CsBZIP40 confers resistance against citrus bacterial canker by repressing CsWRKY43-CsPrx53/CsSOD13 cascade mediated ROS scavenging

Qiang Li , Xiujuan Qin , Miao Zhang , Qiyuan Yu , Ruirui Jia , Jie Fan , Xin Huang , Jia Fu , Chenxi Zhang , Baohang Xian , Wen Yang , Qin Long , Aihong Peng , Lixiao Yao , Shanchun Chen , Yongrui He

Horticulture Research ›› 2023, Vol. 10 ›› Issue (8) : 138

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Horticulture Research ›› 2023, Vol. 10 ›› Issue (8) :138 DOI: 10.1093/hr/uhad138
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CsBZIP40 confers resistance against citrus bacterial canker by repressing CsWRKY43-CsPrx53/CsSOD13 cascade mediated ROS scavenging
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Abstract

As the bacterial etiologic agent causing citrus bacterial canker (CBC), Xanthomonas citri subsp. citri (Xcc) seriously impacts citrus plantation and fruit production globally. In an earlier study, we demonstrated that CsBZIP40 can positively impact CBC resistance in the sweet orange (Citrus sinensis). However, the mechanistic basis for the protective benefits conferred by CsBZIP40 is yet to be delineated. Here, we show that CsBZIP40 positively regulates CBC resistance and reactive oxygen species (ROS) homeostasis in transgenic sweet orange overexpressing CsBZIP40. CsBZIP40 directly binds to the TGA-box of the CsWRKY43 promoter to repress its transcriptional activity. CsWRKY43 overexpression induces CBC susceptibility in transgenic sweet oranges. In contrast, its inhibition produces strong resistance to CBC. CsWRKY43 directly binds to the W-boxes of the CsPrx53 and CsSOD13 promoters to positively regulate the activities of these antioxidant enzymes, resulting in the negative regulation of ROS homeostasis and CBC resistance in sweet orange plants. CsPrx53/CsSOD13 knockdown enhances ROS accumulation and CBC resistance. Overall, our results outline a regulatory pathway through which CsBZIP40 transcriptionally represses CsWRKY43-CsPrx53/CsSOD13 cascade-mediated ROS scavenging in a manner conducive to CBC resistance. These mechanisms underscore the potential importance of CsBZIP40, CsWRKY43, CsPrx53, and CsSOD13, providing promising strategies for the prevention of CBC.

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Qiang Li, Xiujuan Qin, Miao Zhang, Qiyuan Yu, Ruirui Jia, Jie Fan, Xin Huang, Jia Fu, Chenxi Zhang, Baohang Xian, Wen Yang, Qin Long, Aihong Peng, Lixiao Yao, Shanchun Chen, Yongrui He. CsBZIP40 confers resistance against citrus bacterial canker by repressing CsWRKY43-CsPrx53/CsSOD13 cascade mediated ROS scavenging. Horticulture Research, 2023, 10 (8) : 138 DOI:10.1093/hr/uhad138

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Acknowledgements

The authors would like to thank all the reviewers who participated in the review and MJEditor (www.mjeditor.com) for its linguistic assistance during the preparation of this manuscript. This study was funded by the National Key Research and Development Program of China (2022YFD1201600, 2021YFD1600800), National Natural Sciences Foundation of China (32 202 425), Earmarked Funds for the China Agriculture Research System (CARS-26).

Author contributions

Q.Li, Y.H. and S.C. conceived and designed the experiments; Q.Li., X.Q., Q.Y., R.J., Q.Long, A.P., L.Y., J.Fan, J.Fu, and C.Z. performed the experiments; Q.Li, J.Fu, M.Z., B.X., W.Y., and Y.H. analysed the data; Q.Li wrote this article; all authors read and approved the final manuscript.

Data availability

The raw RNA-Seq data are archived as Sequence Read Archive (SRA) in the National Center for Biotechnology Information (NCBI) with an accession number PRJNA909460. Other data supporting the findings of this study are available within the article and supplementary data.

