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Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice

Nature Genetics volume 47, pages 827–833 (2015)Cite this article

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Abstract

Global warming threatens many aspects of human life1,2, for example, by reducing crop yields3,4,5. Breeding heat-tolerant crops using genes conferring thermotolerance is a fundamental way to help deal with this challenge4,5,6,7,8,9. Here we identify a major quantitative trait locus (QTL) for thermotolerance in African rice (Oryza glaberrima), Thermo-tolerance 1 (TT1), which encodes an α2 subunit of the 26S proteasome involved in the degradation of ubiquitinated proteins. Ubiquitylome analysis indicated that OgTT1 protects cells from heat stress through more efficient elimination of cytotoxic denatured proteins and more effective maintenance of heat-response processes than achieved with OsTT1. Variation in TT1 has been selected for on the basis of climatic temperature and has had an important role in local adaptation during rice evolution. In addition, we found that overexpression of OgTT1 was associated with markedly enhanced thermotolerance in rice, Arabidopsis and Festuca elata. This discovery may lead to an increase in crop security in the face of the ongoing threat of global warming.

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Figure 1: Identification of TT1.
Figure 2: Role of TT1 in the heat response.
Figure 3: TT1 is involved in the local adaptation of rice.
Figure 4: Applicability of TT1 to breeding.

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References

  1. IPCC. 2014: Summary for policymakers. In Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds. Field, C.B. et al.). 1–32 (Cambridge University Press, 2014).

  2. Bohra-Mishra, P., Oppenheimer, M. & Hsiang, S.M. Nonlinear permanent migration response to climatic variations but minimal response to disasters. Proc. Natl. Acad. Sci. USA 111, 9780–9785 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Peng, S. et al. Rice yields decline with higher night temperature from global warming. Proc. Natl. Acad. Sci. USA 101, 9971–9975 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Battisti, D.S. & Naylor, R.L. Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323, 240–244 (2009).

    Article  CAS  PubMed  Google Scholar 

  5. Lobell, D.B., Schlenker, W. & Costa-Roberts, J. Climate trends and global crop production since 1980. Science 333, 616–620 (2011).

    Article  CAS  PubMed  Google Scholar 

  6. Mba, C., Guimaraes, E.P. & Ghosh, K. Re-orienting crop improvement for the changing climatic conditions of the 21st century. Agriculture & Food Security 1, 7 (2012).

    Article  Google Scholar 

  7. Takeda, S. & Matsuoka, M. Genetic approaches to crop improvement: responding to environmental and population changes. Nat. Rev. Genet. 9, 444–457 (2008).

    Article  CAS  PubMed  Google Scholar 

  8. Zhu, C.L. et al. Mapping QTL for heat-tolerance at grain filling stage in rice. Rice Science 12, 33–38 (2005).

    Google Scholar 

  9. Wei, H. et al. A dominant major locus in chromosome 9 of rice (Oryza sativa L.) confers tolerance to 48 °C high temperature at seedling stage. J. Hered. 104, 287–294 (2013).

    Article  CAS  PubMed  Google Scholar 

  10. Lyman, N.B., Jagadish, K.S.V., Nalley, L.L., Dixon, B.L. & Siebenmorgen, T. Neglecting rice milling yield and quality underestimates economic losses from high-temperature stress. PLoS One 8, e72157 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Trnka, M. et al. Adverse weather conditions for European wheat production will become more frequent with climate change. Nat. Clim. Chang. 4, 637–643 (2014).

    Article  Google Scholar 

  12. Semenov, M.A. & Shewry, P.R. Modelling predicts that heat stress, not drought, will increase vulnerability of wheat in Europe. Sci. Rep. 1, 66 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Sarla, N. & Swamy, B.P.M. Oryza glaberrima: a source for the improvement of Oryza sativa. Curr. Sci. 89, 955–963 (2005).

    Google Scholar 

  14. Sakai, H. et al. Distinct evolutionary patterns of Oryza glaberrima deciphered by genome sequencing and comparative analysis. Plant J. 66, 796–805 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Linares, O.F. African rice (Oryza glaberrima): history and future potential. Proc. Natl. Acad. Sci. USA 99, 16360–16365 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Luo, J.J., Hao, W., Jin, J., Gao, J.P. & Lin, H.X. Fine mapping of Spr3, a locus for spreading panicle from African cultivated rice (Oryza glaberrima Steud.). Mol. Plant 1, 830–838 (2008).

