Abstract
The WRKY transcription factor gene family is known to be involved in plant defense against pathogens and in tolerance to different environmental stresses at different stages of development. The response mechanisms through which these genes act can be influenced by different phytohormones as well as by many trans- and cis-acting elements, making this network an important topic for analysis, but still something complex to fully understand. According to available reports, these genes can also perform important roles in pome species (Malus spp. and Pyrus spp.) metabolism, especially in adaptation of these plants to stressful conditions. Here, we present a quick review of what is known about WRKY genes in Malus and Pyrus genomes offering a simple way to understand what is already known about this topic. We also add information connecting the evolution of these transcription factors with others that can also be found in pomes.
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References
An J, Zhang X, You C, Bi S, Wang X, Hao Y (2019) Md WRKY 40 promotes wounding-induced anthocyanin biosynthesis in association with Md MYB 1 and undergoes Md BT 2-mediated degradation. New Phytol 224:380–395. https://doi.org/10.1111/nph.16008
Bakshi M, Oelmüller R (2014) Wrky transcription factors. Plant Signal Behav 9:37–41. https://doi.org/10.4161/psb.27700
Balan B., Marra F. P., Caruso T., Martinelli F. (2018). Transcriptomic responses to biotic stresses in Malus x domestica: a meta-analysis study. Scientific Reports, 1–12https://doi.org/10.1038/s41598-018-19348-4
Banerjee A, Roychoudhury A (2015) WRKY proteins: signaling and regulation of expression during abiotic stress responses. Scientific World Journal 2015:1–17. https://doi.org/10.1155/2015/807560
Bhatla S. C., and Lal AM. (2018). “Biotic stress,” in Plant Physiology, Development and Metabolism, ed. P. C Bhatla, M. A. Lal (Springer Nature Singapore Pte Ltd.), 1029–1095.
Blum M, Chang HY, Chuguransky S, Grego T, Kandasaamy S, Mitchell A et al (2021) The InterPro protein families and domains database: 20 years on. Nucleic Acids Res 49:D344–D354. https://doi.org/10.1093/nar/gkaa977
Brand LH, Fischer NM, Harter K, Kohlbacher O, Wanke D (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Res 41:9764–9778. https://doi.org/10.1093/nar/gkt732
Chagné D, Crowhurst RN, Pindo M, Thrimawithana A, Deng C, Ireland H et al (2014) The draft genome sequence of European pear (Pyrus communis L. ’Bartlett’). PLoS ONE 9:1–12. https://doi.org/10.1371/journal.pone.0092644
Cai Y., Abdullah M., Cheng X. (2019). “Regulatory sequences of pear Yongping,” in The Pear Genome, ed. S. S. Korban (Springer), 145–152https://doi.org/10.1007/978-3-030-11048-2
Chaki M, Begara-Morales JC, Barroso JB (2020). Oxidative Stress in Plants. https://doi.org/10.3390/antiox9060481
Chen F, Hu Y, Vannozzi A, Wu K, Cai H, Qin Y et al (2017) The WRKY transcription factor family in model plants and crops. Crit Rev Plant Sci 36:311–335. https://doi.org/10.1080/07352689.2018.1441103
Chen X, Li C, Wang H, Guo Z (2019) WRKY transcription factors: evolution, binding, and action. Phytopathology Research 1:1–15. https://doi.org/10.1186/s42483-019-0022-x
Cukrov D, Zermiani M, Brizzolara S, Cestaro A, Licausi F, Luchinat C et al (2016) Extreme hypoxic conditions induce selective molecular responses and metabolic reset in detached apple fruit. Front Plant Sci 7:1–18. https://doi.org/10.3389/fpls.2016.00146
Dalal VK (2021) Modulation of photosynthesis and other proteins during water–stress. Mol Biol Rep. https://doi.org/10.1007/s11033-021-06329-6
