fruit trees. Phytochemistry 50: 1021-1025.
20. Haruta M, Major IT, Christopher ME, Patton JJ, Constabel CP (2001a) A Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.): cloning, functional expression, and induction by wounding and herbivory. Plant Mol Biol 46: 347-359.
21. Haruta M, Pedersen JA, Constabel CP (2001b) Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol Plant 112: 552-558.
22. Hunt MD, Eannetta NT, Yu H, Newman SM, Steffens JC (1993) cDNA cloning and expression of potato polyphenol oxidase. Plant Mol Biol 21: 59-68.
23. Joy RW IV, Sugiyama M, Fukuda H, Komamine A (1995) Cloning and characterization of polyphenol oxidase cDNAs of Phytolacca americana. Plant Physiol 107: 1083-1089.
24. Karimi M, Inze D, Depicker A (2002) Gateway vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195.
25. Kitajima A, Asatsuma S, Okada H, Hamada Y, Kaneko K, Nanjo Y, Kawagoe Y, Toyooka K, Matsuoka K, Takeuchi M, Nakano A, Mitsui T (2009) The rice alpha-amylase glycoprotein is targeted from the Golgi apparatus through the secretory pathway to the plastids. Plant Cell 21: 2844-2858.
26. Köhler RH, Hanson MR (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated. J Cell Sci 113: 81-89.
27. Koussevitzky S, Ne'eman E, Sommer A, Steffens JC, Harel E (1998) Purification and properties of a novel chloroplast stromal peptidase. Processing of polyphenol oxidase and other imported precursors. J Biol Chem 273: 27064-27069.
28. Koussevitzky S, Ne'eman E, Peleg S, Harel E (2008) Polyphenol oxidase can cross thylakoids by both the Tat and the Sec-dependent pathways: a putative role for two stromal processing sites. Physiol Plant 133: 266-277.
29. Larson PR, Isebrands JG (1971) The plastochron index as applied to developmental studies of cottonwood. Can J For Res 1: 1-11.
30. Li L, Steffens JC (2002) Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215: 239-247.
31. Lindroth RL, Hwang SY (1996) Diversity, redundancy, and multiplicity in chemical defense systems of aspen. In: Romeo JT, Saunders JA, Barbosa P (eds) Phytochemical diversity and redundancy in ecological interactions. Plenum Press, New York, pp 25-56.
32. Mahanil S, Attajarusit J, Stout MJ, Thipyapong P (2008) Overexpression of tomato polyphenol oxidase increases resistance to common cutworm. Plant Sci 174: 456-466.
33. Major IT, Constabel CP (2006) Molecular analysis of poplar defense against herbivory. Comparison of wound- and insect elicitor-induced gene expression. New Phytol 172: 617-635.
34. Massa AN, Beecher B, Morris CF (2007) Polyphenol oxidase (PPO) in wheat and wild relatives: molecular evidence for a multigene family. Theor Appl Genet 114: 1239-1247.
35. Matheis G, Whitaker JR (1984) Modification of proteins by polyphenol oxidase and peroxidase and their products. J Food Biochem 8: 137-162.
36. Mazzafera P, Robinson SP (2000) Characterization of polyphenol oxidase in coffee. Phytochemistry 55: 285-296.
37. Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP (2007) The transcriptional response of hybrid poplar (Populus trichocarpa × P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. MPMI 20: 816-831.
38. Nakayama T, Yonekura-Sakakibara K, Sato T, Kikuchi S, Fukui Y, Fukuchi-Mizutani M, Ueda T, Nakao M, Tanaka Y, Kusumi T, Nishino T (2000) Aureusidin synthase: a polyphenol oxidase homolog responsible for flower colouration. Science 290: 1163-1166.
39. Nakayama T, Sato T, Fukui Y, Yonekura-Sakakibara K, Hayashi H, Tanaka Y, Kusumi T, Nishino T (2001) Specificity analysis and mechanism of aurone synthesis catalyzed by aureusidin synthase, a polyphenol oxidase homolog responsible for flower colouration. FEBS Lett 499: 107-111.
