Use of BABA and INA As activators of a primed state in the common bean (Phaseolus vulgaris L.)

Frontiers in Plant Science

Volumn 7, Issue MAY2016, 2016, Pages

  Martínez Aguilar, Keren ^a   Ramírez Carrasco, Gabriela ^a   Hernández Chávez, José Luis ^a   Barraza, Aarón ^b   Alvarez Venegas, Raúl ^a  

^a DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS DEL NOROESTE   (Mexico)

Author keywords

BABA; Common bean; Epigenetics; INA; Priming

Indexed keywords

EID: 84969492203     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00653     Document Type: Article

References (63)

1. Agarwal, P., Reddy, M. P., and Chikara, J. (2011). WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. Mol. Biol. Rep. 38, 3883-3896. doi: 10.1007/s11033-010-0504-5
2. Alvarez-Venegas, R. (2010). Regulation by polycomb and trithorax group proteins in arabidopsis. Arabidopsis Book 8, 1-20. doi: 10.1199/tab.0128
3. Alvarez-Venegas, R., and Avramova, Z. (2005). Methylation patterns of histone H3 Lys 4, Lys 9 and Lys 27 in transcriptionally active and inactive Arabidopsis genes and in atx1 mutants. Nucleic Acids Res. 33, 5199-5207. doi: 10.1093/nar/gki830
4. Arasimowicz-Jelonek, M., Kosmala, A., Janus, Ł., Abramowski, D., and Floryszak-Wieczorek, J. (2013). The proteome response of potato leaves to priming agents and S-nitrosoglutathione. Plant Sci. 198, 83-90. doi: 10.1016/j.plantsci.2012.10.004
5. Audergon, P. N. C. B., Catania, S., Kagansky, A., Tong, P., Shukla, M., Pidoux, A. L., et al. (2015). Restricted epigenetic inheritance of H3K9 methylation. Science 348, 132-135. doi: 10.1126/science.1260638
6. Barraza, A., Cabrera-Ponce, J. L., Gamboa-Becerra, R., Luna-Martínez, F., Winkler, R., and Álvarez-Venegas, R. (2015). The Phaseolus vulgaris PvTRX1h gene regulates plant hormone biosynthesis in embryogenic callus from common bean. Front. Plant Sci. 6:577. doi: 10.3389/fpls.2015.00577
7. Barraza, A., Estrada-Navarrete, G., Rodriguez-Alegria, M. E., Lopez-Munguia, A., Merino, E., Quinto, C., et al. (2013). Down-regulation of PvTRE1 enhances nodule biomass and bacteroid number in common bean. New Phytol.197, 194-206. doi: 10.1111/nph.12002
8. Beckers, G. J., Jaskiewicz, M., Liu, Y., Underwood, W. R., He, S. Y., Zhang, S., et al. (2009). Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21, 944-953. doi: 10.1105/tpc.108.062158
9. Berr, A., McCallum, E. J., Alioua, A., Heintz, D., Heitz, T., and Shen, W. H. (2010). Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi. Plant Physiol. 154, 1403-1414. doi: 10.1104/pp.110.161497
10. Bertini, L., Leonardi, L., Caporale, C., Tucci, M., Cascone, N., Di Berardino, I., et al. (2003). Pathogen responsive wheat PR4 genes are induced by plant activators of systemic acquired resistance and wounding. Plant Sci. 164, 1067-1078. doi: 10.1016/S0168-9452(03)00112-2
11. Bertini, L., Proietti, S., Aleandri, M. P., Mondello, F., Sandini, S., and Caporale, C. (2012). Modular structure of HEL protein from Arabidopsis reveals new potential functions for PR-4 proteins. Biol. Chem. 393, 1533-1546. doi: 10.1515/hsz-2012-0225
12. Boller, T., and Felix, G. (2009). A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors.Annu. Rev. Plant Biol. 60, 379-406. doi: 10.1146/annurev.arplant.57.032905.105346
