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Rice RING E3 ligase may negatively regulate gamma-ray response to mediate the degradation of photosynthesis-related proteins

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Abstract

Main conclusion

In this study, our findings regarding the regulation of GA irradiation-induced OsGIRP1 in relation to the levels of photosynthesis-related proteins such as OsrbcL1 and OsrbcS1 and hypersensitive responses of overexpressing plants to GR irradiation provide insight into the molecular functions of OsGIRP1 as a negative regulator in response to the stress of radiation.

Abstract

The RING (Really Interesting New Gene) finger proteins are known to play crucial roles in various abiotic stresses in plants. Here, we report on RING finger E3 ligase, Oryza sativa gamma rays-induced RING finger protein1 gene (OsGIRP1), which is highly induced by gamma rays (GR) irradiation. In vitro ubiquitination assay demonstrated that a single amino acid substitution (OsGIRP1C196A) of the RING domain showed no E3 ligase activity, supporting the notion that the activity of most E3s is specified by a RING domain. We isolated at least 6 substrate proteins of OsGIRP1, including 2 Rubisco subunits, OsrbcL1 and OsrbcSl, via yeast two-hybridization and bimolecular fluorescence complementation assays. OsGIRP1 and its partner proteins were targeted to the cytosol and the cytosol or chloroplasts, respectively; however, florescence signals of the complexes with OsGIPR1 were observed in the cytosol. Protein degradation in cell extracts showed that OsGIRP1 mediates proteolysis of 2 substrates, OsrbcS1 and OsrbcL1, via the 26S proteasome degradation pathway. The Arabidopsis plants overexpressing OsGIRP1 clearly exhibited increased sensitivity to GR irradiation. These results might suggest that OsGIRP1 acts as a negative regulator of GR response to mediate the degradation of photosynthesis-related proteins.

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Abbreviations

RING:

Really interesting new gene

GR:

Gamma rays

BiFC:

Bimolecular fluorescence complementation

Rubisco:

Ribulose biphosphate carboxylase/oxygenase

DDO/X/A:

Synthetic defined medium lacking Leu and Trp supplemented with 40 μg ml−1 X-α-Gal and 70 ng ml−1 aureobasidin A (AbA)

QDO/X/A:

Synthetic defined medium lacking Ade, His, Leu, and Trp with 40 μg ml−1 X-α-Gal and 70 ng ml−1 AbA

References

  • Al-Salhi M, Ghannam MM, Al-Ayed MS, El-Kameesy SU, Roshdy S (2004) Effect of gamma-irradiation on the biophysical and morphological properties of corn. Nahrung 48:95–98

    Article  CAS  PubMed  Google Scholar 

  • Bauer J, Chen K, Hiltbunner A, Wehrli E, Eugster M, Schnell D, Kessler F (2000) The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403:203–207

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ (2004) Floral dip: Agrobacterium-mediated germ line transformation. Methods Mol Biol 286:91–101

    Google Scholar 

  • Deshaies RJ, Joazeiro CA (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78:399–434

    Article  CAS  PubMed  Google Scholar 

  • Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (2006) 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 USA 103:8281–8286

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Freemont PS, Hanson IM, Trowsdale J (1991) A novel cysteine-rich sequence motif. Cell 64:483–484

    Article  CAS  PubMed  Google Scholar 

  • Gailey FB, Tolbert NE (1958) Effect of ionizing radiation on the development of photosynthesis in etiolated wheat leaves. Arch Biochem Biophys 76:188–195

    Article  CAS  PubMed  Google Scholar 

  • Gao T, Wu Y, Zhang Y, Liu L, Ning Y, Wang D, Tong H, Chen S, Chu C, Xie Q (2011) OsSDIR1 overexpression greatly improves drought tolerance in transgenic rice. Plant Mol Biol 76:145–156

    Article  CAS  PubMed  Google Scholar 

  • Heller H, Hershko A (1990) A ubiquitin-protein ligase specific for type III protein substrates. J Biol Chem 265:6532–6535

    CAS  PubMed  Google Scholar 

  • Hurley JH, Lee S, Prag G (2006) Ubiquitin-binding domains. Biochem J 399:361–372

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hwang JE, Hwang S-G, Kim SH, Lee KJ, Jang CS, Kim JB, Kim SH, Ha BK, Ahn J-W, Kang S-Y, Kim DS (2014) Transcriptome profiling in response to different types of ionizing radiation and identification of multiple radio marker genes in rice. Physiol Plant 150:604–619

