Linked, if not the same, Mi-1 homologues confer resistance to tomato powdery mildew and root-knot nematodes

Molecular Plant-Microbe Interactions

Volumn 24, Issue 4, 2011, Pages 441-450

  Seifi, Alireza ^a   Kaloshian, Isgouhi ^b   Vossen, Jack ^a   Che, Daidi ^c   Bhattarai, Kishor K ^b   Fan, Junmei ^a   Naher, Zabun ^a   Goverse, Aska ^a   Tjallingii, W Freddy ^a   Lindhout, Pim ^a   Visser, Richard G F ^a,d   Bai, Yuling ^a,d  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^d Netherlands Organization for Scientific Research   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MI 1 PROTEIN, LYCOPERSICON ESCULENTUM; MI-1 PROTEIN, LYCOPERSICON ESCULENTUM; VEGETABLE PROTEIN;

ANIMAL; APHID; ARTICLE; ASCOMYCETES; CHROMOSOME MAP; CLADOSPORIUM; GENETIC LINKAGE; GENETICS; HOST PARASITE INTERACTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; MICROBIOLOGY; MOLECULAR GENETICS; MULTIGENE FAMILY; NEMATODE; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT CHROMOSOME; PLANT DISEASE; PLANT GENE; PLANT IMMUNITY; TOMATO;

ANIMALS; APHIDS; ASCOMYCOTA; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; CLADOSPORIUM; GENES, PLANT; GENETIC LINKAGE; HOST-PARASITE INTERACTIONS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NEMATODA; PLANT DISEASES; PLANT IMMUNITY; PLANT PROTEINS; TYLENCHOIDEA;

ALEYRODIDAE; APHIDIDAE; ERYSIPHALES; LYCOPERSICON ESCULENTUM; MELOIDOGYNE; MELOIDOGYNE JAVANICA; NEMATODA; SOLANUM;

EID: 79952594667     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-06-10-0145     Document Type: Article

References (43)

