Please wait a minute...
Journal of Integrative Agriculture  2022, Vol. 21 Issue (1): 153-169    DOI: 10.1016/S2095-3119(21)63619-5
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide identification and analysis of the regulation wheat DnaJ family genes following wheat yellow mosaic virus infection
LIU Ting-ting1, XU Miao-ze1, GAO Shi-qi1, ZHANG Yang2, HU Yang3, JIN Peng1, CAI Lin-na1, CHENG Ye1, CHEN Jian-ping1, YANG Jian1, ZHONG Kai-li1 
1 State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products/Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo 315211, P.R.China
2 Institutes of Biomedical Sciences, Fudan University, Shanghai 200032, P.R.China
3 Institute of Forest Health, Zhejiang Academy of Forestry, Hangzhou 310021, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

DnaJ蛋白最初是在大肠杆菌中鉴定的一种大小约为41kDa的热休克蛋白,其蛋白家族是分子伴侣中最多样化的家族,在蛋白质折叠和各种生理活动的调节中扮演了重要角色,且在植物发育和胁迫应答中发挥重要作用。DnaJ家族蛋白已在许多物种中广泛研究,例如人类,果蝇,蘑菇,西红柿和拟南芥等,但在小麦中的作用以及其与植物病毒之间的相互作用机制却鲜少有研究。在这篇文章中,我们鉴定了236TaDnaJs,并对其保守结构域,基因结构蛋白质基序蛋白质结构染色体定位和共线性以及顺式作用元件进行了全基因组分析。根据分析结果,我们将这些TaDnaJs按其结构域分DJADJBDJC三组,并从分组中随机选择了6个基因进行组织特异性分析和激素胁迫下的基因表达谱分析,结果表明TaDnaJ基因在不同组中存在组织差异表达,DJA组的基因表达集中顶部叶片,对ABAGA更为敏感;DJB组的基因表达水平在根和种子中最高,对ABA更为敏感;DJC组中的基因表达在小麦叶片中最高,其次是根和种子,对SAGA最敏感。另外我们随机选择了17个基因分析植物病毒侵染后基因表达水平的变化,结果显示,在测试的17TaDnaJ基因中,有16个基因在小麦黄花叶病毒(WYMV染后呈现上调表达,这表明TaDnaJ家族可能参与了植物防御反应。随后我们通过酵母两杂交实验验证了WYMV NIaNIb7KD蛋白与WYMV染后表达水平变化最显著的TraesCS7A02G506000相互作用。在这篇文章中,我们探究了DnaJ蛋白介导的胁迫耐受性和敏感性的分子机制,DnaJ基因可能参与了植物对非生物和生物胁迫的抗性。本研究提高了对TaDnaJ基因表达谱认识,并且为TaDnaJ家族与植物防御机制之间的研究提供了一定的研究基础。



Abstract  The co-chaperone DnaJ plays an important role in protein folding and regulation of various physiological activities, and participates in several pathological processes.  DnaJ has been extensively studied in many species including humans, drosophila, mushrooms, tomatoes, and Arabidopsis.  However, few studies have examined the role of DnaJ in wheat (Triticum aestivum), and the interaction mechanism between TaDnaJs and plant viruses.  Here, we identified 236 TaDnaJs and performed a comprehensive genome-wide analysis of conserved domains, gene structure and protein motifs, chromosomal positions and duplication relationships, and cis-acting elements.  We grouped these TaDnaJs according to their domains, and randomly selected six genes from the groups for tissue-specific analysis, and expression profiles analysis under hormone stress, and 17 genes for plant virus infection stress.  In qRT-PCR, we found that among the 17 TaDnaJ genes tested, 16 genes were up-regulated after wheat yellow mosaic virus (WYMV) infection, indicating that the TaDnaJ family is involved in plant defense response.  Subsequent yeast two-hybrid assays verified the WYMV NIa, NIb and 7KD proteins interacted with TaDJC (TraesCS7A02G506000), which had the most significant changes in gene expression levels after WYMV infection.  Insights into the molecular mechanisms of TaDnaJ-mediated stress tolerance and sensitivity could inform different strategies designed to improve crop resistance to abiotic and biotic stress.  This study provides a basis for future investigation of the TaDnaJ family and plant defense mechanisms.
