Genome-Wide Identification and Variation Analysis of JAZ Family Reveals BnaJAZ8.C03 Involved in the Resistance to Plasmodiophora brassicae in Brassica napus
Abstract
:1. Introduction
2. Results
2.1. Genome-Wide Identification of JAZ in B. napus, B. rapa and B. oleracea
2.2. Phylogenetic Analysis of JAZ Family among Arabidopsis, B. napus, B. rapa, and B. oleracea
2.3. Conserved Motifs and Gene Structure Analysis Displayed That the JAZ Proteins Clustered in the Same Group Shared Similar Motif Composition and Distribution Order
2.4. Chromosomal Location and Expression Pattern of JAZ Genes in B. napus under Multiple Treatments
2.5. Haplotype Analysis of SNPs and SVs Reveals BnaJAZ8.C03 Associated with the Resistance to P. brassicae
2.6. Interaction Network of Key JAZs Identified Their Functional Partner in B. napus
3. Discussion
4. Materials and Methods
4.1. Plant Materials, Sequencing and Phenotype Data
4.2. Identification of the JAZs in B. napus, B. rapa and B. oleracea
4.3. Phylogenetic, Gene Structure and Conserved Motif Analyses
4.4. Chromosomal Location and Expression Pattern Analysis of JAZ Genes in B. napus under Multiple Treatment
4.5. Structural Variation Detection, Resistance Difference Analysis and Interaction Network Construction of Target Genes
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Nguyen, T.H.; Goossens, A.; Lacchini, E. Jasmonate: A hormone of primary importance for plant metabolism. Curr. Opin. Plant Biol. 2022, 67, 102197. [Google Scholar] [CrossRef] [PubMed]
- Wasternack, C.; Feussner, I. The Oxylipin Pathways: Biochemistry and Function. Annu. Rev. Plant Biol. 2018, 69, 363–386. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Wang, D.D.; Fang, X.; Chen, X.Y.; Mao, Y.B. Plant Specialized Metabolism Regulated by Jasmonate Signaling. Plant Cell Physiol. 2019, 60, 2638–2647. [Google Scholar] [CrossRef] [PubMed]
- Wasternack, C.; Strnad, M. Jasmonates are signals in the biosynthesis of secondary metabolites—Pathways, transcription factors and applied aspects—A brief review. New Biotechnol. 2019, 48, 1–11. [Google Scholar] [CrossRef]
- Zhang, F.; Yao, J.; Ke, J.; Zhang, L.; Lam, V.Q.; Xin, X.F.; Zhou, X.E.; Chen, J.; Brunzelle, J.; Griffin, P.R. Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling. Nature 2015, 525, 269–273. [Google Scholar] [CrossRef] [Green Version]
- Xie, D. COI1: An Arabidopsis Gene Required for Jasmonate-Regulated Defense and Fertility. Science 1998, 280, 1091–1094. [Google Scholar] [CrossRef]
- Pauwels, L.; Goossens, A. The JAZ proteins: A crucial interface in the jasmonate signaling cascade. Plant Cell 2011, 23, 3089–3100. [Google Scholar] [CrossRef] [Green Version]
- Thines, B.; Katsir, L.; Melotto, M.; Niu, Y.; Mandaokar, A.; Liu, G.; Nomura, K.; He, S.Y.; Howe, G.A.; Browse, J. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 2007, 448, 661–665. [Google Scholar] [CrossRef]
- Chico, J.M.; Chini, A.; Fonseca, S.; Solano, R. JAZ repressors set the rhythm in jasmonate signaling. Curr. Opin. Plant Biol. 2008, 11, 486–494. [Google Scholar] [CrossRef]
- Yan, J.; Li, H.; Li, S.; Yao, R.; Deng, H.; Xie, Q.; Xie, D. The Arabidopsis F-box protein CORONATINE INSENSITIVE1 is stabilized by SCFCOI1 and degraded via the 26S proteasome pathway. Plant Cell 2013, 25, 486–498. [Google Scholar] [CrossRef]
