A novel soybean ERF transcription factor, gmERF113, increases resistance to Phytophthora sojae infection in soybean

Frontiers in Plant Science

Volumn 8, Issue , 2017, Pages

  Zhao, Yuanling ^a,b   Chang, Xin ^a   Qi, Dongyue ^a   Dong, Lidong ^a   Wang, Guangjin ^b   Fan, Sujie ^a   Jiang, Liangyu ^a   Cheng, Qun ^a   Chen, Xi ^a   Han, Dan ^a   Xu, Pengfei ^a   Zhang, Shuzhen ^a  

^a NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^b HEILONGJIANG ACADEMY OF AGRICULTURAL SCIENCES   (China)

Author keywords

Activator; AP2 ERF; Glycine max; GmERF113; Phytophthora sojae

Indexed keywords

EID: 85014941519     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2017.00299     Document Type: Article

References (83)

1. Abe, H., Yamaguchi-Shinozaki, K., Urao, T., Iwasaki, T., Hosokawa, D., and Shinozaki, K. (1997). Role of Arabidopsis MYC and MYB homologs in drought-and abscisic acid-regulated gene expression. Plant Cell 9, 1859–1868. doi: 10. 2307/3870530
2. Ali, M. A., Abbas, A., Kreil, D. P., and Bohlmann, H. (2013). Overexpression of the transcription factor RAP2.6 leads to enhanced callose deposition in syncytia and enhanced resistance against the beet cyst nematode Heterodera schachtii in Arabidopsis roots. BMC Plant Biol. 13:47. doi: 10.1186/1471-2229-13-47
3. Asahina, M., Azuma, K., Pitaksaringkarn, W., Yamazaki, T., Mitsuda, N., OhmeTakagi, M., et al. (2011). Spatially selective hormonal control of RAP2.6L and ANAC071 transcription factors involved in tissue reunion in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 16128–16132. doi: 10.1073/pnas.1110443108
4. Bailey, K. L., Gossen, B. D., Gugel, R. K., and Morrall, R. A. A. (2003). Diseases of Field Crops in Canada. Saskatoon, SK: Canadian Phytopathological Society, 155–156.
5. Barah, P., Winge, P., Kusnierczyk, A., Tran, D. H., and Bones, A. M. (2013). Molecular signatures in Arabidopsis thaliana in response to insect attack and bacterial infection. PLoS ONE 8:e58987. doi: 10.1371/journal.pone. 0058987
6. Berrocallobo, M., Molina, A., and Solano, R. (2002). Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J. 29, 23–32. doi: 10.1046/j.1365-313x.2002. 01191.x
7. Bui, L. T., Giuntoli, B., Kosmacz, M., Parlanti, S., and Licausi, F. (2015). Constitutively expressed ERF-VII transcription factors redundantly activate the core anaerobic response in Arabidopsis thaliana. Plant Sci. 236, 37–43. doi: 10.1016/j.plantsci.2015.03.008
8. Cao, Y., Song, F., Goodman, R. M., and Zheng, Z. (2006). Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. J. Plant Physiol. 163, 1167–1178. doi: 10.1016/j.jplph.2005.11.004
9. Chacón, O., González, M., López, Y., Portieles, R., Pujol, M., González, E., et al. (2010). Over-expression of a protein kinase gene enhances the defense of tobacco against Rhizoctonia solani. Gene 452, 54–62. doi: 10.1016/j.gene.2009. 11.011
10. Chen, S. B., Songkumarn, P., Liu, J. L., and Wang, G. L. (2009). A versatile zero background T-vector system for gene cloning and functional genomics. Plant Physiol. 150, 1111–1121. doi: 10.1104/pp.109.137125
11. Chen, S. B., Tao, L. Z., Zeng, L. R., Vega-Sanchez, M. E., Umemura, K., and Wang, G. L. (2006). A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Mol. Plant Pathol. 7, 417–427. doi: 10.1111/J.1364-3703.2006.00346.X