Keywords:  TaDnaJ       WYMV       wheat        genome-wide        expression        hormone        biotic stress        HSP40  
Received: 01 January 2020   Accepted: 30 December 2020
Fund: This work was supported by the National Key R&D Program of China (2018YFD0200507, 2017YFD-0201701, and 2018YFD0200408), the National Natural Science Foundation of China (31901954), the Natural Science Foundation of Ningbo City, China (2019A610415 and 2019A610410), the National Key Project for Research on Transgenic Biology, China (2016ZX08002-001), the China Modern Agricultural Industry Technology System of MOF and MARA (CARS-03), and the K.C. Wong Magna Funding in Ningbo University, China.
About author:  LIU Ting-ting, E-mail: tl612427@foxmail.com; Correspondence YANG Jian, Tel: +86-574-87605539, E-mail: nather2008@163.com; ZHONG Kai-li, Tel: +86-574-87605521, E-mail: zhongkaili@nbu.edu.cn

Cite this article: 

LIU Ting-ting, XU Miao-ze, GAO Shi-qi, ZHANG Yang, HU Yang, JIN Peng, CAI Lin-na, CHENG Ye, CHEN Jian-ping, YANG Jian, ZHONG Kai-li. 2022. Genome-wide identification and analysis of the regulation wheat DnaJ family genes following wheat yellow mosaic virus infection. Journal of Integrative Agriculture, 21(1): 153-169.

Ajit Tamadaddi C, Sahi C. 2016. J domain independent functions of J proteins. Cell Stress & Chaperones, 21, 563–570.
Albert G I, Schell C, Kirschner K M, Schafer S, Naumann R, Muller A, Kretz O, Kuropka B, Girbig M, Hubner N, Krause E, Scholz H, Huber T B, Knobeloch K P, Freund C. 2015. The GYF domain protein CD2BP2 is critical for embryogenesis and podocyte function. Journal of Molecular Cell Biology 7, 402–414.
Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, Grosdidier A, Hernandez C, Ioannidis V, Kuznetsov D, Liechti R, Moretti S, Mostaguir K, Redaschi N, Rossier G, Xenarios I, et al. 2012. ExPASy: SIB bioinformatics resource portal. Nucleic Acids Research, 40, W597–W603.
Bagos P G, Nikolaou E P, Liakopoulos T D, Tsirigos K D. 2010. Combined prediction of Tat and Sec signal peptides with hidden Markov models. Bioinformatics, 26, 2811–2817.
Bailey T L, Boden M, Buske F A, Frith M, Grant C E, Clementi L, Ren J, Li W W, Noble W S. 2009. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Research 37, W202–W208.
Bekh-Ochir D, Shimada S, Yamagami A, Kanda S, Ogawa K, Nakazawa M, Matsui M, Sakuta M, Osada H, Asami T, Nakano T. 2013. A novel mitochondrial DnaJ/Hsp40 family protein BIL2 promotes plant growth and resistance against environmental stress in brassinosteroid signaling. Planta, 237, 1509–1525.
Benkert P, Biasini M, Schwede T. 2011. Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics, 27, 343–350.
Berman H M, Battistuz T, Bhat T N, Bluhm W F, Bourne P E, Burkhardt K, Feng Z, Gilliland G L, Iype L, Jain S, Fagan P, Marvin J, Padilla D, Ravichandran V, Schneider B, Thanki N, Weissig H, Westbrook J D, Zardecki C. 2002. The protein data bank. Acta Crystallographica (Section D, Biological Crystallography), 58, 899–907.
Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Gallo Cassarino T, Bertoni M, Bordoli L, Schwede T. 2014. SWISS-MODEL: Modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research, 42, W252–W258.
Bolser D M, Kerhornou A, Walts B, Kersey P. 2015. Triticeae resources in Ensembl Plants. Plant & Cell Physiology, 56, e3.
Cannon S B, Mitra A, Baumgarten A, Young N D, May G. 2004. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biology, 4, 10.
Cheetham M E, Caplan A J. 1998. Structure, function and evolution of DnaJ: Conservation and adaptation of chaperone function. Cell Stress & Chaperones, 3, 28–36.
