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American Society of Plant Biologists
Aminotransferases Confer "Enzymatic Resistance" to Downy Mildew in MelonNews and Reviews Editor neckardt{at}aspb.org
Plants use a wide range of mechanisms to resist infection and disease caused by pathogenic organisms. Mechanical or chemical barriers present in the epidermal layer of plant tissues prevent the successful establishment and growth of many potential pathogens. Pathogens that make it past this first line of defense are met by a second battery of defenses, ranging from the specific interactions between plant Resistance gene and pathogen Avirulence gene products to multiple, and far less well understood, nonhost and "basal" defense pathways (Dangl and Jones, 2001
There is increasing evidence that, in some cases, constitutively expressed genes encoding enzymes associated with normal plant metabolism also play critical roles in the induction of plant defenses against pathogens. Last month in these pages (Eckardt, 2003  ), work by Wang et al. (2003) was highlighted suggesting that plant adenosine kinase, which controls flux through the S-adenosyl-L-Met–dependent methylation cycle, also plays a role in viral defense. Previous work by Hao et al. (2003) has shown that the activity of plant SNF1 kinase, which functions in the regulation of carbon metabolism, also is associated with viral defense. Another example is the discovery that Arabidopsis NHO1, which encodes a glycerol kinase, is required for resistance to multiple nonhost pathovars of Pseudomonas syringae bacteria and that virulent P. syringae actively suppresses NHO1 expression through a jasmonic acid signaling pathway (Kang et al., 2003). In this issue of The Plant Cell, Taler et al. (pages 172–184) describe another form of "enzymatic disease resistance" associated with the expression of peroxisomal glyoxylate aminotransferases in Cucumis melo (wild melon) that confers protection against downy mildew caused by the oomycete pathogen Pseudoperonospora cubensis (Figure 1).
P. cubensis is a biotrophic oomycete that causes downy mildew disease in the Cucurbitaceae family. Other oomycetes of the family Peronosporaceae, including Peronospora and Bremia, cause downy mildew in a variety of plant families. Downy mildews are primarily foliage blights (P. cubensis infects only the leaves of susceptible cucurbits). In a favorable environment (typically high RH at moderate air temperatures, which promotes the development of a film of water on leaf surfaces), growth of the pathogen and spread of disease can be rapid and can cause heavy crop losses. A devastating epidemic of downy mildew of grapes caused by the oomycete Plasmopara viticola nearly destroyed the wine industry in France in the latter half of the 19th century and resulted in the discovery of the first widely used fungicide, Bordeaux mixture, in 1885. More recently, downy mildew epidemics caused by Sclerospora graminicola have resulted in severe losses in pearl millet, an important staple crop in India and West Africa. P. cubensis annually causes serious threats to cucurbit crops (e.g., melon, cucumber, squash, and luffa) grown around the world. Although not a "true" downy mildew, the highly destructive late blight of potato and tomato (the cause of the Irish potato famine in the 1840s) is similar to the downy mildews and is caused by another oomycete of the order Peronosporales (family Pythiaceae), Phytophthora infestans.
Yigal Cohen and colleagues previously identified a genotype of melon from India, PI 124111F (PI), that exhibits resistance to all known pathotypes of P. cubensis and determined that this resistance was dependent on two partially dominant complementary loci, Pc1 and Pc2 (Cohen and Eyal, 1987 ; Thomas et al., 1988). Resistance in PI is associated with the induction of a hypersensitive response, leading to the deposition of callose along the inner surface of host cell walls, the encasement of oomycete haustoria within callose-like deposits, and massive lignification of host cell walls (Cohen et al., 1989). Balass et al. (1992) subsequently found that the resistant PI line contains a 45-kD protein (P45) that is not present in two susceptible melon lines, and hybrid progeny of a cross between PI and the susceptible cv Hemed displayed partial resistance and showed intermediate expression of P45. Taler et al. conducted partial sequencing of P45 and cloned two genes from PI corresponding to the sequenced peptides that encode glyoxylate aminotransferases named At1 and At2. Transformation of a susceptible C. melo cultivar with At1 or At2 and assessment of aminotransferase activity in leaf tissue confirmed that the presence and activity of either protein was strongly associated with resistance to P. cubensis (Figure 1).
At1 and At2 are highly similar to a Ser-glyoxylate aminotransferase (SGT) from Fritilaria agrestis and to Arabidopsis Ala-glyoxylate aminotransferase (AGT1). It has been shown that Arabidopsis AGT1 primarily catalyzes SGT transamination (Liepman and Olsen, 2001
Interestingly, Song et al. (2004)
Upstream of SGT/AGT activity in the photorespiration pathway, glycolate oxidase catalyzes the oxidation of glycolic acid to produce glyoxylate and H2O2. Taler et al. also found resistance to be correlated with higher levels of glycolate oxidase activity in leaf extracts, leading to the conclusion that there is a significantly greater overall flux through this pathway in resistant compared with susceptible melon. The authors speculated that H2O2 produced via these reactions may play an important signaling role in the induction of the hypersensitive response that ultimately brings about resistance to P. cubensis in the PI melon. This idea is consistent with the opinion of Corpas et al. (2001) that reactive oxygen species and nitric oxide signal molecules generated in peroxisomes may play important roles in plant responses to both abiotic and biotic stresses.