12. Cheong, Y. H., Moon, B. C., Kim, J. K., Kim, C. Y., Kim, M. C., Kim, I. H., et al. (2003). BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol. 132, 1961–1972. doi: 10.1104/pp.103.023176
13. Choi, D. S., and Hwang, B. K. (2011). Proteomics and functional analyses of pepper abscisic acid-responsive 1 (ABR1), which is involved in cell death and defense signaling. Plant Cell 23, 823–842. doi: 10.1105/tpc.110.082081
14. De Boer, K., Tilleman, S., Pauwels, L., Vanden Bossche, R., De Sutter, V., Vanderhaeghen, R., et al. (2011). APETALA2/ETHYLENE response factor and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis. Plant J. 66, 1053–1065. doi: 10.1111/j. 1365-313X.2011.04566.x
15. Dong, L. D., Cheng, Y. X., Wu, J. J., Cheng, Q., Li, W. B., Fan, S. J., et al. (2015). Overexpression of GmERF5, a new member of the soybean EAR motif-containing ERF transcription factor, enhances resistance to Phytophthora sojae in soybean. J. Exp. Bot. 66, 2635–2647. doi: 10.1093/jxb/erv078
16. Dong, X. (2001). Genetic dissection of systemic acquired resistance. Curr. Opin. Plant Biol. 4, 309–314. doi: 10.1016/S1369-5266(00)00178-3
17. Fan, M., Bai, M. Y., Kim, J. G., Wang, T., Oh, E., Chen, L., et al. (2014). The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis. Plant Cell 26, 828–841. doi: 10.1105/tpc.113.121111
18. Fehr, W. R., Caviness, C. E., Burmood, D. T., and Pennington, J. S. (1971). Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci. 11, 929–931. doi: 10.2135/cropsci1971.0011183X001100060051x
19. Fischer, U., and Droge-Laser, W. (2004). Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to tobacco mosaic virus. Mol. Plant Microbe Interact. 17, 1162–1171. doi: 10.1094/MPMI.2004.17.10.1162
20. Friedrichsen, D. M., Nemhauser, J., Muramitsu, T., Maloof, J. N., Alonso, J., Ecker, J. R., et al. (2002). Three redundant brassinosteroid early response genes encode putative bHLH transcription factors required for normal growth. Genetics 162, 1445–1456.
21. Fujimoto, S. Y., Ohta, M., Usui, A., Shinshi, H., and Ohme-Takagi, M. (2000). Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12, 393–404. doi: 10.2307/3870944
22. Gu, Y. Q., Yang, C., Thara, V. K., Zhou, J., and Martin, G. B. (2000). Pti4 is induced by ethylene and salicylic acid and its product is phosphorylated by the Pto kinase. Plant Cell 12, 771–786. doi: 10.2307/3871000
23. Hao, D. Y., Ohme-Takagi, M., and Sarai, A. (1998). Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plants. J. Biol. Chem. 273, 26857–26861. doi: 10.1074/jbc.273.41.26857
24. Holsters, M., De, W. D., Depicker, A., Messens, E., Van, M. M., and Schell, J. (1978). Transfection and transformation of Agrobacterium tumefaciens. Mol. Genet. Genomics 163, 181–187. doi: 10.1007/BF00267408
25. Hu, L. F., and Liu, S. Q. (2011). Genome-wide identification and phylogenetic analysis of the ERF gene family in cucumbers. Genet. Mol. Biol. 34, 624–633. doi: 10.1590/S1415-47572011005000054
26. Huang, B., Jin, L. G., and Liu, J. Y. (2007). Molecular cloning and functional characterization of a DREB1/CBF-like gene (GhDREB1L) from cotton. Sci. China Life Sci. 50, 7–14. doi: 10.1007/s11427-007-0010-8