    Article  PubMed  CAS  Google Scholar 

  17. Wang, S., Kurepa, J. & Smalle, J.A. The Arabidopsis 26S proteasome subunit RPN1a is required for optimal plant growth and stress responses. Plant Cell Physiol. 50, 1721–1725 (2009).

    Article  CAS  PubMed  Google Scholar 

  18. Peng, Z. et al. The cellular level of PR500, a protein complex related to the 19S regulatory particle of the proteasome, is regulated in response to stresses in plants. Mol. Biol. Cell 12, 383–392 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Nishizawa-Yokoi, A. et al. The 26S proteasome function and Hsp90 activity involved in the regulation of HsfA2 expression in response to oxidative stress. Plant Cell Physiol. 51, 486–496 (2010).

    Article  CAS  PubMed  Google Scholar 

  20. Lee, K.H. et al. The RPT2 subunit of the 26S proteasome directs complex assembly, histone dynamics, and gametophyte and sporophyte development in Arabidopsis. Plant Cell 23, 4298–4317 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Book, A.J. et al. The RPN5 subunit of the 26S proteasome is essential for gametogenesis, sporophyte development, and complex assembly in Arabidopsis. Plant Cell 21, 460–478 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ueda, M. et al. The HALTED ROOT gene encoding the 26S proteasome subunit RPT2a is essential for the maintenance of Arabidopsis meristems. Development 131, 2101–2111 (2004).

    Article  CAS  PubMed  Google Scholar 

  23. Huang, W. et al. The proteolytic function of the Arabidopsis 26S proteasome is required for specifying leaf adaxial identity. Plant Cell 18, 2479–2492 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gallois, J.L. et al. The Arabidopsis proteasome RPT5 subunits are essential for gametophyte development and show accession-dependent redundancy. Plant Cell 21, 442–459 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Brukhin, V., Gheyselinck, J., Gagliardini, V., Genschik, P. & Grossniklaus, U. The RPN1 subunit of the 26S proteasome in Arabidopsis is essential for embryogenesis. Plant Cell 17, 2723–2737 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kurepa, J. & Smalle, J.A. Structure, function and regulation of plant proteasomes. Biochimie 90, 324–335 (2008).

    Article  CAS  PubMed  Google Scholar 

  27. Vierstra, R.D. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10, 385–397 (2009).

    Article  CAS  PubMed  Google Scholar 

  28. Huber, E.M. et al. Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity. Cell 148, 727–738 (2012).

    Article  CAS  PubMed  Google Scholar 

  29. Groll, M. et al. Structure of 20S proteasome from yeast at 2.4 Å resolution. Nature 386, 463–471 (1997).

    Article  CAS  PubMed  Google Scholar 

  30. Vierstra, R.D. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. 8, 135–142 (2003).

    Article  CAS  PubMed  Google Scholar 

  31. Bhattacharyya, S., Yu, H., Mim, C. & Matouschek, A. Regulated protein turnover: snapshots of the proteasome in action. Nat. Rev. Mol. Cell Biol. 15, 122–133 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ruschak, A.M., Religa, T.L., Breuer, S., Witt, S. & Kay, L.E. The proteasome antechamber maintains substrates in an unfolded state. Nature 467, 868–871 (2010).

    Article  CAS  PubMed  Google Scholar 

  33. Groll, M. et al. A gated channel into the proteasome core particle. Nat. Struct. Biol. 7, 1062–1067 (2000).

    Article  CAS  PubMed  Google Scholar 

  34. Kim, W. et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 44, 325–340 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Udeshi, N.D., Mertins, P., Svinkina, T. & Carr, S.A. Large-scale identification of ubiquitination sites by mass spectrometry. Nat. Protoc. 8, 1950–1960 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Wang, M. et al. The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nat. Genet. 46, 982–988 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hao, W., Jin, J., Sun, S.Y., Zhu, M.Z. & Lin, H.X. Construction of chromosome segment substitution lines carrying overlapping chromosome segments of the whole wild rice genome and identification of quantitative trait loci for rice quality. Zhi Wu Sheng Li Yu Fen Zi Sheng Wu Xue Xue Bao 32, 354–362 (2006).

    CAS  PubMed  Google Scholar 

  38. Hao, W., Zhu, M.Z., Gao, J.P., Sun, S.Y. & Lin, H.X. Identification of quantitative trait loci for rice quality in a population of chromosome segment substitution lines. J. Integr. Plant Biol. 51, 500–512 (2009).

    Article  CAS  PubMed  Google Scholar 

  39. Huang, X. et al. A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497–501 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Baniwal, S.K. et al. Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J. Biosci. 29, 471–487 (2004).