Darshan S, Suresha PG, Priya RU, Arya K (2016) Wrky transcription factor: trends in crop improvement. Advances in Life Sciences 5:4344–4346
Dong H, Wang C, Xing C, Yang T, Yan J, Gao J et al (2019) Overexpression of PbrNHX2 gene, a Na+/H+ antiporter gene isolated from Pyrus betulaefolia, confers enhanced tolerance to salt stress via modulating ROS levels. Plant Sci 285:14–25. https://doi.org/10.1016/j.plantsci.2019.04.021
Dong Q, Zhao S, Duan D, Tian Y, Wang Y, Mao K et al (2018) Structural and functional analyses of genes encoding VQ proteins in apple. Plant Sci 272:208–219. https://doi.org/10.1016/j.plantsci.2018.04.029
Dong Q, Zheng W, Duan D, Huang D, Wang Q, Liu C et al (2020) MdWRKY30, a group IIa WRKY gene from apple, confers tolerance to salinity and osmotic stresses in transgenic apple callus and Arabidopsis seedlings. Plant Sci 299:1–12. https://doi.org/10.1016/j.plantsci.2020.110611
Duan GF, Li LJ, Liu QL (2014) A WRKY transcription factor from Malus domestica negatively regulates dehydration stress in transgenic Arabidopsis. Acta Physiol Plant 36:541–548. https://doi.org/10.1007/s11738-013-1434-3
Duan M-R, Nan J, Liang Y-H, Mao P, Lu L, Li L et al (2007) DNA binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein. Nucleic Acids Res 35:1145–1154. https://doi.org/10.1093/nar/gkm001
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206. https://doi.org/10.1016/S1360-1385(00)01600-9
Evans RC, Campbell CS (2002) The origin of the apple subfamily (Maloideae; Rosaceae) is clarified by DNA sequence data from duplicated GBSSI genes. Am J Bot 89:1478–1484. https://doi.org/10.3732/ajb.89.9.1478
Fan H, Wang F, Gao H, Wang L, Xu J, Zhao Z (2011) Pathogen-induced MdWRKY1 in “Qinguan” apple enhances disease resistance. Journal of Plant Biology 54:150–158. https://doi.org/10.1007/s12374-011-9151-1
Feng H, Li H, Zhang M, Song Y, Yuan G, Han Q et al (2019) Responses of Fuji (Malus domestica) and Shandingzi (Malus baccata) apples to Marssonina coronaria infection revealed by comparative transcriptome analysis. Physiol Mol Plant Pathol 106:87–95. https://doi.org/10.1016/j.pmpp.2018.12.007
Gao T, Zhang Z, Liu X, Wu Q, Chen Q, Liu Q et al (2020) Physiological and transcriptome analyses of the effects of exogenous dopamine on drought tolerance in apple. Plant Physiol Biochem 148:260–272. https://doi.org/10.1016/j.plaphy.2020.01.022
Gardiner SE, Norelli JL, de Silva N, Fazio G, Peil A, Malnoy M et al (2012) Putative resistance gene markers associated with quantitative trait loci for fire blight resistance in Malus “Robusta 5” accessions. BMC Genet 13:1. https://doi.org/10.1186/1471-2156-13-25
Gasteiger E, Hoogland C, Gattiker A et al (2005) Protein identification and analysis tools on the ExPASy server. proteomics Protoc. Handb 50:571–607. https://doi.org/10.1385/1-59259-890-0:571
Gu Y, Ji Z, Chi F et al (2015) Bioinformatics and expression analysis of the WRKY gene family in apple. Sci Agric Sin 48:3221–3238. https://doi.org/10.3864/j.issn.0578-1752.2015.16.012
Guo H, Zhang Y, Wang Z, Lin L, Cui M, Long Y et al (2019) Genome-wide identification of WRKY transcription factors in the Asteranae. Plants 8:1–19. https://doi.org/10.3390/plants8100393
HaiFeng X, GuanXian Y, Jing Z, Qi Z, YiCheng W, ChangZhi Q et al (2018) Molecular mechanism of apple MDWRKY18 and MDWRKY40 participating in salt stress. Scientia Agricultura Sinica 51:4514–4521. https://doi.org/10.3864/j.issn.0578-1752.2018.23.010