Chen C, Chen H, Zhang Y, Thomas H R, Frank M H, He Y, Xia R. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13, 1194–1202.
Cho S Y, Cho W K, Sohn S H, Kim K H. 2012. Interaction of the host protein NbDnaJ with Potato virus X minus-strand stem-loop 1 RNA and capsid protein affects viral replication and movement. Biochemical & Biophysical Research Communications, 417, 451–456.
Doncheva N T, Morris J H, Gorodkin J, Jensen L J. 2019. Cytoscape stringApp: Network analysis and visualization of proteomics data. Journal of Proteome Research, 18, 623–632.
El-Gebali S, Mistry J, Bateman A, Eddy S R, Luciani A, Potter S C, Qureshi M, Richardson L J, Salazar G A, Smart A, Sonnhammer E L L, Hirsh L, Paladin L, Piovesan D, Tosatto S C E, Finn R D. 2019. The Pfam protein families database in 2019. Nucleic Acids Research, 47, D427–D432.
Fan F F, Liu F, Yang X, Wan H, Kang Y. 2020. Global analysis of expression profile of members of DnaJ gene families involved in capsaicinoids synthesis in pepper (Capsicum annuum L.). BMC Plant Biology, 20, 326.
Finn R D, Bateman A, Clements J, Coggill P, Eberhardt R Y, Eddy S R, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer E L, Tate J, Punta M. 2014. Pfam: The protein families database. Nucleic Acids Research, 42, D222–D230.
Galas D J. 2001. Sequence interpretation. Making sense of the sequence. Science, 291, 1257–1260.
Gautam V, Sarkar A K. 2015. Laser assisted microdissection, an efficient technique to understand tissue specific gene expression patterns and functional genomics in plants. Molecular Biotechnology, 57, 299–308.
Goodstein D M, Shu S, Howson R, Neupane R, Hayes R D, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar D S. 2012. Phytozome: A comparative platform for green plant genomics. Nucleic Acids Research, 40, D1178–D1186.
Guo K, Li H, Tan X, Wu M, Lv Q, Liu W, Zhang Y. 2017. Molecular chaperone Jiv promotes the RNA replication of classical swine fever virus. Virus Genes, 53, 426–433.
Hashimoto M, Neriya Y, Keima T, Iwabuchi N, Koinuma H, Hagiwara-Komoda Y, Ishikawa K, Himeno M, Maejima K, Yamaji Y, Namba S. 2016. EXA1, a GYF domain protein, is responsible for loss-of-susceptibility to plantago asiatica mosaic virus in Arabidopsis thaliana. The Plant Journal, 88, 120–131.
He L, Chen X, Yang J, Zhang T, Li J, Zhang S, Zhong K, Zhang H, Chen J, Yang J. 2020. Rice black-streaked dwarf virus-encoded P5-1 regulates the ubiquitination activity of SCF E3 ligases and inhibits jasmonate signaling to benefit its infection in rice. New Phytologist, 225, 896–912.
Hernandez-Garcia C M, Finer J J. 2014. Identification and validation of promoters and cis-acting regulatory elements. Plant Science, 217–218, 109–119.
Hernandez-Garcia C M, Finer J J. 2016. A novel cis-acting element in the GmERF3 promoter contributes to inducible gene expression in soybean and tobacco after wounding. Plant Cell Reports, 35, 303–316.
Hofius D, Maier A T, Dietrich C, Jungkunz I, Bornke F, Maiss E, Sonnewald U. 2007. Capsid protein-mediated recruitment of host DnaJ-like proteins is required for Potato virus Y infection in tobacco plants. Journal of Virology, 81, 11870–11880.
Hristova I. 2012a. Role of heat shock proteins (Hsp) in human and mammalian fertilization and pregnancy. Part I. Akusherstvo I Ginekologiia, 51, 45–49.
Hristova I. 2012b. Role of heat shock proteins (Hsp) in human and mammalian fertilization and pregnancy. Part II. Akusherstvo I Ginekologiia, 51, 37–40.
Hu B, Jin J, Guo A Y, Zhang H, Luo J, Gao G. 2015. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics  31, 1296–1297.