27. Jiang, L. Y., Wu, J. J., Fan, S. J., Li, W. B., Dong, L. D., and Cheng, Q. (2015). Isolation and characterization of a novel pathogenesis-related protein gene (GmPRP) with induced expression in soybean (Glycine max) during infection with Phytophthora sojae. PLoS ONE 10:e0129932. doi: 10.1371/journal.pone. 0129932
28. Jin, L. G., and Liu, J. Y. (2008). Molecular cloning, expression profile and promoteranalysis of a novel ethylene responsive transcription factor gene GhERF4 from cotton (Gossypium hirstum). Plant Physiol. Biochem. 46, 46–53. doi: 10.1016/j.plaphy.2007.10.004
29. Kamsvågmagnusson, T., Thorsellcederberg, J., Svanberg, A., Von, E. L., Arvidson, J., Mellgren, K., et al. (2014). Role of ethylene response transcription factor (ERF) and its regulation in response to stress encountered by plants. Plant Mol. Biol. Rep. 33, 1–11. doi: 10.1007/s11105-014-0799-9
30. Kim, Y. J., Jang, M. G., Lee, H. J., Jang, G. H., Sukweenadhi, J., Kwon, W. S., et al. (2014). Functional characterization of the pathogenesis-related protein family 10 gene, PgPR10-4, from Panax ginseng in response to environmental stresses. Plant Cell Tiss. Org. 118, 531–543. doi: 10.1007/s11240-014-0505-5
31. Koyama, T., Okada, T., Kitajima, S., Ohme-Takagi, M., Shinshi, H., and Sato, F. (2003). Isolation of tobacco ubiquitin-conjugating enzyme cDNA in a yeast two-hybrid system with tobacco ERF3 as bait and its characterization of specific interaction. J. Exp. Bot. 54, 1175–1181. doi: 10.1093/jxb/erg136
32. Lai, Y., Dang, F. F., Lin, J., Yu, L., Shi, Y. L., Xiao, Y., et al. (2013). Overexpression of a Chinese cabbage BrERF11 transcription factor enhances disease resistance to Ralstonia solanacearum in tobacco. Plant Physiol. Biochem. 62, 70–78. doi: 10.1016/j.plaphy.2012.10.010
33. Li, Z. F., Zhang, L. X., Yu, Y. W., Quan, R. D., Zhang, Z. J., Zhang, H. W., et al. (2011). The ethylene response factor AtERF11 that is transcriptionally modulated by the bZIP transcription factor HY5 is a crucial repressor for ethylene biosynthesis in Arabidopsis. Plant J. 68, 88–99. doi: 10.1111/j.1365-313X.2011.04670.x
34. Liang, H. X., Lu, Y., Liu, H. X., Wang, F. D., Xin, Z. Y., and Zhang, Z. Y. (2008). A novel activator type ERF of Thinopyrum intermedium, TiERF1, positively regulates defence responses. J. Exp. Bot. 59, 3111–3120. doi: 10.1093/jxb/ern165
35. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., et al. (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain, separate two cellular signal transduction pathways in drought and low temperature responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391–1406. doi: 10.1105/tpc.10.8.1391
36. Liu, Y., Zhao, T. J., Liu, J. M., Liu, W. Q., Liu, Q., Yan, Y. B., et al. (2006). The conserved Ala37 in the ERF/AP2 domain is essential for binding with the DRE element and the GCC box. FEBS Lett. 580, 1303–1308. doi: 10.1016/j.febslet. 2006.01.048
37. Lorenzo, O., Piqueras, R., Sanchez-Serrano, J. J., and Solano, R. (2003). Ethylene response factor 1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15, 165–178. doi: 10.1105/tpc.007468
38. Maruyama, Y., Yamoto, N., Suzuki, Y., Chiba, Y., Yamazaki, K., Sato, T., et al. (2013). The Arabidopsis transcriptional repressor ERF9 participates in resistance against necrotrophic fungi. Plant Sci. 213, 79–87. doi: 10.1016/j. plantsci.2013.08.008