Han D, Ding H, Chai L, Liu W, Zhang Z, Hou Y et al (2018) Isolation and characterization of MbWRKY1, a WRKY transcription factor gene from Malus baccata (L.) Borkh involved in drought tolerance. Journal of Plant Science 98:1–23. https://doi.org/10.1139/cjps-2017-0355
Han D, Han J, Xu T, Li T, Yao C, Wang Y et al (2021) Isolation and preliminary functional characterization of MxWRKY64, a new WRKY transcription factor gene from Malus xiaojinensis Cheng et Jiang. In Vitro Cellular and Developmental Biology - Plant 57:202–213. https://doi.org/10.1007/s11627-021-10171-7
Han D, Hou Y, Ding H, Zhou Z, Li H, Yang G (2018) Isolation and preliminary functional analysis of MbWRKY4 gene involved in salt tolerance in transgenic tobacco. Int J Agri Biol 20:2045–2052. https://doi.org/10.17957/IJAB/15.0728
Han D, Hou Y, Wang Y, Ni B, Li Z, Yang G (2019) Overexpression of a Malus baccata WRKY transcription factor gene (Mbwrky5) increases drought and salt tolerance in transgenic tobacco. Can J Plant Sci 99:173–183. https://doi.org/10.1139/cjps-2018-0053
Han D, Zhang Z, Ding H, Chai L, Liu W, Li H et al (2018) Isolation and characterization of MbWRKY2 gene involved in enhanced drought tolerance in transgenic tobacco. J Plant Interactions 13:163–172. https://doi.org/10.1080/17429145.2018.1447698
Han D, Zhang Z, Ding H, Wang Y, Liu W, Li H et al (2018) Molecular cloning and functional analysis of MbWRKY3 involved in improved drought tolerance in transformed tobacco. J Plant Interactions 13:329–337. https://doi.org/10.1080/17429145.2018.1478994
Han D, Zhou Z, Du M, Li T, Wu X, Yu J et al (2020) Overexpression of a Malus xiaojinensis WRKY transcription factor gene (MxWRKY55) increased iron and high salinity stress tolerance in Arabidopsis thaliana. In Vitro Cellular Develop Biol - Plant 56:600–609. https://doi.org/10.1007/s11627-020-10129-1
He S., Yuan G., Bian S., Han X., Liu K., Cong P., et al. (2020). Major latex protein MdMLP423 negatively regulates defense against fungal infections in apple. Int J Mole Sci 21https://doi.org/10.3390/ijms21051879
Hou Y, Yu X, Chen W, Wang S, Cao L, Geng X et al (2021) Transcriptome sequencing, data-based screening, and functional investigation of MdWRKY75d and MdWRKY75e in disease-resistant apples. J Plant Interactions 16:462–473. https://doi.org/10.1080/17429145.2021.1981471
Hou Y., Yu X., Chen W., Zhuang W., Wang S., Sun C., et al. (2021b). MdWRKY75e enhances resistance to Alternaria alternata in Malus domestica. Horticulture Research 8https://doi.org/10.1038/s41438-021-00701-0
Hu J, Fang H, Wang J, Yue X, Su M, Mao Z et al (2020) Plant science ultraviolet B-induced MdWRKY72 expression promotes anthocyanin synthesis in apple. Plant Sci 292:1–10. https://doi.org/10.1016/j.plantsci.2019.110377
Huang G., Li T., Li X., Tan D., Jiang Z., Wei Y., et al. (2014). Comparative transcriptome analysis of climacteric fruit of Chinese Pear (Pyrus ussuriensis) reveals new insights into fruit ripening. PLoS ONE 9https://doi.org/10.1371/journal.pone.0107562
Huang X, Li K, Xu X, Yao Z, Jin C, Zhang S (2015) Genome-wide analysis of WRKY transcription factors in white pear (Pyrus bretschneideri) reveals evolution and patterns under drought stress. BMC Genomics 16:1104. https://doi.org/10.1186/s12864-015-2233-6
Imadi, S. R., Gul, A., Dikilitas, M., Karakas, S., Sharma, I., and Ahmad, P. (2016). “Water stress: types, causes , and impact on plant growth and development,” in Water stress and crop plants: a sustainable approach, ed. P. Ahmad (John Wiley & Sons), 343–355. https://doi.org/10.1002/9781119054450.ch21.
