Home Life Sciences Distinct expression patterns of the GDP dissociation inhibitor protein gene (OsRhoGDI2) from Oryza sativa during development and abiotic stresses
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Distinct expression patterns of the GDP dissociation inhibitor protein gene (OsRhoGDI2) from Oryza sativa during development and abiotic stresses

  • Jun-jun Huang , Jing Zhang , Yu-fan Hao , Xin-tian Yan , Jia Shi , Gao-hua Wang , Jing-yao Du , Hui-wen Ge , Hua-hua Wang and Wei-hong Liang EMAIL logo
Published/Copyright: December 23, 2016
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Biologia
From the journal Biologia Volume 71 Issue 11

Abstract

Guanine nucleotide dissociation inhibitor (GDI) plays an essential role in regulating the forms of Rac/Rop between GDP-bound inactivity and GTP-bound activity in plants. In this paper, we reported a stress-responsive GDI gene (OsRhoGDI2) from rice (Oryza sativa L.). We analyzed the transcript levels of OsRhoGDI2 gene in various tissues, organs, and developmental stages to obtain information about its function. We further researched the expression patterns of OsRhoGDI2 gene in response to abiotic stress signals. qRT-PCR demonstrated that OsRhoGDI2 was distinctly expressed in various plant tissues and organs at different levels. The expression of OsRhoGDI2 was also highly salty and drought inducible, it also moderately responded to Methyl Jasmonate (MeJA), abscisic acid (ABA), and Indole-3-acetic Acid (IAA), treatment but was only slightly affected by 6-Benzylaminopurine (6-BA) and salicylic acid (SA) treatments. Nevertheless, reduced expression conferred hypersensitivity to gibberellin (GA) stress in rice. The promoter of OsRhoGDI2 gene was used to drive β-glucuronidase (GUS) gene expression. Results of GUS histochemical staining showed the tissue-specific expression patterns of OsRhoGDI2, and GUS gene expression in two-week-old transgenic rice seedling exhibited relatively similar patterns under different stresses of the transgenic rice lines. These results provided insights into the characteristics and roles of the OsRhoGDI2 gene during development and strongly suggested that OsRhoGDI2 may play direct or indirect roles in the tolerance to different stresses in rice and may serve as a basis for further functional studies.

Keywords: Oryza sativa; GUS; OsRhoGDI2; stress response; transgenic rice

Acknowledgements

This work was supported by the research grants from the National Science Foundation of China (31171182; U1204305; 31301252), Program for Innovative Research Team in Science and Technology in University of Henan Province (13IRTSTHN009; 15IRTSTHN020) and the Doctor Initiative Foundation of Henan Normal University (Nos 11126, 11129).

References

Akamatsu A., Wong H., Fujiwara M., Okuda J., Nishide K., Uno K., Imai K., Umemura K., Kawasaki T., Kawano Y. & Shimamoto K. 2013. An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential component of chitin-induced rice immunity. Cell. Host. Microbe. 13:465–476.10.1016/j.chom.2013.03.007Search in Google Scholar PubMed

Bloch D. & Yalovsky S. 2013. Cell polarity signaling. Curr. Opin. Plant. Biol. 16: 734–742.10.1016/j.pbi.2013.10.009Search in Google Scholar PubMed

Carol R.J., Takeda S., Linstead P., Durrant M.C., Kakesova H., Derbyshire P., Drea S., Zarsky V. & Dolan L. 2005. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438: 1013–1016.10.1038/nature04198Search in Google Scholar PubMed

Chen L., Hamada S., Fujiwara M., Zhu T., Thao N.P., Wong H.L., Krishna P., Ueda T., Kaku H., Shibuya N., Kawasaki T. & Shimamoto K. 2010a. The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell. Host. Microbe. 7: 185–196.10.1016/j.chom.2010.02.008Search in Google Scholar PubMed

Chen L., Shiotani K., Togashi T., Miki D., Aoyama M., Wong H.L., Kawasaki T. & Shimamoto K. 2010b. Analysis of the Rac/Rop Small GTPase Family in Rice: expression, subcellular localization and role in disease resistance. Plant Cell Physiol. 51: 585-595.Search in Google Scholar