- Derelle, E.; Ferraz, C.; Rombauts, S.; Rouze, P.; Worden, A.Z.; Robbens, S.; Partensky, F.; Degroeve, S.; Echeynie, S.; Cooke, R.; et al. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc. Natl. Acad. Sci. USA 2006, 103, 11647–11652. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chung, H.S.; Howe, G.A. A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell 2009, 21, 131–145. [Google Scholar] [CrossRef] [Green Version]
- Pauwels, L.; Barbero, G.F.; Geerinck, J.; Tilleman, S.; Grunewald, W.; Perez, A.C.; Chico, J.M.; Bossche, R.V.; Sewell, J.; Gil, E.; et al. NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 2010, 464, 788–791. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chini, A.; Fonseca, S.; Chico, J.M.; Fernandez-Calvo, P.; Solano, R. The ZIM domain mediates homo- and heteromeric interactions between Arabidopsis JAZ proteins. Plant J. 2009, 59, 77–87. [Google Scholar] [CrossRef] [PubMed]
- Yan, Y.; Stolz, S.; Chetelat, A.; Reymond, P.; Pagni, M.; Dubugnon, L.; Farmer, E.E. A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 2007, 19, 2470–2483. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Melotto, M.; Mecey, C.; Niu, Y.; Chung, H.S.; Katsir, L.; Yao, J.; Zeng, W.; Thines, B.; Staswick, P.; Browse, J.; et al. A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J. 2008, 55, 979–988. [Google Scholar] [CrossRef] [Green Version]
- Yamada, S.; Kano, A.; Tamaoki, D.; Miyamoto, A.; Shishido, H.; Miyoshi, S.; Taniguchi, S.; Akimitsu, K.; Gomi, K. Involvement of OsJAZ8 in jasmonate-induced resistance to bacterial blight in rice. Plant Cell Physiol. 2012, 53, 2060–2072. [Google Scholar] [CrossRef] [Green Version]
- Ye, H.; Du, H.; Tang, N.; Li, X.; Xiong, L. Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol. Biol. 2009, 71, 291–305. [Google Scholar] [CrossRef]
- Wang, Y.K.; Qiao, L.Y.; Bai, J.F.; Duan, W.J.; Yuan, S.H. Genome-wide characterization of JASMONATE-ZIM DOMAIN transcription repressors in wheat (Triticum aestivum L.). BMC Genom. 2017, 18, 152. [Google Scholar] [CrossRef] [Green Version]
- Han, Y.; Luthe, D. Identification and evolution analysis of the JAZ gene family in maize. BMC Genom. 2021, 22, 256. [Google Scholar] [CrossRef]
- Thireault, C.; Shyu, C.; Yoshida, Y.; St Aubin, B.; Campos, M.L.; Howe, G.A. Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis. Plant J. 2015, 82, 669–679. [Google Scholar] [CrossRef]
- Gimenez-Ibanez, S.; Boter, M.; Ortigosa, A.; Garcia-Casado, G.; Chini, A.; Lewsey, M.G.; Ecker, J.R.; Ntoukakis, V.; Solano, R. JAZ2 controls stomata dynamics during bacterial invasion. New Phytol. 2017, 213, 1378–1392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, D.; Cai, H.; Luo, X.; Bai, X.; Deyholos, M.K.; Chen, Q.; Chen, C.; Ji, W.; Zhu, Y. Over-expression of a novel JAZ family gene from Glycine soja, increases salt and alkali stress tolerance. Biochem. Biophys. Res. Commun. 2012, 426, 273–279. [Google Scholar] [CrossRef] [PubMed]
- Zhang, G.; Yan, X.; Zhang, S.; Zhu, Y.; Zhang, X.; Qiao, H.; van Nocker, S.; Li, Z.; Wang, X. The jasmonate-ZIM domain gene VqJAZ4 from the Chinese wild grape Vitis quinquangularis improves resistance to powdery mildew in Arabidopsis thaliana. Plant Physiol. Biochem. 2019, 143, 329–339. [Google Scholar] [CrossRef]
