Abstract
Periwinkle facilitates study of the non-culturable pathogen ‘Candidatus Liberibacter asiaticus’ (CaLas), the causal agent of Huanglongbing (HLB) in citrus. Isochorismate synthase (ICS) is involved in the defense responses to pathogens through the salicylic acid (SA) signaling pathway in some plants. In this study, crICS from Catharanthus roseus was identified. The full-length cDNA of crICS is 2206 bp long, with an open reading frame (ORF) encoding a putative protein of 322 amino acids, including a conserved chorismate binding enzyme motif. Phylogenetic analysis revealed the crICS protein to cluster together with those of Rubia cordifolia and Coffea canephora to form a separate clade. Results of a qRT-PCR analysis indicated that crICS was constitutively expressed in leaf, stem, and root tissue of healthy periwinkle plants. During CaLas infection, crICS expression levels increased gradually and reached a peak at 22 days after inoculation (DAI), and then decreased gradually but were still higher than the expression level for the control group (CK) until the end of the experiment. To investigate whether crICS may act to mediate resistance through the SA signaling pathway in periwinkle, we sprayed SA on leaves, and found that SA increased crICS expression levels, but did not decrease the cumulative CaLas-positive rate of infected plants. The results suggest that crICS most likely mediates resistance to CaLas through the SA signaling pathway.
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References
Catinot J, Buchala A, Abou-Mansour E, Metraux JP (2008) Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS Letters 582:473–478
Chen Z, Zheng Z, Huang J, Lai Z, Fan B (2009) Biosynthesis of salicylic acid in plants. Plant Signaling & Behavior 4:493–496
Coletta-Filho HD, Takita MA, Targon MLPN, Machado MA (2005) Analysis of 16S rDNA sequences from citrus huanglongbing bacteria reveal a different ‘Ca. Liberibacter’ strain associated with citrus disease in São Paulo. Plant Disease 89:848–852
DeClue MS, Baldridge KK, Künzler DE, Kast P, Hilvert D (2005) Isochorismate pyruvate lyase: a pericyclic reaction mechanism? Journal of the American Chemical Society 127:15002–15003
Deng X, Gao Y, Chen J, Pu X, Kong W, Li H (2012) Current situation of “Candidatus Liberibacter asiaticus” in Guangdong, China, where citrus Huanglongbing was first described. Journal of Integrative Agriculture 11:424–429
Ding F, Duan Y, Paul C, Brlansky RH, Hartung JS (2015) Localization and distribution of Candidatus Liberibacter asiaticus in citrus and periwinkle by direct tissue blot immuno assay with an anti-OmpA polyclonal antibody. PLoS One 10:e0123939
Durrant WE, Dong X (2004) Systemic acquired resistance. Annual Review of Phytopathology 42:185–209
Dutt M, Barthe G, Irey M, Grosser J (2015) Transgenic citrus expressing an Arabidopsis NPR1 gene exhibit enhanced resistance against Huanglongbing (HLB; Citrus greening). PLoS One 10:e0137134
Hartung JS, Paul C, Achor D, Brlansky RH (2010) Colonization of dodder, Cuscuta indecora, by Candidatus Liberibacter asiaticus and Ca. L. americanus. Phytopathology 100:756–762
Jagoueix S, Bove JM, Garnier M (1994) The phloem-limited bacterium of greening disease of citrus is a member of the alpha subdivision of the Proteobacteria. International Journal of Systematic and Evolutionary Microbiology 44:379–386
Kakizaki T, Matsumura H, Nakayama K, Che FS, Terauchi R, Inaba T (2003) Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. Plant Physiology 151:1339–1353
Killiny N, Nehela Y (2017) Metabolomic response to Huanglongbing: role of carboxylic compounds in Citrus sinensis response to 'Candidatus Liberibacter asiaticus' and its vector, Diaphorina citri. Molecular Plant-Microbe Interactions 30:666–678
Kim JS, Sagaram US, Burns JK, Li JL, Wang N (2009) Response of sweet orange (Citrus sinensis) to 'Candidatus Liberibacter asiaticus' infection: microscopy and microarray analyses. Phytopathology 99:50–57
Leménager D, Ouelhazi L, Mahroug S, Veau B, St-Pierre B, Rideau M, Aguirreolea J, Burlat V, Clastre M (2005) Purification, molecular cloning, and cell-specific gene expression of the alkaloid-accumulation associated protein CrPS in Catharanthus roseus. Journal of Experimental Botany 56:1221–1228
