The E3 ubiquitin ligase activity of an insect anti-apoptotic gene (SfIAP) is required for plant stress tolerance

Physiological and Molecular Plant Pathology

Volumn 74, Issue 5-6, 2010, Pages 351-362

  Kabbage, Mehdi ^a,b   Li, Wei ^c   Chen, Shaorong ^a,b   Dickman, Martin B ^a,b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b Department of Plant Pathology and Microbiology ^*  (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Disease tolerance; E3 ligase; Inhibitor of apoptosis

Indexed keywords

ALTERNARIA ALTERNATA; HEXAPODA; LYCOPERSICON ESCULENTUM;

EID: 77956433774     PISSN: 08855765     EISSN: 10961178     Source Type: Journal    
DOI: 10.1016/j.pmpp.2010.06.002     Document Type: Article

References (40)

1. Crook N.E., Clem R.J., Miller L.K. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J Virol 1993, 67(4):2168-2174.
2. Birnbaum M.J., Clem R.J., Miller L.K. An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J Virol 1994, 68(4):2521-2528.
3. Deveraux Q.L., Reed J.C. IAP family proteins-suppressors of apoptosis. Genes Dev 1999, 13(3):239-252.
4. Richter B.W., Duckett C.S. The IAP proteins: caspase inhibitors and beyond. Sci STKE 2000, 2000(44). PE1.
5. Yang Y.L., Li X.M. The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell Res 2000, 10(3):169-177.
6. Verhagen A.M., Coulson E.J., Vaux D.L. Inhibitor of apoptosis proteins and their relatives: IAPs and other BIRPs. Genome Biol 2001, 2(7). REVIEWS3009.
7. Yang Y., Fang S., Jensen J.P., Weissman A.M., Ashwell J.D. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 2000, 288(5467):874-877.
8. Stone S.L., Hauksdottir H., Troy A., Herschleb J., Kraft E., Callis J. Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 2005, 137(1):13-30.
9. Freemont P.S. Ring for destruction?. Curr Biol 2000, 10:R84-R87.
10. Smalle J., Vierstra R.D. The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 2004, 55:555-590.
11. Wilkinson K.D. Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. Semin Cell Dev Biol 2000, 11:141-148.
12. MacFarlane M., Merrison W., Bratton S.B., Cohen G.M. Proteasome-mediated degradation of Smac during apoptosis: XIAP promotes Smac ubiquitination in vitro. J Biol Chem 2002, 277(39):36611-36616.
13. Green M.C., Monser K.P., Clem R.J. Ubiquitin protein ligase activity of the anti-apoptotic baculovirus protein Op-IAP3. Virus Res 2004, 105(1):89-96.
14. Yang Q.H., Du C. Smac/DIABLO selectively reduces the levels of c-IAP1 and c-IAP2 but not that of XIAP and livin in HeLa cells. J Biol Chem 2004, 279(17):16963-16970.
15. Mazzucotelli E., Belloni, Marone D., De Leonardis A., Guerra D., Di Fonzo N. The E3 ubiquitin ligase gene family in plants: regulation by degradation. Curr Genomics 2006, 7(8):509-522.
16. Huang H., Joazeiro C.A., Bonfoco E., Kamada S., Leverson J.D., Hunter T. The inhibitor of apoptosis, cIAP2, functions as a ubiquitin-protein ligase and promotes in vitro monoubiquitination of caspases 3 and 7. J Biol Chem 2000, 275:26661-26664.
17. Li W., Kabbage M., Dickman M.B. Transgenic expression of an insect inhibitor of apoptosis gene, Sf-IAP, confers abiotic and biotic stress tolerance and delays tomato fruit ripening. Physiological and Molecular Plant Pathology 2010, 74(5-6):363-375.
18. Myung J., Kim K.B., Crews C.M. The ubiquitin-proteasome pathway and proteasome inhibitors. Med Res Rev 2001, 21(4):245-273.
19. Guo H., Ecker J.R. Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 2003, 115(6):667-677.