Conflict of interest statement

The authors declare no conflict of interests.

References

[1]

Reboledo G, Agorio A, Ponce De León I . Moss transcription factors regulating development and defense responses to stress. J Exp Bot. 2022; 73: 4546-61

[2]

Li Q, Jia R, Dou W et al. CsBZIP40, a BZIP transcription factor in sweet orange, plays a positive regulatory role in citrus bacterial canker response and tolerance. PLoS One. 2019; 14: e0223498

[3]

Barah P, Jayavelu ND, Mundy J et al. Genome scale transcriptional response diversity among ten ecotypes of Arabidopsis thaliana during heat stress . Front Plant Sci. 2013; 4: 532

[4]

Jin Z, Xu W, Liu A . Genomic surveys and expression analysis of bZIP gene family in castor bean (Ricinus communis L.). Planta. 2014; 239: 299-312

[5]

Nijhawan A, Jain M, Tyagi AK et al. Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol. 2008; 146: 333-50

[6]

Zhang M, Liu Y, Li Z et al. The bZIP transcription factor GmbZIP15 facilitates resistance against. iScience. 2021; 24: 102642

[7]

He Q, Cai H, Bai M et al. A soybean bZIP transcription factor gene GmbZIP2 confers drought and salt resistances in transgenic plants . Int J Mol Sci. 2020; 21: 670

[8]

Lim CW, Baek W, Lim S et al. Expression and functional roles of the pepper pathogen-induced bZIP transcription factor CabZIP2 in enhanced disease resistance to bacterial pathogen infection. Mol Plant-Microbe Interact. 2015; 28: 825-33

[9]

Li Q, Yu H, Cao PB et al. Explosive tandem and segmental duplications of multigenic families in Eucalyptus grandis. Genome Biol Evol. 2015; 7: 1068-81

[10]

Mittler R, Zandalinas SI, Fichman Y et al. Reactive oxygen species signalling in plant stress responses. Nat Rev Mol Cell Biol. 2022; 23: 663-79

[11]

Hirt H . Aquaporins link ROS signaling to plant immunity. Plant Physiol. 2016; 171: 1540

[12]

Li Q, Hu AH, Qi JJ et al. CsWAKL08, a pathogen-induced wall-associated receptor-like kinase in sweet orange, confers resistance to citrus bacterial canker via ROS control and JA signaling. Hortic Res. 2020; 7: 15

[13]

Mittler R, Blumwald E . The roles of ROS and ABA in systemic acquired acclimation. Plant Cell. 2015; 27: 64-70

[14]

Alves MS, Dadalto SP, Gonçalves AB et al. Plant bZIP transcription factors responsive to pathogens: a review. Int J Mol Sci. 2013; 14: 7815-28

[15]

Amorim LLB, da Fonseca Dos Santos R, Neto JPB et al. Transcription factors involved in plant resistance to pathogens. Curr Protein Pept Sci. 2017; 18: 335-51

[16]

Kaminaka H, Näke C, Epple P et al. bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J. 2006; 25: 4400-11

[17]

Li Q, Qi J, Qin X et al. Systematic identification of lysin-motif receptor-like kinases (LYKs) in Citrus sinensis, and analysis of their inducible involvements in citrus bacterial canker and phytohormone signaling . Sci Hortic. 2021; 276: 109755

[18]

Fawal N, Li Q, Savelli B et al. PeroxiBase: a database for large-scale evolutionary analysis of peroxidases. Nucleic Acids Res. 2013; 41: D441-4

[19]

Pandey S, Fartyal D, Agarwal A et al. Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front Plant Sci. 2017; 8: 581

[20]

Smirnoff N, Arnaud D . Hydrogen peroxide metabolism and functions in plants. New Phytol. 2019; 221: 1197-214

[21]

Tian S, Wang X, Li P et al. Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways . Plant Physiol. 2016; 171: 1635-50

[22]

