Anatomy of a nonhost disease resistance response of pea to Fusarium solani: PR gene elicitation via DNase, chitosan and chromatin alterations

Frontiers in Plant Science

Volumn 6, Issue June, 2015, Pages

  Hadwiger, Lee A ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Chromatin; Defense gene transcription; DNA conformation; Fusarium solani sp; Nonhost resistance; Pathogenesis related (PR) genes; Pea endocarp system; Stalled RNA polymerase complexes

Indexed keywords

FUSARIUM PHASEOLI; FUSARIUM SOLANI; PISUM SATIVUM;

EID: 84935831933     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00373     Document Type: Article

References (67)

1. Adkins, M. W., and Tyler, J. K. (2006). Transcriptional activators are dispensable for transcription in the absence of Spt6-mediated chromatin reassembly of promoter regions. Mot. Cell 21,452-453. doi: 10.1016/j.molcel.2005.12.010
2. Allaire, B. S., and Hadwiger, L. A. (1994). Immunogold localization of a disease resistance response protein in Pisum sativum endocarp cells. Physiol. Molec. Plant Pathol. 44, 9-17. doi: 10.1016/S0885-5765(05)80091-8
3. Almeida, M. S., Cabral, K. M., Zingali, R. B., and Kurtenbach, E. (2006). Characterization of two novel defense peptides from pea (Pisum sativum) seeds. Arch. Biochem. Biophys. 378,278-286. doi: 10.1006/abbi.2000.1824
4. Berendes, H. D. (1968). Factors involved in the expression of gene activity in polytene chromosomes. Chromosoma 24, 418-437. doi: 10.1007/bf00285017
5. Biamonti, G., and Cacres, J. F. (2008). Cellular stress and RNA splicing. Trends Biochem. Sci. 34, 146-153. doi: 10.1016/j.ttibs.2008.11.004
6. Bonner, J. J., and Pardue, M. L. (1977). "Polytene chromosone puffing and in situ hybridization measure different aspects of RNA metabolism." Cell 12, 227-234 doi: 10.1016/0092-8674(77)90200-8
7. Chandrasekharan, M. B., Huang, F., and Zu-Wen, S. (2009). Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc. Natl. Acad. Sci. U.S.A. 106, 16686-16691. doi: 10.1073/pnas 0907862106
8. Chang, M. M., Chiang, C. C., Martin, M. W., and Hadwiger, L. A. (1993).Expression of a pea disease resistance response protein in potatoes. Amer. Pot. J. 70, 635-647. doi: 10.1007/BF02849153
9. Chiang, C. C., and Hadwiger, L. A. (1991). The Fusarium solani-induced expression of a pea gene family encoding cysteine content proteins. Mol. Plant Microbe Interact. 4, 324-331. doi: 10.1094/MPMI-4-324
10. Choi, J. J., Klosterman, S. J., and Hadwiger, L. A. (2001). A comparison of the effects of DNA-damaging agents and biological elicitors on the induction of plant defense genes, nuclear distortion and cell death. Plant Physiol. 125, 752-762. doi: 10.1104/pp.125.2.752
11. Choi, J. J., Klosterman, S. J., and Hadwiger, L. A. (2004). A promoter from pea gene DRR206 is suitable to regulate an elicitor-coding gene and develop disease resistance. Phytopathology 94, 651-660. doi: 10.1094/PHYTO.2004.94.6.651
12. Cooke, M. C., Evans, M. C., Dizdaroglu, M., and Lunec, J. (2003). Oxidative DNA damage: mechanisms, mutation and disease. FASEB J. 17,1195-1214. doi: 10.1096/fj.02-0752rev
13. Cruickshank, I. A. M., and Perrin, D. R. (1962). Studies on phytoalexins. VI. Pisatin: the effect of some factors on its formation in Pisum sativum L., and the significance of pisatin in disease resistance. Aust. J. Biol Sci. 16, 111-128.
14. Daniels, C. H., Fristensky, B. W., Wagoner, W., and Hadwiger, L. A. (1986). Pea genes associated with non-host disease resistance to Fusarium are also active in race-specific disease resistance to Pseudomonas. Plant Mol Biol. 8, 309-316. doi: 10.1007/BF00021310
15. DiCenzo, G. L., and VanEtten, H. D. (2006). Studies on the late steps of (+) pisatin biosynthesis: evidence for (-) enantiomeric intermediates. Phytochemistry 67, 675-683. doi: 10.1016/j.phytochem.2005.12.027
