Hostname: page-component-745bb68f8f-f46jp Total loading time: 0 Render date: 2025-02-08T17:41:42.724Z Has data issue: false hasContentIssue false
  • English
  • Français

Microarray Analysis of the Semicompatible, Pathogenic Response and Recovery of Leafy Spurge (Euphorbia esula) Inoculated with the Cassava Bacterial Blight Pathogen Xanthomonas axonopodis pv. manihotis

Published online by Cambridge University Press:  20 January 2017

David P. Horvath ,
María A. Santana  and
James V. Anderson
David P. Horvath*
Affiliation:
Sunflower and Plant Biology Research Unit, Red River Valley Agricultural Research Center, U.S. Department of Agriculture–Agricultural Research Service, Fargo, ND 58102
María A. Santana
Affiliation:
Departamento de Biología Celular, División de Ciencias Biológicas, Universidad Simón Bolivar, Caracas, Venezuela, and the Instituto de Estudios Avanzados, Centro de Biotecnología, Caracas, Venezuela
James V. Anderson
Affiliation:
Sunflower and Plant Biology Research Unit, Red River Valley Agricultural Research Center, U.S. Department of Agriculture–Agricultural Research Service, Fargo, ND 58102
*
Corresponding author's E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Infection by Xanthomonas axonopodis pv. manihotis (Xam) of the perennial rangeland weed leafy spurge was tested to see whether Xam might serve a potential biological control agent for this invasive weed. Although leafy spurge was susceptible to Xam infection, it recovered within 21 d after inoculation (DAI). Microarray resources available for leafy spurge allowed us to follow the physiological and signaling pathways that were altered as leafy spurge was infected and then recovered from Xam infection. The first physiological effect of Xam infection was a down-regulation of photosynthetic processes within 1 DAI. By 7 DAI, numerous processes associated with well-documented pathogenesis responses of plants were observed. Although some pathogenesis responses were still detectable at 21 DAI, other processes associated with meristem development were noted. Ontological analysis of potential signaling systems indicated jasmonic acid plays a significant role in the recovery processes.