    Article  CAS  PubMed  Google Scholar 

  • Jacobson AD, Zhang NY, Xu P, Han KJ, Noone S, Peng J, Liu CW (2009) The lysine 48 and lysine 63 ubiquitin conjugates are processed differently by the 26s proteasome. J Biol Chem 284:35485–35494

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jung CG, Lim SD, Hwang S-G, Jang CS (2012) Molecular characterization and concerted evolution of two genes encoding RING-C2 type proteins in rice. Gene 505:9–18

    Article  CAS  PubMed  Google Scholar 

  • Kim JH, Chung BY, Kim JS, Wi SG (2005) Effects of in planta gamma-irradiation on growth, photosynthesis, and antioxidative capacity of red pepper (Capsicum annuum L.) plants. J Plant Biol 48:47–56

    Article  CAS  Google Scholar 

  • Kim DS, Kim JB, Goh EJ, Kim W-J, Kim SH, Seo YW, Jang CS, Kang S-Y (2011) Antioxidant response of Arabidopsis plants gamma irradiation: genome-wide expression profiling of the ROS scavenging and signal transduction pathways. J Plant Physiol 168:1960–1971

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Song M, Lee KJ, Hwang SG, Jang CS, Kim JB, Ha BK, Kang SY, Kim DS (2012) Genome-wide transcriptome profiling of ROS scavenging and signal transduction pathways in rice (Oryza sativa L.) in response to different types of ionizing radiation. Mol Biol Rep 39:11231–11248

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Hwang SG, Hwang JE, Jang CS, Velusamy V, Kim JB, Kim SH, Ha B-K, Kang S-Y, Kim DS (2013) The identification of candidate radio marker genes using a coexpression network analysis in gamma-irradiated rice. Physiol Plant 149:554–570

    Article  CAS  Google Scholar 

  • Kovacs E, Keresztes A (2002) Effect of gamma and UV-B/C radiation on plant cells. Micron 33:199–210

    Article  CAS  PubMed  Google Scholar 

  • Kuzin AM, Uzorin EK, Chirkovskii VI (1963) Examination of remote post-irradiation effects in some plant species of the Nicotiana family following gamma irradiation of the seed. Radiobiologiia 3:903–908

    CAS  PubMed  Google Scholar 

  • Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK (2001) The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Genes Dev 15:912–924

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lim SD, Yim WC, Moon JC, Kim DS, Lee BM, Jang CS (2010) A gene family encoding RING finger proteins in rice: their expansion, expression diversity, and co-expressed genes. Plant Mol Biol 72:369–380

    Article  CAS  PubMed  Google Scholar 

  • Lim SD, Cho HY, Park YC, Ham DJ, Lee JK, Jang CS (2013a) The rice RING finger E3 ligase, OsHCI1, drives nuclear export of multiple substrate proteins and its heterogeneous overexpression enhances acquired thermotolerance. J Exp Bot 64:2899–2914

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lim SD, Hwang JG, Jung CG, Hwang SG, Moon JC, Jang CS (2013b) Comprehensive analysis of the rice RING E3 ligase family reveals their functional diversity in response to abiotic stress. DNA Res 20:299–314

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lim SD, Hwang JG, Han AR, Park YC, Lee C, Ok YS, Jang CS (2014a) Positive regulation of rice RING E3 ligase OsHIR1 in arsenic and cadmium uptakes. Plant Mol Biol 85:365–379

    Article  CAS  PubMed  Google Scholar 

  • Lim SD, Lee C, Jang CS (2014b) The rice RING E3 ligase, OsCTR1, inhibits trafficking to the chloroplasts of OsCP12 and OsRP1, and its overexpression confers drought tolerance in Arabidopsis. Plant Cell Environ 37:1097–1113

    Article  CAS  PubMed  Google Scholar 

  • Lin H, Wang H, Ding H, Chen YL, Li QZ (2009) Prediction of subcellular localization of apoptosis protein using Chou’s pseudo amino acid composition. Acta Biotheor 57:321–330

    Article  PubMed  Google Scholar 

  • Mehta RA, Fawcett TW, Porath D, Mattoo AK (1992) Oxidative stress causes rapid membrane translocation and in vivo degradation of rubulose-1-5-bisphosphate carboxylase/oxygenase. J Biol Chem 267:2810–2816

    CAS  PubMed  Google Scholar 

  • Minoda A, Weber APM, Tanaka L, Miyagishima SY (2010) Nucleus-independent control of the Rubisco operon by the plastid-encoded transcription factor Ycf30 in the red alga Cyanidioschyzon merolae. Plant Physiol 154:1532–1540

