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Journal of Integrative Agriculture  2022, Vol. 21 Issue (6): 1658-1672    DOI: 10.1016/S2095-3119(21)63816-9
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide characterization and expression analysis of WRKY family genes during development and resistance to Colletotrichum fructicola in cultivated strawberry (Fragaria×ananassa Duch.)
ZOU Xiao-hua, DONG Chao, LIU Hai-ting, GAO Qing-hua

Shanghai Key Laboratory of Protected Horticultural Technology, Forestry and Fruit Tree Research Institute, Shanghai Academy of Agricultural Sciences (SAAS), Shanghai 201403, P.R.China

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摘要  

该研究根据2019年公布的栽培草莓“Camarosa”全基因组信息,在“Camarosa”基因组中鉴定出了222个FaWRKY基因,并均匀分布在7条染色体上。通过系统发育分析表明,222个FaWRKY候选基因分为3组,其中41个在Ⅰ组,142个在Ⅱ组,39个在Ⅲ组。比较不同栽培草莓基因组中WRKY基因发现,WRKY基因外显子-内含子结构和基序在不同栽培草莓基因组中具有进化多样性。此外,通过实时荧光定量PCR分析发现FaWRKY133在草莓叶片中表达相对较高;FaWRKY63在根中特异表达。而且,FaWRKY在果实发育不同阶段的草莓种子中有特异性的积累,其中FaWRKY1781425, 263436414345在成熟果实的种子中特异性表达。进一步发现FaWRKY179205的表达量在浸染草莓炭疽病菌C. fructicola之后不同时期均显著性下调。此研究表明,不同栽培草莓基因组中WRKY基因具有进化多样性,其中栽培草莓 “Camarosa”中的FaWRKY基因表达具有组织特异性和果实发育特异性,而且FaWRKY基因的表达也显著性响应草莓炭疽菌C. fructicola的侵染。这对草莓FaWRKY基因的功能研究提供了新的理论基础




Abstract  Based on the recently published whole-genome sequence of cultivated strawberry ‘Camarosa’, in this study, 222 FaWRKY genes were identified in the ‘Camarosa’ genome.  Phylogenetic analysis showed that the 222 FaWRKY candidate genes were classified into three groups, of which 41 were in group I, 142 were in group II, and 39 were in group III.  The 222 FaWRKY genes were evenly distributed among the seven chromosomes.  The exon–intron structures and motifs of the WRKY genes had evolutionary diversity in different cultivated strawberry genomes.  Regarding differential expression, the expression of FaWRKY133 was relatively high in leaves, while FaWRKY63 was specifically expressed in roots.  FaWRKY207, 59, 46, 182, 156, 58, 39, 62 and 115 were up-regulated during achene development from the green to red fruit transition.  FaWRK181, 166 and 211 were highly expressed in receptacles at the ripe fruit stage.  One interesting finding was that FaWRKY179 and 205 were significantly repressed after Colletotrichum fructicola inoculation in both ‘Benihoppe’ and ‘Sweet Charlie’ compared with Mock.  The data reported here provide a foundation for further comparative genomics and analyses of the distinct expression patterns of FaWRKY genes in various tissues and in response to C. fructicola inoculation.
Keywords:  Fragaria×ananassa        FaWRKY       Colletotrichum fructicola        structure        evolution  
Received: 01 February 2021   Accepted: 23 August 2021
Fund: 

This work was supported by the National Natural Science Foundation of China (31601731).

About author:  ZOU Xiao-hua, E-mail: zouxh_113@126.com; Correspondence GAO Qing-hua, E-mail: qhgao20338@sina.com

Cite this article: 

ZOU Xiao-hua, DONG Chao, LIU Hai-ting, GAO Qing-hua. 2022. Genome-wide characterization and expression analysis of WRKY family genes during development and resistance to Colletotrichum fructicola in cultivated strawberry (Fragaria×ananassa Duch.). Journal of Integrative Agriculture, 21(6): 1658-1672.

