Temporal Gene Expression Profiling of the Wheat Leaf Rust Pathosystem Using cDNA Microarray Reveals Differences in Compatible and Incompatible Defence Pathways

Fofana, Bourlaye; Banks, Travis W.; McCallum, Brent; Strelkov, Stephen E.; Cloutier, Sylvie

doi:https://doi.org/10.1155/2007/17542

International Journal of Plant Genomics

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Research Article | Open Access

Volume 2007 | Article ID 017542 | https://doi.org/10.1155/2007/17542

Temporal Gene Expression Profiling of the Wheat Leaf Rust Pathosystem Using cDNA Microarray Reveals Differences in Compatible and Incompatible Defence Pathways

Bourlaye Fofana,¹Travis W. Banks,¹Brent McCallum,¹Stephen E. Strelkov,²and Sylvie Cloutier¹

Academic Editor: Patrick Gulick

Received29 Dec 2006

Accepted20 Jul 2007

Published24 Sept 2007

Abstract

In this study, we detail the construction of a custom cDNA spotted microarray containing 7728 wheat ESTs and the use of the array to identify host genes that are differentially expressed upon challenges with leaf rust fungal pathogens. Wheat cultivar RL6003 (Thatcher Lr1) was inoculated with Puccinia triticina virulence phenotypes BBB (incompatible) or TJB (7-2) (compatible) and sampled at four different time points (3, 6, 12, and 24 hours) after inoculation. Transcript expression levels relative to a mock treatment were measured. One hundred ninety two genes were found to have significantly altered expression between the compatible and incompatible reactions. Among those were genes involved in photosynthesis, the production of reactive oxygen species, ubiquitination, signal transduction, as well as in the shikimate/phenylpropanoid pathway. These data indicate that various metabolic pathways are affected, some of which might be used by RL6003 to mount a coordinated defense against an incompatible fungal pathogen.