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mukhopadhyay D, Riezman H (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315:201–205

    Article  CAS  PubMed  Google Scholar 

  • Penate L, Martin O, Cardenas R, Agusti S (2010) Short-term effects of gamma ray bursts on oceanic photosynthesis. Astrophys Space Sci 330:211–217

    Article  CAS  Google Scholar 

  • Shyu YJ, Hiatt SM, Duren HM, Ellis RE, Kerppola TK, Hu CD (2008) Visualization of protein interactions in living Caenorhabditis elegans using bimolecular fluorescence complementation analysis. Nat Protoc 3:588–596

    Article  CAS  PubMed  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590

    Article  CAS  PubMed  Google Scholar 

  • Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39:623–630

    Article  CAS  PubMed  Google Scholar 

  • Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137:13–30

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10:385–397

    Article  CAS  PubMed  Google Scholar 

  • von Arnim AG, Deng XW (1994) Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 79:1035–1045

    Article  Google Scholar 

  • Wakasugi T, Tsudzuki T, Sugiura M (2001) The genomics of land plant chloroplasts: gene content and alteration of genomic information by RNA editing. Photosynth Res 70:107–118

    Article  CAS  PubMed  Google Scholar 

  • Wi SG, Chung BY, Kim JH, Baek MH, Yang DH, Lee JW, Kim JS (2005) Ultrastructural changes of cell organelles in Arabidopsis stems after gamma irradiation. J Plant Biol 48:195–200

    Article  Google Scholar 

  • Wi SG, Chung BY, Kim JS, Kim JH, Baek MH, Lee JW, Kim YS (2007) Effects of gamma irradiation on morphological changes and biological responses in plants. Micron 38:553–564

    Article  CAS  PubMed  Google Scholar 

  • Zhang YY, Yang CW, Li Y, Zheng NY, Chen H, Zhao QZ, Gao T, Guo HS, Xie Q (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19:1912–1929

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Research Foundation of Korea Funded by the Ministry of Education, Science, and Technology (NRF-2013R1A1A4A01011064) and by grants from the Nuclear R&D Program of the Ministry of Science, ICT, and Future Planting (MSIP), Republic of Korea.

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Authors and Affiliations

  1. Plant Genomics Lab, Department of Applied Plant Sciences, Kangwon National University, Chuncheon, 200-713, Republic of Korea

    Yong Chan Park, Jung Ju Kim & Cheol Seong Jang

  2. Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute, 1266 Sinjeong, Jeongeup, Jeonbuk, 580-185, South Korea

    Dong Sub Kim

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  1. Yong Chan Park
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Correspondence to Cheol Seong Jang.

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425_2015_2242_MOESM1_ESM.pdf

Supplementary material 1 (PDF 269 kb) Fig. S1 Subcellular localization and BiFC assay of 4 OsGIRP1-interacting proteins. Four full-length genes were cloned into 35S:EYFP vector (for subcellular localization) and SPYNE(R) vector (for BiFC assay), respectively. Each construct vector was transfected into rice protoplasts. OsPPT1 (a), OsDNLZ1 (b), OsMSR1 (c), and Os4NPP1 (d) were separately transfected for subcellular localization, and transfected with OsGIRP1-SPYCE(M) for BiFC assay into rice protoplastsFig. S2 Semi-quantitative RT-PCR of OsGIRP1-overexpressing Arabidopsis and control plants. Two-week-old seedlings of each of T3 transgenic plants were used for RT-PCR. AtUBC was used for the internal controlFig. S3 The transcript levels of OsrbcS1 (a) and OsrbcL1 (b) genes in irradiated rice. Irradiated rice samples were used for quantitative RT-PCR. The cDNA was mixed with a with TOPreal™ qPCR2XPreMix with SYBR green (Enzynomics, South Korea) and 10 pmol of each of the primers. PCR was performed using the CFX96 real-Time PCR Detection System (BioRad). The transcript level was standardized on the basis of cDNA amplification with Actinll as an internal control

Supplementary material 2 (PDF 114 kb) Table S1 Primer list for cloning and semi-quantitative RT-PCR used in this study

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Park, Y.C., Kim, J.J., Kim, D.S. et al. Rice RING E3 ligase may negatively regulate gamma-ray response to mediate the degradation of photosynthesis-related proteins. Planta 241, 1119–1129 (2015). https://doi.org/10.1007/s00425-015-2242-3

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