39. Mazarei, M., Puthoff, D. P., Hart, J. K., Rodermel, S. R., and Baum, T. J. (2002). Identification and characterization of a soybean ethylene responsive element binding protein gene whose mRNA expression changes during soybean cyst nematode infection. Mol. Plant Microbe Interact. 15, 577–586. doi: 10.1094/MPMI.2002.15.6.577
40. Moffat, C. S., Ingle, R. A., Wathugala, D. L., Saunders, N. J., Knight, H., and Knight, M. R. (2012). ERF5 and ERF6 play redundant roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis. PLoS ONE 7:e35995. doi: 10.1371/journal.pone.0035995
41. Morris, P. F., Savard, M. E., and Ward, E. W. B. (1991). Identification and accumulation of isoflavonoids and isoflavone glucosides in soybean leaves and hypocotyls in resistance responses to Phytophthora megasperma f. sp. glycinea. Physiol. Mol. Plant Pathol. 39, 229–244. doi: 10.1016/0885-5765(91)90006-4
42. Nakano, T., Suzuki, K., Fujimura, T., and Shinshi, H. (2006). Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140, 411–432. doi: 10.1104/pp.105.073783
43. Ohme-Takagi, M., and Shinshi, H. (1995). Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7, 173–182. doi: 10.1105/tpc.7.2.173
44. Okamuro, J. K., Caster, B., Villarroel, R., Montagu, M. V., and Jofuku, K. D. (1997). The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 94, 7076–7081. doi: 10.1073/pnas.94.13.7076
45. Paz, M. M., Shou, H., Guo, Z., Zhang, Z., Banerjee, A. K., and Wang, K. (2004). Assessment of conditions affecting Agrobacterium-mediated soybean transformation using the cotyledonary node explants. Euphytica 136, 167–179. doi: 10.1023/B:EUPH.0000030669.75809.dc
46. Pieterse, C. M. J., Leon-Reyes, A., Vander, E. S., and Van, W. S. (2009). Networking by small- molecule hormones in plant immunity. Nat. Chem. Biol. 5, 308–316. doi: 10.1038/nchembio.164
47. Qi, X. N., Xiao, Y. Y., Fan, Z. Q., Chen, J. Y., Lu, W. J., and Kuang, J. F. (2016). A banana fruit transcriptional repressor MaERF10 interacts with MaJAZ3 to strengthen the repression of JA biosynthetic genes involved in MeJA-mediated cold tolerance. Postharvest Biol. Technol. 120, 222–231. doi: 10.1016/j.postharvbio.2016.07.001
48. Qiu, Z. G., Xu, Z. S., Zheng, T. H., Li, L. C., Chen, M., and Ma, Y. Z. (2011). Screening and identi?cation of proteins interacting with ERF transcription factor W17 in wheat. Acta Agron. Sin. 37, 1–8. doi: 10.3724/SP.J.1006.2011. 00803
49. Rehman, S., and Mahmood, T. (2015). Functional role of DREB and ERF transcription factors: regulating stress-responsive network in plants. Acta Physiol. Plant. 37, 1–14. doi: 10.1007/s11738-015-1929-1
50. Sakuma, Y., Liu, Q., Dubouzet, J. G., Abe, H., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2002). DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration and cold-inducible gene expression. Biochem. Biophys. Res. Commun. 290, 998–1009. doi: 10.1006/bbrc.2001.6299
51. Schwechheimer, C., and Bevan, M. (1998). The regulation of transcription factor activity in plants. Trends Plant Sci. 3, 378–383. doi: 10.1016/S1360-1385(98) 01302-8
52. Seo, J. S., Joo, J., Kim, M. J., Kim, Y. K., Nahm, B. H., Song, S. I., et al. (2011). OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J. 65, 907–921. doi: 10.1111/j.1365-313X.2010.04477.x
