Biologia plantarum 62:569-578, 2018 | DOI: 10.1007/s10535-018-0787-2

Expression and characteristics of rice xylanase inhibitor OsXIP, a member of a new class of antifungal proteins

R.-J. Sun1, Y. Xu2, C.-X. Hou3, Y.-H. Zhan2, M.-Q. Liu4, X.-Y. Weng2,*
1 College of Animal Science, Zhejiang University, Hangzhou, P.R. China
2 College of Life Science, Zhejiang University, Hangzhou, P.R. China
3 The Institute of Rural Development and Information Institute, Zhejiang Academy of Agricultural Sciences, Hangzhou, P.R. China
4 College of Life Science, China JiLiang University, Hangzhou, P.R. China

It has been hypothesized that xylanase inhibitors play important roles in plant defense against microbial pathogens. Currently, there is little information available about xylanase inhibitor OsXIP in rice and its gene expression. We cloned a xylanase inhibitor gene OsXIP from rice (Oryza sativa L. cv. Nipponbare) genomic DNA. To determine the function of OsXIP, we generated OsXIP-overexpressing transgenic rice plants. The transgenic plants had significantly higher OsXIP expression and showed enhanced defense response to Magnaporthe oryzae compared to the wild-type plants. The results also showed that the increased OsXIP expression was accompanied by the up-regulation of pathogenesisrelated genes. To clarify the OsXIP expression pattern, a ProOsXIP::GUS vector was constructed and transgenic plants were obtained. GUS staining results revealed that OsXIP showed organ-specific expressions in rice plants. OsXIP was primarily expressed in the roots and in the veins, but it was weakly expressed in the leaves. Analyses of the OsXIP expression in response to biotic and abiotic stresses indicated that it was drastically induced by biotic stresses and methyl jasmonate treatment. OsXIP, a member of a new class of antifungal proteins, may function as a barrier that prevents the cell wall degradation by xylanases excreted by fungal pathogens. The OsXIP was found to be a stressresponsive gene and it could take part in plant defense via a JA-mediated signaling pathway.

Keywords: biotic stress; gene expression; Magnaporthe oryzae; methyl jasmonate; Oryza sativa
Subjects: antifungal proteins; xylanase; gene expression; subcellular localization; methyl jasmonate; transgenic plants; rice

Received: February 27, 2017; Revised: November 4, 2017; Accepted: November 10, 2017; Published: September 1, 2018Show citation

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Sun, R.-J., Xu, Y., Hou, C.-X., Zhan, Y.-H., Liu, M.-Q., & Weng, X.-Y. (2018). Expression and characteristics of rice xylanase inhibitor OsXIP, a member of a new class of antifungal proteins. Biologia plantarum, 62(3), 569-578. doi: 10.1007/s10535-018-0787-2.
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    References