Hwang D J, Tumer N E, Wilson T M. 1998. Chaperone protein GrpE and the GroEL/GroES complex promote the correct folding of tobacco mosaic virus coat protein for ribonucleocapsid assembly in vivo. Archives of Virology,  143, 2203–2214.
Jeffares D C, Penkett C J, Bahler J. 2008. Rapidly regulated genes are intron poor. Trends in Genetics, 24, 375–378.
Kampinga H H, Craig E A. 2010. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nature Reviews Molecular Cell Biology, 11, 579–592.
Knox C, Luke G A, Blatch G L, Pesce E R. 2011. Heat shock protein 40 (Hsp40) plays a key role in the virus life cycle. Virus Research, 160, 15–24.
Kofler M M, Freund C. 2006. The GYF domain. FEBS Journal, 273, 245–256.
Krne P H, Sass J B. 1994. HSP 90 alpha and HSP 90 beta genes are present in the zebrafish and are differentially regulated in developing embryos. Biochemical & Biophysical Research Communications, 204, 746–752.
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones S J, Marra M A. 2009. Circos: An information aesthetic for comparative genomics. Genome Research, 19, 1639–1645.
Kumar J, Kline N L, Masison D C. 2018. Human DnaJB6 antiamyloid chaperone protects yeast from polyglutamine toxicity separately from spatial segregation of aggregates. Molecular and Cellular Biology, 38, doi: 10.1128/MCB.00437-18.
Lamb J, Jarmolinska A I, Michel M, Menendez-Hurtado D, Sulkowska J I, Elofsson A. 2019. PconsFam: An interactive database of structure predictions of pfam families. Journal of Molecular Biology, 431, 2442–2448.
Lang B J, Guerrero-Gimenez M E, Prince T L, Ackerman A, Bonorino C, Calderwood S K. 2019. Heat shock proteins are essential components in transformation and tumor progression: Cancer cell intrinsic pathways and beyond. International Journal of Molecular Sciences, 20, doi: 10.3390/ijms20184507.
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 30, 325–327.
Li L, Andika I B, Xu Y, Zhang Y, Xin X, Hu L, Sun Z, Hong G, Chen Y, Yan F, Yang J, Li J, Chen J. 2017. Differential characteristics of viral siRNAs between leaves and roots of wheat plants naturally infected with wheat yellow mosaic virus, a soil-borne virus. Front Microbiol, 8, 1802.
Liberek K, Marszalek J, Ang D, Georgopoulos C, Zylicz M. 1991. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proceedings of the National Academy of Sciences of the United States of America, 88, 2874–2878.
Luo Y, Fang B, Wang W, Yang Y, Rao L, Zhang C. 2019. Genome-wide analysis of the rice J-protein family: Identification, genomic organization, and expression profiles under multiple stresses. 3 Biotech, 9, 358.
Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R. 2013. Gene duplication as a major force in evolution. Journal of Genetics, 92, 155–161.
Matsui H, Nomura Y, Egusa M, Hamada T, Hyon G S, Kaminaka H, Watanabe Y, Ueda T, Trujillo M, Shirasu K, Nakagami H. 2017. The GYF domain protein PSIG1 dampens the induction of cell death during plant-pathogen interactions. PLoS Genetics, 13, e1007037.
Matsuoka E, Kato N, Hara M. 2019. Induction of the heat shock response in Arabidopsis by heat shock protein 70 inhibitor VER-155008. Functional Plant Biology, 46, 925–932.
Mertz-Henning L M, Pegoraro C, Maia L C, Venske E, Rombaldi C V, Costa de Oliveira A. 2016. Expression profile of rice Hsp genes under anoxic stress. Genetics and Molecular Research, 15, doi: 10.4238/gmr.15027954.
Miernyk J A. 2001. The J-domain proteins of Arabidopsis thaliana: An unexpectedly large and diverse family of chaperones. Cell Stress & Chaperones, 6, 209–218.
Muller A, Rinck G, Thiel H J, Tautz N. 2003. Cell-derived sequences in the N-terminal region of the polyprotein of a cytopathogenic pestivirus. Journal of Virology, 77, 10663–10669.
Muller M, Munne-Bosch S. 2017. Hormone profiling in plant tissues. Methods in Molecular Biology, 1497, 249–258.