Keywords

Leafy spurge, Euphorbia esula L. EPHESNetwork analysispathogenesistranscriptomics
Type
Weed Biology and Ecology
Information
Weed Science , Volume 61 , Issue 3 , September 2013 , pp. 428 - 436
Copyright
Copyright © Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Alvarez, A. M., Buddenhagen, I. W., Buddenhagen, E. S., and Domen, H. Y. 1978. Bacterial blight of onion, a new disease caused by Xanthomonas sp. Phytopathology 68:1132–1136.CrossRefGoogle Scholar
Anderson, J. V., Horvath, D. P., Chao, W. S., Foley, M. E., Hernandez, A. G., Thimmapuram, J., Liu, L., Gong, G. L., Band, M., Kim, R., and Mikel, M. A. 2007. Characterization of an EST database for the perennial weed leafy spurge: an important resource for weed biology research. Weed Sci. 55:193–203.CrossRefGoogle Scholar
Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W. L., Gomez-Gomez, L., Boller, T., Ausubel, F. M., and Sheen, J. 2002. MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415:977–983.Google ScholarPubMed
Ascencio-Ibáñez, J. T., Sozzani, R., Lee, T.-J., Chu, T.-M., Wolfinger, R. D., Cella, R., and Hanley-Bowdoin, L. 2008. global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol. 148:436–454.CrossRefGoogle ScholarPubMed
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. 2000. Gene ontology: tool for the unification of biology—the Gene Ontology Consortium. Nat. Genet. 25:25–29.CrossRefGoogle ScholarPubMed
Balaji, V., Gibly, A., Debbie, P., and Sessa, G. 2007. Transcriptional analysis of the tomato resistance response triggered by recognition of the Xanthomonas type III effector AvrXv3 . Funct. Integr. Genomics 7:305–316.CrossRefGoogle ScholarPubMed
Berger, S., Papadopoulos, M., Schreiber, U., Kaiser, W., and Roitsch, T. 2004. Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato Physiol. Plant. 122:419–428.Google Scholar
Cao, H., Bowling, S. A., Gordon, S., and Dong, X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592.Google ScholarPubMed
Casacuberta, J. M., Raventós, D., Puigdoménech, P., and San Segundo, B. 1992. Expression of the gene encoding the PR-like protein PRms in germinating maize embryos. Mol. Gen. Genet. 234:97–104.CrossRefGoogle ScholarPubMed
Chang, S., Puryear, J., and Cairney, J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11:113–116.CrossRefGoogle Scholar
Chao, W. and Anderson, J. V. 2004. Euphorbia esula . In: Crop Protection Compendium. 2004 ed. Wallingford, UK CABI (CD-ROM).Google Scholar
Chao, W. S., Horvath, D. P., Anderson, J. V., and Foley, M. E. 2005. Potential model weeds to study genomics, ecology, and physiology in the 21st century. Weed Sci. 53:929–937.CrossRefGoogle Scholar
Churchill, G. A. 2002. Fundamentals of experimental design for cDNA microarrays. Nat. Gen. 32:490–495.CrossRefGoogle ScholarPubMed
Civerolo, E. 1984. Bacterial canker disease of citrus. J. Rio Grande Val Hortic. Soc. 37:127–145.Google Scholar
Durner, J., Shah, J., and Klessig, D. F. 1997. Salicylic acid and disease resistance in plants. Trends Plant Sci. 2:266–274.CrossRefGoogle Scholar
Genoud, T., Millar, A. J., Nishizawa, N., Kay, S. A., Schäfer, E., Nagatani, A., and Chua, N-H. 1998. An Arabidopsis mutant hypersensitive to red and far-red light signals. Plant Cell 10:889–904.CrossRefGoogle ScholarPubMed
Gibly, A., Bonshtien, A., Balaji, V., Debbie, P., Martin, G. B., and Sessa, G. 2004. Identification and expression profiling of tomato genes differentially regulated during a resistance response to Xanthomonas campestris pv. vesicatoria . Mol. Plant-Microbe Interact. 17:1212–1222.Google ScholarPubMed
Horvath, D. P., Chao, W. S., Suttle, J. C., Thimmapuram, J., and Anderson, J. V. 2008. Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). BMC Genomics. 9:536. DOI:10.1186/1471-2164-9-536.CrossRefGoogle ScholarPubMed