13. Borges, A., Tsai, S. M., and Gomes Caldas, D. G. (2012). Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Rep. 31, 827-838. doi: 10.1007/s00299-011-1204-x
14. Broughton, W. J., and Dilworth, M. J. (1971). Control of leghaemoglobin synthesis in snake beans. Biochem. J. 125, 1075-1080.
15. Bruce, T. J. A., Matthes, M. C., Napier, J. A., and Pickett, J. A. (2007). Stressful memories of plants: evidence and possible mechanisms. Plant Sci. 173, 603-608. doi: 10.1016/j.plantsci.2007.09.002
16. Conrath, U. (2009). "Priming of induced plant defense responses," in Advances in Botanical Research, Vol. 51, ed L. C. Van Loon (London, UK: Elsevier), 361-395.
17. Conrath, U. (2011). Molecular aspects of defence priming. Trends Plant Sci. 16, 524-531. doi: 10.1016/j.tplants.2011.06.004
18. Conrath, U., Beckers, G. J., Flors, V., García-Agustín, P., Jakab, G., Mauch, F., et al. (2006). Priming: getting ready for battle. Mol. Plant Microbe Interact. 19, 1062-1071. doi: 10.1094/MPMI-19-1062
19. Conrath, U., Beckers, G. J., Langenbach, C. J., and Jaskiewicz, M. R. (2015). Priming for enhanced defense. Annu. Rev. Phytopathol. 53, 97-119. doi: 10.1146/annurev-phyto-080614-120132
20. Conrath, U., Chen, Z., Ricigliano, J. R., and Klessig, D. F. (1995). Two inducers of plant defense responses, 2,6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activity in tobacco. Proc. Natl. Acad. Sci. U.S.A. 92, 7143-7147. doi: 10.1073/pnas.92.16.7143
21. Conrath, U., Pieterse, C. M., and Mauch-Mani, B. (2002). Priming in plant-pathogen interactions. Trends Plant Sci. 7, 210-216. doi: 10.1016/S1360-1385(02)02244-6
22. de la Cruz, X., Lois, S., Sánchez-Molina, S., and Martínez-Balbás, M. A. (2005). Do protein motifs read the histone code? Bioessays 27, 164-175. doi: 10.1002/bies.20176
23. De-La-Peña, C., Rangel-Cano, A., and Alvarez-Venegas, R. (2012). Regulation of disease-responsive genes mediated by epigenetic factors: interaction of Arabidopsis-Pseudomonas. Mol. Plant Pathol. 13, 388-398. doi: 10.1111/j.1364-3703.2011.00757.x
24. Ding, B., and Wang, G.-L. (2015). Chromatin versus pathogens: the function of epigenetics in plant immunity. Front. Plant Sci. 6:675. doi: 10.3389/fpls.2015.00675
25. Eberharter, A., and Becker, P. B. (2002). Histone acetylation: a switch between repressive and permissive chromatin. EMBO Rep. 3, 224-229. doi: 10.1093/embo-reports/kvf053
26. Estrada-Navarrete, G., Alvarado-Affantranger, X., Olivares, J. E., Guillén, G., Díaz-Camino, C., Campos, F., et al. (2007). Fast, efficient and reproducible genetic transformation of Phaseolus spp. by Agrobacterium rhizogenes. Nat Protoc. 2, 1819-1824. doi: 10.1038/nprot.2007.259
27. Jaskiewicz, M., Conrath, U., and Peterhänsel, C. (2011). Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep.12, 50-55. doi: 10.1038/embor.2010.186
28. Jones, B. (2015). Histones pass the message on. Nat. Rev. Genet. 16, 3. doi: 10.1038/nrg3876
29. Jung, H. W., Tschaplinski, T. J., Wang, L., Glazebrook, J., and Greenberg, J. T. (2009). Priming in systemic plant immunity. Science 324, 89-91. doi: 10.1126/science.1170025
