CsPrx25, a class III peroxidase in Citrus sinensis, confers resistance to citrus bacterial canker through the maintenance of ROS homeostasis and cell wall lignification

Qiang Li , Xiujuan Qin , Jingjing Qi , Wanfu Dou , Christophe Dunand , Shanchun Chen , Yongrui He

Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) : 192

PDF (1572KB)
Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) :192 DOI: 10.1038/s41438-020-00415-9
Article
research-article
CsPrx25, a class III peroxidase in Citrus sinensis, confers resistance to citrus bacterial canker through the maintenance of ROS homeostasis and cell wall lignification
Author information +
History +
PDF (1572KB)

Abstract

Citrus bacterial canker (CBC) results from Xanthomonas citri subsp. citri (Xcc) infection and poses a grave threat to citrus production. Class III peroxidases (CIII Prxs) are key proteins to the environmental adaptation of citrus plants to a range of exogenous pathogens, but the role of CIII Prxs during plant resistance to CBC is poorly defined. Herein, we explored the role of CsPrx25 and its contribution to plant defenses in molecular detail. Based on the expression analysis, CsPrx25 was identified as an apoplast-localized protein that is differentially regulated by Xcc infection, salicylic acid, and methyl jasmone acid in the CBC-susceptible variety Wanjincheng (C. sinensis) and the CBC-resistant variety Calamondin (C. madurensis). Transgenic Wanjincheng plants overexpressing CsPrx25 were generated, and these transgenic plants exhibited significantly increased CBC resistance compared with the WT plants. In addition, the CsPrx25-overexpressing plants displayed altered reactive oxygen species (ROS) homeostasis accompanied by enhanced H2O2 levels, which led to stronger hypersensitivity responses during Xcc infection. Moreover, the overexpression of CsPrx25 enhanced lignification as an apoplastic barrier for Xcc infection. Taken together, the results highlight how CsPrx25-mediated ROS homeostasis reconstruction and cell wall lignification can enhance the resistance of sweet orange to CBC.

Cite this article

Download citation ▾
Qiang Li, Xiujuan Qin, Jingjing Qi, Wanfu Dou, Christophe Dunand, Shanchun Chen, Yongrui He. CsPrx25, a class III peroxidase in Citrus sinensis, confers resistance to citrus bacterial canker through the maintenance of ROS homeostasis and cell wall lignification. Horticulture Research, 2020, 7 (1) : 192 DOI:10.1038/s41438-020-00415-9

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Molina, L. & Kahmann, R. An ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 19, 2293-2309 (2007).

[2]

Peters, L. P. et al. Functional analysis of oxidative burst in sugarcane smut-resistant and -susceptible genotypes. Planta 245, 749-764 (2017).

[3]

Pitino, M., Armstrong, C. M. & Duan, Y. Rapid screening for citrus canker resistance employing pathogen-associated molecular pattern-triggered immunity responses. Hortic. Res. 2, 15042 (2015).

[4]

Ostergaard, L. et al. Expression and high-resolution structure of a plant peroxidase with implications for lignification. Plant Mol. Biol. 44, 231-243 (2000).

[5]

Passardi, F., Penel, C. & Dunand, C. Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci. 9, 534-540 (2004).

[6]

Schweizer, P. Tissue-specific expression of a defence-related peroxidase in transgenic wheat potentiates cell death in pathogen-attacked leaf epidermis. Mol. Plant Pathol. 9, 45-57 (2008).

[7]

Liu, G. et al. Profiling of wheat class III peroxidase genes derived from powdery mildew-attacked epidermis reveals distinct sequence-associated expression patterns. Mol. Plant Microbe Interact. 18, 730-741 (2005).

[8]

Han, F. P., Fedak, G., Ouellet, T., Dan, H. & Somers, D. J. Mapping of genes expressed in Fusarium graminearum-infected heads of wheat cultivar ‘Frontana’. Genome 48, 88-96 (2005).

[9]

Mittler, R. et al. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc. Natl Acad. Sci. USA 96, 14165-14170 (1999).

[10]

Barna, B., Fodor, J., Harrach, B. D., Pogány, M. & Király, Z. The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiol. Biochem. 59, 37-43 (2012).