Horvath, D. P., Kudrna, D., Talag, J., Anderson, J. V., Chao, W. S., Wing, R. A., Foley, M. E., and Doğramacı, M. 2013. BAC library development, and clone characterization for dormancy-responsive DREB4A, DAM, and FT from leafy spurge (Euphorbia esula L.) identifies differential splicing and conserved promoter motifs. Weed Sci. DOI: 10.1614/WS-D-12-00175.1.CrossRefGoogle Scholar
Jones, J. B., Lacy, G. H., Bouzar, H., Stall, R. E., and Schaad, N. W. 2004. Reclassification of the xanthomonads associated with bacterial spot disease of tomato and pepper. Syst. Appl. Microbiol. 27:755–762.CrossRefGoogle ScholarPubMed
Kamada, I., Yamauchl, S., Yousseflan, S., and Sano, H. 1992. Transgenic tobacco plants expressing rgp7, a gene encoding a ras-related GTP-binding protein from rice, show distinct morphological characteristics. Plant J. 2:799–807.CrossRefGoogle Scholar
Kapulnik, Y., Volpin, H., Itzhaki, H., Ganon, D., Galili, S., David, R., Shaul, O., Elad, Y., Chet, I., and Okon, Y. 1996. Suppression of defense responses in mycorrhizal alfalfa and tobacco roots. New Phytol. 133:59–64.CrossRefGoogle Scholar
Kpémoua, K., Boher, B., Nicole, M., Calatayud, P. and Geiger, J. P. 1996. Cytochemistry of defense responses of cassava to Xanthomonas campestris pv. manihotis . Can. J. Microbiol. 42:1131–1149.CrossRefGoogle Scholar
Kremer, R. J., Caesar, A. J., and Souissi, T. 2006. Soilborne microorganisms of Euphorbia are potential biological control agents of the invasive weed leafy spurge. Appl. Soil Ecol. 32:27–37.CrossRefGoogle Scholar
Kumaran, M. K., Bowman, J. L., and Sundaresan, V. 2002. YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis . Plant Cell 14:2761–2770.CrossRefGoogle ScholarPubMed
Kumaran, M. K., Ye, D., Yang, W. C., Griffith, M. E., Chaudhury, A. M., and Sundaresan, V. 1999. Molecular cloning of abnormal floral organs: a gene required for flower development in Arabidopsis . Sex. Plant Reprod. 12:118–122.Google Scholar
Lee, S., Kim, S. Y., Chung, E., Joung, Y. H., Pai, H. S., Hur, C. G., and Choi, D. 2004. EST and microarray analyses of pathogen-responsive genes in hot pepper (Capsicum annuum L.) non-host resistance against soybean pustule pathogen (Xanthomonas axonopodis pv. glycines). Funct. Integr. Genomics. 4:196–205.Google ScholarPubMed
Livak, K. J. and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method. Methods 25:402–408.CrossRefGoogle Scholar
Lokko, Y., Anderson, J. V., Rudd, S., Raji, A., Horvath, D., Mikel, M. A., Kim, R., Liu, L., Hernandez, A., Dixon, A.G.O., and Ingelbrecht, I. 2007. Characterization of an 18,166 EST dataset for cassava (Manihot esculenta Crantz) enriched for drought-responsive genes. Plant Cell Rep. 26:1605–1618.Google Scholar
Lopez, C., Soto, M., Restrepo, S., Piegu, B., Cooke, R., Delseny, M., Tohme, J., and Verdier, V. 2005. Gene expression profile in response to Xanthomonas axonopodis pv. manihotis infection in cassava using a cDNA microarray. Plant Mol. Biol. 57:393–410.CrossRefGoogle ScholarPubMed
Lorenzo, O. and Solano, R. 2005. Molecular players regulating the jasmonate signalling network. Curr. Opin. Plant Biol. 8:532–540.CrossRefGoogle ScholarPubMed
Lozoya, E., Block, A., Lois, R., Hahlbrock, K., and Scheel, D. 1991. Transcriptional repression of light-induced flavonoid synthesis by elicitor treatment of cultured parsley cells. Plant J. 1:227–234.CrossRefGoogle Scholar
Mizuno, T. and Yamashino, T. 2008. Comparative transcriptome of diurnally oscillating genes and hormone-responsive genes in Arabidopsis thaliana: insight into circadian clock-controlled daily responses to common ambient stresses in plants. Plant Cell Physiol. 49:481–487.Google ScholarPubMed
Qiu, J.-L., Zhou, L., Yun, B.-W., Nielsen, H. B., Fiil, B. K., Petersen, K., MacKinlay, J., Loake, G. J., Mundy, J., and Morris, P. C. 2008. Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signalling mediated by MEKK1, MPK4, and MKS1 . Plant Physiol. 148:212–222.CrossRefGoogle ScholarPubMed