    1. Bellincampi, D., Cervone. F., Lionetti, V.: Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. - Front. Plant Sci. 5: 228, 2014. Go to original source...
    2. Beliën, T., Van Campenhout, S., Van Acker, M., Robben, J., Courtin, C.M., Delcour, J.A., Volckaert, G.: Mutational analysis of endoxylanases XylA and XylB from the phytopathogen Fusarium graminearum reveals comprehensive insights into their inhibitor insensitivity. - Appl. environ. Microbiol. 73: 4602-4608, 2007.
    3. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
    4. Chen, X.W., Shang, J.J., Chen, D.X., Lei, C.L., Zou, Y., Zhai, W.X., Liu, G.Z., Xu, J.C., Ling, Z.Z., Cao, G., Ma, B.T., Wang, Y.P., Zhao, X.F., Li, S.G., Zhu, L.H.: A B-lectin receptor kinase gene conferring rice blast resistance. - Plant J. 46: 794-804, 2006. Go to original source...
    5. Croes, E., Gebruers, K., Luyten, N., Delcour, J.A., Courtin, C M.: The three classes of wheat xylanase inhibiting proteins accumulate in an analogous way during wheat ear development and germination. - J. Plant Physiol. 166: 1253-1262, 2009.
    6. Debyser, W., Peumans, W.J., Van Damme, E.J.M., Delcour, J.A.: Triticum aestivum xylanase inhibitor (TAXI), a new class of enzyme inhibitor affecting breadmaking performance. - J. Cereal Sci. 30: 39-43, 1999. Go to original source...
    7. Dornez, E., Croes E., Gebruers, K., De Coninck, B., Cammue, B.P.A., Delcour, J.A., Courtin, C.M.: Accumulated evidence substantiates a role for three classes of wheat xylanase inhibitors in plant defense. - Crit. Rev. Plant Sci. 29: 244-264, 2010.
    8. Elliott, G.O., McLauchlan, W.R., Williamson, G., Kroon, P.A.: A wheat xylanase inhibitor protein (XIP-I) accumulates in the grain and has homologues in other cereals. - J. Cereal Sci. 37: 187-194, 2003. Go to original source...
    9. Flatman, R., McLauchlan, W.R., Juge, N., Furniss, C., Berrin, J.G., Hughes, R.K., Manzanares, P., Ladbury, J.E., O'Brien, R., Williamson, G.: Interactions defining the specificity between fungal xylanases and the xylanase-inhibiting protein XIP-I from wheat. - Biochem. J. 365: 773-781, 2002. Go to original source...
    10. Fierens, E., Rombouts S., Gebruers, K., Goesaert, H., Brijs, K., Beaugrand, J., Volckaert, G., Van Campenhout, S., Proost, P., Courtin, C.M., Delcour, J.A.: TLXI, a novel type of xylanase inhibitor from wheat (Triticum aestivum) belonging to the thaumatin family. - Biochem. J. 403: 583-591, 2007.
    11. Fierens, K., Brijs, K., Courtin, C.M., Gebruers, K., Goesaert, H., Raedschelders, G., Robben, J., Van Campenhout, S., Volckaert, G., Delcour, J.A.: Molecular identification of wheat endoxylanase inhibitor TAXI-I, member of a new class of plant proteins. - FEBS Lett. 540: 259-263, 2003.
    12. Goesaert, H., Elliott, G., Kroon, P.A., Gebruers, K., Courtin, C.M., Robben, J., Delcour, J.A., Juge, N.: Occurrence of proteinaceous endoxylanase inhibitors in cereals. - Biochim. biophys. Acta 1696: 193-202, 2004.
    13. Hiei, Y., Ohta S., Komari, T., Kumashiro, T.: Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. - Plant J. 6: 271-282, 1994. Go to original source...
    14. Hou, C.X., Lv, T., Zhan, Y.H., Peng, Y.Y., Huang, Y.Y., Jiang, D.A., Weng, X.Y.: Overexpression of the RIXI xylanase inhibitor improves disease resistance to the fungal pathogen, Magnaporthe oryzae, in rice. - Plant Cell Tissue Organ Cult. 120: 167-177, 2015. Go to original source...
    15. Igawa, T., Ochiai-Fukuda, T., Takahashi-Ando, N., Ohsato, S., Shibata, T., Yamaguchi, I., Kimura, M.: New TAXI-type xylanase inhibitor genes are inducible by pathogens and wounding in hexaploid wheat. - Plant Cell Physiol. 45: 1347-1360, 2004. Go to original source...
    16. Jefferson, R.A., Kavanagh, T.A., Bevan, M.W.: GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. - EMBO J. 6: 3901-3907, 1987. Go to original source...
    17. Kunkel, B.N., Brooks, D.M.: Cross talk between signaling pathways in pathogen defense. - Curr. Opin. Plant Biol. 5: 325-331, 2002. Go to original source...
    18. Lee, M.W., Qi, M., Yang, Y.O.: A novel jasmonic acidinducible rice myb gene associates with fungal infection and host cell death. - Mol. Plant Microbe Interact. 14: 527-535, 2001. Go to original source...