53. Sharma, M. K., Kumar, R., Solanke, A. U., Sharma, R., Tyagi, A. K., and Sharma, A. K. (2010). Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol. Genet. Genomics 284, 455–475. doi: 10.1007/s00438-010-0580-1
54. Shinozaki, K., Yamaguchi-Shinozaki, K., and Seki, M. (2003). Regulatory network of gene expression in the drought and cold stress responses. Cur. Opin. Plant Biol. 6, 410–417. doi: 10.1016/S1369-5266(03)00092-X
55. Singh, K. B., Foley, R. C., and Onate-Sanchez, L. (2002). Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 5, 430–436. doi: 10.1016/S1369-5266(02)00289-3
56. Son, G. H., Wan, J., Kim, H. J., Nguyen, X. C., Chung, W. S., Hong, J. C., et al. (2012). Ethylene-responsive element-binding factor 5, ERF5, is involved in chitin-induced innate immunity response. Mol. Plant Microbe Interact. 25, 48–60. doi: 10.1094/MPMI-06-11-0165
57. Song, C. P., Agarwal, M., Ohta, M., Guo, Y., Halfter, U., Wang, P. C., et al. (2005). Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17, 2384–2396. doi: 10.1105/tpc. 105.033043
58. Sugano, S., Sugimoto, T., Takatsuji, H., and Jianga, C. J. (2013). Induction of resistance to Phytophthora sojae in soybean (Glycine max) by salicylic acid and ethylene. Plant Pathol. 62, 1048–1056. doi: 10.1111/ppa.12011
59. Thagun, C., Imanishi, S., Kudo, T., Nakabayashi, R., Ohyama, K., Mori, T., et al. (2016). Jasmonate-responsive ERF transcription factors regulate steroidal glycoalkaloid biosynthesis in tomato. Plant Cell Physiol. 57, 961–975. doi: 10.1093/pcp/pcw067
60. Thomashow, M. F. (1999). Plant cold acclimation: freezing tolerance genes and regulatory mechanism. Annu. Rev. Plant Biol. 50, 571–599. doi: 10.1146/annurev.arplant.50.1.571
61. Tyler, B. M. (2007). Phytophthora sojae: root rot pathogen of soybean and model oomycete. Mol. Plant Pathol. 8, 1–8. doi: 10.1111/j.1364-3703.2006. 00373.x
62. Wan, L. Y., Wu, Y. S., Huang, J. Q., Dai, X. F., Lei, Y., Yan, L. Y., et al. (2014). Identification of ERF genes in peanuts and functional analysis of AhERF008 and AhERF019 in abiotic stress response. Funct. Integr. Genomic. 14, 467–477. doi: 10.1007/s10142-014-0381-4
63. Ward, E. W. B., Lazarovits, G., Unwin, C. H., and Buzzell, R. I. (1979). Hypocotyl reactions and glyceollin in soybeans inoculated with zoospores of Phytophthora megasperma var. sojae. Phytopathology 69, 951–955.
64. Wei, P. C., Tan, F., Gao, X. Q., Zhang, X. Q., Wang, G. Q., Xu, H., et al. (2010). Overexpression of AtDOF4.7, an Arabidopsis DOF family transcription factor, induces floral organ abscission deficiency in Arabidopsis. Plant Physiol. 153, 1031–1045. doi: 10.1104/pp.110.153247
65. Wrather, J. A., Anderson, T. R., Arsyad, D. M., Tan, Y., Ploper, L. D., Porta-Puglia, A., et al. (1997). Soybean disease loss estimates for the top 10 soybean producing countries in 1994. Plant Dis. 81, 107–110. doi: 10.1094/PDIS.1997. 81.1.107
66. Xu, P., Narasimhan, M. L., Samson, T., Coca, M. A., Huh, G. H., Zhou, J., et al. (1998). A nitrilase-like protein interacts with GCC Box DNA-binding proteins involved in ethylene and defense responses. Plant Physiol. 118, 867–874. doi: 10.1104/pp.118.3.867
67. Xu, P. F., Wu, J. J., Allen, X., Li, W. B., Chen, W. Y., Wei, L., et al. (2012). Differentially expressed genes of soybean during infection by Phytophthora sojae. J. Integr. Agr. 11, 368–377.