[11]

Apel, K. & Hirt, H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399 (2004).

[12]

Torres, M. A. ROS in biotic interactions. Physiol. Plant 138, 414-429 (2010).

[13]

Aviello, G. & Knaus, U. G. NADPH oxidases and ROS signaling in the gastrointestinal tract. Mucosal Immunol. 11, 1011-1023 (2018).

[14]

Peters, L. P. et al. Differential responses of the antioxidant system of ametryn and clomazone tolerant bacteria. PLoS ONE 9, e112271 (2014).

[15]

Pieterse, C. M., Leon-Reyes, A., Van der Ent, S. & Van Wees, S. C. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5, 308-316 (2009).

[16]

Thomma, B. P. et al. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl Acad. Sci. USA 95, 15107-15111 (1998).

[17]

Pieterse, C. M. et al. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489-521 (2012).

[18]

Li, Q. et al. Explosive tandem and segmental duplications of multigenic families in Eucalyptus grandis. Genome Biol. Evol. 7, 1068-1081 (2015).

[19]

Li, Q., San Clemente, H., He, Y. R., Fu, Y. Y. & Dunand, C. Global evolutionary analysis of 11 gene families part of reactive oxygen species (ROS) gene network in four Eucalyptus species. Antioxidants 9, 19 (2020).

[20]

Savelli, B. et al. RedoxiBase: a database for ROS homeostasis regulated proteins. Redox Biol. 26, 101247 (2019).

[21]

Mbadinga Mbadinga, D., Li, Q., Ranocha, P., Martinez, Y. & Dunand, C. Global analysis of non-animal peroxidases provides insights into the evolution of this gene family in the green lineage. J. Exp. Bot. 71, 3350-3360 (2020).

[22]

Tognolli, M., Penel, C., Greppin, H. & Simon, P. Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288, 129-138 (2002).

[23]

Cosio, C. & Dunand, C. Transcriptome analysis of various flower and silique development stages indicates a set of class III peroxidase genes potentially involved in pod shattering in Arabidopsis thaliana. BMC Genom. 11, 528 (2010).

[24]

Passardi, F., Longet, D., Penel, C. & Dunand, C. The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65, 1879-1893 (2004).

[25]

Yan, J. et al. Genome-wide and evolutionary analysis of the class III peroxidase gene family in wheat and Aegilops tauschii reveals that some members are involved in stress responses. BMC Genom. 20, 666 (2019).

[26]

Ren, L. L. et al. Subcellular relocalization and positive selection play key roles in the retention of duplicate genes of populus class III peroxidase family. Plant Cell 26, 2404-2419 (2014).

[27]

Cao, Y. et al. Structural, evolutionary, and functional analysis of the class III peroxidase gene family in chinese pear. Front. Plant Sci. 7, 1874 (2016).

[28]

Li, Q. et al. Genomewide analysis of the CIII peroxidase family in sweet orange (Citrus sinensis) and expression profiles induced by Xanthomonas citri subsp. citri and hormones. J. Genet. 99, 13 (2020).

[29]

Fernández-Pérez, F., Pomar, F., Pedreño, M. A. & Novo-Uzal, E. Suppression of arabidopsis peroxidase 72 alters cell wall and phenylpropanoid metabolism. Plant Sci. 239, 192-199 (2015).

[30]

Pandey, V. P. & Dwivedi, U. N. A ripening associated peroxidase from papaya having a role in defense and lignification: heterologous expression and in-silico and in-vitro experimental validation. Gene 555, 438-447 (2015).

[31]

Shigeto, J. & Tsutsumi, Y. Diverse functions and reactions of class III peroxidases. N. Phytol. 209, 1395-1402 (2016).

[32]

Passardi, F., Cosio, C., Penel, C. & Dunand, C. Peroxidases have more functions than a swiss army knife. Plant Cell Rep. 24, 255-265 (2005).

[33]

Liszkay, A., Kenk, B. & Schopfer, P. Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta 217, 658-667 (2003).