    19. McLauchlan, W.R., Garcia, C.M.T., Roza, M., Ravestein, P., Maat, J.: A novel class of protein from wheat which inhibits xylanases. - Biochem. J. 338: 441-446, 1999. Go to original source...
    20. Miller, G.L., Blum, R., Glennom, W.E., Burton, A.L.: Measurement of methods for assay of xylanase activity. - Anal. Biochem. 2: 127-132, 1959.
    21. Misas-Villamil, J.C., Van der Hoorn, R.A.: Enzyme-inhibitor interactions at the plant-pathogen interface. - Curr. Opin. Plant Biol. 11: 380-388, 2008. Go to original source...
    22. Moscetti, I., Faoro, F., Moro, S., Sabbadin, D., Sella, L., Favaron, F., D'Ovidio, R.: The xylanase inhibitor TAXI-III counteracts the necrotic activity of a Fusarium graminearum xylanase in vitro and in durum wheat transgenic plants. - Mol. Plant Pathol. 16: 583-592, 2015. Go to original source...
    23. Moscetti, I., Tundo, S., Janni, M., Sella, L., Gazzetti, K., Tauzin, A., Giardina, T., Masci, S., Favaron, F., D'Ovidio, R.: Constitutive expression of the xylanase inhibitor TAXIIII delays Fusarium head blight symptoms in durum wheat transgenic plants. - Mol. Plant Microbe Interact. 26: 1464-1472, 2013. Go to original source...
    24. Peng, L., Jack, H.W., Tzi, B.N., Vincent, S.M.H., Li, X.X.: A sorghum xylanase inhibitor-like protein with highly potent antifungal, antitumor and HIV-1 reverse transcriptase inhibitory activities. - Food Chem. 141: 2916-2922, 2013.
    25. Pieterse, C.M., Van der Does, D., Zamioudis, C., Leon-Reyes, A., Van Wees, S.C.: Hormonal modulation of plant immunity. - Annu. Rev. Cell Dev. Biol. 28: 489-521, 2012. Go to original source...
    26. Takahashi-Ando, N., Inaba, M., Ohsato, S., Igawa, T., Usami, R., Kimura, M.: Identification of multiple highly similar XIP-type xylanase inhibitor genes in hexaploid wheat. - Biochem. biophys. Res. Commun. 360: 880-884, 2007. Go to original source...
    27. Tokunaga, T., Esaka, M.: Induction of a novel XIP-type xylanase inhibitor by external ascorbic acid treatment and differential expression of XIP-family genes in rice. - Plant Cell Physiol. 48: 700-714, 2007. Go to original source...
    28. Tokunaga, T., Miyata, Y., Fujikawa, Y., Esaka, M.: RNAimediated knockdown of the XIP-type endoxylanase inhibitor gene, OsXIP, has no effect on grain development and germination in rice. - Plant Cell Physiol. 49: 1122-1127, 2008. Go to original source...
    29. Tundo, S., Kalunke, R M., Janni, M., Volpi, C., Lionetti, V., Bellincampi, D., Favaron, F., D'Ovidio, R.: Pyramiding PvPGIP2 and TAXI-III but not PvPGIP2 and PMEI enhances wheat resistance against Fusarium graminearum. - Mol. Plant Microbe Interact. 29: 629-639, 2016. Go to original source...
    30. Tundo, S., Moscetti, I., Faoro, F., Lafond, M., Giardina, T., Favaron, F., Sella, L., D'Ovidio, R.: Fusarium graminearum produces different xylanases causing host cell death that is prevented by the xylanase inhibitors XIP-I and TAXI-III in wheat. - Plant Sci. 240: 161-169, 2015. Go to original source...
    31. Turner, J.G., Ellis, C., Devoto, A.: The jasmonate signal pathway. - Plant Cell 14: S153-S164, 2002. Go to original source...
    32. Vasconcelos, E.A.R., Santana, C.G., Godoy, C.V., Seixas, C.D.S., Silva, M.S., Moreira, L.R.S., Neto, O.B.O., Price, D., Fitches, E., Filho, E.X.F., Mehta, A., Gatehouse, J.A., Grossi-de-Sa, M.F.: A new chitinase-like xylanase inhibitor protein (XIP) from coffee (Coffea arabica) affects Soybean Asian rust (Phakopsora pachyrhizi) spore germination. - BMC Biotechnol. 11: 14, 2011. Go to original source...
    33. Wang, C., Ying, S., Huang, H., Li, K., Wu, P., Shou, H.: Involvement of OsSPX1 in phosphate homeostasis in rice. - Plant J. 57: 895-904, 2009. Go to original source...
    34. Weng, X.Y., Huang, Y.Y., Hou, C.X., Jiang, D.A.: Effects of an exogenous xylanase gene expression on the growth of transgenic rice and the expression level of endogenous xylanase inhibitor gene RIXI. - J. Sci. Food Agr. 93: 173-179, 2013. Go to original source...
    35. Wroblewski, T., Tomczak, A., Michelmore, R.: Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. - Plant Biotechnol. J. 3: 259-273, 2005. Go to original source...
    36. Zhou, G., Qi, J., Ren, N., Cheng, J., Erb, M., Mao, B., Lou, Y.: Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. - Plant J. 60: 638-648, 2009. Go to original source...

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