El-Shetehy M, Wang C, Shine MB et al. Nitric oxide and reactive oxygen species are required for systemic acquired resistance in plants. Plant Signal Behav. 2015; 10: e998544

[23]

Foyer CH . How plant cells sense the outside world through hydrogen peroxide. Nature. 2020; 578: 518-9

[24]

Planas-Riverola A, Markaide E, Caño-Delgado AI . New role for LRR-receptor kinase in sensing of reactive oxygen species. Trends Plant Sci. 2021; 26: 102-4

[25]

Wu F, Chi Y, Jiang Z et al. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature. 2020; 578: 577-81

[26]

He Y, Jia R, Qi J et al. Functional analysis of citrus AP2 transcription factors identified CsAP2-09 involved in citrus canker disease response and tolerance. Gene. 2019; 707: 178-88

[27]

Khan M, Hu J, Dahro B et al. ERF108 from Poncirus trifoliata (L.) Raf. Functions in cold tolerance by modulating raffinose synthesis through transcriptional regulation of PtrRafS . Plant J. 2021; 108: 705-24

[28]

Jiang Y, Tong S, Chen N et al. The PalWRKY77 transcription factor negatively regulates salt tolerance and abscisic acid signaling in Populus. Plant J. 2021; 105: 1258-73

[29]

Hu Y, Zhang J, Jia H et al. Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc Natl Acad Sci U S A. 2014; 111: E521-9

[30]

Li Q, Qin X, Qi J et al. CsPrx25, a class III peroxidase in Citrus sinensis, confers resistance to citrus bacterial canker through the maintenance of ROS homeostasis and cell wall lignification . Hortic Res. 2020; 7: 192

[31]

Liu H, Wang X, Liu S et al. Citrus pan-genome to breeding database (CPBD): a comprehensive genome database for citrus breeding. Mol Plant. 2022; 15: 1503-5

[32]

Wang J, Chen D, Lei Y et al. Citrus sinensis annotation project (CAP): a comprehensive database for sweet orange genome . PLoS One. 2014; 9: e87723

[33]

Kumar S, Stecher G, Li M et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018; 35: 1547-9

[34]

Hu B, Jin J, Guo AY et al. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. 2015; 31: 1296-7

[35]

Fornes O, Castro-Mondragon JA, Khan A et al. JASPAR 2020: update of the open-access database of transcription factor binding profiles. Nucleic Acids Res. 2020; 48: D87-92

[36]

Finn RD, Clements J, Eddy SR . HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011; 39: W29-37

[37]

Sendín LN, Orce IG, Gómez RL et al. Inducible expression of Bs2 R gene from Capsicum chacoense in sweet orange (Citrus sinensis L. Osbeck) confers enhanced resistance to citrus canker disease . Plant Mol Biol. 2017; 93: 607-21

[38]

Peng A, Chen S, Lei T et al. Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J. 2017; 15: 1509-19

[39]

Gietz RD, Schiestl RH . Quick and easy yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc. 2007; 2: 35-7

[40]

Long Q, Du MX, Long JH et al. Transcription factor WRKY22 regulates canker susceptibility in sweet orange (Citrus sinensis Osbeck) by enhancing cell enlargement and CsLOB1 expression . Hortic Res. 2021; 8: 15

[41]

Duan S, Jia H, Pang Z et al. Functional characterization of the citrus canker susceptibility gene CsLOB1. Mol Plant Pathol. 2018; 19: 1908-16

[42]

Wang F, Wang M, Liu X et al. Identification of putative genes involved in limonoids biosynthesis in citrus by comparative transcriptomic analysis. Front Plant Sci. 2017; 8: 782

[43]

Livak KJ, Schmittgen TD . Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001; 25: 402-8

[44]

Fu J, Yu Q, Zhang C et al. CsAP2-09 confers resistance against citrus bacterial canker by regulating CsGH3.1L-mediated phytohormone biosynthesis. Int J Biol Macromol. 2023; 229: 964-73

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