Chen X., Naramoto S., Robert S., Tejos R., Löfke C., Lin D., Yang Z. & Friml J. 2012. ABP1 and ROP6 GTPase signaling regulate clathrinmediated endocytosis in Arabidopsis roots. Curr. Biol. 22: 1326–1332.10.1016/j.cub.2012.05.020Search in Google Scholar PubMed

Dormann P., Kim H., Ott T., Schulze-Lefert P., Trujillo M., Wewer V. & Huckelhoven R. 2014. Cell-autonomous defense, re-organization and trafficking of membranes in plant – microbe interactions. New Phytol. 204: 815–822.10.1111/nph.12978Search in Google Scholar PubMed

Fior S. & Gerola P.D. 2009. Impact of ubiquitous inhibitors on the GUS gene reporter system: evidence from the model plantsArabidopsis, tobacco and rice and correction methods for quantitative assays of transgenic and endogenous GUS. Plant Methods 5: 314–321.Search in Google Scholar

Heo J.B., Yi Y.B. & Bahk J.D. 2011. Rice GDP dissociation inhibitor 3 inhibits OsMAPK2 activity through physical interaction. Biochem. Biophys. Res. Commun. 414: 814–819.10.1016/j.bbrc.2011.10.018Search in Google Scholar PubMed

Hoefle C., Huesmann C., Schultheiss H., Bornke F., Hensel G., Kumlehn J. & Hückelhoven R. 2011. A barley ROP GTPase activating protein associates with microtubules and regulates entry of the barley powdery mildew fungus into leaf epidermal cells. Plant Cell 23: 2422–2439.10.1105/tpc.110.082131Search in Google Scholar PubMed PubMed Central

Hofgen R. & Willmitzer L. 1988. Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res. 16: 9877.10.1093/nar/16.20.9877Search in Google Scholar PubMed PubMed Central

Hwang J.U., Vernoud V., Szumlanski A., Nielsen E. & Yang Z. 2008. A tip localized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Curr. Biol. 18: 1907–1916.10.1016/j.cub.2008.11.057Search in Google Scholar PubMed PubMed Central

Hwang J.U., Wu G., Yan A., Lee Y.J., Grierson C.S. & Yang Z.B. 2010. Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity. J. Cell. Sci. 123: 340–350.10.1242/jcs.039180Search in Google Scholar

Jones M.A., Shen J.J., Fu Y., Li H., Yang Z. & Grierson C.S. 2002. The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14: 763–776.10.1105/tpc.010359Search in Google Scholar

Jung Y.H., Agrawal G.K., Rakwal R., Kim J.A., Lee M.O., Choi P.G., Kim Y.J., Kim M.J., Shibato J., Kim S.H., Iwahashi H. & Jwa N.S. 2006. Functional characterization of OsRacB GTPase – a potentially negative regulator of basal disease resistance in rice. Plant Physiol. Biochem. 44: 68–77.10.1016/j.plaphy.2005.12.001Search in Google Scholar

Kawano Y., Kaneko-Kawano T. & Shimamoto K. 2014a. Rho family GTPase-dependent immunity in plants and animals. Front. Plant Sci. 5: 522–533.10.3389/fpls.2014.00522Search in Google Scholar

Kawano Y., Fujiwara T., Yao A., Housen Y., Hayashi K. & Shimamoto K. 2014b. Palmitoylation-dependent membrane localization of the rice R protein Pit is critical for the activation of the small GTPase OsRac1. J. Biol. Chem. 289: 19079–19088.10.1074/jbc.M114.569756Search in Google Scholar

Kawano Y. & Shimamoto K 2013. Early signaling network in rice PRR- and R-mediated immunity. Curr. Opin. Plant. Biol. 16: 496–504.10.1016/j.pbi.2013.07.004Search in Google Scholar

