Tomato SlPUB24 enhances resistance to Xanthomonas euvesicatoria pv. perforans race T3

Liu , Ge Meng , Mengrui Wang , Zilin Qian , Yaxian Zhang , Wencai Yang

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 30

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :30 DOI: 10.1038/s41438-021-00468-4
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Tomato SlPUB24 enhances resistance to Xanthomonas euvesicatoria pv. perforans race T3
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Abstract

Solanum lycopersicum var. cerasiforme accession PI 114490 has broad-spectrum resistance to bacterial spot caused by several species of Xanthomonas. Resistance is quantitatively inherited, and a common quantitative trait locus QTL-11B on chromosome 11 has been identified previously. In this study, the SlPub24 gene was characterized in QTL-11B. SlPub24 in PI 114490 was upregulated by infection with X. euvesicatoria pv. perforans race T3, but its transcription was low in the susceptible line OH 88119 whether or not it was infected by the pathogen. The differential expression of SlPub24 between PI 114490 and OH 88119 was due to great sequence variation in the promoter region. The promoter of SlPub24 in OH 88119 had very low activity and did not respond to pathogen infection. Transgenic lines of OH 88119 overexpressing SlPub24 isolated from PI 114490 showed significantly enhanced resistance, while mutants of Slpub24 generated by CRISPR/Cas9 editing showed more susceptibility to race T3 and to other races. The mutants also showed spontaneous cell death in leaves. The expression of the salicylic acid (SA) pathway gene phenylalanine ammonia-lyase (PAL) and signaling-related genes pathogenesis-related (PR1) and nonexpresser of PR1 (NPR1) were influenced by SlPub24. The content of SA in tomato plants was consistent with the level of SlPub24 expression. Furthermore, SlPUB24 interacted with the cell wall protein SlCWP and could regulate the degradation of SlCWP. The expression levels of SlCWP and SlCWINV1, a cell wall invertase gene, showed opposite patterns during pathogen infection. The activity of SlCWINV1 was lower in mutants than in PI 114490. The results are discussed in terms of the roles of the abovementioned genes, and a potential model for SlPUB24-mediated resistance to bacterial spot is proposed.

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Liu, Ge Meng, Mengrui Wang, Zilin Qian, Yaxian Zhang, Wencai Yang. Tomato SlPUB24 enhances resistance to Xanthomonas euvesicatoria pv. perforans race T3. Horticulture Research, 2021, 8 (1) : 30 DOI:10.1038/s41438-021-00468-4

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References

[1]

Jones, J. B., Lacy, G. H., Bouzar, H., Stall, R. E. & Schaad, N. W. Reclassification of the xanthomonads associated with bacterial spot disease of tomato and pepper. Syst. Appl. Microbiol. 27, 755-762 (2004).

[2]

Timisina, S. et al. Reclassification of Xanthomonas gardneri (ex Sutic 1957) Jones et al. 2006 as a later heterotypic synonym of Xanthomonas cynarae Trebaol et al. 2000 and description of X. cynarae pv. cynarae and X. cynarae pv. gardneri based on whole genome analyses. Int. J. Syst. Evol. Microbiol. 69, 343-349 (2019).

[3]

Constantin, E. C. et al. Genetic characterization of strains named as Xanthomonas axonopodis pv. dieffenbachiae leads to a taxonomic revision of the X. axonopodis species complex. Plant Pathol. 65, 792-806 (2016).

[4]

Wang, Y., Zhang, Y., Gao, Z. & Yang, W. Breeding for resistance to tomato bacterial diseases in China: challenges and prospects. Hortic. Plant J. 4, 193-207 (2018).

[5]

Adhikari, P., Adhikari, T. B., Louws, F. J. & Panthee, D. R. Advances and challenges in bacterial spot resistance breeding in tomato (Solanum lycopersicum L.). Int. J. Mol. Sci. 21, 1734 (2020).

[6]

Li, N., Zhang, X. & Yang, W. Marker-assisted development and characterization of near-isogenic lines carrying the Rx4 gene for hypersensitive resistance to Xanthomonas euvesicatoria pv. perforans race T3 in tomato. Mol. Breed. 39, 172 (2019).

[7]

Scott, J. W., Hutton, S. F., Shekasteband, R., Sim, S. C. & Francis, D. M. Identification of tomato bacterial spot race T1, T2, T3, T4, and Xanthomonas gardneri resistance QTLs derived from PI 114490 populations selected for race T4. Acta Hortic. 1069, 53-58 (2015).

[8]

Scott, J. W., Francis, D. M., Miller, S. A., Somodi, G. C. & Jones, J. B. Tomato bacterial spot resistance derived from PI 114490; Inheritance of resistance to race T2 and relationship across three pathogen races. J. Am. Soc. Hortic. Sci. 128, 698-703 (2003).

[9]

Bernal, E., Liabeuf, D. & Francis, D. M. Evaluating quantitative trait locus resistance in tomato to multiple Xanthomonas spp. Plant Dis. 104, 423-429 (2020).