40. Nanjo T, Sakurai T, Totoki Y, Toyoda A, Nishiguchi M, Kado T, Igasaki T, Futamura N, Seki M, Sakaki Y, Shinozaki K, Shinohara K (2007) Functional annotation of 19, 841 Populus nigra full-length enriched cDNA clones. BMC Genomics 8: 448.
41. Newman SM, Eannetta NT, Yu H, Prince JP, de Vicente MC, Tanksley SD, Steffens JC (1993) Organisation of the tomato polyphenol oxidase gene family. Plant Mol Biol 21: 1035-1051.
42. Newman SM, Tantasawat P, Steffens JC (2011) Tomato polyphenol oxidase B is spatially and temporally regulated during development and in response to ethylene. Molecules 16: 493-517.
43. Ono E, Hatayama M, Isono Y, Sato T, Watanabe R, Yonekura-Sakakibara K, Fukuchi-Mizutani M, Tanaka Y, Kusumi T, Nishino T, Nakayama T (2006) Localization of a flavonoid biosynthetic polyphenol oxidase in vacuoles. Plant J 45: 133-143.
44. Parveen I, Threadgill MD, Moorby JM, Winters A (2010) Oxidative phenols in forage crops containing polyphenol oxidase enzymes. J Agric Food Chem 58: 1371-1382.
45. Pinto MST, Siqueira FP, Oliveira AEA, Fernandes KVS (2008) A wounding-induced PPO from cowpea (Vigna unguiculata) seedlings. Phytochemistry 69: 2297-2302.
46. Prieto H, Utz D, Castro Á, Aguirre C, Gonzalez-Aguero M, Valdes H, Cifuentes N, Defilippi BG, Zamora P, Zuniga G, Campos-Vargas R (2007) Browning in Annonacherimola fruit: role of polyphenol oxidase and characterization of a coding sequence of the enzyme. J Agric Food Chem 55: 9208-9218.
47. Ralph S, Oddy C, Cooper D, Yueh H, Jancsik S, Kolosova N, Philippe RN, Aeschliman D, White R, Huber D, Ritland CE, Benoit F, Rigby T, Nantel A, Butterfield YS, Kirkpatrick R, Chun E, Liu J, Palmquist D, Wynhoven B, Stott J, Yang G, Barber S, Holt RA, Siddiqui A, Jones SJM, Marra MA, Ellis BE, Douglas CJ, Ritland K, Bohlmann J (2006) Genomics of hybrid poplar (Populus trichocarpa × P. deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol Ecol 15: 1275-1297.
48. Richter H, Lieberei R, von Schwartzenberg K (2005) Identification and characterisation of a bryophyte polyphenol oxidase encoding gene from Physcomitrella patens. Plant Biol 7: 283-291.
49. Rinaldi C, Kohler A, Frey P, Duchaussoy F, Ningre N, Couloux A, Wincker P, Le Thiec D, Fluch S, Martin F, Duplessis S (2007) Transcript profiling of poplar leaves upon infection with compatible and incompatible strains of the foliar rust Melampsora larici-populina. Plant Physiol 144: 347-366.
50. Schmidt DD, Voelckel C, Hartl M, Schmidt S, Baldwin IT (2005) Specificity in ecological interactions. Attack from the same lepidopteran herbivore results in species-specific transcriptional responses in two Solanaceous host plants. Plant Physiol 138: 1763-1773.
51. Scott A, Wyatt S, Tsou PL, Robertson D, Allen NS (1999) Model system for plant cell biology: GFP imaging in living onion epidermal cells. BioTechniques 26: 1125-1132.
52. Shahar T, Hennig N, Gutfinger T, Hareven D, Lifschitz E (1992) The tomato 66. 3-kD polyphenoloxidase gene: molecular identification and developmental expression. Plant Cell 4: 135-147.
53. Sommer A, Ne'eman E, Steffens JC, Mayer AM, Harel E (1994) Import, targeting and processing of a plant polyphenol oxidase. Plant Physiol 105: 1301-1311.
54. Steiner U, Schliemann W, Böhm H, Strack D (1999) Tyrosinase involved in betalain biosynthesis of higher plants. Planta 208: 114-124.