Kim S.H., Oikawa T., Kyozuka J., Wong H.L., Umemura K., Kishi-Kaboshi M., Takahashi A., Kawano Y., Kawasaki T. & Shimamoto K. 2012. The bHLH Rac immunity1 (RAI1) is activated by OsRac1 via OsMAPK3 and OsMAPK6 in rice immunity. Plant Cell Physiol. 53: 740–754.10.1093/pcp/pcs033Search in Google Scholar

Kieffer F., Elmayan T., Rubier S., Simon-Plas F., Dagher M.C. & Blein J.P. 2000. Cloning of Rac and Rho-GDI from tobacco using an heterologous two-hybrid screen. Biochimie 82: 1099–1105.10.1016/S0300-9084(00)01199-8Search in Google Scholar

Klahre U., Becker C., Schmitt A.C. & Kost B. 2006. Nt-RhoGDI2 regulates Rac/Rop signaling and polar cell growth in tobacco pollen tubes. Plant J. 46: 1018–1031.10.1111/j.1365-313X.2006.02757.xSearch in Google Scholar PubMed

Klahre U. & Kost B. 2006. Tobacco RhoGTPase activating protein1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes. Plant Cell 18: 3033–3046.10.1105/tpc.106.045336Search in Google Scholar PubMed PubMed Central

Lemichez E., Wu Y., Sanchez J.P., Mettouchi A., Mathur J. & Chua N.H. 2001. Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev. 15: 1808–1816.10.1101/gad.900401Search in Google Scholar PubMed PubMed Central

Lescot M., De’hais P., Thijs G., Marchal K., Moreau Y., Van de Peer Y., Rouz P. & Rombauts S. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30: 325–327.10.1093/nar/30.1.325Search in Google Scholar PubMed PubMed Central

Li H, Shen J.J., Zheng Z.L., Lin Y.K. & Yang Z.B. 2001. The Rop GTPase switch controls multiple developmental processes inArabidopsis. Plant Physiol. 126: 670–684.10.1104/pp.126.2.670Search in Google Scholar PubMed PubMed Central

Li Z., Kang J., Sui N. & Liu D. 2012. ROP11 GTPase is a negative regulator of multiple ABA responses in Arabidopsis. J. Integr. Plant Biol. 54: 169–179.10.1111/j.1744-7909.2012.01100.xSearch in Google Scholar PubMed

Liang W.H., Tang C.R. & Wu N.H. 2004. Isolation and characterization of two GDP dissociation inhibitor genes from Oryza sativa L. Chin. J. Biochem. Mol. Biol. 20: 785–791.Search in Google Scholar

Lieberherr D., Thao N.P., Nakashima A., Umemura K., Kawasaki T. & Shimamoto K. 2005. A sphingolipid elicitor-inducible mitogen-activated protein kinase is regulated by the small GTPase OsRac1 and heterotrimeric G-protein in rice. Plant Physiol. 138: 1644–1652.10.1104/pp.104.057414Search in Google Scholar PubMed PubMed Central

Lin D., Nagawa S., Chen J., Cao L., Chen X., Xu T., Li H., Dhonukshe P., Yamamuro C., Friml J., Scheres B., Fu Y. & Yang Z. 2012. A ROP GTPase-dependent auxin signaling pathway regulates the subcellular distribution of PIN2 in Arabidopsis roots. Curr. Biol. 22: 1319–1325.10.1016/j.cub.2012.05.019Search in Google Scholar PubMed PubMed Central

Livak K.J. & Schmittgen T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) method. Methods 25: 402–408.10.1006/meth.2001.1262Search in Google Scholar PubMed

Moller S.G. & Chua N.H. 1999. Interactions and intersections of plant signaling pathways. J. Mol. Biol. 293: 219–234.10.1006/jmbi.1999.2992Search in Google Scholar PubMed

Mucha E., Fricke I., Schaefer A., Wittinghofer A. & Berken A. 2011. Rho proteins of plants Functional cycle and regulation of cytoskeletal dynamics. Eur. J. Cell. Biol. 90: 934–943.10.1016/j.ejcb.2010.11.009Search in Google Scholar PubMed