Irisarri P, Binczycki P, Errea P, Martens HJ, Pina A (2015) Oxidative stress associated with rootstock-scion interactions in pear/quince combinations during early stages of graft development. J Plant Physiol 176:25–35. https://doi.org/10.1016/j.jplph.2014.10.015
Ishiguro S, Nakamura K (1994) Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5′ upstream regions of genes coding for sporamin and β-amylase from sweet potato. MGG Mole General Gene 244:563–571. https://doi.org/10.1007/BF00282746
Jia X, Zhu Y, Zhang R, Zhu Z, Zhao T, Cheng L et al (2020) Ionomic and metabolomic analyses reveal the resistance response mechanism to saline-alkali stress in Malus halliana seedlings. Plant Physiol Biochem 147:77–90. https://doi.org/10.1016/j.plaphy.2019.12.001
Jiang J, Ma S, Ye N, Jiang M, Cao J, Zhang J (2017) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59:86–101. https://doi.org/10.1111/jipb.12513
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8:275–282. https://doi.org/10.1093/bioinformatics/8.3.275
Kar MM, Raichaudhuri A (2021) Role of microRNAs in mediating biotic and abiotic stress in plants. Plant Gene 26:397–398. https://doi.org/10.1016/j.plgene.2021.100277
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Letunic I, Bork P (2018) 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 46:D493–D496. https://doi.org/10.1093/nar/gkx922
Li C, Meng D, Zhang J, Cheng L (2019) Genome-wide identification and expression analysis of calmodulin and calmodulin-like genes in apple (Malus × domestica). Plant Physiol Biochem 139:600–612. https://doi.org/10.1016/j.plaphy.2019.04.014
Li C., Wu J., Hu K. Di Wei S. W., Sun H. Y., Hu L. Y., et al. (2020a). PyWRKY26 and PybHLH3 cotargeted the PyMYB114 promoter to regulate anthocyanin biosynthesis and transport in red-skinned pears. Horticulture Res 7https://doi.org/10.1038/s41438-020-0254-z
Li H, Li Y, Yu J, Wu T, Zhang J, Tian J et al (2020) MdMYB8 is associated with flavonol biosynthesis via the activation of the MdFLS promoter in the fruits of Malus crabapple. Horticulture Res 7:1–13. https://doi.org/10.1038/s41438-020-0238-z
Li H, Lin J, Yang QS, Li XG, Chang YH (2017) Comprehensive analysis of differentially expressed genes under salt stress in pear (Pyrus betulaefolia) using RNA-Seq. Plant Growth Regul 82:409–420. https://doi.org/10.1007/s10725-017-0266-3
Li Q, Shen J, Li P, Li D, Zheng C, Li D et al (2012) Correlations among six hormone-induced transcription factors and the alcohol acyltransferase gene in apple. J Plant Biol 55:290–297. https://doi.org/10.1007/s12374-011-0261-6
Li W, Pang S, Lu Z, Jin B (2020) Function and mechanism of WRKY transcription factors in abiotic stress responses of plants. Plants 9:1–15. https://doi.org/10.3390/plants9111515
Li X, Guo W, Li J, Yue P, Bu H, Jiang J et al (2020) Histone acetylation at the promoter for the transcription factor PUWRKY31 affects sucrose accumulation in pear fruit. Plant Physiol 182:2035–2046. https://doi.org/10.1104/PP.20.00002
Li X, Li M, Zhou B, Yang Y, Wei Q, Zhang J (2019) Transcriptome analysis provides insights into the stress response crosstalk in apple (Malus × domestica) subjected to drought, cold and high salinity. Sci Rep 9:1–10. https://doi.org/10.1038/s41598-019-45266-0
Li T, Li Y, Sun Z, Xi X, Sha G, Tian Y, Wang C et al (2021) Resveratrol alleviates the KCl salinity stress of Malus hupenensis Rhed. Front Plant Sci 52:1–26. https://doi.org/10.21203/rs.3.rs-148384/v1
Lin M, Chen J, Wu D, Chen K (2021) Volatile profile and biosynthesis of post-harvest apples are affected by the mechanical damage. J Agric Food Chem 69:9716–9724. https://doi.org/10.1021/acs.jafc.1c03532
Liu C., Li H., Lin J., Wang Y., Xu X., Max Cheng Z. M., et al. (2018). Genome-wide characterization of DNA demethylase genes and their association with salt response in Pyrus. Genes 9https://doi.org/10.3390/genes9080398
Liu W, Wang Y, Yu L, Jiang H, Guo Z, Xu H et al (2019) MdWRKY11 participates in anthocyanin accumulation in red-fleshed apples by affecting MYB transcription factors and the photoresponse factor MdHY5. J Agric Food Chem. https://doi.org/10.1021/acs.jafc.9b02920
Liu X, Li X, Wen X, Zhang Y, Ding Y, Zhang Y et al (2021) PacBio full-length transcriptome of wild apple (Malus sieversii) provides insights intocanker disease dynamic response. BMC Genomics 22:1–19. https://doi.org/10.1186/s12864-021-07366-y
Liu Y, Sun J, Zhang M, Yang G, Wang R, Xu J et al (2020) Identification of key genes related to seedlessness by genome-wide detection of structural variation and transcriptome analysis in ‘Shijiwuhe’ pear. Gene 738:144480. https://doi.org/10.1016/j.gene.2020.144480
Liu, Y., Yang, T., Lin, Z., Gu, B., Xing, C., Zhao, L., et al. (2019b). A WRKY transcription factor PbrWRKY53 from Pyrus betulaefolia is involved in drought tolerance and AsA accumulation. Plant Biotechnology Journal, pbi.13099. https://doi.org/10.1111/pbi.13099.