- Jiang, Y.; Yu, D. The WRKY57 transcription factor affects the expression of Jasmonate ZIM-Domain genes transcriptionally to compromise Botrytis cinerea resistance. Plant Physiol. 2016, 171, 2771–2782. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xiong, L.Z.; Zhang, T.; Wu, H.; Ye, H.Y.; Yao, R.F. OsJAZ9 acts as a transcriptional regulator in jasmonate signaling and modulates salt stress tolerance in rice. Plant Sci. 2015, 232, 1–12. [Google Scholar]
- Demianski, A.J.; Chung, K.M.; Kunkel, B.N. Analysis of Arabidopsis JAZ gene expression during Pseudomonas syringae pathogenesis. Mol. Plant Pathol. 2012, 13, 46–57. [Google Scholar] [CrossRef]
- Chai, A.L.; Xie, X.W.; Shi, Y.X.; Li, B.J. Research status of clubroot (Plasmodiophora brassicae) on cruciferous crops in China. Can. J. Plant Pathol. 2014, 36 (Suppl. S1), 142–153. [Google Scholar] [CrossRef]
- Li, L.; Long, Y.; Li, H.; Wu, X. Comparative transcriptome analysis reveals key pathways and hub genes in rapeseed during the early stage of Plasmodiophora brassicae infection. Front. Genet. 2019, 10, 1275. [Google Scholar] [CrossRef] [Green Version]
- Hu, J.; Chen, B.; Zhao, J.; Zhang, F.; Xie, T.; Xu, K.; Gao, G.; Yan, G.; Li, H.; Li, L.; et al. Genomic selection and genetic architecture of agronomic traits during modern rapeseed breeding. Nat. Genet. 2022, 54, 694–704. [Google Scholar] [CrossRef]
- Jiang, Y.; Qiu, Y.; Hu, Y.; Yu, D. Heterologous expression of AtWRKY57 confers drought tolerance in Oryza sativa. Front. Plant Sci. 2016, 7, 145. [Google Scholar] [CrossRef] [PubMed]
- Behrens, F.H.; Schenke, D.; Hossain, R.; Ye, W.; Schemmel, M.; Bergmann, T.; Hader, C.; Zhao, Y.; Ladewig, L.; Zhu, W.; et al. Suppression of abscisic acid biosynthesis at the early infection stage of Verticillium longisporum in oilseed rape (Brassica napus). Mol. Plant Pathol. 2019, 20, 1645–1661. [Google Scholar] [CrossRef] [PubMed]
- Reiner, T.; Hoefle, C.; Huckelhoven, R. A barley SKP1-like protein controls abundance of the susceptibility factor RACB and influences the interaction of barley with the barley powdery mildew fungus. Mol. Plant Pathol. 2016, 17, 184–195. [Google Scholar] [CrossRef] [PubMed]
- Shen, J.; Zou, Z.; Xing, H.; Duan, Y.; Zhu, X.; Ma, Y.; Wang, Y.; Fang, W. Genome-wide analysis reveals stress and hormone responsive patterns of JAZ family genes in Camellia Sinensis. Int. J. Mol. Sci. 2020, 21, 2433. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, W.; Xia, X.C.; Han, L.H.; Ni, P.; Yan, J.Q.; Tao, M.; Huang, G.Q.; Li, X.B. Genome-wide identification and characterization of JAZ gene family in upland cotton (Gossypium hirsutum). Sci. Rep. 2017, 7, 2788. [Google Scholar] [CrossRef] [Green Version]
- Xie, S.; Cui, L.; Lei, X.; Yang, G.; Li, J.; Nie, X.; Ji, W. The TIFY gene family in wheat and its progenitors: Genome-Wide iIdentification, evolution and expression analysis. Curr. Genom. 2019, 20, 371–388. [Google Scholar] [CrossRef]
- Zhang, Y.; Gao, M.; Singer, S.D.; Fei, Z.; Wang, H.; Wang, X. Genome-wide identification and analysis of the TIFY gene family in grape. PLoS ONE 2012, 7, e44465. [Google Scholar] [CrossRef] [Green Version]
- Zhu, D.; Bai, X.; Luo, X.; Chen, Q.; Cai, H.; Ji, W.; Zhu, Y. Identification of wild soybean (Glycine soja) TIFY family genes and their expression profiling analysis under bicarbonate stress. Plant Cell Rep. 2013, 32, 263–272. [Google Scholar] [CrossRef]
- Dai, Z.; Dong, S.; Miao, H.; Liu, X.; Han, J.; Li, C.; Gu, X.; Zhang, S. Genome-wide identification of TIFY genes and their response to various pathogen infections in cucumber (Cucumis sativus L.). Sci. Hortic. 2022, 295, 110814. [Google Scholar] [CrossRef]