Prathuangwong, S. and Amnuaykit, K. 1987. Studies on tolerance and rate reducing bacterial pustule of soybean cultivars/lines. Kasetsart J. (Nat. Sci.) 21:408–20.Google Scholar
Rybak, M., Minsavage, G. V., Stall, R. E., and Jones, J. B. 2009. Identification of Xanthomonas citri ssp. citri host specificity genes in a heterologous expression host. Mol. Plant Pathol. 10:249–262.CrossRefGoogle Scholar
Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor, NY Cold Spring Harbor Laboratory, Volume 1. Pp. 7.43–7.45.Google Scholar
Sano, H., Seo, S., Orudgev, E., Youssefian, S., Ishizuka, K., and Ohashi, Y. 1994. Expression of the gene for a small GTP binding protein in transgenic tobacco elevates endogenous cytokinin levels, abnormally induce salicylic acid in response to wounding and increases resistance to tobacco mosaic virus infection. Proc. Natl. Acad. Sci. U. S. A. 91:10556–10560.CrossRefGoogle ScholarPubMed
Sano, H., Seo, S., Koizumi, N., Niki, T., Iwamura, H., and Ohashi, Y. 1996. Regulation by cytokinins of endogenous levels of jasmonic and salicylic acids in mechanically wounded tobacco plants. Plant Cell Physiol. 37:762–769.CrossRefGoogle Scholar
Searle, I. R., Men, A. E., Laniya, T. S., Buzas, D. M., Iturbe-Ormaetxe, I., Carroll, B. J., and Gresshoff, P. M. 2003. Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109–112.CrossRefGoogle ScholarPubMed
Sessa, G., Yang, X.-Q., Raz, V., Eyal, Y., and Fluhr, R. 1995. Dark induction and subcellular localization of the pathogenesis-related PRB-1b protein. Plant Mol. Biol. 28:537–547.CrossRefGoogle ScholarPubMed
Siemens, J., Keller, I., Sarx, J., Kunz, S., Schuller, A., Nagel, W., Schmülling, T., Parniske, M., and Ludwig-Müller, J. 2006. Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Mol. Plant-Microbe Interact. 19:480–494.CrossRefGoogle ScholarPubMed
Suarez-Rodriguez, M. C., Adams-Phillips, L., Liu, Y., Wang, H., Su, S.-H., Jester, P. J., Zhang, S., Bent, A. F., and Krysan, P. J. 2007. MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol. 143:661–669.CrossRefGoogle ScholarPubMed
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., et al. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 102:15545–15550.CrossRefGoogle ScholarPubMed
Takada, S., Hibara, K., Ishida, T., and Tasaka, M. 2001. The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128:127–1135.Google ScholarPubMed
Usadel, B., Nagel, A., Thimm, O., Redestig, H., Blaesing, O. E., Palacios-Rojas, N., Selbig, J., Hannemann, J., Piques, M. C., Steinhauser, D., Scheible, W-R., Gibon, Y., Morcuende, R., Weicht, D., Meyer, S., and Stitt, M. 2005. Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiol. 138:1195–1204.CrossRefGoogle Scholar
van Verk, M. C., Pappaioannou, D., Neeleman, L., Bol, J. F., and Linthorst, H.J.M. 2008. A novel WRKY transcription factor is required for induction of PR-1a gene expression by salicylic acid and bacterial elicitors. Plant Physiol. 146:1983–1995.Google ScholarPubMed
Vauterin, L., Rademaker, J., and Swings, J. 2000. Synopsis on the taxonomy of the genus Xanthomonas . Phytopathology 90:677–682.CrossRefGoogle ScholarPubMed
Wan, J., Dunning, F. M., and Bent, A. F. 2002. Probing plant–pathogen interactions and downstream defense signaling using DNA microarrays. Funct. Integr. Genomics 2:259–273.CrossRefGoogle ScholarPubMed
Xie, D. X., Feys, B. F., James, S., Nieto-Rostro, M., and Turner, J. G. 1998. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094.CrossRefGoogle ScholarPubMed
Zou, J., Rodriguez-Zas, S., Aldea, M., Li, M., Zhu, J., Gonzalez, D. O., Vodkin, L. O., DeLucia, E., and Clough, S. J. 2005. Expression profiling soybean response to Pseudomonas syringae reveals new defense-related genes and rapid hr-specific down-regulation of photosynthesis. Mol. Plant-Microbe Interact. 18:161–1174.CrossRefGoogle ScholarPubMed
Supplementary material: File

Horvath et al. supplementary material

Tables S1-S9

Download Horvath et al. supplementary material(File)
File 14.8 MB