References

M. G. Eversmeyer and C. L. Kramer, “Epidemiology of wheat leaf and stem rust in the central great plains of the USA,” Annual Review of Phytopathology, vol. 38, pp. 491–513, 2000.
View at: Publisher Site | Google Scholar
J. A. Kolmer, “Genetics of resistance to wheat leaf rust,” Annual Review of Phytopathology, vol. 34, pp. 435–455, 1996.
View at: Publisher Site | Google Scholar
M. William, R. P. Singh, J. Huerta-Espino, S. O. Islas, and D. Hoisington, “Molecular marker mapping of leaf rust resistance gene Lr46 and its association with stripe rust resistance gene Yr29 in wheat,” Phytopathology, vol. 93, no. 2, pp. 153–159, 2003.
View at: Publisher Site | Google Scholar
L. Zhang, H. Meakin, and M. Dickinson, “Isolation of genes expressed during compatible interactions between leaf rust (Puccinia triticina) and wheat using cDNA-AFLP,” Molecular Plant Pathology, vol. 4, no. 6, pp. 469–477, 2003.
View at: Publisher Site | Google Scholar
M. A. Ayliffe, M. Steinau, and R. F. Park et al., “Aberrant mRNA processing of the maize Rp1-D rust resistance gene in wheat and barley,” Molecular Plant-Microbe Interactions, vol. 17, no. 8, pp. 853–864, 2004.
View at: Publisher Site | Google Scholar
R. Rohringer and R. Heitefuss, “Histology and molecular biology of hostparasite specificity,” in The Cereal Rusts, W. R. Bushnell and A. P. Roelfs, Eds., vol. 1, pp. 193–229, Academic Press, Orlando, Fla, USA, 1984.
View at: Google Scholar
G. Hu and F. H. J. Rijkenberg, “Subcellular localization of $β$ -1,3-glucanase in Puccinia recondita f.sp. tritici-infected wheat leaves,” Planta, vol. 204, no. 3, pp. 324–334, 1998.
View at: Publisher Site | Google Scholar
V. K. Thara, J. P. Fellers, and J.-M. Zhou, “In planta induced genes of Puccinia triticina,” Molecular Plant Pathology, vol. 4, no. 1, pp. 51–56, 2003.
View at: Publisher Site | Google Scholar
G. Hu and F. H. J. Rijkenberg, “Scanning electron microscopy of early infection structure formation by Puccinia recondita f. sp. tritici on and in susceptible and resistant wheat lines,” Mycological Research, vol. 102, no. 4, pp. 391–399, 1998.
View at: Publisher Site | Google Scholar
J. D. Faris, W. L. Li, D. J. Liu, P. D. Chen, and B. S. Gill, “Candidate gene analysis of quantitative disease resistance in wheat,” Theoretical and Applied Genetics, vol. 98, no. 2, pp. 219–225, 1999.
View at: Publisher Site | Google Scholar
V. S. Anguelova-Merhar, A. J. Van Der Westhuizen, and Z. A. Pretorius, “ $β$ -1,3-glucanase and chitinase activities and the resistance response of wheat to leaf rust,” Journal of Phytopathology, vol. 149, no. 7-8, pp. 381–384, 2001.
View at: Publisher Site | Google Scholar
K. C. Lin, W. R. Bushnell, A. G. Smith, and L. J. Szabo, “Temporal accumulation patterns of defence response gene transcripts in relation to resistant reactions in oat inoculated with Puccinia graminis,” Physiological and Molecular Plant Pathology, vol. 52, no. 2, pp. 95–114, 1998.
View at: Publisher Site | Google Scholar
S. G. Southerton and B. J. Deverall, “Changes in phenylalanine ammonia-lyase and peroxidase activities in wheat cultivars expressing resistance to the leaf-rust fungus,” Plant Pathology, vol. 39, no. 2, pp. 223–230, 1990.
View at: Publisher Site | Google Scholar
L. E. Browder, “A compendium of information about named genes for low reaction to Puccinia recondita in wheat,” Crop Science, vol. 20, no. 6, pp. 775–779, 1980.
View at: Google Scholar
D. J. Duggan, M. Bittner, Y. Chen, P. Meltzer, and J. M. Trent, “Expression profiling using cDNA microarrays,” Nature Genetics, vol. 21, supplement 1, pp. 10–14, 1999.
View at: Publisher Site | Google Scholar
T. Richmond and S. Somerville, “Chasing the dream: plant EST microarrays,” Current Opinion in Plant Biology, vol. 3, no. 2, pp. 108–116, 2000.
View at: Publisher Site | Google Scholar
P. Reymond, “DNA microarrays and plant defence,” Plant Physiology and Biochemistry, vol. 39, no. 3-4, pp. 313–321, 2001.
View at: Publisher Site | Google Scholar
R. A. Caldo, D. Nettleton, and R. P. Wise, “Interaction-dependent gene expression in Mla-specified response to barley powdery mildew,” The Plant Cell, vol. 16, no. 9, pp. 2514–2528, 2004.
View at: Publisher Site | Google Scholar
Y. Tao, Z. Xie, and W. Chen et al., “Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae,” The Plant Cell, vol. 15, no. 2, pp. 317–330, 2003.
View at: Publisher Site | Google Scholar
T. Eulgem, “Regulation of the Arabidopsis defense transcriptome,” Trends in Plant Science, vol. 10, no. 2, pp. 71–78, 2005.
View at: Publisher Site | Google Scholar
P. M. Schenk, K. Kazan, and I. Wilson et al., “Coordinated plant defense responses in Arabidopsis revealed by microarray analysis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 21, pp. 11655–11660, 2000.
View at: Publisher Site | Google Scholar
K. Maleck, A. Levine, and T. Eulgem et al., “The transcriptome of Arabidopsis thaliana during systemic acquired resistance,” Nature Genetics, vol. 26, no. 4, pp. 403–410, 2000.
View at: Publisher Site | Google Scholar