- He, X.; Kang, Y.; Li, W.; Liu, W.; Xie, P.; Liao, L.; Huang, L.; Yao, M.; Qian, L.; Liu, Z.; et al. Genome-wide identification and functional analysis of the TIFY gene family in the response to multiple stresses in Brassica napus L. BMC Genom. 2020, 21, 736. [Google Scholar] [CrossRef]
- Liu, X.; Zhao, C.; Yang, L.; Zhang, Y.; Wang, Y.; Fang, Z.; Lv, H. Genome-wide identification, expression profile of the TIFY gene family in Brassica oleracea var. capitata, and their divergent response to various pathogen infections and phytohormone treatments. Genes 2020, 11, 127. [Google Scholar]
- Gopal, S.; Jong-In, P.; Abdul, K.M.; Ill-Sup, N. A genome-wide analysis reveals stress and hormone responsive patterns of TIFY family genes in Brassica rapa. Front. Plant Sci. 2016, 7, 936. [Google Scholar]
- Bai, Y.; Meng, Y.; Huang, D.; Qi, Y.; Chen, M. Origin and evolutionary analysis of the plant-specific TIFY transcription factor family. Genomics 2011, 98, 128–136. [Google Scholar] [CrossRef] [PubMed]
- Chalhoub, B.; Denoeud, F.; Liu, S.; Parkin, I.A.; Tang, H.; Wang, X.; Chiquet, J.; Belcram, H.; Tong, C.; Samans, B.; et al. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 2014, 345, 950–953. [Google Scholar] [CrossRef] [Green Version]
- Yang, N.; Liu, J.; Gao, Q.; Gui, S.; Chen, L.; Yang, L.; Huang, J.; Deng, T.; Luo, J.; He, L.; et al. Genome assembly of a tropical maize inbred line provides insights into structural variation and crop improvement. Nat. Genet. 2019, 51, 1052–1059. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.; Du, H.; Li, P.; Shen, Y.; Peng, H.; Liu, S.; Zhou, G.A.; Zhang, H.; Liu, Z.; Shi, M.; et al. Pan-genome of wild and cultivated soybeans. Cell 2020, 182, 162–176.e113. [Google Scholar] [CrossRef]
- Sun, H.J.; Uchii, S.; Watanabe, S.; Ezura, H. A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics. Plant Cell Physiol. 2006, 47, 426–431. [Google Scholar] [CrossRef]
- Guan, J.; Xu, Y.; Yu, Y.; Fu, J.; Ren, F.; Guo, J.; Zhao, J.; Jiang, Q.; Wei, J.; Xie, H. Genome structure variation analyses of peach reveal population dynamics and a 1.67 Mb causal inversion for fruit shape. Genome Biol. 2021, 22, 13. [Google Scholar] [CrossRef]
- Guo, J.; Cao, K.; Deng, C.; Li, Y.; Zhu, G.; Fang, W.; Chen, C.; Wang, X.; Wu, J.; Guan, L.; et al. An integrated peach genome structural variation map uncovers genes associated with fruit traits. Genome Biol. 2020, 21, 258. [Google Scholar] [CrossRef]
- Zhou, H.; Ma, R.; Gao, L.; Zhang, J.; Zhang, A.; Zhang, X.; Ren, F.; Zhang, W.; Liao, L.; Yang, Q.; et al. A 1.7-Mb chromosomal inversion downstream of a PpOFP1 gene is responsible for flat fruit shape in peach. Plant Biotechnol. J. 2021, 19, 192–205. [Google Scholar] [CrossRef]
- Li, S.; Xu, B.; Niu, X.; Lu, X.; Cheng, J.; Zhou, M.; Hooykaas, P.J.J. JAZ8 interacts with VirE3 Attenuating Agrobacterium mediated root Tumorigenesis. Front. Plant Sci. 2021, 12, 685533. [Google Scholar] [CrossRef] [PubMed]
- Ingle, R.A.; Stoker, C.; Stone, W.; Adams, N.; Smith, R.; Grant, M.; Carre, I.; Roden, L.C.; Denby, K.J. Jasmonate signalling drives time-of-day differences in susceptibility of Arabidopsis to the fungal pathogen Botrytis cinerea. Plant J. 2015, 84, 937–948. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, L.; Luo, Y.; Chen, B.; Xu, K.; Zhang, F.; Li, H.; Huang, Q.; Xiao, X.; Zhang, T.; Hu, J.; et al. A Genome-wide association study reveals new loci for resistance to clubroot disease in Brassica napus. Front. Plant Sci. 2016, 7, 1483. [Google Scholar] [CrossRef] [PubMed]