    Article  CAS  PubMed  Google Scholar 

  41. Hasanuzzaman, M., Nahar, K., Alam, M.M., Roychowdhury, R. & Fujita, M. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 14, 9643–9684 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Yanagawa, Y. et al. Purification and characterization of the 26S proteasome from cultured rice (Oryza sativa) cells. Plant Sci. 149, 33–41 (1999).

    Article  CAS  Google Scholar 

  43. Shibahara, T., Kawasaki, H. & Hirano, H. Identification of the 19S regulatory particle subunits from the rice 26S proteasome. Eur. J. Biochem. 269, 1474–1483 (2002).

    Article  CAS  PubMed  Google Scholar 

  44. International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature 436, 793–800 (2005).

    Article  CAS  Google Scholar 

  45. Mao, J., Zhang, Y.C., Sang, Y., Li, Q.H. & Yang, H.Q. A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc. Natl. Acad. Sci. USA 102, 12270–12275 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Warthmann, N., Chen, H., Ossowski, S., Weigel, D. & Herve, P. Highly specific gene silencing by artificial miRNAs in rice. PLoS One 3, e1829 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. 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).

    Article  CAS  PubMed  Google Scholar 

  48. Gao, C., Liu, J.X. & Nielsen, K.K. Agrobacterium-mediated transformation of meadow fescue (Festuca pratensis Huds.). Plant Cell Rep. 28, 1431–1437 (2009).

    Article  CAS  PubMed  Google Scholar 

  49. Clough, S.J. & Bent, A.F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

    Article  CAS  PubMed  Google Scholar 

  50. Sun, S.Y. et al. OsHAL3 mediates a new pathway in the light-regulated growth of rice. Nat. Cell Biol. 11, 845–851 (2009).

    Article  CAS  PubMed  Google Scholar 

  51. Wiśniewski, J.R., Zougman, A., Nagaraj, N. & Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods 6, 359–362 (2009).

    Article  CAS  PubMed  Google Scholar 

  52. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545–15550 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Mootha, V.K. et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267–273 (2003).

    Article  CAS  PubMed  Google Scholar 

  54. Huang, X. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961–967 (2010).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank G.Q. Zhang and the National Mid-term Genebank for Rice of China National Rice Research Institute for kindly providing O. glaberrima and O. sativa from Africa, respectively. We thank Y. Li for help with bioinformatics analysis. This work was supported by grants from the Ministry of Science and Technology of China (2012AA10A302, 2012CB944800), the National Natural Science Foundation of China (31421093, 31101128), the CAS-Croucher Funding Scheme for Joint Laboratories, the China Postdoctoral Science Foundation, and the Research Grants Council of Hong Kong (CUHK2/CRF/11G and AoE/M-05/12).

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Authors and Affiliations

  1. National Key Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

    Xin-Min Li, Dai-Yin Chao, Yuan Wu, Ke Chen, Long-Gang Cui, Lei Su, Wang-Wei Ye, Hao Chen, Hua-Chang Chen, Nai-Qian Dong, Tao Guo, Min Shi, Peng Zhang, Jun-Xiang Shan, Ji-Ping Gao & Hong-Xuan Lin

  2. National Center for Gene Research, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

    Xuehui Huang, Qi Feng & Bin Han

  3. Collaborative Innovation Center of Genetics and Development, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

    Bin Han & Hong-Xuan Lin

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  1. Xin-Min Li
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Contributions

H.-X.L. conceived and supervised the project. H.-X.L., J.-P.G., J.-X.S. and X.-M.L. designed the experiments. X.-M.L. carried out most of the experiments. D.-Y.C., Y.W., X.H., K.C., L.-G.C., L.S., W.-W.Y., H.C., H.-C.C., N.-Q.D., T.G., M.S., Q.F., P.Z., B.H., J.-X.S., J.-P.G. and H.-X.L. carried out some of the experiments. X.-M.L., D.-Y.C. and H.-X.L. analyzed data and wrote the manuscript.

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Correspondence to Jun-Xiang Shan, Ji-Ping Gao or Hong-Xuan Lin.

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Supplementary Figures 1–16 and Supplementary Tables 2 and 3 (PDF 44712 kb)

Supplementary Table 1

Summary of differentially ubiquitinated sites and corresponding proteins identified and quantified (two-way ANOVA, P(interaction) < 0.05) (XLSX 125 kb)

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Li, XM., Chao, DY., Wu, Y. et al. Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nat Genet 47, 827–833 (2015). https://doi.org/10.1038/ng.3305

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