Nakashima K., Fujita Y., Katsura K., Maruyama K., Narusaka Y., Seki M., Shinozaki K. & Yamaguchi-Shinozaki K. 2006. Transcriptional regulation of ABI3- and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol. Biol. 60: 51–68.10.1007/s11103-005-2418-5Search in Google Scholar PubMed

Nibau C., Tao L., Levasseur K., Wu H.M. & Cheung A.Y. 2013. The Arabidopsis small GTPase AtRAC7/ROP9 is a modulator of auxin and abscisic acid signaling. J. Exp. Bot. 64: 3425–3437.10.1093/jxb/ert179Search in Google Scholar PubMed PubMed Central

Ota T., Maeda M., Okamoto M. & Tatsuka M. 2015. Positive regulation of Rho GTPase activity by RhoGDIs as a result of their direct interaction with GAPs. BMC Syst. Biol. 9: 3.10.1186/s12918-015-0143-5Search in Google Scholar PubMed PubMed Central

Pathuri I.P., Zellerhoff N., Schaffrath U., Hensel G., Kumlehn J., Kogel K.H., Eichmann R. & Hückelhoven R. 2008. Constitutively activated barley ROPs modulate epidermal cell size, defense reactions and interactions with fungal leaf pathogens. Plant Cell Rep. 27: 1877–1887.10.1007/s00299-008-0607-9Search in Google Scholar PubMed

Poraty-Gavra L., Zimmermann P., Haigis S., Bednarek P., Hazak O., Stelmakh O.R., Sadot E., Schulze-Lefert P., Gruissem W. & Yalovsky S. 2013. The Arabidopsis Rho of plants GTPase AtROP6 functions in developmental and pathogen response pathways. Plant Physiol. 161: 1172–1188.10.1104/pp.112.213165Search in Google Scholar PubMed PubMed Central

Potikha T.S., Collins C.C., Johnson D.I., Delmer D.P. & Levine A. 1999. The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol. 119: 849–858.10.1104/pp.119.3.849Search in Google Scholar PubMed PubMed Central

Rech P., Grima-Pettenati J. & Jauneau A. 2003. Fluorescence microscopy: a powerful technique to detect low GUS activity in vascular tissues. Plant J. 33: 205–209.10.1046/j.1365-313X.2003.016017.xSearch in Google Scholar

Rogers S.O. & Bendich A.J. 1985. Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol. Biol. 5: 69–76.10.1007/BF00020088Search in Google Scholar PubMed

Schultheiss H., Hensel G., Imani J., Broeders S., Sonnewald U., Kogel K.H., Kumlehn J. & Hückelhoven R. 2005. Ectopic expression of constitutively activated RACB in barley enhances susceptibility to powdery mildew and abiotic stress. Plant Physiol. 139: 353–362.10.1104/pp.105.066613Search in Google Scholar PubMed PubMed Central

Sun H., Huang X., Xu X., Lan H., Huang J. & Zhang H.S. 2012. ENAC1, a NAC transcription factor, is an early and transient response regulator induced by abiotic stress in rice (Oryza sativa L.). Mol. Biotechnol. 52: 101–110.10.1007/s12033-011-9477-4Search in Google Scholar PubMed

Tao L.Z., Cheung A.Y. & Wu H.M. 2002. Plant Rac-like GTPases are activated by auxin and mediate auxin-responsive gene expression. Plant Cell 14: 2745-2760.10.1105/tpc.006320Search in Google Scholar PubMed PubMed Central

Tao L.Z., Cheung A.Y., Nibau C. & Wu H.M. 2005. RAC GT-Pases in tobacco and Arabidopsis mediate auxin-induced formation of proteolytically active nuclear protein bodies that contain AUX/IAA proteins. Plant Cell 17: 2369–2383.10.1105/tpc.105.032987Search in Google Scholar PubMed PubMed Central

Thao N.P., Chen L., Nakashima A., Hara S., Umemura K., Takahashi A., Shirasu K., Kawasaki T. & Shimamoto K. 2007. RAR1 and HSP90 form a complex with Rac/Rop GTPase and function in innate-immune responses in rice. Plant Cell 19: 4035–4045.10.1105/tpc.107.055517Search in Google Scholar PubMed PubMed Central

