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Host gene expression in response to Egyptian broomrape (Orobanche aegyptiaca)

Published online by Cambridge University Press:  20 January 2017

Amanda A. Griffitts
Affiliation:
Department of Plant Pathology, Physiology, and Weed Science, Virginia Tech, 410 Price Hall, Blacksburg, VA 24061-0331
Carole L. Cramer
Affiliation:
Department of Plant Pathology, Physiology, and Weed Science, Virginia Tech, 410 Price Hall, Blacksburg, VA 24061-0331

Abstract

Selective control of Egyptian broomrape is extremely difficult because the close association between host crop and parasite limits the use of most mechanical and herbicidal approaches. However, this host–parasite interaction can also form the basis of the simplest control strategy: parasite-resistant crops. Although much work has been conducted to identify and characterize mechanisms of parasite resistance, varieties with stable resistance are still unavailable for most affected crops. The development of resistant crops can be accelerated by genetic engineering to the extent that important aspects of the host–parasite interaction are understood. In this study, we characterize a variety of gene promoter elements with respect to parasite induction and expression pattern. Studies were conducted using transgenic plants expressing fusions of the β-glucuronidase reporter gene with promoter elements from several genes. Promoters from genes known to have increased expression in response to pathogen attack or wounding showed localized, induced expression after parasitism. These included phenylalanine ammonia lyase, chalcone synthase, sesquiterpene cyclase, and HMG1 (3-hydroxy-3-methylglutaryl CoA reductase). In contrast, the systemic acquired resistance–associated gene PR-1a was not induced by parasitism. Non–defense-related genes varied in response, with squalene synthase being repressed, whereas farnesyltransferase was highly expressed in the region of parasite attachment. These results demonstrate a range of expression, both in intensity and tissue specificity, in response to parasitism.

