CsWAKL08, a pathogen-induced wall-associated receptor-like kinase in sweet orange, confers resistance to citrus bacterial canker via ROS control and JA signaling

Qiang Li , Anhua Hu , Jingjing Qi , Wanfu Dou , Xiujuan Qin , Xiuping Zou , Lanzhen Xu , Shanchun Chen , Yongrui He

Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) : 42

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Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) :42 DOI: 10.1038/s41438-020-0263-y
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CsWAKL08, a pathogen-induced wall-associated receptor-like kinase in sweet orange, confers resistance to citrus bacterial canker via ROS control and JA signaling
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Abstract

Citrus bacterial canker (CBC) is a disease resulting from Xanthomonas citri subsp. citri (Xcc) infection and poses a grave threat to citrus production worldwide. Wall-associated receptor-like kinases (WAKLs) are proteins with a central role in resisting a range of fungal and bacterial diseases. The roles of WAKLs in the context of CBC resistance, however, remain unclear. Here, we explored the role of CsWAKL08, which confers resistance to CBC, and we additionally analyzed the molecular mechanisms of CsWAKL08-mediated CBC resistance. Based on systematic annotation and induced expression analysis of the CsWAKL family in Citrus sinensis, CsWAKL08 was identified as a candidate that can be upregulated by Xcc infection in the CBC-resistant variety. CsWAKL08 can also be induced by the phytohormones salicylic acid (SA) and methyl jasmonic acid (MeJA) and spans the plasma membrane. Overexpression of CsWAKL08 resulted in strong CBC resistance in transgenic sweet oranges, whereas silencing of CsWAKL08 resulted in susceptibility to CBC. The peroxidase (POD) and superoxide dismutase (SOD) activities were significantly enhanced in the CsWAKL08-overexpressing plants compared to the control plants, thereby mediating reactive oxygen species (ROS) homeostasis in the transgenic plants. Moreover, the JA levels and the expression of JA biosynthesis and JA responsive genes were substantially elevated in the CsWAKL08 overexpression plants relative to the controls upon Xcc infection. Based on these findings, we conclude that the wall-associated receptor-like kinase CsWAKL08 positively regulates CBC resistance through a mechanism involving ROS control and JA signaling. These results further highlight the importance of this kinase family in plant pathogen resistance.

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Qiang Li, Anhua Hu, Jingjing Qi, Wanfu Dou, Xiujuan Qin, Xiuping Zou, Lanzhen Xu, Shanchun Chen, Yongrui He. CsWAKL08, a pathogen-induced wall-associated receptor-like kinase in sweet orange, confers resistance to citrus bacterial canker via ROS control and JA signaling. Horticulture Research, 2020, 7 (1) : 42 DOI:10.1038/s41438-020-0263-y

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References

[1]

Krattinger, S. G. & Keller, B. Molecular genetics and evolution of disease resistance in cereals. N. Phytol. 212, 320-332 (2016).

[2]

Yang, P. et al. Fungal resistance mediated by maize wall-associated kinase ZmWAK-RLK1 correlates with reduced benzoxazinoid content. N. Phytol. 221, 976-987 (2019).

[3]

Hurni, S. et al. The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase. Proc. Natl Acad. Sci. USA 112, 8780-8785 (2015).

[4]

Boller, T. & Felix, G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev. Plant Biol. 60, 379-406 (2009).

[5]

Dardick, C., Schwessinger, B. & Ronald, P. Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures. Curr. Opin. Plant Biol. 15, 358-366 (2012).

[6]

Macho, A. P. & Zipfel, C. Plant PRRs and the activation of innate immune signaling. Mol. Cell 54, 263-272 (2014).

[7]

Hu, K. et al. Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement. Nat. Plants 3, 17009 (2017).

[8]

Cayrol, B., Delteil, A., Gobbato, E., Kroj, T. & Morel, J. B. Three wall-associated kinases required for rice basal immunity form protein complexes in the plasma membrane. Plant Signal Behav. 11, e1149676 (2016).

[9]

Chandran, D. et al. Atypical E2F transcriptional repressor DEL1 acts at the intersection of plant growth and immunity by controlling the hormone salicylic acid. Cell Host Microbe 15, 506-513 (2014).

[10]

Cui, H., Tsuda, K. & Parker, J. E. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66, 487-511 (2015).

[11]

Thaler, J. S., Humphrey, P. T. & Whiteman, N. K. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci. 17, 260-270 (2012).

[12]

Kanneganti, V. & Gupta, A. K. Wall associated kinases from plants - an overview. Physiol. Mol. Biol. Plants 14, 109-118 (2008).

[13]

He, Z. H., Fujiki, M. & Kohorn, B. D. A cell wall-associated, receptor-like protein kinase. J. Biol. Chem. 271, 19789-19793 (1996).

[14]

He, Z. H., Cheeseman, I., He, D. & Kohorn, B. D. A cluster of five cell wall-associated receptor kinase genes, Wak1-5, are expressed in specific organs of Arabidopsis. Plant Mol. Biol. 39, 1189-1196 (1999).

[15]

Verica, J. A. & He, Z. H. The cell wall-associated kinase (WAK) and WAK-like kinase gene family. Plant Physiol. 129, 455-459 (2002).

[16]

Anderson, C. M. et al. WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol. Biol. 47, 197-206 (2001).