[34]

McInnis, S. M., Desikan, R., Hancock, J. T. & Hiscock, S. J. Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signalling crosstalk? N. Phytol. 172, 221-228 (2006).

[35]

Mei, W., Qin, Y., Song, W., Li, J. & Zhu, Y. Cotton GhPOX1 encoding plant class III peroxidase may be responsible for the high level of reactive oxygen species production that is related to cotton fiber elongation. J. Genet. Genomics 36, 141-150 (2009).

[36]

Cao, J., Jiang, M., Li, P. & Chu, Z. Genome-wide identification and evolutionary analyses of the PP2C gene family with their expression profiling in response to multiple stresses in Brachypodium distachyon. BMC Genom. 17, 175 (2016).

[37]

Van Loon, L. C., Rep, M. & Pieterse, C. M. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135-162 (2006).

[38]

Almagro, L. et al. Class III peroxidases in plant defence reactions. J. Exp. Bot. 60, 377-390 (2009).

[39]

Radwan, M. A., El-Gendy, K. S. & Gad, A. F. Biomarkers of oxidative stress in the land snail, Theba pisana for assessing ecotoxicological effects of urban metal pollution. Chemosphere 79, 40-46 (2010).

[40]

Johrde, A. & Schweizer, P. A class III peroxidase specifically expressed in pathogen-attacked barley epidermis contributes to basal resistance. Mol. Plant Pathol. 9, 687-696 (2008).

[41]

Altpeter, F. et al. Stable expression of a defense-related gene in wheat epidermis under transcriptional control of a novel promoter confers pathogen resistance. Plant Mol. Biol. 57, 271-283 (2005).

[42]

Omar, A. A., Murata, M. M., El-Shamy, H. A., Graham, J. H. & Grosser, J. W. Enhanced resistance to citrus canker in transgenic mandarin expressing Xa21 from rice. Transgenic Res 27, 179-191 (2018).

[43]

Schaad, N. W. et al. Reclassification of Xanthomonas campestris pv. citri (ex Hasse 1915) Dye 1978 forms A, B/C/D, and E as X. smithii subsp. citri (ex Hasse) sp. nov. nom. rev. comb. nov., X. fuscans subsp. aurantifolii (ex Gabriel 1989) sp. nov. nom. rev. comb. nov., and X. alfalfae subsp. citrumelo (ex Riker and Jones) Gabriel et al., 1989 sp. nov. nom. rev. comb. nov.; X. campestris pv malvacearum (ex smith 1901) Dye 1978 as X. smithii subsp. smithii nov. comb. nov. nom. nov.; X. campestris pv. alfalfae (ex Riker and Jones, 1935) dye 1978 as X. alfalfae subsp. alfalfae (ex Riker et al., 1935) sp. nov. nom. rev.; and “var. fuscans” of X. campestris pv. phaseoli (ex Smith, 1987) Dye 1978 as X. fuscans subsp. fuscans sp. nov. Syst. Appl. Microbiol. 28, 494-518 (2005).

[44]

Fawal, N. et al. PeroxiBase: a database for large-scale evolutionary analysis of peroxidases. Nucleic Acids Res. 41, D441-D444 (2013).

[45]

Savelli, B. et al. RedoxiBase: A database for ROS homeostasis regulated proteins. Redox Biol. 26, 5 (2019).

[46]

Wang, J. et al. Citrus sinensis annotation project (CAP): a comprehensive database for sweet orange genome. PLoS ONE 9, e87723 (2014).

[47]

Welinder, K. G. et al. Structural diversity and transcription of class III peroxidases from Arabidopsis thaliana. Eur. J. Biochem. 269, 6063-6081 (2002).

[48]

He, Y. et al. Functional analysis of citrus AP2 transcription factors identified CsAP2-09 involved in citrus canker disease response and tolerance. Gene 707, 178-188 (2019).

[49]

Zuo, W. et al. A maize wall-associated kinase confers quantitative resistance to head smut. Nat. Genet. 47, 151-157 (2015).

[50]

Li, Q. 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. Hort. Res. 7, 15 (2020).

[51]

Sendín, L. N. 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. 93, 607-621 (2017).