Wu H.M., Hazak O., Cheung A.Y. & Yalovsky S. 2011. RAC/ROP GTPases and auxin signaling. Plant Cell 23: 1208–1218.10.1105/tpc.111.083907Search in Google Scholar PubMed PubMed Central

Wu Y., Zhao S., Tian H., He Y., Xiong W., Guo L. & Wu Y. 2013. CPK3-phosphorylated RhoGDI1 is essential in the development of Arabidopsis seedlings and leaf epidermal cells. J. Exp. Bot. 64: 3327–3338.10.1093/jxb/ert171Search in Google Scholar PubMed PubMed Central

Yalovsky S., Bloch D., Sorek N. & Kost B. 2008. Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiol. 147: 1527–1543.10.1104/pp.108.122150Search in Google Scholar PubMed PubMed Central

Yang Z. 2002. Small GTPases: versatile signaling switches in plants. Plant Cell (Suppl.) 14: S375-S388.10.1105/tpc.001065Search in Google Scholar PubMed PubMed Central

Zhang Y. & McCormick S. 2007. A distinct mechanism regulating a pollen specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104: 18830-18835.10.1073/pnas.0705874104Search in Google Scholar PubMed PubMed Central

Zhao Z., Gu W., Cai T., Tagliani L., Hondred D., Bond O., Schroeder S., Rudert M. & Pierce D. 2001. High throughput genetic transformation mediated by Agrobacterium tumefaciens in maize. Mol. Breed. 8: 323-333.10.1023/A:1015243600325Search in Google Scholar

Zheng Z.L., Nafisi M., Tam A., Li H., Crowell D.N., Chary S.N., Schroeder J.I., Shen J. & Yang Z. 2002. Plasma membrane-associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in Arabidopsis. Plant Cell 14: 2787–2797.10.1105/tpc.005611Search in Google Scholar PubMed PubMed Central

Received: 2016-6-23
Accepted: 2016-9-19
Published Online: 2016-12-23
Published in Print: 2016-11-1

© 2016 Institute of Botany, Slovak Academy of Sciences

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https://doi.org/10.1515/biolog-2016-0146
Keywords for this article
Oryza sativa; GUS; OsRhoGDI2; stress response; transgenic rice

Articles in the same Issue

  1. Cellular and Molecular Biology
  2. The evolutionary pathway of the staphylococcal cassette chromosome element
  3. Cellular and Molecular Biology
  4. Detection of the antibacterial effect of Chaetomium cochliodes Palliser CCM F-232 based on agar plugs and unprocessed fungal substances from cultivation media
  5. Botany
  6. Identification and molecular characterization of one novel 1Sl-encoded s-type low molecular weight glutenin B-subunit from 1Sl(1B) substitution line of wheat variety Chinese Spring (Triticum aestivum)
  7. Botany
  8. Bioinformatic analysis of Arabidopsis reverse transcriptases with a zinc-finger domain
  9. Botany
  10. Distinct expression patterns of the GDP dissociation inhibitor protein gene (OsRhoGDI2) from Oryza sativa during development and abiotic stresses
  11. Botany
  12. An application of genetics-chemicals constituents to the relatedness of three Euphorbia species
  13. Zoology
  14. Centipede (Chilopoda) richness, diversity and community structure in the forest-steppe nature reserve “Bielinek” on the Odra River (NW Poland, Central Europe)
  15. Zoology
  16. Genetic differentiating Aphis fabae and Aphis craccivora (Hemiptera: Sternorranycha: Aphididae) populations in Egypt using mitochondrial COI
  17. Zoology
  18. A faunistic study on Carabidae and Scarabaeidae in alfalfa fields from Central Greece
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  22. Late flooding combined with warm autumn – potential possibility for prolongation of transmission of mosquito-borne diseases
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  24. Temperature and precipitation effects on breeding productivity of some passerines – a multivariate analysis of constant effort mist-netting data
  25. Cellular and Molecular Biology
  26. The direct action of hyaluronic acid on human U-937 and HL-60 cells – modification of native and model membranes
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