- Song, J.M.; Liu, D.X.; Xie, W.Z.; Yang, Z.; Guo, L.; Liu, K.; Yang, Q.Y.; Chen, L.L. BnPIR: Brassica napus pan-genome information resource for 1689 accessions. Plant Biotechnol. J. 2020, 19, 412–414. [Google Scholar] [CrossRef] [PubMed]
- Cai, X.; Wu, J.; Liang, J.; Lin, R.; Zhang, K.; Cheng, F.; Wang, X. Improved Brassica oleracea JZS assembly reveals significant changing of LTR-RT dynamics in different morphotypes. Theor. Appl. Genet. 2020, 133, 13. [Google Scholar] [CrossRef]
- Zhang, L.; Cai, X.; Wu, J.; Liu, M.; Wang, X. Improved Brassica rapa reference genome by single-molecule sequencing and chromosome conformation capture technologies. Hortic. Res. 2018, 5, 11. [Google Scholar] [CrossRef] [Green Version]
- Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An iIntegrative tToolkit developed for interactive analyses of big biological data. Mol. Plant 2020, 13, 9. [Google Scholar] [CrossRef]
- Edgar, R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32, 1792–1797. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)). Method 2001, 25, 402–408. [Google Scholar] [CrossRef]
- Layer, R.M.; Hall, I.M.; Quinlan, A.R. LUMPY: A probabilistic framework for structural variant discovery. Genome Biol. 2014, 15, R84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, X.; Schulz-Trieglaff, O.; Shaw, R.; Barnes, B.; Schlesinger, F.; Källberg, M.; Cox, A.J.; Kruglyak, S.; Saunders, C.T. Manta: Rapid detection of structural variants and indels for germline and cancer sequencing applications. Bioinformatics 2016, 32, 1220–1222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jeffares, D.C.; Jolly, C.; Hoti, M.; Speed, D.; Sedlazeck, F.J. Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast. Nat. Commun. 2017, 8, 14061. [Google Scholar] [CrossRef] [PubMed]
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Li, L.; Ji, G.; Guan, W.; Qian, F.; Li, H.; Cai, G.; Wu, X. Genome-Wide Identification and Variation Analysis of JAZ Family Reveals BnaJAZ8.C03 Involved in the Resistance to Plasmodiophora brassicae in Brassica napus. Int. J. Mol. Sci. 2022, 23, 12862. https://doi.org/10.3390/ijms232112862
Li L, Ji G, Guan W, Qian F, Li H, Cai G, Wu X. Genome-Wide Identification and Variation Analysis of JAZ Family Reveals BnaJAZ8.C03 Involved in the Resistance to Plasmodiophora brassicae in Brassica napus. International Journal of Molecular Sciences. 2022; 23(21):12862. https://doi.org/10.3390/ijms232112862
Chicago/Turabian StyleLi, Lixia, Gaoxiang Ji, Wenjie Guan, Fang Qian, Hao Li, Guangqin Cai, and Xiaoming Wu. 2022. "Genome-Wide Identification and Variation Analysis of JAZ Family Reveals BnaJAZ8.C03 Involved in the Resistance to Plasmodiophora brassicae in Brassica napus" International Journal of Molecular Sciences 23, no. 21: 12862. https://doi.org/10.3390/ijms232112862
APA StyleLi, L., Ji, G., Guan, W., Qian, F., Li, H., Cai, G., & Wu, X. (2022). Genome-Wide Identification and Variation Analysis of JAZ Family Reveals BnaJAZ8.C03 Involved in the Resistance to Plasmodiophora brassicae in Brassica napus. International Journal of Molecular Sciences, 23(21), 12862. https://doi.org/10.3390/ijms232112862