Lopez G, Boini A, Manfrini L, Torres-ruiz JM, Pierpaoli E, Zibordi M et al (2018) Effect of shading and water stress on light interception, physiology and yield of apple trees. Agric Water Manag 210:140–148. https://doi.org/10.1016/j.agwat.2018.08.015
Lui S, Luo C, Zhu L, Sha R, Qu S, Cai B et al (2017) Identification and expression analysis of WRKY transcription factor genes in response to fungal pathogen and hormone treatments in apple (Malus domestica). J Plant Biol 60:215–230. https://doi.org/10.1007/s12374-016-0577-3
Ma Y, Xue H, Zhang F, Jiang Q, Yang S, Yue P et al (2021) The miR156/SPL module regulates apple salt stress tolerance by activating MdWRKY100 expression. Plant Biotechnol J 19:311–323. https://doi.org/10.1111/pbi.13464
Meng D, Li Y, Bai Y, Li M, Cheng L (2016) Genome-wide identification and characterization of WRKY transcriptional factor family in apple and analysis of their responses to waterlogging and drought stress. Plant Physiol Biochem 103:71–83. https://doi.org/10.1016/j.plaphy.2016.02.006
Mingyu Z, Zhengbin Z, Shouyi C, Jinsong Z, Hongbo S (2012) WRKY transcription factor superfamily: structure, origin and functions. Afr J Biotech 11:8051–8059. https://doi.org/10.5897/AJB11.549
Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL et al (2021) Pfam: the protein families database in 2021. Nucleic Acids Res 49:D412–D419. https://doi.org/10.1093/nar/gkaa913
Mittler, R. (2017). “Estresse Abiótico,” in Fisiologia e Desenvolvimento Vegetal, eds. L. Taiz and E. Zeiger (Porto Alegre: Artmed), 731–761. Available at: https://linkinghub.elsevier.com/retrieve/pii/0307441276901217.
Moriya S, Iwanami H, Haji T, Okada K, Yamada M, Yamamoto T et al (2015) Identification and genetic characterization of a quantitative trait locus for adventitious rooting from apple hardwood cuttings. Tree Genet Genomes 11:59. https://doi.org/10.1007/s11295-015-0883-9
Moustafa-Farag M, Mahmoud A, Arnao MB, Sheteiwy MS, Dafea M, Soltan M et al (2020) Melatonin-induced water stress tolerance in plants: recent advances. Antioxidants 9:809. https://doi.org/10.3390/antiox9090809
Mpelasoka BS, Behboudian MH, Green SR (2001) Water use, yield and fruit quality of lysimeter-grown apple trees: responses to deficit irrigation and to crop load. Irrig Sci 0:107–113. https://doi.org/10.1007/s002710100041
Onik J. C., Hu X., Lin Q., Wang Z. (2018). Comparative transcriptomic profiling to understand pre- and post-ripening hormonal regulations and anthocyanin biosynthesis in early ripening apple fruit. Molecules (Basel, Switzerland) 23https://doi.org/10.3390/molecules23081908
Osakabe Y, Osakabe K, Shinozaki K, Tran LSP (2014) Response of plants to water stress. Front Plant Sci 5:1–8. https://doi.org/10.3389/fpls.2014.00086
Ou C, Jiang S, Wang F, Tang C, Hao N (2015) An RNA-Seq analysis of the pear (Pyrus communis L.) transcriptome, with a focus on genes associated with dwarf. Plant Gene 4:69–77. https://doi.org/10.1016/j.plgene.2015.08.003
Phukan UJ, Jeena GS, Shukla RK (2016) WRKY transcription factors: molecular regulation and stress responses in plants. Front Plant Sci 7:1–14. https://doi.org/10.3389/fpls.2016.00760
Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 97:55–74. https://doi.org/10.1016/j.ejmech.2015.04.040
Premathilake AT, Ni J, Shen J, Bai S, Teng Y (2020) Transcriptome analysis provides new insights into the transcriptional regulation of methyl jasmonate-induced flavonoid biosynthesis in pear calli. BMC Plant Biol 20:1–14. https://doi.org/10.1186/s12870-020-02606-x
Qiu HR, Zhou QQ, He XW, Zhang ZY, Zhang SZ, Chen XS et al (2017) Identification of MdWRKY40 promoter specific response to salicylic acid by transcriptome sequencing. Scientia Agricultura Sinica 50:3970–3990. https://doi.org/10.3864/j.issn.0578-1752.2017.20.012
Rinerson, C. I., Rabara, R. C., Tripathi, P., Shen†, Q. J., and Rushton, P. J. (2016). Structure and evolution of WRKY transcription factors. Elsevier Inc. https://doi.org/10.1016/B978-0-12-800854-6.00011-7.