16. El Gueddari, N. E., Rauchhaus, U., Moerschbacher, V. M., and Deising, H. V. (2002). Develop-mentally regulated conversion of surface-exposed chitin to chitosan in walls of plant pathogenic fungi. New Phytol. 156, 103-112. doi: 10.1046/j.1469-8137.2002.00487.x
17. Flor, H. H. (1971). Current status of the gene-for-gene concept. Ann. Rev. Phytopathol. 9, 275-296. doi: 10.1146/annurev.py.09.090171.001423
18. Fuchs, G., Hollander, D., Voichek, Y., Ast, G., and Oren, M. (2015). Cotranscriptional histone H2B monoubiquitylation is tightly coupled with RNA polymerase II. Genome Res. 24, 1572-1583. doi: 10.1101/gr.176487.114
19. Gerhold, D. L., Pettinger, A. J., and Hadwiger, L. A. (1993). Characterization of a plant stimulated nuclease from Fusarium solani. Physiol. Mol. Plant Pathol. 43, 33-46. doi: 10.1006/pmpp.1993.1038
20. Griffin, D. H. (1994). Fungal Physiol. New York, NY: Wiley-Liss.
21. Hadwiger, L. A. (2008). Pea-Fusarium solani interactions contributions of a system toward understanding disease resistance. Phytopath 98, 372-379. doi: 10.1094/PHYTO-98-4-0372
22. Hadwiger, L. A. (2009). Localization predictions for gene products involved in non-host responses in a model plant/fungal pathogen interaction. Plant Sci. 177, 257-265. doi: 10.1016/j.plantsci.2009.06.010
23. Hadwiger, L. A. (2013). Multiple effects of chitosan on plant systems: solid science or hype. Plant Sci. 208, 42-49. doi: 10.1016/j.plantsci.2013.03.007
24. Hadwiger, L. A., and Adams, M. J. (1978). Nuclear changes associated with the host-parasite interaction between Fusarium solani and peas. Physiol. Plant Pathol. 12, 63-72. doi: 10.1016/0048-4059(78)90019-X
25. Hadwiger, L. A., Beckman, J. M., and Adams, M. J. (1981). Localization of fungal components in the pea-Fusarium interaction detected immunochemically with antichitosan and antifungal cell wall antisera. Plant Physiol. 67, 170-175. doi: 10.1104/pp.67.1.170
26. Hadwiger, L. A., Chang, M. M., and Parsons, M. A. (1995). Fusarium solani DNase is a signal for increasing expression of nonhost disease resistance response genes, hypersensitivity and pisatin production. Mol. Plant Microbe Interact. 8, 871-879. doi: 10.1094/MPMI-8-0871
27. Hadwiger, L. A., Chiang, C., Victory, S., and Horovitz, D. (1989). "The molecular biology of chitosan in plant/pathogen interaction and its application in agriculture," in Chitin and Chitosan, Sources, Chemistry, Biochemistry, Physical Properties and Applications, eds G. Skjak-Braek, T. Authonsen, P. Sandford. (London: Elsevier), 119-131.
28. Hadwiger, L. A., Kendra, D. F., Fristensky, B. W., and Wagoner, W. (1986). "Chitosan both activates genes in plants and inhibits RNA synthesis in fungi," in Chitin in Nature and Technology, eds R. Muzzaraelli, C. Jeuniaux, and G. W. Gooday (New York, NY: Plenum Press), 209-221.
29. Hadwiger, L. A., and Line, R. F. (1981). Hexosamine accumulations are associated with the terminated growth of Puccinia striiformis on wheat isolines. Physiol. Plant Path. 19, 249-255. doi: 10.1016/S0048-4059(81)80028-8
30. Hadwiger, L. A., and Polashock, J. (2013). Fungal mitochondrial DNases. Effectors with the potential to activate plant defenses in nonhost resistance. Phytopathology 103, 81-90. doi: 10.1094/PHYTO-04-12-0085-R
31. Hadwiger, L. A., and Schwochau, M. E. (1971). Ultraviolet light-induced formation of pisatin and phenylalanine ammonia-lyase. Plant Physiol. 47, 588-590. doi: 10.1104/pp.47.4.588
32. Hadwiger, L. A., and Wagoner, W. (1983). Effect of heat shock on the mRNA-directed disease resistance response of peas. Plant Physiol. 72, 553-556. doi: 10.1104/pp.72.2.553
33. Hartney, S., Carson, J., and Hadwiger, L. A. (2007). The use of chemical genomics to detect functional systems affecting the non-host disease resistance of pea to Fusarium solani f. sp. phaseoli. Plant Sci. 172, 45-56. doi: 10.1016/j.plantsci.2006.07.014
34. Isaac, J., Hartney, S. L., Druffel, K., and Hadwiger, L. A. (2009). The non-host disease resistance in peas; alterations in phosphorylation and ubiquitination of HMGA and histone H2A/H2B. Plant Sci. 177, 439-449. doi:10.1016/j.plantsci.2009.07.007