Li Y, Xu MR, Dai LP, Deng XL (2018) Distribution pattern and titer of Candidatus Liberibacter asiaticus in periwinkle (Catharanthus roseus). Journal of Integrative Agriculture 17:2501–2508
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC T method. Methods 25:402–408
Lu L, Cheng B, Yao J, Peng A, Du D, Fan G, Hu X, Zhang L, Chen G (2013) A new diagnostic system for detection of Candidatus Liberibacter asiaticus infection in citrus. Plant Disease 97:1295–1300
Martinelli F, Reagan RL, Uratsu SL, Phu ML, Albrecht U, Zhao W, Davis CE, Bowman KD, Dandekar AM (2013) Gene regulatory networks elucidating huanglongbing disease mechanisms. PLoS One 8:e74256
Mauch F, Mauch-Mani B, Gaille C, Kull B, Haas D, Reimmann C (2001) Manipulation of salicylate content in Arabidopsis thaliana by the expression of an engineered bacterial salicylate synthase. Plant Journal 25:67–77
Mizutani M, Ohta D, Sato R (1997) Isolation of a cDNA and a genomic clone encoding cinnamate 4-hydroxylase from Arabidopsis and its expression manner in planta. Plant Physiology 113:755–763
Senaratna T, Touchell D, Bunn E, Dixon K (2000) Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regulation 30:157–161
Serino L, Reimmann C, Baur H, Beyeler M, Visca P, Haas D (1995) Structural genes for salicylate biosynthesis from chorismate in Pseudomonas aeruginosa. Molecular Genetics and Genomics 249:217–228
Shi Q, Febres VJ, Jones JB, Moore GA (2015) Responsiveness of different citrus genotypes to the Xanthomonas citri ssp. citri-derived pathogen-associated molecular pattern (PAMP) flg22 correlates with resistance to citrus canker. Molecular Plant Pathology 16:507–520
Shine MB, Yang JW, El-Habbak M, Nagyabhyru P, Fu DQ, Navarre D, Ghabrial S, Kachroo P, Kachroo A (2016) Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean. New Phytologist 212:627–636
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2010) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739
Tsai CJ, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan Y (2006) Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytologist 172:47–62
Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A, Mysore KS, Bender CL (2007) The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Molecular Plant-Microbe Interactions 20:955–965
van Tegelen LJ, Moreno PR, Croes AF, Verpoorte R, Wullems GJ (1999) Purification and cDNA cloning of isochorismate synthase from elicited cell cultures of Catharanthus roseus. Plant Physiology 119:705–712
Wang N, Trivedi P (2013) Citrus huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology 103:652–665
Wang X, Gao J, Zhu Z, Dong X, Wang X, Ren G, Zhou X, Kuai B (2015) TCP transcription factors are critical for the coordinated regulation of ISOCHORISMATE SYNTHASE 1 expression in Arabidopsis thaliana. Plant Journal 82:151–162
Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565
Zhang X, Chen S, Mou Z (2010a) Nuclear localization of NPR1 is required for regulation of salicylate tolerance, isochorismate synthase 1 expression and salicylate accumulation in Arabidopsis. Journal of Plant Physiology 167:144–148
Zhang M, Duan Y, Zhou L, Turechek WW, Stover E, Powell CA (2010b) Screening molecules for control of citrus Huanglongbing using an optimized regeneration system for Candidatus Liberibacter asiaticus-infected periwinkle (Catharanthus roseus) cuttings. Phytopathology 100:239–245
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This study was supported by Natural Science Foundation of Guangdong Province (No. 2018A0303070019), Doctoral Starting Foundation of Guangdong Ocean University (No. R17060) and School Selective Project of Guangdong Ocean University (No. C17385).
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Li, Y., Yu, Q., Wang, B. et al. Differential expression of Isochorismate synthase in Catharanthus roseus during ‘Candidatus Liberibacter asiaticus’ infection. Trop. plant pathol. 44, 363–370 (2019). https://doi.org/10.1007/s40858-019-00287-y
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DOI: https://doi.org/10.1007/s40858-019-00287-y