Rinerson CI, Rabara RC, Tripathi P, Shen QJ, Rushton PJ (2015) The evolution of WRKY transcription factors. BMC Plant Biol 15:66. https://doi.org/10.1186/s12870-015-0456-y
Rohrer JR, Robertson KR, Phipps JB (1991) Variation in structure among fruits of Maloideae (Rosaceae). Am J Bot 78:1617–1635. https://doi.org/10.1002/j.1537-2197.1991.tb14528.x
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258. https://doi.org/10.1016/j.tplants.2010.02.006
Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15:5690–5700. https://doi.org/10.1002/j.1460-2075.1996.tb00953.x
Saijo Y, Loo EP (2020) Plant immunity in signal integration between biotic and abiotic stress responses. New Phytol 225:87–104. https://doi.org/10.1111/nph.15989
Shan D., Wang C., Song H., Bai Y., Zhang H., Hu Z., et al. (2021). The MdMEK2–MdMPK6–MdWRKY17 pathway stabilizes chlorophyll levels by directly regulating MdSUFB in apple under drought stress. Plant J 1–15https://doi.org/10.1111/tpj.15480
Sharma S, Ciufo S, Starchenko E, Darji D, Chlumsky L, Karsch-Mizrachi I et al (2018) The NCBI BioCollections database. Database 2018:1–8. https://doi.org/10.1093/database/bay006
Shi HY, Cao LW, Xu Y, Yang X, Liu SL, Liang ZS et al (2021) Transcriptional profiles underlying the effects of salicylic acid on fruit ripening and senescence in pear (Pyrus pyrifolia Nakai). J Integr Agric 20:2424–2437. https://doi.org/10.1016/S2095-3119(20)63568-7
Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131. https://doi.org/10.1016/j.sjbs.2014.12.001
Singh J, Fabrizio J, Desnoues E, Silva JP, Busch W, Khan A (2019) Root system traits impact early fire blight susceptibility in apple (Malus × domestica). BMC Plant Biol 19:1–14. https://doi.org/10.1186/s12870-019-2202-3
Sun J, Shi S, Li J, Yu J, Wang L, Yang X et al (2018) Phylogeny of Maleae (Rosaceae) based on multiple chloroplast regions: implications to genera circumscription. Biomed Res Int 2018:6–9. https://doi.org/10.1155/2018/7627191
Sun X, Jiao C, Schwaninger H, Chao CT, Ma Y, Duan N et al (2020) Phased diploid genome assemblies and pan-genomes provide insights into the genetic history of apple domestication. Nat Genet 52:1423–1432. https://doi.org/10.1038/s41588-020-00723-9
Takatsuji H (1998) Zinc-finger transcription factors in plants. Cellular Mole Life Sci CMLS 54:582–596. https://doi.org/10.1007/s000180050186
Thomas L., Singh I. (2020). Microbe-mediated biotic stress signaling and resistance mechanisms in plants. Plant Stress Biol, 297–334https://doi.org/10.1007/978-981-15-9380-2_10
Ülker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498. https://doi.org/10.1016/j.pbi.2004.07.012
Vico G, Porporato A (2011) From rainfed agriculture to stress-avoidance irrigation: II. Sustainability, crop yield, and profitability. Adv Water Resour 34:272–281. https://doi.org/10.1016/j.advwatres.2010.11.011
Wang M., Tang W., Xiang L., Chen X., Shen X., Yin C., et al. (2021). Involvement of MdWRKY40 in the defense of mycorrhizal apple against Fusarium solani. Research Square, 28. https://doi.org/10.21203/rs.3.rs-915570/v1
Wang M, Vannozzi A, Wang G, Liang Y-H, Tornielli GB, Zenoni S et al (2014) Genome and transcriptome analysis of the grapevine (Vitis vinifera L) WRKY gene family. Horticulture Res 1:14016. https://doi.org/10.1038/hortres.2014.16.