Muthusamy S K, Dalal M, Chinnusamy V, Bansal K C. 2017. Genome-wide identification and analysis of biotic and abiotic stress regulation of small heat shock protein (HSP20) family genes in bread wheat. Journal of Plant Physiology,  211, 100–113.
Newburn L R, White K A. 2015. Cis-acting RNA elements in positive-strand RNA plant virus genomes. Virology,  479–480, 434–443.
Nielsen H, Engelbrecht J, von Heijne G, Brunak S. 1996. Defining a similarity threshold for a functional protein sequence pattern: The signal peptide cleavage site. Proteins, 24, 165–177.
Ohki T, Sasaya T, Maoka T. 2019. Cylindrical inclusion protein of wheat yellow mosaic virus is involved in differential infection of wheat cultivars. Phytopathology, 109, 1475–1480.
Panchy N, Lehti-Shiu M, Shiu S H. 2016. Evolution of gene duplication in plants. Plant Physiology, 171, 2294–2316.
Park M Y, Kim S Y. 2014. The Arabidopsis J protein AtJ1 is essential for seedling growth, flowering time control and ABA response. Plant & Cell Physiology, 55, 2152–2163.
Piecuch A, Oblak E. 2013. Mechanisms of yeast resistance to environmental stress. Advances in Hygiene and Experimental Medicine, 67, 238–254.
Prasad B D, Goel S, Krishna P. 2010. In silico identification of carboxylate clamp type tetratricopeptide repeat proteins in Arabidopsis and rice as putative co-chaperones of Hsp90/Hsp70. PLoS ONE, 5, e12761.
Pulido P, Leister D. 2018. Novel DNAJ-related proteins in Arabidopsis thaliana. New Phytologist, 217, 480–490.
Qian J, Chen J, Liu Y F, Yang L L, Li W P, Zhang L M. 2014. Overexpression of Arabidopsis HsfA1a enhances diverse stress tolerance by promoting stress-induced Hsp expression. Genetics & Molecular Research, 13, 1233–1243.
Rajan V B, D’Silva P. 2009. Arabidopsis thaliana J-class heat shock proteins: Cellular stress sensors. Functional & Integrative Genomics, 9, 433–446.
Rampelt H, Mayer M P, Bukau B. 2018. Nucleotide exchange factors for Hsp70 chaperones. Methods in Molecular Biology, 1709, 179–188.
Reiser L, Subramaniam S, Li D, Huala E. 2017. Using the Arabidopsis Information Resource (TAIR) to find information about arabidopsis genes. Current Protocols in Bioinformatics, 60, 11111–111145.
Ritossa F M. 1964. Experimental activation of specific loci in polytene chromosomes of drosophila. Experimental Cell Research, 35, 601–607.
Sery A, Housset D, Serre L, Bonicel J, Hatchikian C, Frey M, Roth M. 1994. Crystal structure of the ferredoxin I from Desulfovibrio africanus at 2.3 A resolution. Biochemistry,  33, 15408–15417.
Shimizu T, Yoshii A, Sakurai K, Hamada K, Yamaji Y, Suzuki M, Namba S, Hibi T. 2009. Identification of a novel tobacco DnaJ-like protein that interacts with the movement protein of tobacco mosaic virus. Archives of Virology, 154, 959–967.
Sporn Z A, Hines J K. 2015. Hsp40 function in yeast prion propagation: Amyloid diversity necessitates chaperone functional complexity. Prion, 9, 80–89.
Sterrenberg J N, Blatch G L, Edkins A L. 2011. Human DNAJ in cancer and stem cells. Cancer Letters, 312, 129–142.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology & Evolution, 30, 2725–2729.
Tan J, Bernstein J A. 2013. Fertility and human seminal plasma (HSP) hypersensitivity. Annals of Allergy Asthma & Immunology, 111, 145–146.
Tutar L, Tutar Y. 2010. Heat shock proteins; an overview. Current Pharmaceutical Biotechnology, 11, 216–222.
Urano E, Morikawa Y, Komano J. 2013. Novel role of HSP40/DNAJ in the regulation of HIV-1 replication. Journal of Acquired Immune Deficiency Syndromes, 64, 154–162.