Aragüez I, Osorio S, Hoffmann T, Rambla J L, Medina-Escobar N, Granell A, Botella Á M, Schwab W, Valpuesta V. 2013. Eugenol production in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics. Plant Physiology, 163, 946–958.
Aslam R, Wali Q, Sarwar M, Naeem M, Bakar M A. 2019. A comprehensive overview of transcription factors (WRKY, NAC and BZIP) in plants. Journal of Biosciences, 14, 495–509.
Ayadi M, Hanana M, Kharrat N, Merchaoui H, Marzoug R B, Lauvergeat V, Rebaï A, Mzid R. 2016. The WRKY transcription factor family in Citrus: Valuable and useful candidate genes for citrus breeding. Applied Biochemistry & Biotechnology, 180, 516–543.
Bailey T L, Boden M, Buske F A, Frith M, Grant C E, Clementi L, Ren J Y, Li W W, Noble W S. 2009. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Research, 37, 202–208.
Banerjee A, Roychoudhury A. 2015. WRKY proteins: Signaling and regulation of expression during abiotic stress responses. The Scientific World Journal, 2015, 807560.
Brand L H, Fischer N M, Klaus H, Oliver K, Dierk W. 2013. Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Research, 41, 9764–9778.
Chen C, Chen H, Zhang Y, Thomas H R, Xia R. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13, 1194–1202.
Chen P, Liu Q Z. 2019. Genome-wide characterization of the WRKY gene family in cultivated strawberry (Fragaria×ananassa Duch.) and the importance of several group III members in continuous cropping. Scientific Reports, 9, 8423.
Estradajohnson E, Csukasi F, Pizarro C M, Vallarino J G, Kiryakova Y, Vioque A, Brumos J, Medinaescobar N, Botella M A, Alonso J M. 2017. Transcriptomic analysis in strawberry fruits reveals active auxin biosynthesis and signaling in the ripe receptacle. Frontiers in Plant Science, 8, 889–891.
Eulgem T, Rushton P J, Robatzek S, Somssich I E. 2000. The WRKY superfamily of plant transcription factors. Trends in Plant Science, 5, 199–206.
Fu M, Crous P W, Bai Q, Zhang P F, Xiang J, Guo Y S, Zhao F F, Yang M M, Hong N, Xu W X, Wang G P. 2018. Colletotrichum species associated with anthracnose of Pyrus spp. in China. Persoonia Molecular Phylogeny and Evolution of Fungi, 42, 1–35.
Fait A, Hanhineva K, Beleggia R, Dai N, Rogachev I, Nikiforova V J, Fernie A R, Aharoni A. 2008. Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development. Plant Physiology, 48, 730–750.
Garrido G J, Higuera J J, Muoz B J, Amil F, Caballero J L. 2019. The VQ motif-containing proteins in the diploid and octoploid strawberry. Scientific Reports, 9, 4942.
Gonzalez A, Brown M, Hatlestad G, Akhavan N, Smith T, Hembd A, Moore J, Montes D, Mosley T, Resendez J. 2016. TTG2 controls the developmental regulation of seed coat tannins in Arabidopsis by regulating vacuolar transport steps in the proanthocyanidin pathway. Developmental Biology, 419, 54–63.
Gu Y B, Ji Z R, Chi F M, Qiao Z, Xu C N, Zhang J X, Dong Q L, Zhou Z S. 2015. Bioinformatics and expression analysis of the WRKY gene family in apple. Scientia Agricultura Sinica, 48, 3221–3238. (in Chinese)
Hirayama Y, Asano S, Watanabe K, Sakamoto Y, Ozaki M, Okayama K O, Ohki S T, Tojo M. 2016. Control of Colletotrichum fructicola on strawberry with a foliar spray of neutral electrolyzed water through an overhead irrigation system. Journal of General Plant Pathology, 82, 186–189.
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.
Huang Y, Feng C Z, Ye Q, Wu W H, Chen Y F. 2016. Arabidopsis WRKY6 transcription factor acts as a positive regulator of abscisic acid signaling during seed germination and early seedling development. PLoS Genetics, 12, e1005833.