Wang N, Liu W, Zhang T, Jiang S, Xu H, Wang Y et al (2018) Transcriptomic analysis of red-fleshed apples reveals the novel role of MdWRKY11 in flavonoid and anthocyanin biosynthesis. J Agric Food Chem 66:7076–7086. https://doi.org/10.1021/acs.jafc.8b01273
Wang N, Yue ZY, Wang P, Sun X, Gong XQ, Ma FW (2017) Function of Malus prunifolia WRKY6 transcription factor in response to different stresses. Biol Plant 61:284–292. https://doi.org/10.1007/s10535-016-0701-8
Wang Q, Wang M, Zhang X, Hao B, Kaushik SK, Pan Y (2011) WRKY gene family evolution in Arabidopsis thaliana. Genetica 139:973–983. https://doi.org/10.1007/s10709-011-9599-4
Wang Z, Du H, Zhai R, Song L, Ma F, Xu L (2017) Transcriptome analysis reveals candidate genes related to color fading of ‘Red Bartlett’ (Pyrus communis L). Frontiers in Plant Sci 8:10. https://doi.org/10.3389/fpls.2017.00455
Weiß S, Winkelmann T (2017) Transcriptome profiling in leaves representing aboveground parts of apple replant disease affected Malus domestica ‘M26’ plants. Sci Hortic 222:111–125. https://doi.org/10.1016/j.scienta.2017.05.012
Whitaker B (2004) Oxidative stress and superficial scald of apple fruit. HortScience 39:933–937. https://doi.org/10.21273/HORTSCI.39.5.933
Wu S, Wang Y, Zhang J, Wang Y, Yang Y, Chen X et al (2020) How does Malus crabapple resist ozone? Transcriptomics and metabolomics analyses. Ecotoxicol Environ Saf 201:110832. https://doi.org/10.1016/j.ecoenv.2020.110832
Xiang L, Wang M, Junxia H, Jiang W, Zhubing Y, Chen X et al (2021) MdWRKY74 is involved in resistance response to apple replant disease. Plant Growth Regul 1:2021. https://doi.org/10.1007/s10725-021-00766-w
Xiang, L., Wang, M., Pan, F., Wang, G., Jiang, W., Wang, Y., et al. (2021b). Transcriptome analysis Malus domestica ‘M9T337’ root molecular responses to Fusarium solani infection. Physiol Mole Plant Pathol 113, 101567 https://doi.org/10.1016/j.pmpp.2020.101567
Xing L, Qi S, Zhou H, Zhang W, Zhang C, Ma W et al (2020) Epigenomic regulatory mechanism in vegetative phase transition of Malus hupehensis. J Agric Food Chem 68:4812–4829. https://doi.org/10.1021/acs.jafc.0c00478
Yan Y, Zheng X, Apaliya MT, Yang H, Zhang H (2018) Transcriptome characterization and expression profile of defense-related genes in pear induced by Meyerozyma guilliermondii. Postharvest Biol Technol 141:63–70. https://doi.org/10.1016/j.postharvbio.2018.03.011
Yang F., Shen F., Liu Z., He M., Wang Y., Wu T., et al. (2020). Development and validation of functional markers from Dw1 and Dw2 loci to accurately predict apple rootstock dwarfing ability. Research Square, 1–27. https://doi.org/10.21203/rs.2.24669/v2.