[17]

Verica, J. A., Chae, L., Tong, H., Ingmire, P. & He, Z. H. Tissue-specific and developmentally regulated expression of a cluster of tandemly arrayed cell wall-associated kinase-like kinase genes in Arabidopsis. Plant Physiol. 133, 1732-1746 (2003).

[18]

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

[19]

Delteil, A. et al. Several wall-associated kinases participate positively and negatively in basal defense against rice blast fungus. BMC Plant Biol. 16, 17 (2016).

[20]

Shi, G. et al. The hijacking of a receptor kinase-driven pathway by a wheat fungal pathogen leads to disease. Sci. Adv. 2, e1600822 (2016).

[21]

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).

[22]

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).

[23]

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).

[24]

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).

[25]

de Oliveira, L. F. V. et al. The Wall-associated Kinase gene family in rice genomes. Plant Sci. 229, 181-192 (2014).

[26]

Xu, Q. et al. The draft genome of sweet orange (Citrus sinensis). Nat. Genet. 45, 59-66 (2013).

[27]

Zhang, S. et al. Evolutionary expansion, gene structure, and expression of the rice wall-associated kinase gene family. Plant Physiol. 139, 1107-1124 (2005).

[28]

Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874 (2016).

[29]

Bailey, T. L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202-W208 (2009).

[30]

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

[31]

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

[32]

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

[33]

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

[34]

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

[35]

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).

[36]

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).

[37]

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).

[38]

Pieterse, C. M., Van der Does, D., Zamioudis, C., Leon-Reyes, A. & Van Wees, S. C. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489-521 (2012).

[39]

Balmer, D., de Papajewski, D. V., Planchamp, C., Glauser, G. & Mauch-Mani, B. Induced resistance in maize is based on organ-specific defence responses. Plant J. 74, 213-225 (2013).

[40]

Zhang, C. et al. GmBTB/POZ, a novel BTB/POZ domain-containing nuclear protein, positively regulates the response of soybean to Phytophthora sojae infection. Mol. Plant Pathol. 20, 78-91 (2019).

[41]

Wang, Y., Wang, Q., Zhao, Y., Han, G. & Zhu, S. Systematic analysis of maize class III peroxidase gene family reveals a conserved subfamily involved in abiotic stress response. Gene 566, 95-108 (2015).

[42]

Catinot, J., Buchala, A., Abou-Mansour, E. & Métraux, J. P. Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS Lett. 582, 473-478 (2008).

[43]

Huang, J. et al. Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol. 153, 1526-1538 (2010).

[44]

Takahashi, F. et al. The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell 19, 805-818 (2007).

[45]

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

[46]

Fawal, N., Li, Q., Mathé, C. & Dunand, C. Automatic multigenic family annotation: risks and solutions. Trends Genet. 30, 323-325 (2014).

[47]

Solovyev, V., Kosarev, P., Seledsov, I. & Vorobyev, D. Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol. 7(Suppl 1), S10.11-12 (2006).

[48]

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

[49]

El-Gebali, S. et al. The Pfam protein families database in 2019. Nucleic Acids Res. https://doi.org/10.1093/nar/gky995 (2018).

[50]

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

[51]

Keller, O., Odronitz, F., Stanke, M., Kollmar, M. & Waack, S. Scipio: using protein sequences to determine the precise exon/intron structures of genes and their orthologs in closely related species. BMC Bioinforma. 9, 278 (2008).

[52]

Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).

[53]

Tippmann, H. F. Analysis for free: comparing programs for sequence analysis. Brief. Bioinform. 5, 82-87 (2004).

[54]

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

[55]

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).

[56]

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

[57]

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).

[58]

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).

[59]

Li, H., Zhou, S. Y., Zhao, W. S., Su, S. C. & Peng, Y. L. A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol. Biol. 69, 337-346 (2009).

[60]

Hufnagel, B. et al. Duplicate and conquer: multiple homologs of PHOSPHORUS-STARVATION TOLERANCE1 enhance phosphorus acquisition and sorghum performance on low-phosphorus soils. Plant Physiol. 166, 659-677 (2014).

[61]

Bagnaresi, P. et al. Comparative transcriptome profiling of the early response to Magnaporthe oryzae in durable resistant vs susceptible rice (Oryza sativa L.) genotypes. PLoS ONE 7, e51609 (2012).

[62]

Rosli, H. G. et al. Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity. Genome Biol. 14, R139 (2013).

[63]

He, Z. H., He, D. & Kohorn, B. D. Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. Plant J. 14, 55-63 (1998).

[64]

Diener, A. C. & Ausubel, F. M. RESISTANCE TO FUSARIUM OXYSPORUM 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 171, 305-321 (2005).

[65]

Häffner, E., Karlovsky, P., Splivallo, R., Traczewska, A. & Diederichsen, E. ERECTA, salicylic acid, abscisic acid, and jasmonic acid modulate quantitative disease resistance of Arabidopsis thaliana to Verticillium longisporum. BMC Plant Biol. 14, 85 (2014).

[66]

Brutus, A., Sicilia, F., Macone, A., Cervone, F. & De Lorenzo, G. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl Acad. Sci. USA 107, 9452-9457 (2010).

[67]

Kohorn, B. D. & Kohorn, S. L. The cell wall-associated kinases, WAKs, as pectin receptors. Front. Plant Sci. 3, 88 (2012).

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