D. Baldwin, V. Crane, and D. Rice, “A comparison of gel-based, nylon filter and microarray techniques to detect differential RNA expression in plants,” Current Opinion in Plant Biology, vol. 2, no. 2, pp. 96–103, 1999.
View at: Publisher Site | Google Scholar
J. Boddu, S. Cho, W. M. Kruger, and G. J. Muehlbauer, “Transcriptome analysis of the barley-Fusarium graminearum interaction,” Molecular Plant-Microbe Interactions, vol. 19, no. 4, pp. 407–417, 2006.
View at: Publisher Site | Google Scholar
D. L. Long and J. A. Kolmer, “A North American system of nomenclature for Puccinia triticina,” Phytopathology, vol. 79, pp. 525–529, 1989.
View at: Google Scholar
B. Ewing, L. Hillier, M. C. Wendl, and P. Green, “Base-calling of automated sequencer traces using PhredI>. Accuracy assessment,” Genome Research, vol. 8, no. 3, pp. 175–185, 1998.
View at: Google Scholar
X. Huang and A. Madan, “CAP3: a DNA sequence assembly program,” Genome Research, vol. 9, no. 9, pp. 868–877, 1999.
View at: Publisher Site | Google Scholar
N. N. Iscove, M. Barbara, M. Gu, M. Gibson, C. Modi, and N. Winegarden, “Representation is faithfully preserved in global cDNA amplified exponentially from sub-picogram quantities of mRNA,” Nature Biotechnology, vol. 20, no. 9, pp. 940–943, 2002.
View at: Publisher Site | Google Scholar
S. F. Altschul, T. L. Madden, and A. A. Schäffer et al., “Gapped BLAST and PSI-BLAST: a new generation of protein database search programs,” Nucleic Acids Research, vol. 25, no. 17, pp. 3389–3402, 1997.
View at: Publisher Site | Google Scholar
A. R. Portis Jr., “Rubisco activase—Rubisco's catalytic chaperone,” Photosynthesis Research, vol. 75, no. 1, pp. 11–27, 2003.
View at: Publisher Site | Google Scholar
C. Lamb and R. A. Dixon, “The oxidative burst in plant disease resistance,” Annual Review of Plant Physiology and Plant Molecular Biology, vol. 48, pp. 251–275, 1997.
View at: Publisher Site | Google Scholar
K. Apel and H. Hirt, “Reactive oxygen species: metabolism, oxidative stress, and signal transduction,” Annual Review of Plant Biology, vol. 55, pp. 373–399, 2004.
View at: Publisher Site | Google Scholar
J. L. Dangl and J. D. G. Jones, “Plant pathogens and integrated defence responses to infection,” Nature, vol. 411, no. 6839, pp. 826–833, 2001.
View at: Publisher Site | Google Scholar
K. Shirasu and P. Schulze-Lefert, “Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways,” Trends in Plant Science, vol. 8, no. 6, pp. 252–258, 2003.
View at: Publisher Site | Google Scholar
P. Schulze-Lefert and S. Bieri, “Recognition at a distance,” Science, vol. 308, no. 5721, pp. 506–508, 2005.
View at: Publisher Site | Google Scholar
G. Coaker, A. Falick, and B. Staskawicz, “Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin,” Science, vol. 308, no. 5721, pp. 548–550, 2005.
View at: Publisher Site | Google Scholar
M. H. Glickman and A. Ciechanover, “The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction,” Physiological Reviews, vol. 82, no. 2, pp. 373–428, 2002.
View at: Google Scholar
M. C. Heath, “Signalling between pathogenic rust fungi and resistant or susceptible host plants,” Annals of Botany, vol. 80, no. 6, pp. 713–720, 1997.
View at: Publisher Site | Google Scholar
G. G. Hu and F. H. J. Rijkenberg, “Development of early infection structures of Puccinia recondita f.sp. tritici in non-host cereal species,” Journal of Phytopathology, vol. 146, no. 1, pp. 1–10, 1998.
View at: Google Scholar
C. Jantasuriyarat, M. Gowda, and K. Haller et al., “Large-scale identification of expressed sequence tags involved in rice and rice blast fungus interaction,” Plant Physiology, vol. 138, no. 1, pp. 105–115, 2005.
View at: Publisher Site | Google Scholar
J. Zou, S. Rodriguez-Zas, and M. Aldea et al., “Expression profiling soybean response to Pseudomonas syringae reveals new defense-related genes and rapid HR-specific downregulation of photosynthesis,” Molecular Plant-Microbe Interactions, vol. 18, no. 11, pp. 1161–1174, 2005.
View at: Publisher Site | Google Scholar
M. C. Heath, “Hypersensitive response-related death,” Plant Molecular Biology, vol. 44, no. 3, pp. 321–334, 2000.
View at: Publisher Site | Google Scholar
M. Trujillo, K.-H. Kogel, and R. Hückelhoven, “Superoxide and hydrogen peroxide play different roles in the nonhost interaction of barley and wheat with inappropriate formae speciales of Blumeria graminis,” Molecular Plant-Microbe Interactions, vol. 17, no. 3, pp. 304–312, 2004.
View at: Publisher Site | Google Scholar
H. Vanacker, T. L. W. Carver, and C. H. Foyer, “Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves,” Plant Physiology, vol. 117, no. 3, pp. 1103–1114, 1998.
View at: Publisher Site | Google Scholar
S. Davletova, L. Rizhsky, and H. Liang et al., “Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis,” The Plant Cell, vol. 17, no. 1, pp. 268–281, 2005.
View at: Publisher Site | Google Scholar
L. J. Allen, K. B. Macgregor, R. S. Koop, D. H. Bruce, J. Karner, and A. W. Bown, “The relationship between photosynthesis and a mastoparan-induced hypersensitive response in isolated mesophyll cells,” Plant Physiology, vol. 119, no. 4, pp. 1233–1241, 1999.