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. Molecular & General Genetics, 244, 563–571.
Jiang J, Zhai H, Li H, Wang Z, Chen Y, Hong N, Wang G, Chofong N, Xu W. 2014. Identification and characterization of Colletotrichum fructicola causing black spots on young fruits related to bitter rot of pear (Pyrus bretschneideri Rehd.) in China. Crop Protection, 58, 41–48.
Jiang J J, Ma S H, Ye N H, Jiang M, Cao J H, Zhang J H. 2016. WRKY transcription factors in plant responses to stresses. Journal of Integrative Plant Biology, 59, 86–101.
Jiang Y J, Liang G, Yang S Z, Yu D Q. 2014. Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence. Plant Cell, 26, 230–245.
Kloth K J, Wiegers G L, Busscherlange J, Haarst J C, Kruijer W, Bouwmeester H J, Dicke M, Jongsma M A. 2016. AtWRKY22 promotes susceptibility to aphids and modulates salicylic acid and jasmonic acid signalling. Journal of Experimental Botany, 67, 3383–3396.
Knoth C, Ringler J, Dangl J L, Eulgem T. 2007. Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Molecular Plant–Microbe Interactions, 20, 120–128.
Lagacé M, Matton D P. 2004. Characterization of a WRKY transcription factor expressed in late torpedo-stage embryos of Solanum chacoense. Planta, 219, 185–189.
Li W, Wang H, Yu D. 2016. Arabidopsis WRKY transcription factors WRKY12 and WRKY13 oppositely regulate flowering under short-day conditions. Molecular Plant, 9, 1492–1503.
Liu H T, Ly W Y, Tian S H, Zou X H, Duan K. 2019. The SWEET family genes in strawberry: Identification and expression profiling during fruit development. South African Journal of Botany, 125, 176–187.
Mackenzie S J, Legard D E, Timmer L W, Chandler C K, Peres N A. 2006. Resistance of strawberry cultivars to crown rot caused by Colletotrichum gloeosporioides isolates from Florida is nonspecific. Plant Disease, 90, 1091–1097.
Miao Y, Laun T, Zimmermann P, Zentgraf U. 2004. Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Molecular Biology, 55, 853–867.
Nam M H, Park M S, Lee H D, Yu S H. 2013. Taxonomic re-evaluation of Colletotrichum gloeosporioides isolated from strawberry in Korea. Plant Pathology Journal, 29, 317–322.
Pandey S P, Somssich I E. 2009. The role of WRKY transcription factors in plant immunity. Plant Physiology, 150, 1648–1655.
Rinerson C I, Rabara R C, Tripathi P, Shen Q J, Rushton P J. 2015. The evolution of WRKY transcription factors. BMC Plant Biology, 15, 1–18.
Ross C A, Liu Y, Shen Q J. 2007. The WRKY gene family in rice (Oryza sativa). Journal of Integrative Plant Biology, 49, 827–842.
Rushton D L, Tripathi P, Rabara R C, Lin J, Ringler P, Boken A K, Langum T J, Smidt L, Boomsma D D, Emme N J. 2011. WRKY transcription factors: Key components in abscisic acid signalling. Plant Biotechnology Journal, 10, 2–11.
Silke R, Somssich I E. 2002. Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes & Development, 16, 1139–1149.
Singh K B, Fole R C, Oate-Sánchez L. 2002. Transcription factors in plant defense and stress responses. Current Opinion in Plant Biology, 5, 430–436.
Sudhir K, Glen S, Koichiro T. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology & Evolution, 7, 1870–1873.
Ülker B, Somssich I E. 2004. WRKY transcription factors: From DNA binding towards biological function. Current Opinion in Plant Biology, 7, 491–498.
Valérie L, Ian M, Caroline L, Laurence T, John M K, Armand S. 2009. Expression profiling and functional analysis of Populus WRKY23 reveals a regulatory role in defense. New Phytologist, 184, 48–70.