Yang P, Chen C, Wang Z, Fan B, Chen Z (1999) A pathogen- and salicylic acid-induced WRKY DNA-binding activity recognizes the elicitor response element of the tobacco class I chitinase gene promoter. Plant J 18:141–149. https://doi.org/10.1046/j.1365-313X.1999.00437.x
Yang T, Li K, Hao S, Zhang J, Song T, Tian J et al (2018) The use of RNA sequencing and correlation network analysis to study potential regulators of crabapple leaf color transformation. Plant Cell Physiol 59:1027–1042. https://doi.org/10.1093/pcp/pcy044
Yang, Y., Yao, G., Yue, W., Zhang, S., and Wu, J. (2015). Transcriptome profiling reveals differential gene expression in proanthocyanidin biosynthesis associated with red/green skin color mutant of pear (Pyrus communis L.). Frontiers in Plant Science 6. https://doi.org/10.3389/fpls.2015.00795.
Yu X, Shi P, Hui C, Miao L, Liu C, Zhang Q et al (2019) Effects of salt stress on the leaf shape and scaling of Pyrus betulifolia Bunge. Symmetry 11:1–15. https://doi.org/10.3390/sym11080991
Zhang F, Wang F, Yang S, Zhang Y, Xue H, Wang Y et al (2019) MdWRKY100 encodes a group I WRKY transcription factor in Malus domestica that positively regulates resistance to Colletotrichum gloeosporioides infection. Plant Sci 286:68–77. https://doi.org/10.1016/j.plantsci.2019.06.001
Zhang Q, Zhang Y, Wang S et al (2019) Characterization of genome-wide microRNAs and their roles in development and biotic stress in pear. Planta 249:693–707. https://doi.org/10.1007/s00425-018-3027-2
Zhang Q, Li Y, Zhang Y, Wu C, Wang SSSS, Hao L et al (2017) Md-MiR156ab and Md-mir395 target WRKY transcription factors to influence apple resistance to leaf spot disease. Front Plant Sci 8:1–14. https://doi.org/10.3389/fpls.2017.00526
Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1–12. https://doi.org/10.1186/1471-2148-5-1
Zhao X-Y, Qi C-H, Jiang H, Zhong M-S, Zhao Q, You C-X et al (2019) MdWRKY46-enhanced apple resistance to Botryosphaeria dothidea by activating the expression of MdPBS3.1 in the salicylic acid signaling pathway. Mol Plant Microbe Interact 32:1391–1401. https://doi.org/10.1094/MPMI-03-19-0089-R
Zhao X-Y, Qi C-H, Jiang H, Zhong M-S, You C-X, Li Y-Y et al (2019) MdHIR4 transcription and translation levels associated with disease in apple are regulated by MdWRKY31. Plant Mol Biol 101:149–162. https://doi.org/10.1007/s11103-019-00898-8
Zhao X. Y., Qi C. H., Jiang H., You C. X., Guan Q. M., Ma F. W., et al. (2019c). The MdWRKY31 transcription factor binds to the MdRAV1 promoter to mediate ABA sensitivity. Horticulture Research 6https://doi.org/10.1038/s41438-019-0147-1
Zheng X, Zhao Y, Shan D, Shi K, Wang L, Li Q et al (2018) MdWRKY9 overexpression confers intensive dwarfing in the M26 rootstock of apple by directly inhibiting brassinosteroid synthetase MdDWF4 expression. New Phytol 217:1086–1098. https://doi.org/10.1111/nph.14891
Zhu J (2016) Review abiotic stress signaling and responses in plants. Cell 167:313–324. https://doi.org/10.1016/j.cell.2016.08.029
Acknowledgements
The authors are thankful to Dr. Luciano C. da Maia, for discussions and suggestions.
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This research received external funding from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES) -Finance Code 001, the Conselho Nacional de Desenvolvimento Científco e Tecnológico (CNPq -process n° 407591/2018–4), and from Fundação de Amparo a Pesquisa do Rio Grande do Sul (FAPERGS).
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W.F. wrote the main manuscript text and K.E.J.F. prepared figures. R.S.S. and R.R.Y. conducted the analysis and contributed to the main text of the manuscript. A.C. led the research. All the authors reviewed the manuscript.
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Felipez, W., de Freitas, K.E.J., dos Santos, R.S. et al. The roles of WRKY transcription factors in Malus spp. and Pyrus spp.. Funct Integr Genomics 22, 713–729 (2022). https://doi.org/10.1007/s10142-022-00886-0
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DOI: https://doi.org/10.1007/s10142-022-00886-0