[10]

Hutton, S. F. et al. Identification of QTL associated with resistance to bacterial spot race T4 in tomato. Theor. Appl. Genet. 121, 1275-1287 (2010).

[11]

Sun, H., Wei, J., Zhang, J. & Yang, W. A comparison of disease severity measurements using image analysis and visual estimates using a category scale for genetic analysis of resistance to bacterial spot in tomato. Eur. J. Plant Pathol. 139, 125-136 (2014).

[12]

Sun, H. et al. QTL analysis of resistance to bacterial spot race T3 in tomato. Acta Hortic. Sin. 38, 2297-2308 (2011).

[13]

Yang, W., Miller, S. A., Francis, D. M., Scott, J. W. & Jones, J. B. Mining tomato genome sequence databases for molecular markers: application to bacterial resistance and marker assisted selection. Acta Hortic. 695, 241-249 (2005).

[14]

Du, H. S., Wang, Y. Q., Yang, J. J. & Yang, W. C. Comparative transcriptome analysis of resistant and susceptible tomato lines in response to infection by Xanthomonas perforans race T3. Front. Plant Sci. 6, 1173 (2015).

[15]

Du, H., Li, W., Wang, Y. & Yang, W. Identification of genes differentially expressed between resistant and susceptible tomato lines during time-course interactions with Xanthomonas perforans race T3. PLoS One 9, e93476 (2014).

[16]

Zeng, L. R. et al. Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16, 2795-2808 (2004).

[17]

Yin, Z. C. et al. Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol. Plant Microbe Interact. 13, 869-876 (2000).

[18]

Li, W. et al. The U-Box/ARM E3 ligase PUB13 regulates cell death, defense, and flowering time in Arabidopsis. Plant Physiol. 159, 239-250 (2012).

[19]

Liu, J. et al. The U-Box E3 ligase SPL11/PUB13 is a convergence point of defense and flowering signaling in plants. Plant Physiol. 160, 28-37 (2012).

[20]

Trujillo, M., Ichimura, K., Casais, C. & Shirasu, K. Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr. Biol. 18, 1396-1401 (2008).

[21]

Stegmann, M. et al. The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis. Plant Cell 24, 4703-4716 (2012).

[22]

He, Q. et al. U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans. J. Exp. Bot. 66, 3189-3199 (2015).

[23]

Yang, C. W. et al. The E3 ubiquitin ligase activity of Arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense. Plant Cell 18, 1084-1098 (2006).

[24]

Kirsch, C., Logemann, E., Lippok, B., Schmelzer, E. & Hahlbrock, K. A highly specific pathogen-responsive promoter element from the immediate-early activated CMPG1 gene in Petroselinum crispum. Plant J. 26, 217-227 (2001).

[25]

Navarro, L. et al. The transcriptional innate immune response to flg22. interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135, 1113-1128 (2004).

[26]

Zhu, Y. et al. E3 ubiquitin ligase gene CMPG1-V from Haynaldia villosa L. contributes to powdery mildew resistance in common wheat (Triticum aestivum L.). Plant J. 84, 154-168 (2015).

[27]

Gonzalez-Lamothe, R. et al. The U-Box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell 18, 1067-1083 (2006).

[28]

Lee, D. H., Choi, H. W. & Hwang, B. K. The pepper E3 ubiquitin ligase RING1 gene, CaRING1, is required for cell death and the salicylic acid-dependent defense response. Plant Physiol. 156, 2011-2025 (2011).

[29]

Han, P.-L. et al. The apple U-box E3 ubiquitin ligase MdPUB29 contributes to activate plant immune response to the fungal pathogen Botryosphaeria dothidea. Planta 249, 1177-1188 (2019).

[30]

Han, P.-L. et al. BTB-BACK domain E3 ligase MdPOB1 suppresses plant pathogen defense against Botryosphaeria dothidea by ubiquitinating and degrading MdPUB29 protein in apple. Plant Cell Physiol. 60, 2129-2140 (2019).

[31]

Liu, X., Geng, X., Zhang, H., Shen, H. & Yang, W. Association and genetic identification of loci for four fruit traits in tomato using InDel markers. Front. Plant Sci. 8, 1269 (2017).

[32]

Cantu, D., Vicente, A. R., Labavitch, J. M., Bennett, A. B. & Powell, A. L. T. Strangers in the matrix: plant cell walls and pathogen susceptibility. Trends Plant Sci. 13, 610-617 (2008).

[33]

Harhouri, K. et al. MG132-induced progerin clearance is mediated by autophagy activation and splicing regulation. EMBO Mol. Med. 9, 1294-1313 (2017).

[34]

Zhao, H. et al. Melatonin regulates carbohydrate metabolism and defenses against Pseudomonas syringae pv. tomato DC3000 infection in Arabidopsis thaliana. J. Pineal Res. 59, 109-119 (2015).