Type
Physiology, Chemistry, and Biochemistry
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Ben-Hod, G., Losner, D., Joel, D. M., and Mayer, M. 1993. Pectin methylesterase in calli and germinating seeds of Orobanche aegyptiaca . Phytochemistry 32:13991402.CrossRefGoogle Scholar
Brindle, P. A., Kuhn, P. J., and Threlfall, D. R. 1988. Biosynthesis and metabolism of sesquiterpenoid phytoalexins and triterpenoids in potato cell suspension cultures. Phytochemistry 27:133150.Google Scholar
Chappell, J. 1995. The biochemistry and molecular biology of isoprenoid metabolism. Plant Physiol 107:16.Google Scholar
Choi, D., Bostock, R. M., Avdiushko, S., and Hilderbrand, D. F. 1994. Lipid-derived signals that discriminate wound- and pathogen-responsive isoprenoid pathways in plants: methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes and antimicrobial isoprenoids in Solanum tuberosum L. Proc. Natl. Acad. Sci. USA 91:23292333.Google Scholar
Choi, D., Ward, B. L., and Bostock, R. M. 1992. Differential induction and suppression of potato 3-hydroxy-3-methylglutaryl coenzyme A reductase genes in response to Phytophthora infestans and to its elicitor arachidonic acid. Plant Cell 4:13331344.Google Scholar
Church, G. M. and Gilbert, W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81:19911995.Google Scholar
Cramer, C. L., Weissenborn, D. L., Cottingham, C. K., Denbow, C. J., Eisenback, J. D., Radin, D. N., and Yu, X. 1993. Regulation of defense-related gene expression during plant-pathogen interactions. J. Nematol 25:507518.Google Scholar
Cubero, J. I., Pieterse, A. H., Khalil, S. A., and Sauerborn, J. 1994. Screening techniques and sources of resistance to parasitic angiosperms. Euphytica 73:5158.Google Scholar
Doerner, P. W., Stermer, B., Schmid, J., Dixon, R. A., and Lamb, C. J. 1990. Plant defense gene promoter–reporter gene fusions in transgenic plants: tools for identification of novel inducers. Biotechnology 8:845848.Google Scholar
Dörr, I. 1996. New results on interspecific bridges between parasites and their hosts. Pages 195201 in Moreno, M. T., Cubero, J. I., Berner, D., Joel, D., and Musselman, L. J. eds. Advances in Parasitic Plant Research. Cordoba, Spain: Junta de Andalucia.Google Scholar
Eyal, Y., Meller, Y., Lev-Yadun, S., and Fluhr, R. 1993. A basic-type PR-1 promoter directs ethylene responsiveness, vascular and abscission zone-specific expression. Plant J 4:225234.Google Scholar
Eyal, Y., Sagee, O., and Fluhr, R. 1992. Dark-induced accumulation of a basic pathogenesis-related (PR-1) transcript and a light requirement for its induction by ethylene. Plant Mol. Biol 19:589599.Google Scholar
Goldwasser, Y., Hershenhorn, J., Plakhine, D., Kleifeld, Y., and Rubin, B. 1999. Biochemical factors involved in vetch resistance to Orobanche aegyptiaca . Physiol. Mol. Plant Pathol 54:8796.Google Scholar
Hoagland, D. R. and Arnon, D. I. 1950. The water-culture method for growing plants without soil. Calif. Agric. Exp. Sta. Circ 347:132.Google Scholar
Hunt, M. D. and Ryals, J. A. 1996. Systemic acquired resistance signal transduction. Crit. Rev. Plant Sci 15:583606.Google Scholar
Jefferson, R. A. 1987. Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol. Biol. Rept 5:387405.Google Scholar
Jelesko, J. G., Jenkins, S. M., Rodriguez-Concepcion, M., and Gruissem, W. 1999. Regulation of tomato HMG1 during cell proliferation and growth. Planta 208:310318.Google Scholar
Joel, D. M., Kleifeld, Y., Losner-Goshen, D., and Gressel, J. 1995a. Transgenic crops against parasites. Nature 374:220221.Google Scholar
Joel, D. M. and Losner-Goshen, D. 1994. The attachment organ of the parasitic angiosperms Orobanche cumana and O. aegyptiaca and its development. Can. J. Bot 72:564574.Google Scholar
Joel, D. M. and Portnoy, V. H. 1998. The angiospermous root parasite Orobanche L. (Orobanchaceae) induces expression of a pathogenesis related (PR) gene in susceptible tobacco roots. Ann. Bot 81:779781.Google Scholar
Joel, D. M., Steffens, J. C., and Matthews, D. E. 1995b. Germination of weedy root parasites. Pages 567597 in Kigel, J. and Galili, G. eds. Seed Development and Germination. New York: Marcel Dekker.Google Scholar
Kuijt, J. 1977. Haustoria of phanerogamic parasites. Ann. Rev. Phytopathol 17:91118.Google Scholar
Liang, X., Dron, M., Schmid, J., Dixon, R. A., and Lamb, C. L. 1989. Developmental and environmental regulation of a phenylalanine ammonia-lyase-B-glucuronidase gene fusion in transgenic tobacco plants. Proc. Natl. Acad. Sci. USA 86:92849288.Google Scholar