35. Kendra, D. F., Christian, D. A., and Hadwiger, L. A. (1989). Chitosan oligomers from Fusarium solani/pea interactions, chitinase/ß-glucanase digestion of sporelings and from fungal wall chitin actively inhibit fungal growth and enhance disease resistance. Physiol. Mol. Plant Path. 35, 215-230. doi: 10.1016/0885-5765(89)90052-0
36. Klosterman, S. J., Chen, J., Choi, J. J., Chinn, E. E., and Hadwiger, L. A. (2001).Characterization of a 20 kDa DNase elicitor from Fusarium solani f. sp. Phaseoli and its expression at the onset of induced resistance in Pisum sativum. Molec. Plant Pathol. 2, 147-158. doi: 10.1046/j.1364-3703.2001.00062.x
37. Klostermann, S. J., Choi, J. J., and Hadwiger, L. A. (2003). Analysis of pea HMG-I/Y (HMG A) expression suggests a role in defence gene regulation. Mol. Plant Pathol. 4, 249-258. doi: 10.1046/j.1364-3703.2003.00171.x
38. Lee, H. A., Kim, S. Y., Oh, S. K., Yeom, S. I., Kim, S. B., Kamoun, S., et al. (2014). Multiple recognition of RXLR effectors is associated with nonhost resistance of pepper against Phytophthora infestans. New Phytol. 203, 926-938. doi: 10.1111/nph.12861
39. Loschke, D. C., Hadwiger, L. A., Schroder, J., and Hahlbrock, K. (1981). In vivo studies on the response of phenylalanine ammonia-lyase in peas to light and to pathogenic and non-pathogenic races of Fusarium solani. Plant Physiol. 68, 680-685. doi: 10.1104/pp.68.3.680
40. Loschke, D. C., Hadwiger, L. A., and Wagoner, W. (1983). Comparison of mRNA populations coding for phenylalanine ammonia-lyase and other peptides from pea tissue treated with biotic and abiotic phytoalexin inducers. Physiol. Plant Pathol. 23, 163-173. doi: 10.1016/0048-4059(83)90043-7
41. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997). Crystal structure of the nucleosome core particle at 2.8 Ä resolution. Nature 389, 251-260. doi: 10.1038/38444
42. Mao, P., Meas, R., Dorgan, K. M., and Smerdon, M. J. (2014). UV damage-induced RNA polymerase II stalling stimulates H2B deubiquitylation. Proc. Natl. Acad. Sci. U.S.A. 111, 12811-12816. doi: 10.1073/pnas.1403901111
43. Mauch, F., Hadwiger, L. A., and Boller, T. (1984). Ethylene: symptom not signal for the induction of chitinase and ß-1, 3-glucanase in pea pods by pathogens and elicitors. Plant Physiol. 76, 607-611. doi: 10.1104/pp.76.3.607
44. Parsons, M. A., and Hadwiger, L. A. (1998). Photoactivated psoralens elicit defense genes and phytoalexins production in the pea plant. Photochem. Photobiol 67, 438-445. doi: 10.1111/j.1751-1097.1998.tb05224.x
45. Pilet-Nayel, M. L., Muehlbauer, F. J., McGee, R. J., Kraft, J. M., Baranger, A., and Coyne, C. J. (2002). Quantitative trait loci for partial resistance to Aphanomyces root rot in pea. Theor. Appl. Genet. 106,28-39. doi: 10.1007/s00122-002-0985-2
46. Prioul-Gervais, S., Deniot, G., Recevur, E.-M., Frankewitz, A., Fourmann, M., Rameau, C., et al. (2007). Candidate genes for quantitative resistance to Mycosphaerella pinodes in peas (Pisum sativum L.). Theor. Appi. Genet. 114, 971-984. doi: 10.1007/s00122-006-0492-y
47. Riggleman, R. D., Fristensky, B., and Hadwiger, L. A. (1985). The disease resistance response in pea is associated with increased levels of specific mRNAs. Plant Mol. Biol. 4, 81-86. doi: 10.1007/BF02418753
48. Rojas, C. M., Senthil-Kumar, M., Wang, K., Ryu, C.-M., Kaundal, A., and Mysore, K. S. (2012). Glycolate oxidase modulates reactive oxygen species-mediated signal transduction during nonhost resistance in Nicotiana bethamiana and Arabidopsis. Plant Cell 24, 336-352. doi: 10.1105/tpc.111.093245
49. Sander, C., and Hadwiger, L. A. (1979). L-phenylalanine ammonia-lyase and pisatin induction by5-bromodeoxyuridine in Pisum sativum. Biochem. Biophys. Acta 563, 278-292. doi: 10.1016/0005-2787(79)90047-9