1. Ammiraju, J., Veremis, J., Huang, X., Roberts, P., and Kaloshian, I. 2003. The heat-stable root-knot nematode resistance gene Mi-9 from Lyc-opersicon peruvianum is localized on the short arm of chromosome 6. Theor. Appl. Genet. 106:478-484. (Pubitemid 36599861)
2. Bai, Y., van der Hulst, R., Bonnema, G., Marcel, T., Meijer-Dekens, F., Niks, R., and Lindhout, P. 2005. Tomato defense to Oidium neolycoper-sici: Dominant Ol genes confer isolate-dependent resistance via a different mechanism than recessive ol-2. Mol. Plant-Microbe Interact. 18:354-362. (Pubitemid 40383903)
3. Bisgrove, S., Simonich, M., Smith, N., Sattler, A., and Innes, R. 1994. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6:927.
4. Dangl, J. L. and Jones J. D. G. 2001. Plant pathogens and integrated defence responses to infection. Nature 411:826-833. (Pubitemid 32588110)
5. De Ilarduya, O., Xie, Q., and Kaloshian, I. 2003. Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol. Plant-Microbe Interact. 16:699-708. (Pubitemid 36914672)
6. Dickinson, M. J., Jones, D. A., and Jones, J. D. G. 1993. Close linkage between the Cf-2/Cf-5 and Mi resistance loci in tomato. Mol. Plant-Microbe Interact. 6:341-347.
7. Dixon, M., Hatzixanthis, K., Jones, D., Harrison, K., and Jones, J. 1998. The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10:1915.
8. Dixon, M. S., Jones, D. A., Keddie, J. S., Thomas, C. M., Harrison, K., and Jones, J. D. G. 1996. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451-459. (Pubitemid 26058570)
9. Dropkin, V., Helgeson, J., and Upper, C. 1969. The hypersensitivity reaction of tomatoes resistant to Meloidogyne incognita: Reversal by cyto-kinins. J. Nematol. 1:55.
10. Ellis, J., Lawrence, G., Luck, J., and Dodds, P. 1999. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11:495.
11. Glazebrook, J. 2005. Contrasting mechanisms of defense against biotro-phic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205-227. (Pubitemid 41318871)
12. Ho, J. Y., Weide, R., Ma, H. M., Vanwordragen, M. F., Lambert, K. N., Koornneef, M., Zabel, P., and Williamson, V. M. 1992. The root-knot nematode resistance gene (Mi) in tomato-construction of a molecular linkage map and identification of dominant cDNA markers in resistant genotypes. Plant J. 2:971-982.
13. Jablonska, B., Ammiraju, J. S. S., Bhattarai, K. K., Mantelin, S., de Ilarduya, O. M., Roberts, P. A., and Kaloshian, I. 2007. The Mi-9 gene from Solanum arcanum conferring heat-stable resistance to root-knot nematodes is a homolog of Mi-1. Plant Physiol. 143:1044-1054. (Pubitemid 46940982)
14. Kaloshian, I., Yaghoobi, J., Liharska, T., Hontelez, J., Hanson, D., Hogan, P., Jesse, T., Wijbrandi, J., Simons, G., Vos, P., Zabel, P., and Williamson, V. M. 1998. Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato. Mol. Gen. Genet. 257:376-385.
15. Kaloshian, I., Kinsey, M. G., Williamson, V. M., and Ullman, D. E. 2000. Mi-mediated resistance against the potato aphid Macrosiphum euphor-biae (Hemiptera: Aphididae) limits sieve element ingestion. Environ. Entomol. 29:690-695.
16. Kim, Y., Lin, N., and Martin, G. 2002. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589-598. (Pubitemid 34628722)
17. Li, C., Bonnema, G., Che, D., Dong, L., Lindhout, P., Visser, R., and Bai, Y. 2007. Biochemical and molecular mechanisms involved in monogenic resistance responses to tomato powdery mildew. Mol. Plant-Microbe Interact. 20:1161-1172. (Pubitemid 47281782)
18. Li, Q., Xie, Q., Smith-Becker, J., Navarre, D., and Kaloshian, I. 2006. Mi-1-mediated aphid resistance involves salicylic acid and mitogen-acti-vated protein kinase signaling cascades. Mol. Plant-Microbe Interact. 19:655-664. (Pubitemid 43787730)
19. Lindhout, P., Pet, G., and Beek, H. 1993. Screening wild Lycopersicon species for resistance to powdery mildew (Oidium lycopersicum). Euphytica 72:43-49. (Pubitemid 2077792)
20. Livak, K., and Schmittgen, T. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-[delta][delta] CT method. Methods 25:402-408. (Pubitemid 34164012)
21. Michelmore, R., and Meyers, B. 1998. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8:1113.
22. Milligan, S. B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P., and Williamson, V. M. 1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307-1319. (Pubitemid 28542166)
23. Narusaka, M., Shirasu, K., Noutoshi, Y., Kubo, Y., Shiraishi, T., Iwabuchi, M., and Narusaka, Y. 2009. RRS1 and RPS4 provide a dual resistance gene system against fungal and bacterial pathogens. Plant J. 60:218-226.
24. Nimchuk, Z., Eulgem, T., Holt, B. E., and Dangl, J. L. 2003. Recognition and response in the plant immune system. Annu. Rev. Genet. 37:579-609. (Pubitemid 38041438)
25. Nombela, G., Williamson, V. M., and Muniz, M. 2003. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol. Plant-Microbe Interact. 16:645-649. (Pubitemid 36755626)
26. Roberts, P., and Thomason, I. 1986. Variability in reproduction of isolates of Meloidogyne incognita and Meloidogyne javanica on resistant tomato genotypes. Plant Dis. 70:547-551.
27. Rossi, M., Goggin, F. L., Milligan, S. B., Kaloshian, I., Ullman, D. E., and Williamson, V. M. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. U. S. A. 95:9750-9754. (Pubitemid 28415241)
28. Saitou, N., and Nei, M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406.
29. Seah, S., Yaghoobi, J., Rossi, M., Gleason, C, and Williamson, V. 2004. The nematode-resistance gene, Mi-1, is associated with an inverted chromosomal segment in susceptible compared to resistant tomato. Theor. Appl. Genet. 108:1635-1642. (Pubitemid 38791272)
30. Seah, S., Telleen, A. C., and Williamson, V. M. 2007. Introgressed and endogenous Mi-1 gene clusters in tomato differ by complex rearrangements in flanking sequences and show sequence exchange and diversifying selection among homologues. Theor. Appl. Genet. 114:1289-1302. (Pubitemid 46697837)
31. Staskawicz, B. J., Ausubel, F. M., Baker, B. J., Ellis, J. G., and Jones, J. D. G. 1995. Molecular genetics of plant disease resistance. Science 268:661-667.
32. Tamura, K., Nei, M., and Kumar, S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. U. S. A. 101:11030.
33. Tamura, K., Dudley, J., Nei, M., and Kumar, S. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596.
34. Tjallingii, W 1988. Electrical recording of stylet penetration activities. Pages 95-107 in: Aphids, Their Biology, Natural Enemies and Control, Vol. B. A. K. Minks and P. Harrewijn, eds. Elsevier Science Publishers, Amsterdam.
35. van der Vossen, E. A. G., van der Voort, J., Kanyuka, K., Bendahmane, A., Sandbrink, H., Baulcombe, D. C., Bakker, J., Stiekema, W. J., and Klein-Lankhorst, R. M. 2000. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: A virus and a nematode. Plant J. 23:567-576.
36. Veremis, J., Van Heusden, A., and Roberts, P. 1999. Mapping a novel heat-stable resistance to Meloidogyne in Lycopersicon peruvianum. Theor. Appl. Genet. 98:274-280. (Pubitemid 29163229)
37. Vossen, E., Gros, J., Sikkema, A., Muskens, M., Wouters, D., Wolters, P., Pereira, A., and Allefs, S. 2005. The Rpi-blb2 gene from Solanum bul-bocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. Plant J. 44:208-222.
38. Wang, Y., Bao, Z., Zhu, Y, and Hua, J. 2009. Analysis of temperature modulation of plant defense against biotrophic microbes. Mol. Plant-Microbe Interact. 22:498-506.
39. Whitham, S., McCormick, S., and Baker, B. 1996. The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc. Natl. Acad. Sci. U. S. A. 93:8776.
40. Williamson, V. M., and Kumar, A. 2006. Nematode resistance in plants: The battle underground. Trends Genet. 22:396-403. (Pubitemid 44015970)
41. Yang, S., and Hua, J. 2004. A haplotype-specific resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabi-dopsis. Plant Cell 16:1060.
42. Zamir, D., Michelson, I., Zakay, Y., Navot, N., Zeidan, N., Sarfatti, M., Eshed, Y., Harel, E., Pleban, T., van-Oss, H., Kedar, N., Rabinowitch, H. D., and Czosnek, H. 1994. Mapping and introgression of a tomato yellow leaf curl virus tolerance gene, Ty-1. Theor. Appl. Genet. 88:141-146. (Pubitemid 2109094)
43. Zhang, L., Khan, A., Nino-Liu, D., and Foolad, M. 2002. A molecular linkage map of tomato displaying chromosomal locations of resistance gene analogs based on a Lycopersicon esculentum × Lycopersicon hirsutum cross. Genome 45:133-146. (Pubitemid 34190681)