Linke, K-H. 1992. Biology and control of Orobanche in legume crops. PLITS 10:62.Google Scholar
Losner-Goshen, D., Portnoy, V. H., Mayer, A. M., and Joel, D. M. 1998. Pectolytic activity by the haustorium of the parasitic plant Orobanche L. (Orobanchaceae) in host roots. Ann. Bot 81:319326.CrossRefGoogle Scholar
Mangnus, E. M., Stommen, P. L. A., and Zwanenburg, B. 1992. A standardized bioassay for evaluation of potential germination stimulants for seeds of parasitic weeds. J. Plant Growth Regul 11:9198.Google Scholar
Mitsuhara, I., Matsufuru, H., Ohshima, M., Kaku, H., Nakajima, Y., Murai, N., Natori, S., and Ohashi, Y. 2000. Induced expression of sarcotoxin IA enhanced host resistance against both bacterial and fungal pathogens in transgenic tobacco. Mol. Plant Microbe Interact 13:860868.CrossRefGoogle ScholarPubMed
Oerke, E-C., Dehne, H-W., Schonbeck, F., and Weber, A. 1994. Crop Production and Crop Protection. Estimated Losses in Major Food and Cash Crops. Amsterdam: Elsevier. Pp. 372387.Google Scholar
Parker, C. and Riches, C. R. 1993. Parasitic Weeds of the World: Biology and Control. Wallingford, Oxon: CAB International. Pp. 111164.Google Scholar
Pei, Z-M., Ghassemian, M., Kwak, C. M., McCourt, P., and Schroeder, J. I. 1998. Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss. Science 282:287290.Google Scholar
Qian, D., Zhou, D., Rong, J., Cramer, C. L., and Yang, Z. 1996. Protein farnesyltransferase in plants: molecular characterization and involvement in cell cycle control. Plant Cell 8:23812394.Google Scholar
Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press. Pp. 7.39–7.52.Google Scholar
Schmid, J., Doerner, P. W., Clouse, S. D., Dixon, R. A., and Lamb, C. J. 1990. Developmental and environmental regulation of a bean chalcone synthase promoter in transgenic tobacco. Plant Cell 2:619631.Google Scholar
Serghini, K., Pérez de Luque, A., Castejón-Muñoz, M., García-Torres, L., and Jorrín, J. V. 2001. Sunflower (Helianthus annuus L.) response to broomrape (Orobanche cernua Loefl.) parasitism: induced synthesis and excretion of 7-hydroxylated simple coumarins. J. Exp. Bot 52:22272234.Google Scholar
Shomer-Ilan, A. 1993. Germinating seeds of the root parasite Orobanche aegyptiaca Pers. excrete enzymes with carbohydrase activity. Symbiosis 15:6170.Google Scholar
Tjamos, E. C. and Kuc, J. A. 1982. Inhibition of steroid glycoalkaloid accumulation by arachidonic and eicosapentaenoic acids in potato. Science 217:542544.Google Scholar
Vieira Dos Santos, C., Letousey, P., Delavault, P., and Thalouarn, P. 2003. Defense gene expression analysis of Arabidopsis thaliana parasitized by Orobanche ramosa . Phytopathology 93:451457.Google Scholar
Vögeli, U. and Chappell, J. 1988. Induction of sesquiterpene cyclase and suppression of squalene synthetase activities in plant cell cultures treated with fungal elicitor. Plant Physiol 88:12911296.Google Scholar
Ward, E. R., Uknes, S. J., Williams, S. C., Dincher, S. S., Wierderhold, D. L., Alexander, D. C., Ahi-Goy, P., Metraux, J-P., and Ryals, J. A. 1991. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:10851094.Google Scholar
Weissenborn, D. L., Denbow, C. J., Laine, M., Lang, S., Yang, Z., Yu, X., and Cramer, C. L. 1995. HMG-CoA reductase and terpenoid phytoalexins: molecular specialization within a complex pathway. Physiol. Plant 93:393400.Google Scholar
Westwood, J. H., Yu, X., Foy, C. L., and Cramer, C. L. 1998. Expression of a defense-related 3-hydroxy-3-methylglutaryl CoA reductase gene in response to parasitization by Orobanche spp. Mol. Plant-Microbe Interact 11:530536.CrossRefGoogle ScholarPubMed
Yin, S., Mei, L., Newman, J., Back, K., and Chappell, J. 1997. Regulation of sesquiterpene cyclase gene expression: characterization of an elicitor- and pathogen-inducible promoter. Plant Physiol 115:437451.Google Scholar
Yoder, J. I. 1999. Parasitic plant responses to host plant signals: a model for subterranean plant-plant interactions. Curr. Opin. Plant Biol 2:6570.CrossRefGoogle Scholar
Yoder, J. I. 2001. Host-plant recognition by parasitic Scrophulariaceae. Curr. Opin. Plant Biol 4:359365.Google Scholar
Zhou, D., Qian, D., Cramer, C. L., and Yang, Z. 1997. Developmental and environmental regulation of tissue- and cell-specific expression of a pea protein farnesyltransferase gene in transgenic plants. Plant J 12:921930.Google Scholar
Zook, M. N. and Kuc, J. A. 1991. Induction of sesquiterpene cyclase and suppression of squalene synthetase activity in elicitor-treated or fungal-infected potato tuber tissue. Physiol. Mol. Plant Pathol 39:377390.Google Scholar