Verchot J. 2012. Cellular chaperones and folding enzymes are vital contributors to membrane bound replication and movement complexes during plant RNA virus infection. Frontiers in Plant Science, 3, 275.
Walsh P, Bursac D, Law Y C, Cyr D, Lithgow T. 2004. The J-protein family: Modulating protein assembly, disassembly and translocation. EMBO Reports, 5, 567–571.
Wang G, Cai G, Kong F, Deng Y, Ma N, Meng Q. 2014. Overexpression of tomato chloroplast-targeted DnaJ protein enhances tolerance to drought stress and resistance to Pseudomonas solanacearum in transgenic tobacco. Plant Physiology & Biochemistry, 82, 95–104.
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer F T, de Beer T A P, Rempfer C, Bordoli L, Lepore R, Schwede T. 2018. SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Research, 46, W296–W303.
Wilkins M R, Gasteiger E, Bairoch A, Sanchez J C, Williams K L, Appel R D, Hochstrasser D F. 1999. Protein identification and analysis tools in the ExPASy server. Methods in Molecular Biology, 112, 531–552.
Winterberg B, Uhlmann S, Linne U, Lessing F, Marahiel M A, Eichhorn H, Kahmann R, Schirawski J. 2010. Elucidation of the complete ferrichrome A biosynthetic pathway in Ustilago maydis. Molecular Microbiology, 75, 1260–1271.
Xu Y, Hu L, Li L, Zhang Y, Sun B, Meng X, Zhu T, Sun Z, Hong G, Chen Y, Yan F, Yang J, Li J, Chen J. 2018. Ribotypes of Polymyxa graminis in wheat samples infected with Soilborne Wheat Viruses in China. Plant Disease, 102, 948–954.
Yan J, Ma Z, Xu X, Guo A Y. 2014. Evolution, functional divergence and conserved exon-intron structure of bHLH/PAS gene family. Molecular Genetics & Genomics, 289, 25–36.
Yang J, Zhang T Y, Liao Q S, He L, Li J, Zhang H M, Chen X, Li J, Yang J, Li J B, Chen J P. 2018. Chinese wheat mosaic virus-induced gene silencing in monocots and dicots at low temperature. Frontiers in Plant Science, 9, 1627.
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden T L. 2012. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics,  13, 134.
Yeh F L, Hsu T. 2002. Differential regulation of spontaneous and heat-induced HSP 70 expression in developing zebrafish (Danio rerio). Journal of Experimental Zoology,  293, 349–359.
Yu X, Duan X, Zhang R, Fu X, Ye L, Kong H, Xu G, Shan H. 2016. Prevalent exon–intron structural changes in the APETALA1/FRUITFULL, SEPALLATA, AGAMOUS-LIKE6, and FLOWERING LOCUS C MADS-Box gene subfamilies provide new insights into their evolution. Frontiers in Plant Science, 7, 598.
Yu X, Han J, Wang E, Xiao J, Hu R, Yang G, He G. 2019. Genome-wide identification and homoeologous expression analysis of PP2C genes in wheat (Triticum aestivum L.). Frontiers in Genetics, 10, doi: 10.3389/fgene.2019.00561.
Zhang B, Qiu H L, Qu D H, Ruan Y, Chen D H. 2018. Phylogeny-dominant classification of J-proteins in Arabidopsis thaliana and Brassica oleracea. Genome, 61, 405–415.
Zhang T, Liu P, Zhong K, Zhang F, Xu M, He L, Jin P, Chen J, Yang J. 2019. Wheat yellow mosaic virus NIb interacting with host light induced protein (LIP) facilitates its infection through perturbing the abscisic acid pathway in wheat. Biology (Basel), 8, doi: 10.3390/biology8040080.
Zhou X, Park B, Choi D, Han K. 2018. A generalized approach to predicting protein–protein interactions between virus and host. BMC Genomics, 19, 568.
Zong T, Yin J, Jin T, Wang L, Luo M, Li K, Zhi H. 2020. A DnaJ protein that interacts with soybean mosaic virus coat protein serves as a key susceptibility factor for viral infection. Virus Research, 281, 197870.

No related articles found!
No Suggested Reading articles found!