30. Kanof, N. M. (1967). Allergic sensitization of plants (Bean) to a simple chemical (Copper Sulfate). J. Invest. Dermatol. 48, 275-277. doi: 10.1038/jid.1967.47
31. Katz, V. A., Thulke, O. U., and Conrath, U. (1998). A benzothiadiazole primes parsley cells for augmented elicitation of defense responses. Plant Physiol. 117, 1333-1339. doi: 10.1104/pp.117.4.1333
32. Kauss, H., Theisinger-Hinkel, E., Mindermann, R., and Conrath, U. (1992). Dichloroisonicotinic and salicylic acid, inducers of systemic acquired resistance, enhance fungal elicitor responses in parsley cells. Plant J. 2, 655-660. doi: 10.1111/j.1365-313X.1992.tb00134.x
33. Kessmann, H., Staub, T., Hofmann, C., Maetzke, T., Herzog, J., Ward, E., et al. (1994). Induction of systemic acquired disease resistance in plants by chemicals. Annu. Rev. Phytopathol. 32, 439-459. doi: 10.1146/annurev.py.32.090194.002255
34. King's B medium-Recipe (2009). Cold Spring Harbor Protocols. Available online at:http://cshprotocols.cshlp.org/content/2009/7/pdb.rec11326.short
35. Kinoshita, T., and Seki, M. (2014). Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol. 55, 1859-1863. doi: 10.1093/pcp/pcu125
36. Kohler, A., Schwindling, S., and Conrath, U. (2002). Benzothiazole induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/ NIM1 gene in Arabidopsis. Plant Physiol. 128, 1046-1056. doi: 10.1104/pp.010744
37. Kumar, S., Kumari, R., and Sharma, V. (2015). Transgenerational inheritance in plants of acquired defence against biotic and abiotic stresses: implications and applications.Agric. Res. 4, 109-120. doi: 10.1007/s40003-015-0170-x
38. Li, G., Liu, S., Wang, J., He, J., Huang, H., Zhang, Y., et al. (2014). ISWI proteins participate in the genome-wide nucleosome distribution in Arabidopsis. Plant J. 78, 706-714. doi: 10.1111/tpj.12499
39. Li, Y., Mukherjee, I., Thum, K. E., Tanurdzic, M., Katari, M. S., Obertello, M., et al. (2015). The histone methyltransferase SDG8 mediates the epigenetic modification of light and carbon responsive genes in plants. Genome Biol. 16, 79. doi: 10.1186/s13059-015-0640-2
40. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
41. Luna, E., Bruce, T. J., Roberts, M. R., Flors, V., and Ton, J. (2012). Next-generation systemic acquired resistance. Plant Physiol. 158, 844-853. doi: 10.1104/pp.111.187468
42. Luna, E., López, A., Kooiman, J., and Ton, J. (2014). Role of NPR1 and KYP in long-lasting induced resistance by β-aminobutyric acid. Front. Plant Sci. 5:184. doi: 10.3389/fpls.2014.00184
43. Oostendorp, M., Kunz, W., Dietrich, B., and Staub, T. (2001). Induced disease resistance in plants by chemicals. Eur. J. Plant Pathol. 107, 19-28. doi: 10.1023/A:1008760518772
44. Palma, K., Thorgrimsen, S., Malinovsky, F. G., Fiil, B. K., Nielsen, H. B., Brodersen, P., et al. (2010). Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor. PLoS Pathog. 6:e1001137. doi: 10.1371/journal.ppat.1001137
45. Ragunathan, K., Jih, G., and Moazed, D. (2015). Epigenetic inheritance uncoupled from sequence-specific recruitment. Science 348:1258699. doi: 10.1126/science.1258699
46. Saleh, A., Alvarez-Venegas, R., and Avramova, Z. (2008). An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat. Protoc. 3, 1018-1025. doi: 10.1038/nprot.2008.66
47. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682. doi: 10.1038/nmeth.2019
48. Siegrist, J., Glenewinkel, D., Kolle, C., and Schmidtke, M. (1997). Chemical induced resistance in green bean against bacterial and fungal pathogens. J. Plant Dis. Prot. 104, 599-610.
49. Singh, P., Yekondi, S., Chen, P. W., Tsai, C. H., Yu, C. W., Wu, K., et al. (2014). Environmental history modulates Arabidopsis pattern-triggered immunity in a HISTONE ACETYLTRANSFERASE1-dependent manner. Plant Cell 26, 2676-2688. doi: 10.1105/tpc.114.123356
50. Singh, V., Roy, S., Singh, D., and Nandi, A. K. (2014). Arabidopsis flowering locus D influences systemic-acquired-resistance-induced expression and histone modifications of WRKY genes. J. Biosci. 39, 119-126. doi: 10.1007/s12038-013-9407-7
51. Slaughter, A., Daniel, X., Flors, V., Luna, E., Hohn, B., and Mauch-Mani, B. (2012). Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol. 158, 835-843. doi: 10.1104/pp.111.191593
52. Springer, N. M. (2013). Epigenetics and crop improvement. Trends Genet. 29, 241-247. doi: 10.1016/j.tig.2012.10.009
53. Sticher, L., Mauch-Mani, B., and Métraux, J. P. (1997). Systemic acquired resistance.Annu. Rev. Phytopathol. 35:235-270. doi: 10.1146/annurev.phyto.35.1.235
54. Stroud, H., Otero, S., Desvoyes, B., Ramírez-Parra, E., Jacobsen, S. E., and Gutierrez, C. (2012). Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 109, 5370-5375. doi: 10.1073/pnas.1203145109
55. Thomma, B. P., Penninckx, I. A., Broekaert, W. F., and Cammue, B. P. (2001). The complexity of disease signalling in Arabidopsis. Curr. Opin. Immunol. 13, 63-68. doi: 10.1016/S0952-7915(00)00183-7
56. Thulke, O., and Conrath, U. (1998). Salicylic acid has a dual role in the activation of defense-related genes in parsley. Plant J. 14, 35-42. doi: 10.1046/j.1365-313X.1998.00093.x
57. Ton, J., and Mauch-Mani, B. (2004). Beta-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J. 38, 119-130. doi: 10.1111/j.1365-313X.2004.02028.x
58. van den Burg, H. A., and Takken, F. L. (2009). Does chromatin remodeling mark systemic acquired resistance? Trends Plant Sci. 14, 286-294. doi: 10.1016/j.tplants.2009.02.003
59. Vermeulen, M., Mulder, K. W., Denissov, S., Pijnappel, W. W., van Schaik, F. M., Varier, R. A., et al. (2007). Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131, 58-69. doi: 10.1016/j.cell.2007.08.016
60. Workman, J. L. (2006). Nucleosome displacement in transcription. Genes Dev. 20, 2009-2017. doi: 10.1101/gad.1435706
61. Xu, L., Zhao, Z., Dong, A., Soubigou-Taconnat, L., Renou, J.-P., Steinmetz, A., et al. (2008). Di-and tri-but not monomethylation on histone H3 Lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana. Mol. Cell. Biol. 28:1348-1360. doi: 10.1128/MCB.01607-07
62. Zhang, T., Zhang, W., and Jiang, J. (2015). Genome-wide nucleosome occupancy and positioning and their impact on gene expression and evolution in plants. Plant Physiol.168, 1406-1416. doi: 10.1104/pp.15.00125
63. Zimmerli, L., Jakab, G., Metraux, J. P., and Mauch-Mani, B. (2000). Potentiation of pathogen-specific defense mechanisms in Arabidopsis by beta-aminobutyric acid.Proc. Natl. Acad. Sci. U.S.A. 97, 12920-12925. doi: 10.1073/pnas.230416897