Vallarino J G, Merchante C, Sánchez-Sevilla J F, de Luis Balaguer M A, Pott D M, Ariza M T, Casaal A, Posé D, Vioque A, Amaya I, Willmitzer L, Solano R, Sozzani R, Fernie A R, Botella M A, Giovannoni J J, Valpuesta V, Osorio S. 2019. Characterizing the involvement of FaMADS9 in the regulation of strawberry fruit receptacle development. Plant Biotechnology Journal, 18, 929–943.
Wang D, Amornsiripanitch N, Dong X. 2006. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathogens, 2, e123.
Wang H Z, Avci U, Nakashima J, Hahn M G, Chen F, Dixon R A. 2010. Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proceedings of the National Academy of Sciences of the United States of America, 51, 22338–22343.
Wang Y, Li W, Chang H, Zhou J, Luo Y, Zhang K, Zuo J, Wang B. 2020. SRNAome and transcriptome analysis provide insight into strawberry fruit ripening. Genomics, 112, 2369–2378.
Wei W, Hu Y, Han Y T, Zhang K, Zhao F L, Feng J Y. 2016. The WRKY transcription factors in the diploid woodland strawberry Fragaria vesca: Identification and expression analysis under biotic and abiotic stresses. Plant Physiology and Biochemistry, 105, 129–144.
Xie T, Chen C, Li C, Liu J, Liu C, He Y. 2018. Genome-wide investigation of WRKY gene family in pineapple: Evolution and expression profiles during development and stress. BMC Genomics, 19, 490.
Ye J, Wang X, Hu T, Zhang F, Wang B, Li C, Yang T, Li H Y, Lu Y, Giovannoni J, Zhang Y, Ye Z. 2017. An InDel in the promoter of Al-ACTIVATED MALATE TRANSPORTER9 selected during tomato domestication determines fruit malate contents and aluminum tolerance. Plant Cell, 29, 2249–2268.
Zha Q, Xi X, Jiang A, Wang S, Tian Y. 2016. Changes in the protective mechanism of photosystem II and molecular regulation in response to high temperature stress in grapevines. Plant Physiology & Biochemistry, 101, 43–53.
Zhang L Q, Huang X, He C, Zhang Q Y, Zou, X, Duan K, Gao Q G. 2018. Novel fungal pathogenicity and leaf defense strategies are revealed by simultaneous transcriptome analysis of Colletotrichum fructicola and strawberry infected by this fungus. Frontiers in Plant Science, 9, 434.
Zhang Q Y, Liu F C, Duan K, Wang F, Wang Y X, Gao Q H. 2014. Effects of salicylic acid on the expression of FaNBS20 gene resonsive to Colletotrichum gloeosporioides infection in Fragaria×ananassa. Acta Horticulturae Sinica, 41, 53–62. (in Chinese)
Zhang Y, Wang L. 2005. The WRKY transcription factor superfamily: Its origin in eukaryotes and expansion in plants. BMC Evolutionary Biology, 5, 1.
Zhao Y Q, Wu X X, Zheng H, Lu H, Guo Y D. 2012. Regenerating haploid callus and plantlets from anther culture of strawberry ‘Sweet Charlie’ and ‘Akihime’. Journal of China Agricultural University, 17, 39–45. (in Chinese)
Zhou H, Li Y, Zhang Q, Ren S, Shen Y, Qin L, Xing Y. 2016. Genome-wide analysis of the expression of WRKY family genes in different developmental stages of wild strawberry (Fragaria vesca) fruit. PLoS ONE, 11, e0154312.
Zou X H, Guo G, Zhang L, Duan K, Gao Q. 2018. Identification of FaNBS-encoding genes responsive to Colletotrichum fructicola infection in strawberry (Fragaria×ananassa Duchase). Australasian Plant Pathology, 47, 499–510.
Zou X H, Yang H Y, Kuang H Y, Gao Q H. 2020. A preliminary study on tissue culture and rapid propagation of virus-free plantlets of Benihoppe strawberry. Northern Horticulture, 5, 39–45. (in Chinese)
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