20. Khedr A.H., Abbas M.A., Abdel Wahid A.A., Quick W.P., Abogadallah G.M. Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. J Exp Bot 2003, 54(392):2553-2562.
21. Higashi K., Takasawa R., Yoshimori A., Goh T., Tanuma S., Kuchitsu K. Identification of a novel gene family, paralogs of inhibitor of apoptosis proteins present in plants, fungi, and animals. Apoptosis 2005, 10(3):471-480.
22. Dreher K., Callis J. Ubiquitin, hormones and biotic stress in plants. Ann Bot 2007, 99:787-822.
23. Austin M.J., Muskett P., Kahn K., Feys B.J., Jones J.D., Parker J.E. Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 2002, 295(5562):2077-2080.
24. Azevedo C., Sadanandom A., Kitagawa K., Freialdenhoven A., Shirasu K., Schulze-Lefert P. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 2002, 295(5562):2073-2076.
25. Dong C.H., Agarwal M., Zhang Y., Xie Q., Zhu J.K. The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci U S A 2006, 103:8281-8286.
26. Gonzalez-Lamothe R., Tsitsigiannis D.I., Ludwig A.A., Panicot M., Shirasu K., Jones J.D. The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell 2006, 18:1067-1083.
27. Liu Y., Schiff M., Serino G., Deng X.W., Dinesh-Kumar S.P. Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to tobacco mosaic virus. Plant Cell 2002, 14(7):1483-1496.
28. Liu Y., Burch-Smith T., Schiff M., Feng S., Dinesh-Kumar S.P. Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J Biol Chem 2004, 279(3):2101-2108.
29. Hubert D.A., Tornero P., Belkhadir Y., Krishna P., Takahashi A., Shirasu K., Dangl J.L. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. Embo J 2003, 22(21):5679-5689.
30. Holt B.F., Belkhadir Y., Dangl J.L. Antagonistic control of disease resistance protein stability in the plant immune system. Science 2005, 309(5736):929-932.
31. Takahashi A., Casais C., Ichimura K., Shirasu K. HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci U S A 2003, 100(20):11777-11782.
32. Lahaye T., Shirasu K., Schulze-Lefert P. Chromosome landing at the barley Rar1 locus. Mol Gen Genet 1998, 260(1):92-101.
33. Doukhanina E.V., Chen S., Van der Zalm E., Godzik A., Reed J., Dickman M.B. Identification and functional Characterization of the BAG protein family in Arabidopsis thaliana. J Biol Chem 2006, 281(27):18793-18801.
34. Kabbage M., Dickman M.B. The BAG proteins: a ubiquitous family of chaperone regulators. Cell Mol Life Sci 2008, 65(9):1390-1402.
35. Williams B, Kabbage M, Britt R, Dickman MB. AtBAG7, an Arabidopsis Bcl2-associated athanogene resides in the endoplasmic reticulum and is involved in the unfolded protein response. Proc Natl Acad Sci U S A, 2010;107(13):6088-93.
36. Takken F.L., Luderer R., Gabriëls S.H., Westerink N., Lu R., de Wit P.J., Joosten M.H. A functional cloning strategy, based on a binary PVX-expression vector, to isolate HR-inducing cDNAs of plant pathogens. Plant J 2000, 24(2):275-283.
37. Chen S., Vaghchhipawala Z., Li W., Asard H., Dickman M.B. Tomato phospholipid hydroperoxide glutathione peroxidase inhibits cell death induced by Bax and oxidative stresses in yeast and plants. Plant Physiol 2004, 135(3):1630-1641.
38. Fu D.Q., Zhu B.Z., Zhu H.L., Jiang W.B., Luo Y.B. "Virus-induced gene silencing in tomato fruit." Plant J 2005, 43(2):299-308.
39. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162(1):156-159.
40. Reuber T.L., Ausubel F.M. Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell 1996, 8:241-249.