50. Scheel, D. (1998). Resistance response physiology and signal tranduction. Curr. Opin. Plant Biol. 1, 305-310. doi: 10.1016/1369-5266(88)80051-7
51. Schwochau, M. E., and Hadwiger, L. A. (1968). Stimulation of pisatin production in Pisum sativum by actinomycin D and other compounds. Arch. Biochem. Biophys. 126, 731-733. doi: 10.1016/0003-9861(68)90463-3
52. Seneviratne, H. K., Dalisay, D. S., Dim, K.-W., Moinuddin, S. G. A., and Yang, H. (2014). Non-host disease resistance response in pea (Pisum sativum) pods: biochemical function of DRR-206 and phytoalexin pathway localization. Phytochemistry 113, 140-148. doi: 10.1016/j.phytochem.2014.10.013
53. Simons-Walker, M., Hadwiger, L. A., and Ryan, C. A. (1983). Chitosans and pectic polysaccharides both induce the accumulation of the antifungal phytoalexin pisatin in pea pods and antinutrient proteinase inhibitors in tomato leaves. Biochem. Biophy. Res. Com. 110, 194-199. doi: 10.1016/0006-291X(83)91279-2
54. Stam, R., Jupe, J., Howden, S. J., Morris, J. A., Boevink, P. C., Hedley, P. E., et al. (2013). Identification and characterization CRN effectors in Phytophthora capsici shows modularity and functional diversity. PLoS ONE 8:e59517. doi: 10.1371/journal.pone.0059517
55. Stam, R., Mantelin, S., McLellan, H., and Thilliez, G. (2014). The role of effectors in nonhost resistance to filamentous splant pathogens. Front. Plant Sci. 5:582. doi: 10.3389/fpls.2014.00582
56. von Broembsen, S. L., and Hadwiger, L. A. (1972). Characterization of disease resistance responses in certain gene-for-gene interactions between flax and Melampsora lini. Physiol. Plant Pathol. 2, 207-215. doi: 10.1016/0048-4059(72)90003-3
57. Wagoner, W., Loschke, D. C., and Hadwiger, L. A. (1982). Two-dimensional electrophoretic analysis of in vivo and in vitro protein synthesis in peas inoculated with compatible and incompatible Fusarium solani. Physiol. Plant Pathol. 20, 99-107. doi: 10.1016/0048-4059(82)90028-5
58. Wan, J., Xhang, S.-C., Neece, D., Pamonell, K. M., Clough, S., Kim, S., et al. (2008). A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20, 471-481. doi: 10.1105/tpc.107.056754
59. Wang, Y., Nowak, G., Culley, D., Hadwiger, L. A., and Fristensky, B. (1999). Constitutive expression of pea defense gene DRR206 confers resistance to blackleg (Leptosphaeria maculans) disease in transgenic canola (Brassica maculans). MPMI 12, 410-414. doi: 10.1094/MPMI.1999.12.5.410
60. Watson, J. D., Hopkins, N. H., Roberts, J. W., Steitz, J. A., and Weiner, A. M. (1987). Molecular Biology of the Gene, 4th Edn. Menlo Park CA: Benjamin/Cummings Publishing Co.
61. Weake, V. M., and Workman, J. L. (2008). Histone ubiquitination triggering gene activity. Mol. Cell 29, 653-663. doi: 10.1016/j.molcel.2008.02.014
62. Woloshuk, C. P., and Kollatukudy, P. E. (1986). Mechanism by which contact with plant cuticle triggers cutinase gene expression in the spores of Fusarium solani. Proc. Natl. Acad. Sci. U.S.A. 83, 1704-1708. doi: 10.1073/pnas.83.6.1704
63. Wu, J. Q., and Snyder, M. (2008). RNA polymerase II stalling: loading at the start prepares genes for a sprint. Genome Biol. 9, 220-227. doi: 10.1186/gb-2008-9-5-220
64. Yan, S., Wang, W., Marques, J., Mohan, R., Saleh, A., Durrant, W. E., et al. (2013). Salicylic acid activates DNA damage responses to potentiate plant immunity. Mol. Cell. 52, 602-610. DOI: 10.1016/j.molcel.2013.009.019
65. Yu, D., Chen, C., and Zhixiang, C. (2001). Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13, 1527-1539. doi: 10.1105/tpc.13.7.1527
66. Zellerhoff, N., Himmelbach, A., Dong, W., Bieri, S., Schaffrath, U., and Schweizer, P. (2010). Nonhost resistance of barley to different fungal pathogens is associated with largely distinct, quantitative transcriptional responses. Plant Physiol. 152,2053-2066. doi: 10.1104/pp.109.151829
67. Zhang, Y. (2003). Transcriptional regulation by histone ubiquitination and deubiquitination. GenesDev. 17, 2733-2740. doi: 10.1101/gad.1156403