55. Sterky F, Bhalerao RR, Unneberg P, Segerman B, Nilsson P, Brunner AM, Charbonnel-Campaa L, Jonsson Lindvall J, Tandre K, Strauss SH, Sundberg B, Gustafsson P, Uhlén M, Bhalerao RP, Nilsson O, Sandberg G, Karlsson J, Lundeberg J, Stefan Jansson (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci USA 101: 13951-13956.
56. Stewart RJ, Sawyer BJB, Bucheli CS, Robinson SP (2001) Polyphenol oxidase is induced by chilling and wounding in pineapple. Aust J Plant Physiol 28: 181-191.
57. Sun DJ, He ZH, Xia XC, Zhang LP, Morris CF, Appels R, Ma WJ, Wang H (2005) A novel STS marker for polyphenol oxidase activity in bread wheat. Mol Breed 16: 209-218.
58. Sun Y, He Z, Ma W, Xia X (2011) Alternative splicing in the coding region of Ppo-A1 directly influences the polyphenol oxidase activity in common wheat (Triticum aestivum L.). Funct Integr Genomics 11: 85-93.
59. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol Biol Evol 24: 1596-1599.
60. Thipyapong P, Steffens JC (1997) Tomato polyphenol oxidase. Differential response of the polyphenol oxidase F promoter to injuries and wound signals. Plant Physiol 115: 409-418.
61. Thipyapong P, Hunt MD, Steffens JC (1995) Systemic wound induction of potato (Solanum tuberosum) polyphenol oxidase. Phytochemistry 40: 673-676.
62. Thipyapong P, Joel DM, Steffens JC (1997) Differential expression and turnover of the tomato polyphenol oxidase gene family during vegetative and reproductive development. Plant Physiol 113: 707-718.
63. Thipyapong P, Hunt MD, Steffens JC (2004) Antisense downregulation of polyphenol oxidase results in enhanced disease susceptibility. Planta 220: 105-117.
64. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
65. Thygesen PW, Dry IB, Robinson SP (1995) Polyphenol oxidase in potato: a multigene family that exhibits differential expression patterns. Plant Physiol 109: 525-531.
66. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, van der Peer Y (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
67. Vámos-Vigyázó L (1981) Polyphenol oxidase and peroxidase in fruits and vegetables. Crit Rev Food Sci Nutr 15: 49-127.
68. van Gelder CWG, Flurkey WH, Wichers HJ (1997) Sequence and structural features of plant and fungal tyrosinases. Phytochemistry 45: 1309-1323.
69. von Heijne G, Steppuhn J, Herrmann RG (1989) Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 180: 535-545.
70. Wahler D, Schulze Gronover C, Richter C, Foucu F, Twyman RM, Moerschbacher BM, Fischer R, Muth J, Prüfer D (2009) Polyphenoloxidase silencing affects latex coagulation in Taraxacum species. Plant Physiol 151: 334-346.
71. Wang J, Constabel CP (2003) Biochemical characterization of two differentially expressed polyphenol oxidases from hybrid poplar. Phytochemistry 64: 115-121.
72. Wang J, Constabel CP (2004a) Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220: 87-96.
73. Wang J, Constabel CP (2004b) Three polyphenol oxidases from hybrid poplar are differentially expressed during development and after wounding and elicitor treatment. Physiol Plant 122: 344-353.
74. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, LeRoy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nature 7: 510-523.
75. Winters A, Heywood S, Farrar K, Donnison I, Thomas A, Webb KJ (2009) Identification of an extensive gene cluster among a family of PPOs in Trifoliumpratense L. (red clover) using a large insert BAC library. BMC Plant Biol 9: 94.
76. Yamamoto K, Kobayashi N, Yoshitama K, Teramoto S, Komamine A (2001) Isolation and purification of tyrosine hydroxylase from callus cultures of Portulaca grandiflora. Plant Cell Physiol 42: 969-975.
77. Zhou Y, O'Hare TJ, Jobin-Décor M, Underhill SJR, Wills RBH, Graham MW (2003) Transcriptional regulation of a pineapple polyphenol oxidase gene and its relationship to blackheart. Plant Biotechnol J 1: 463-478.