[52]

Du, X. M., Yin, W. X., Zhao, Y. X. & Zhang, H. The production and scavenging of reactive oxygen species in plants. Sheng Wu Gong. Cheng Xue Bao 17, 121-125 (2001).

[53]

Hückelhoven, R. & Kogel, K. H. Reactive oxygen intermediates in plant-microbe interactions: who is who in powdery mildew resistance? Planta 216, 891-902 (2003).

[54]

Soosaar, J. L., Burch-Smith, T. M. & Dinesh-Kumar, S. P. Mechanisms of plant resistance to viruses. Nat. Rev. Microbiol. 3, 789-798 (2005).

[55]

Mishra, M. K. et al. Overexpression of WsSGTL1 gene of Withania somnifera enhances salt tolerance, heat tolerance and cold acclimation ability in transgenic Arabidopsis plants. PLoS ONE 8, e63064 (2013).

[56]

Pontier, D., Tronchet, M., Rogowsky, P., Lam, E. & Roby, D. Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. Mol. Plant Microbe Interact. 11, 544-554 (1998).

[57]

Pontier, D., Godiard, L., Marco, Y. & Roby, D. Hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. Plant J. 5, 507-521 (1994).

[58]

Tronchet, M., Ranty, B., Marco, Y. & Roby, D. Hsr203 antisense suppression in tobacco accelerates development of hypersensitive cell death. Plant J. 27, 115-127 (2001).

[59]

Herrero, J. et al. Bioinformatic and functional characterization of the basic peroxidase 72 from Arabidopsis thaliana involved in lignin biosynthesis. Planta 237, 1599-1612 (2013).

[60]

Hiraga, S., Sasaki, K., Ito, H., Ohashi, Y. & Matsui, H. A large family of class III plant peroxidases. Plant Cell Physiol. 42, 462-468 (2001).

[61]

Elfstrand, M., Sitbon, F., Lapierre, C., Bottin, A. & von Arnold, S. Altered lignin structure and resistance to pathogens in spi 2-expressing tobacco plants. Planta 214, 708-716 (2002).

[62]

Li, Q. et al. CitGVD: a comprehensive database of citrus genomic variations. Hort. Res. 7, 12 (2020).

[63]

Letunic, I. & Bork, P. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res. 46, D493-D496 (2018).

[64]

Hu, B. et al. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31, 1296-1297 (2015).

[65]

Petersen, T. N., Brunak, S., von Heijne, G. & Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786 (2011).

[66]

Yu, C. S., Chen, Y. C., Lu, C. H. & Hwang, J. K. Prediction of protein subcellular localization. Proteins 64, 643-651 (2006).

[67]

Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845-858 (2015).

[68]

Li, Q. et al. CsBZIP40, a BZIP transcription factor in sweet orange, plays a positive regulatory role in citrus bacterial canker response and tolerance. PloS ONE 14, e0223498 (2019).

[69]

Peng, A. et al. Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol. J. 15, 1509-1519 (2017).

[70]

Li, Q. et al. Systematic analysis and functional validation of citrus XTH genes reveal the role of CsXTH04 in citrus bacterial canker resistance and tolerance. Front. Plant Sci. 10, 1109 (2019).

[71]

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. Methods 25, 402-408 (2001).

[72]

Caruso, C. et al. A basic peroxidase from wheat kernel with antifungal activity. Phytochemistry 58, 743-750 (2001).

[73]

Kawano, T. Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep. 21, 829-837 (2003).

[74]

Coego, A. et al. An Arabidopsis homeodomain transcription factor, OVEREXPRESSOR OF CATIONIC PEROXIDASE 3, mediates resistance to infection by necrotrophic pathogens. Plant Cell 17, 2123-2137 (2005).

[75]

Sun, X. et al. MdATG18a overexpression improves tolerance to nitrogen deficiency and regulates anthocyanin accumulation through increased autophagy in transgenic apple. Plant Cell Environ. 41, 469-480 (2018).

[76]

Murata, M. M. et al. Novel plastid-nuclear genome combinations enhance resistance to citrus canker in cybrid grapefruit. Front. Plant Sci. 9, 1858 (2018).

PDF (1572KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/