Polyphenol oxidase as a biochemical seed defense mechanism

Frontiers in Plant Science

Volumn 5, Issue DEC, 2014, Pages

  Fuerst, E P ^a   Okubara, Patricia A ^a   Anderson, James V ^b   Morris, Craig F ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

Seed decay; Seed defense; Seed longevity; Weed seed bank

Indexed keywords

AVENA FATUA; FUNGI; FUSARIUM; PALEA;

EID: 84917672979     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00689     Document Type: Article

References (75)

1. AACC International. (2000). Approved Methods of the American Association of Cereal Chemists, 10th Edn. Saint Paul, MN: AACC International.
2. Almagro, L., Gomez Ros, L. V., Belchi-Navarro, S., Bru, R., Ros Barcelo, A., and Pedreno, M. A. (2009). Class III peroxidases in plant defence reactions. J. Exp. Bot. 60, 377-390. doi: 10.1093/jxb/ern277
3. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W.,et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein search programs. Nucleic Acids Res. 25, 3389-3402. doi: 10.1093/nar/25.17.3389
4. Anderson, J. V., Fuerst, E. P., Hurkman, W. J., Vensel, W. H., and Morris, C. F. (2006). Biochemical and genetic characterization of wheat (Triticum spp.) kernel polyphenol oxidases. J. Cereal Sci. 44, 353-367. doi: 10.1016/j.jcs.2006.06.008
5. Anderson, J. V., Fuerst, E. P., Tedrow, T., Hulke, B., and Kennedy, A. C. (2010). Activation of polyphenol oxidase in dormant wild oat caryopses by a seed decay isolate of Fusarium avenaceum. J. Agric. Food Chem. 58, 10597-10605. doi: 10.1021/jf102625a
6. Anderson, J. V., and Morris, C. F. (2001). An improved whole-seed assay for screening wheat germplasm for polyphenol oxidase activity. Crop Sci. 41, 1697-1705. doi: 10.2135/cropsci2001.1697
7. Baskin, C. C., and Baskin, J. M. (2006). The natural history of soil seed banks of arable land. Weed Sci. 54, 549-557. doi: 10.1614/WS-05-034R.1
8. Beckie, H. J., Francis, A., and Hall, L. M. (2012). The biology of Canadian weeds. 27. Avena fatua L. Can. J. Plant Sci. 92, 1329-1357. doi: 10.4141/cjps2012-005
9. Beecher, B. S., Carter, A. H., and See, D. R. (2012). Genetic mapping of new seed-expressed polyphenol oxidase genes in wheat (Triticum aestivum L.). Theor. Appl. Genet. 124, 1463-1473. doi: 10.1007/s00122-012-1801-2
10. Berna, A., and Bernier, F. (1997). Regulated expression of a wheat germin gene in tobacco: oxalate oxidase activity and apoplastic localization of the heterologous protein. Plant Mol. Biol. 33, 417-419. doi: 10.1023/A:1005745015962
11. Chee-Sanford, J. C. (2008). Weed seeds as nutritional resources for soil Ascomycota and characterization of specific associations between plant and fungal species. Biol. Fertil. Soils 44, 763-771. doi: 10.1007/s00374-007-0259-x
12. Chee-Sanford, J. C., Williams, M. M, Davis, A. S., and Sims, G. K. (2006). Do microorganisms influence seed-bank dynamics? Weed Sci. 54, 575-587. doi: 10.1614/WS-05-055R.1
13. Constabel, C. P., and Barbehenn, R. (2008). "Defensive roles of polyphenol oxidase in plants," in Induced Plant Resistance to Herbivory, ed. A. Schaller (Dordrecht: Springer Science and Business Media B.V.), 253-269. doi: 10.1007/978-1-4020-8182-8_12
14. Constabel, C. P., Bergey, D. R., and Ryan, C. A. (1998). A survey of wound- and methyl jasmonate-induced leaf polyphenol oxidase in crop plants. Phytochemistry 47, 507-511. doi: 10.1016/S0031-9422(97)00539-6
15. Cosio, C., and Dunand, C. (2009). Specific functions of individual class III peroxidase genes. J. Exp. Bot. 60, 391-408. doi: 10.1093/jxb/ern318
16. Dalling, J. W., Davis, A. S., Schutte, B. J., and Arnold, A. E. (2011). Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. J. Ecol. 99, 89-95. doi: 10.1111/j.1365-2745.2010.01739.x
17. Davis, A. S. (2006). When does it make sense to target the weed seed bank? Weed Sci. 54, 558-565. doi: 10.1614/WS-05-058R.1