View at: Publisher Site | Google Scholar
S. Seo, M. Okamoto, and T. Iwai et al., “Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction,” The Plant Cell, vol. 12, no. 6, pp. 917–932, 2000.
View at: Publisher Site | Google Scholar
R. Mittler, X. Feng, and M. Cohen, “Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco,” The Plant Cell, vol. 10, no. 3, pp. 461–473, 1998.
View at: Publisher Site | Google Scholar
M. Yoshioka, S. Uchida, and H. Mori et al., “Quality control of photosystem—II: cleavage of reaction center D1 protein in spinach thylakoids by FtsH protease under moderate heat stress,” Journal of Biological Chemistry, vol. 281, no. 31, pp. 21660–21669, 2006.
View at: Publisher Site | Google Scholar
C. Spetea, T. Hundal, F. Lohmann, and B. Andersson, “GTP bound to chloroplast thylakoid membranes is required for light-induced, multienzyme degradation of the photosystem II D1 protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 11, pp. 6547–6552, 1999.
View at: Publisher Site | Google Scholar
A. Devoto, P. R. Muskett, and K. Shirasu, “Role of ubiquitination in the regulation of plant defence against pathogens,” Current Opinion in Plant Biology, vol. 6, no. 4, pp. 307–311, 2003.
View at: Publisher Site | Google Scholar
J. P. Rathjen and P. Moffett, “Early signal transduction events in specific plant disease resistance,” Current Opinion in Plant Biology, vol. 6, no. 4, pp. 300–306, 2003.
View at: Publisher Site | Google Scholar
R. A. Dixon and N. L. Paiva, “Stress-induced phenylpropanoid metabolism,” The Plant Cell, vol. 7, no. 7, pp. 1085–1097, 1995.
View at: Publisher Site | Google Scholar
F. Daayf, A. Schmitt, and R. R. Bélanger, “Evidence of phytoalexins in cucumber leaves infected with powdery mildew following treatment with leaf extracts of Reynoutria sachalinensis,” Plant Physiology, vol. 113, no. 3, pp. 719–727, 1997.
View at: Google Scholar
E. Nakane, K. Kawakita, N. Doke, and H. Yoshioka, “Elicitation of primary and secondary metabolism during defense in the potato,” Journal of General Plant Pathology, vol. 69, no. 6, pp. 378–384, 2003.
View at: Publisher Site | Google Scholar
B. Fofana, N. Benhamou, D. J. McNally, C. Labbé, A. Séguin, and R. R. Bélanger, “Suppression of induced resistance in cucumber through disruption of the flavonoid pathway,” Phytopathology, vol. 95, no. 1, pp. 114–123, 2005.
View at: Publisher Site | Google Scholar
S. Yoshimura, U. Yamanouchi, and Y. Katayose et al., “Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 4, pp. 1663–1668, 1998.
View at: Publisher Site | Google Scholar
S. Zhang and D. F. Klessig, “MAPK cascades in plant defense signaling,” Trends in Plant Science, vol. 6, no. 11, pp. 520–527, 2001.
View at: Publisher Site | Google Scholar
J. Dong, C. Chen, and Z. Chen, “Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response,” Plant Molecular Biology, vol. 51, no. 1, pp. 21–37, 2003.
View at: Publisher Site | Google Scholar
C. Azevedo, A. Sadanandom, K. Kitagawa, A. Freialdenhoven, K. Shirasu, and P. Schulze-Lefert, “The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance,” Science, vol. 295, no. 5562, pp. 2073–2076, 2002.
View at: Publisher Site | Google Scholar
K. Kitagawa, D. Skowyra, S. J. Elledge, J. W. Harper, and P. Hieter, “SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex,” Molecular Cell, vol. 4, no. 1, pp. 21–33, 1999.
View at: Publisher Site | Google Scholar
S. Shigeoka, T. Ishikawa, and M. Tamoi et al., “Regulation and function of ascorbate peroxidase isoenzymes,” Journal of Experimental Botany, vol. 53, no. 372, pp. 1305–1319, 2002.
View at: Publisher Site | Google Scholar
S. Barak, A. Nejidat, Y. Heimer, and M. Volokita, “Transcriptional and posttranscriptional regulation of the glycolate oxidase gene in tobacco seedlings,” Plant Molecular Biology, vol. 45, no. 4, pp. 399–407, 2001.
View at: Publisher Site | Google Scholar
N. Zhang and A. R. Portis Jr., “Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 16, pp. 9438–9443, 1999.
View at: Publisher Site | Google Scholar
I. Cohen, J. A. Knopf, V. Irihimovitch, and M. Shapira, “A proposed mechanism for the inhibitory effects of oxidative stress on Rubisco assembly and its subunit expression,” Plant Physiology, vol. 137, no. 2, pp. 738–746, 2005.
View at: Publisher Site | Google Scholar
R. Hauschild and A. von Schaewen, “Differential regulation of glucose-6-phosphate dehydrogenase isoenzyme activities in potato,” Plant Physiology, vol. 133, no. 1, pp. 47–62, 2003.
View at: Publisher Site | Google Scholar
R. Entus, M. Poling, and K. M. Herrmann, “Redox regulation of Arabidopsis 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase,” Plant Physiology, vol. 129, no. 4, pp. 1866–1871, 2002.
View at: Publisher Site | Google Scholar

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Copyright © 2007 Bourlaye Fofana et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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