[35]

Wang, Y. Q., Zhang, X. F., Li, N. & Liu, X. Comparison of cellular responses to Xanthomonas perforans infection between resistant and susceptible tomato accessions. J. Plant Physiol. 209, 105-114 (2017).

[36]

Sim, S. C. et al. Association analysis for bacterial spot resistance in a directionally selected complex breeding population of tomato. Phytopathology 105, 1437-1445 (2015).

[37]

Frary, A. et al. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85-88 (2000).

[38]

Nesbitt, T. C. & Tanksley, S. D. Comparative sequencing in the genus Lycopersicon: implications for the evolution of fruit size in the domestication of cultivated tomatoes. Genetics 162, 365-379 (2002).

[39]

Ye, J. et al. Tomato SD1, encoding a kinase interacting protein, is a major locus controlling stem development. J. Exp. Bot. https://doi.org/10.1093/jxb/eraa144 (2020).

[40]

Roemer, P. et al. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318, 645-648 (2007).

[41]

Roemer, P. et al. Recognition of AvrBs3-like proteins is mediated by specific binding to promoters of matching pepper Bs3 alleles. Plant Physiol. 150, 1697-1712 (2009).

[42]

Roemer, P., Recht, S. & Lahaye, T. A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proc. Natl Acad. Sci. USA 106, 20526-20531 (2009).

[43]

Vicente,, M. R.-S. & Plasencia, J. Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 62, 3321-3338 (2011).

[44]

Klessig, D. F., Choi, H. W. & Dempsey, D. M. A. Systemic acquired resistance and salicylic acid: past, present, and future. Mol. Plant Microbe Interact. 31, 871-888 (2018).

[45]

Dempsey, D. M. A., Vlot, A. C., Wildermuth, M. C. & Klessig, D. F. Salicylic acid biosynthesis and metabolism. Arabidopsis Book. 9, e0156- e0156 (2011).

[46]

Gao, Q.-M., Zhu, S., Kachroo, P. & Kachroo, A. Signal regulators of systemic acquired resistance. Front. Plant Sci. 6, 228 (2015).

[47]

Khan, M. I. R., Fatma, M., Per, T. S., Anjum, N. A. & Khan, N. A. Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front. Plant Sci. 6, 462 (2015).

[48]

Seyfferth, C. & Tsuda, K. Salicylic acid signal transduction: the initiation of biosynthesis, perception and transcriptional reprogramming. Front. Plant Sci. 5, 697 (2014).

[49]

Herrera-Vasquez, A., Salinas, P. & Holuigue, L. Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front. Plant Sci. 6, 171 (2015).

[50]

Kim, D. S. & Hwang, B. K. An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. J. Exp. Bot. 65, 2295-2306 (2014).

[51]

Shine, M. B. et al. Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean. N. Phytol. 212, 627-636 (2016).

[52]

Wang, J. et al. The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity. BMC Plant Biol. 15, 49 (2015).

[53]

Ishikawa, K. et al. Bacterial effector modulation of host E3 ligase activity suppresses PAMP-triggered immunity in rice. Nat. Commun. 5, 5430 (2014).

[54]

Link, M., Rausch, T. & Greiner, S. In Arabidopsis thaliana, the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles. FEBS Lett. 573, 105-109 (2004).

[55]

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547-1549 (2018).

[56]

Cui, J. et al. Tomato MYB49 enhances resistance to Phytophthora infestans and tolerance to water deficit and salt stress. Planta 248, 1487-1503 (2018).

[57]

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25, 402-408 (2001).

[58]

Hull, G. A. & Devic, M. The beta-glucuronidase (gus) reporter gene system: gene fusions; spectrophotometric, fluorometric, and histochemical detection. Methods Mol. Biol. 49, 125-141 (1995).

[59]

Chen, P. Y., Wang, C. K., Soong, S. C. & To, K. Y. Complete sequence of the binary vector pBI121 and its application in cloning T-DNA insertion from transgenic plants. Mol. Breed. 11, 287-293 (2003).

[60]

Fillatti, J. J., Kiser, J., Rose, R. & Comai, L. Efficient transfer of a glyphosafe tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Bio-Technol. 5, 726-730 (1987).

[61]

Xing, H.-L. et al. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 14, 327 (2014).

[62]

Jansen, A. Modifying post-harvest sucrose loss in sugar beet: assessment of transgenic approaches. PhD thesis. University at Heidelberg, Heidelberg, Germany, (2009).

[63]

Chien, C. T., Bartel, P. L., Sternglanz, R. & Fields, S. The two-hybrid systems: a methods to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl Acad. Sci. USA 88, 9578-9582 (1991).

[64]

Chen, H. et al. Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 146, 368-376 (2008).

[65]

MacPhee, D. J. Methodological considerations for improving Western blot analysis. J. Pharmacol. Toxicol. Methods 61, 171-177 (2010).

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