18. Dumas, B., Freyssinet, G., and Pallett, K. E. (1995). Tissue-specific expression of germin-like oxalate oxidase during development and fungal infection of barley seedlings. Plant Physiol. 107, 1091-1096.
19. Dunwell, J. M., Gibbings, J. G., Mahmood, T., and Saqlan Naqvi, S. M. (2008). Germin and germin-like proteins: evolution, structure and function. Crit. Rev. Plant Sci. 27, 342-375. doi: 10.1080/07352680802333938
20. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016. doi: 10.1006/jmbi.2000.3903
21. Flurkey, W. H., and Inlow, J. K. (2008). Proteolytic processing of polyphenol oxidase from plants and fungi. J. Inorg. Biochem. 102, 2160-2170. doi: 10.1016/j.jinorgbio.2008.08.007
22. Fraignier, M. P., Michaux-Ferriere, N., and Kobrehel, K. (2000). Distribution of peroxidases in durum wheat (Triticum durum). Cereal Chem. 77, 11-17. doi: 10.1094/CCHEM.2000.77.1.11
23. Fuerst, E. P., Anderson, J. V., Kennedy, A. C., and Gallagher, R. S. (2011). Induction of polyphenol oxidase activity in dormant wild oat (Avena fatua) seeds and caryopsis: a defense response to seed decay fungi. Weed Sci. 59, 137-144. doi: 10.1614/WS-D-10-00123.1
24. Fuerst, E. P., Anderson, J. V., and Morris, C. F. (2006). Polyphenol oxidase in wheat grain: whole-kernel and bran assays for total and soluble activity. Cereal Chem. 83, 10-16. doi: 10.1094/CC-83-0010
25. Fuerst, E. P., Anderson, J. V., and Morris, C. F. (2010). "Effects of polyphenol oxidase on noodle color: mechanisms, measurement, and improvement," in Asian Noodles: Science, Technology, and Processing, Chap. 12, ed. G. G. Hou (Hoboken, NJ: John Wiley & Sons, Inc.), 285-312.
26. Gallagher, R. S., Ananth, R., Bradley, B., Granger, K., Anderson, J. V., and Fuerst, E. P. (2010). Phenolic and short-chained aliphatic organic acid constituents of wild oat (Avena fatua L.) seeds. J. Agric. Food Chem. 58, 218-225. doi: 10.1021/jf9038106
27. Gallery, R. E., Dalling, J. W., and Arnold, A. E. (2007). Diversity, host affinity, and distribution of seed-infecting fungi: a case study with Cecropia. Ecology 88, 582-588. doi: 10.1890/05-1207
28. Gallery, R. E., Moore, D. J. P., and Dalling, J. W. (2010). Interspecific variation in susceptibility to fungal pathogens in seeds of 10 tree species in the Neotropical genus Cecropia. J. Ecol. 98, 147-155. doi: 10.1111/j.1365-2745.2009.01589.x
29. Gijzen, M., Kuflu, K., Qutob D., and Chernys, J. T. (2001). A class I chitinase from soybean seed coat. J. Exp. Bot. 52, 2283-2289. doi: 10.1093/jexbot/52.365.2283
30. Gijzen, M., van Huystee, R., and Buzzell, R. I. (1993). Soybean seed coat peroxidase. Plant Physiol. 103, 1061-1066.
31. Grover, A. (2012). Plant chitinases: genetic diversity and physiological roles. Crit. Rev. Plant Sci. 31, 57-73. doi: 10.1080/07352689.2011.616043
32. Gutensohn, M., Fan, E., Frielingsdorf, S., Hanner, P., Hou, B., Hust, B.,et al. (2006). Toc, Tic, Tat et al.: structure and function of protein transport machineries in chloroplasts. J. Plant Physiol. 163, 333-347. doi: 10.1016/j.jplph.2005.11.009
33. Haruta, M., Pedersen, J. A., and Constabel, C. P. (2001). Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol. Plant. 112, 552-558. doi: 10.1034/j.1399-3054.2001.1120413.x
34. Hendry, G. A. F., Thompson, K., Moss, C. J., Edwards, E., and Thorpe, P. C. (1994). Seed persistence: a correlation between seed longevity in the soil and ortho-dihydroxyphenol concentration. Funct. Ecol. 8, 658-664. doi: 10.2307/2389929
35. Hiraga, S., Sasaki, K., Ito, H., Ohashi, Y., and Matsui, H. (2001). A large family of class III plant peroxidases. Plant Cell Physiol. 42, 462-468. doi: 10.1093/pcp/pce061
36. Hücklehoven, R. (2007). Cell wall-associated mechanisms of disease resistance and susceptibility. Annu. Rev. Phytopathol. 45, 101-127. doi: 10.1146/annurev.phyto.45.062806.094325
37. Hurkman, W. J., and Tanaka, C. K. (1996). Germin gene expression is induced in wheat leaves by powdery mildew infection. Plant Physiol. 111, 735-739.