68. Xu, Z. S., Chen, M., Li, L. C., and Ma, Y. Z. (2011). Functions and application of the AP2/ERF transcription factor family in crop improvement. J. Integr. Plant Biol. 53, 570–585. doi: 10.1111/j.1744-7909.2011.01062.x
69. Xu, Z. S., Xia, L. Q., Chen, M., Cheng, X. G., Zhang, R. Y., Li, L. C., et al. (2007). Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol. Biol. 65, 719–732. doi: 10.1007/s11103-007-9237-9
70. Yamaguchi-Shinozaki, K., and Shinozaki, K. (1994). A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6, 251–264. doi: 10.1105/tpc.6.2.251
71. Yang, Z., Tian, L., Latoszek-Green, M., Brown, D., and Wu, K. (2005). Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol. Biol. 58, 585–596. doi: 10.1007/s11103-005-7294-5
72. Yoo, S. D., Cho, Y. H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565–1572. doi: 10.1038/nprot.2007.199
73. Zhai, Y., Li, J. W., Li, X. W., Lei, T. T., Yan, F., Zhao, Y., et al. (2013a). Isolation and characterization of a novel transcriptional repressor GmERF6 from soybean. Biol. Plant. 57, 26–32. doi: 10.1007/s10535-012-0146-7
74. Zhai, Y., Wang, Y., Li, Y. J., Lei, T. T., Yan, F., Su, L. T., et al. (2013b). Isolation and molecular characterization of GmERF7, a soybean ethylene-response factor that increases salt stress tolerance in tobacco. Gene 513, 174–183. doi: 10.1016/j.gene.2012.10.018
75. Zhang, G. Y., Chen, M., Chen, X. P., Xu, Z. S., Guan, S., Li, L. C., et al. (2008). Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J. Exp. Bot. 59, 4095–4107. doi: 10.1093/jxb/ern248
76. Zhang, G. Y., Chen, M., Chen, X. P., Xu, Z. S., Li, L. C., Guo, J. M., et al. (2010). Isolation and characterization of a novel EAR-motif-containing gene GmERF4 from soybean (Glycine max L.). Mol. Biol. Rep. 37, 809–818. doi: 10.1007/s11033-009-9616-1
77. Zhang, G. Y., Chen, M., Li, L. C., Xu, Z. S., Chen, X. P., Guo, J. M., et al. (2009). Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J. Exp. Bot. 60, 3781–3796. doi: 10.1093/jxb/erp214
78. Zhang, H. W., Huang, Z. J., Xie, B. Y., Chen, Q., Tian, X., Zhang, X. L., et al. (2004). The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220, 262–270. doi: 10.1007/s00425-004-1347-x
79. Zhang, H. W., Zhang, J. F., Quan, R. D., Pan, X. W., Wan, L. Y., and Huang, R. F. (2013). EAR motif mutation of rice OsERF3 alters the regulation of ethylene biosynthesis and drought tolerance. Planta 237, 1443–1451. doi: 10.1007/s00425-013-1852-x
80. Zhang, S. Z., Xu, P. F., Wu, J. J., Allen, X., Zhang, J. X., Li, W. B., et al. (2010). Races of Phytophthora sojae and their virulences on commonly grown soybean varieties in Heilongjiang, China. Plant Dis. 94, 87–91.
81. Zhao, Y., Cheng, S. F., Song, Y. L., Huang, Y. L., Zhou, S. L., Liu, X. Y., et al. (2015). The interaction between rice ERF3 and WOX11 promotes crown root development by regulating gene expression involved in cytokinin signaling. Plant Cell 27, 2469–2483. doi: 10.1105/tpc.15.00227
82. Zhou, J., Tang, X., and Martin, G. B. (1997). The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. Embo. J. 16, 3207–3218. doi: 10.1093/emboj/16. 11.3207
83. Zhu, Z. G., Shi, J. L., Xu, W. R., Li, H. E., He, M. Y., Xu, Y., et al. (2013). Three ERF transcription factors from Chinese wild grapevine Vitis pseudoreticulata participate in different biotic and abiotic stress-responsive pathways. J. Plant Physiol. 170, 923–933. doi: 10.1016/j.jplph.2013.01.017