The peroxisome is the site of many oxidative reactions, including those associated with photorespiration, fatty acid
Taler et al. found that overexpression of At1 or At2 in line BU21/3, which is susceptible to both P. cubensis and powdery mildew caused by the ascomycete Sphaerotheca fuliginea, resulted in resistance only to P. cubensis. Therefore, aminotransferase activity has some specificity against downy mildew in C. melo and evidently does not contribute to S. fuliginea resistance in the PI line, which is dependent on the powdery mildew resistance genes Pm3 and Pm6 (which are not functional in line BU21/3). P. cubensis causes disease only in the Cucurbitaceae, but other oomycetes that cause downy mildew in other plant families have similar modes of infection, fungal development, and reproduction. It will be of considerable interest to test the ability of glyoxylate aminotransferases to confer resistance against downy mildew in other plant species. In particular, what is the genomic status and potential role in disease resistance of genes that encode these enzymes in other Cucurbitaceae genera and in other agronomically important species? Does the single gene that encodes peroxisomal glyoxylate aminotransferase in Arabidopsis (AGT1) perform any function in disease resistance in this species? Other questions include whether aminotransferase-dependent resistance also is dependent on known disease resistance signaling pathways involving salicylic acid, jasmonic acid, or ethylene. The work of Taler et al. thus opens new avenues of investigation with important implications for understanding and engineering plant disease resistance.
Balass, M., Cohen, Y., and Bar-Joseph, M. (1992). Identification of a constitutive 45 kD soluble protein associated with resistance to downy mildew in muskmelon (Cucumis melo L.) line PI 124111F. Physiol. Mol. Plant Pathol. 41, 387–396. Cohen, Y., and Eyal, H. (1987). Downy mildew-, powdery mildew- and fusarium wilt-resistant muskmelon breeding line PI-124111F. Phytoparasitica 15, 187–195. Cohen, Y., Eyal, H., Hanania, J., and Malik, Z. (1989). Ultrastructure of Pseudoperonospora cubensis in muskmelon genotype susceptible and resistant to downy mildew. Physiol. Mol. Plant Pathol. 34, 27–40. Corpas, F.J., Barroso, J.B., and del Rio, L.A. (2001). Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci. 6, 145–150.[CrossRef][Web of Science][Medline] Dangl, J., and Jones, J.D.G. (2001). Plant pathogens and integrated defence responses to infection. Nature 411, 826–833.[CrossRef][Medline]
Eckardt, N.A. (2003). Viral defense and counter-defense: A role for adenosine kinase in innate defense and RNA silencing. Plant Cell 15, 2758–2761. Feys, B.J., and Parker, J.E. (2000). Interplay of signaling pathways in plant disease resistance. Trends Genet. 16, 449–455.[CrossRef][Web of Science][Medline]
Hao, L., Wang, H., Sunter, G., and Bisaro, D.M. (2003). Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase. Plant Cell 15, 1034–1048.
Kang, L., Li, J., Zhao, T., Xiao, F., Tang, X., Thilmony, R., He, S.Y., and Zhou, J.-M. (2003). Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc. Natl. Acad. Sci. USA 100, 3519–3524. Liepman, A.H., and Olsen, L.J. (2001). Peroxisomal alanine:glyoxylate aminotransferase (AGT1) is a photorespiratory enzyme with multiple substrates in Arabidopsis thaliana. Plant J. 25, 487–498.[CrossRef][Web of Science][Medline] Mahalingam, R., and Fedoroff, N. (2003). Stress response, cell death and signaling: The many faces of reactive oxygen species. Physiol. Plant. 119, 56–68.[CrossRef] Song, J.T., Lu, H., and Greenberg, J.T. (2004). Divergent roles in Arabidopsis development and defense of two homologous genes, AGD2 and ALD1, encoding novel aminotransferases. Plant Cell, in press.
Taler, D., Galperin, M., Benjamin, I., Cohen, Y., and Kenigsbuch, D. (2004). Plant enzymatic resistance (eR) genes encoding for photorespiratory enzymes confer resistance against disease. Plant Cell 16, 172–184. Thomas, C.E., Cohen, Y., McCreight, Y.D., Jourdion, E.L., and Cohen, S. (1988). Inheritance of resistance to downy mildew in Cucumis melo. Plant Dis. 72, 33–35.
Wang, H., Hao, L., Shung, C.-Y., Sunter, G., and Bisaro, D.M. (2003). Adenosine kinase is inactivated by geminivirus AL2 and L2 proteins. Plant Cell 15, 3020–3032. This article has been cited by other articles:
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ENZYMATIC RESISTANCE
DOWNY MILDEW DISEASE
-oxidation, the glyoxylate cycle, and the metabolism of ureides. Corpas et al. (2001)