38. Imai, K., and Nakai, K. (2010). Prediction of subcellular locations of proteins: where to proceed? Proteomics 10, 3970-3983. doi: 10.1002/pmic.201000274
39. International Wheat Genome Sequencing Consortium [IWGSC]. (2014). A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788. doi: 10.1126/science.1251788
40. Jerkovic, A., Kriegel, A. M., Bradner, J. R., Atwell, B. J., Roberts, T. H., and Willows, R. D. (2010). Strategic distribution of protective proteins within bran layers of wheat protects the nutrient-rich endosperm. Plant Physiol.152, 1459-1470. doi: 10.1104/pp.109.149864
41. Lane, B. G. (1994). Oxalate, germin, and the extracellular matrix of higher plants. FASEB J. 8, 294-301.
42. Lane, B. G. (2002). Oxalate, germins, and higher-plant pathogens. IUBMB Life 53, 67-75. doi: 10.1080/15216540211474
43. Lane, B. G., Bernier, F., Dratewka-Kos, E., Shafai, R., Kennedy, T. D., Pyne, C.,et al. (1991). Homologies between members of the germin gene family in hexaploid wheat and similarities between these wheat germins and certainPhysarum spherulins. J. Biol. Chem. 266, 10461-10469.
44. Lane, B. G., Dunwell, J. M., Ray, J. A., Schmitt, M. R., and Young, A. C. (1993). Germin, a protein marker of early plant development, is an oxalate oxidase. J. Biol. Chem. 268, 12239-12242.
45. Laugesen, S., Bak-Jensen, K. S., Hägglund, P., Henriksen, A., Finnie, C., Svensson, B.,et al. (2007). Barley peroxidase isozymes expression and post-translational modification in mature seeds as identified by two-dimensional gel electrophoresis and mass spectrometry. Int. J. Mass Spectrom. 268, 244-253. doi: 10.1016/j.ijms.2007.06.003
46. Leah, R., Skriver, K., Knudsen, S., Ruud-Hansen, J., Raikhel, N. V., and Mundy, J. (1994). Identification of an enhancer/silencer sequence directing the aleurone-specific expression of a barley chitinase gene. Plant J. 6, 579-598. doi: 10.1046/j.1365-313X.1994.6040579.x
47. Liang, H., Maynard, C. A., Allen, R. D., and Powell, W. A. (2001). Increased Septoria musiva resistance in transgenic hybrid poplar leaves expressing a wheat oxalate oxidase gene. Plant Mol. Biol. 45, 619-629. doi: 10.1023/A:1010631318831
48. Long, R. L., Gorecki, M. J., Renton, M., Scott, J. K., Colville, L., Goggin, D. E.,et al. (2014). The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biol. Rev. Camb. Philos. Soc. doi: 10.1111/brv.12095 [Epub ahead of print].
49. Marles, M. A. S., Vandenberg, A., and Bett, K. E. (2008). Polyphenol oxidase activity and differential accumulation of polyphenolics in seed coats of pinto bean (Phaseolus vulgaris L.) characterize postharvest color changes. J. Agric. Food Chem. 56, 7049-7056. doi: 10.1021/jf8004367
50. Massa, A. N., Beecher, B., and Morris, C. F. (2007). Polyphenol oxidase (PPO) in wheat and wild relatives: molecular evidence for a multigene family. Theor. Appl. Genet. 114, 1239-1247. doi: 10.1007/s00122-007-0514-4
51. Matsumoto, T., Tanaka, T., Sakai, H., Amano, N., Kanamori, H., Kurita, K.,et al. (2011). Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol. 156, 20-28. doi: 10.1104/pp.110.171579
52. Mayer, A. M. (2006). Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67, 2318-2331. doi: 10.1016/j.phytochem.2006.08.006
53. Mohammadi, M., and Kazemi, H. (2002). Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Sci. 162, 491-498. doi: 10.1016/S0168-9452(01)00538-6
54. Naylor, J. M., and Fedec, P. (1978). Dormancy studies in seed of Avena fatua. 8. Genetic diversity affecting response to temperature. Can. J. Bot. 54, 2224-2229. doi: 10.1139/b78-267
55. Newman, S. M., Tantasawat, P., and Steffens, J. C. (2011). Tomato polyphenol oxidase B is spatially and temporally regulated during development and in response to ethylene. Molecules 16, 493-517. doi: 10.3390/molecules16010493
56. Passardi, F., Cosio, C., Penel, C., and Dunand, C. (2005). Peroxidases have more functions than a Swiss army knife.Plant Cell Rep. 24, 255-265. doi: 10.1007/s00299-005-0972-6
57. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011). SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786. doi: 10.1038/nmeth.1701
58. Pimentel, D., Zuniga, R., and Morrison, D. (2005). Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econ. 52, 273-288. doi: 10.1016/j.ecolecon.2004.10.002
59. Poiatti, V. A. D., Dalmas, F. R., and Astarita, L. V. (2009). Defense mechanisms of Solanum tuberosum L. in response to attack by plant-pathogenic bacteria. Biol. Res. 42, 205-215. doi: 10.4067/S0716-97602009000200009
60. Ramamoorthy, V., Raguchander, T., and Samiyappan, R. (2002). Induction of defense-related proteins in tomato roots treated with Pseudomonas fluorescens Pf1 and Fusarium oxysporum f. sp. lycopersici. Plant Soil 239, 55-68. doi: 10.1023/A:1014904815352
61. Rani, K. U., Prasada-Rao, U. J. S., Leelavathi, K., and Haridas-Rao, P. (2001). Distribution of enzymes in wheat flour mill streams. J. Cereal Sci. 34, 233-242. doi: 10.1006/jcrs.2000.0393
62. Shen, H.-B., and Chou, K.-C. (2007). Signal-3L: a 3-layer approach for predicting signal peptides. Biochem. Biophys. Res. Commun. 363, 297-303. doi: 10.1016/j.bbrc.2007.08.140
63. Steffens, J. C., Harel, E., and Hunt, M. D. (1994). "Polyphenol oxidase," in Recent Advances in Phytochemistry, Genetic Engineering of Plant Secondary Metabolism, eds B. E. Ellis, G.W. Kuroki, and H. A. Stafford (New York: Plenum Press), 275-312. doi: 10.1007/978-1-4615-2544-8_11
64. Thipyapong, P., Joel, D. M., and Steffens, J. C. (1997). Differential expression and turnover of the tomato polyphenol oxidase gene family during vegetative and reproductive development. Plant Physiol. 113, 707-718.
65. Thipyapong, P., Stout, M. J., and Attajarusit, J. (2007). Functional analysis of polyphenol oxidases by antisense/sense technology. Molecules 12, 1569-1595. doi: 10.3390/12081569
66. Thygesen, P. W., Dry, I. B., and Robinson, S. P. (1995). Polyphenol oxidase in potato, a multigene family that exhibits differential expression patterns. Plant Physiol. 109, 525-531. doi: 10.1104/pp.109.2.525
67. Till-Bottraud, I., and Brabant, P. (1990). Inheritance of some Mendelian factors in intra- and interspective crosses between Setaria italic and Setaria viridis. Theor. Appl. Genet. 80, 687-692. doi: 10.1007/BF00224230
68. Tran, L. T., Taylor, J. S., and Constabel, C. P. (2012). The polyphenol oxidase gene family in plants: lineage-specific duplication and gene expansion. BMC Genomics 13:395. doi: 10.1186/1471-2164-13-395
69. Vadlamani, K. R., and Seib, P. A. (1996). Reduced browning in raw oriental noodles by heat and moisture treatment of wheat. Cereal Chem. 73, 88-95.
70. van Gelder, C. W. G., Flurkey, W. H., and Wichers, H. J. (1997). Sequence and structural features of plant and fungal tyrosinases. Phytochemistry 45, 1309-1323. doi: 10.1016/S0031-9422(97)00186-6
71. van Loon, L. C., Rep, M., and Pieterse, C. M. J. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135-162. doi: 10.1146/annurev.phyto.44.070505.143425
72. Yan, R., Hou, J., Ding, D., Guan, W., Wang, C., Wu, Z.,et al. (2008). In vitro antifungal activity and mechanism of action of chitinase against four plant pathogenic fungi. J. Basic Microbiol. 48, 293-301. doi: 10.1002/jobm.200700392
73. Yan, S., and Wu, G. (2014). Signal peptides of cellulose. Appl. Microbiol. Biotechnol. 98, 5329-5362. doi: 10.1007/s00253-014-5742-3
74. Yoruk, R., and Marshall, M. R. (2003). Physicochemical properties and function of plant polyphenol oxidase: A review. J. Food Biochem. 27, 361-422. doi: 10.1111/j.1745-4514.2003.tb00289.x
75. Zhang, X. Y., Nie, Z. H., Wang, W. J., Leung, D. W. M., Xu, D. G., Chen, B. L.,et al. (2013). Relationship between disease resistance and rice oxalate oxidases in transgenic rice. PLoS ONE 8:e78348. doi: 10.1371/journal.pone.0078348