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The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency

Abstract

As an essential macroelement for all living cells, phosphorus is indispensable in agricultural production systems. Natural phosphorus reserves are limited1, and it is therefore important to develop phosphorus-efficient crops. A major quantitative trait locus for phosphorus-deficiency tolerance, Pup1, was identified in the traditional aus-type rice variety Kasalath about a decade ago2,3. However, its functional mechanism remained elusive4,5 until the locus was sequenced, showing the presence of a Pup1-specific protein kinase gene6, which we have named phosphorus-starvation tolerance 1 (PSTOL1). This gene is absent from the rice reference genome and other phosphorus-starvation-intolerant modern varieties7,8. Here we show that overexpression of PSTOL1 in such varieties significantly enhances grain yield in phosphorus-deficient soil. Further analyses show that PSTOL1 acts as an enhancer of early root growth, thereby enabling plants to acquire more phosphorus and other nutrients. The absence of PSTOL1 and other genes—for example, the submergence-tolerance gene SUB1A—from modern rice varieties underlines the importance of conserving and exploring traditional germplasm. Introgression of this quantitative trait locus into locally adapted rice varieties in Asia and Africa is expected to considerably enhance productivity under low phosphorus conditions.

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Figure 1: Origin of the donor variety Kasalath and Pup1 candidate genes.
Figure 2: PSTOL1 overexpression enhances tolerance of P deficiency.
Figure 3: PSTOL1 is an enhancer of root growth.
Figure 4: PSTOL1 putative downstream genes co-localize with root and drought QTLs.

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Accession codes

Data deposits

GenBank protein accession numbers for OsPupK04-1, OsPupK05-1, OsPupK20-2, OsPupK29-1 and PSTOL1/OsPupK46-2 are BAH79993, BAH79994, BAK26565, BAH80018 and BAK26566, respectively.

References

  1. Van Kauwenbergh, S. J. World Phosphate Rock Reserves and Resources http://www.ifdc.org/getdoc/56358fb1-fc9b-49ba-92fe-187dc08e9586/T-75_World_Phosphate_Rock_Reserves_and_Resources (International Fertilizer Development Center, 2010)

    Google Scholar 

  2. Wissuwa, M., Yano, M. & Ae, N. Mapping of QTLs for phosphorus-deficiency tolerance in rice (Oryza sativa L.). Theor. Appl. Genet. 97, 777–783 (1998)

    Article  CAS  Google Scholar 

  3. Wissuwa, M. & Ae, N. Genotypic variation for tolerance to phosphorus deficiency in rice and the potential for its exploitation in rice improvement. Plant Breed. 120, 43–48 (2001)

    Article  CAS  Google Scholar 

  4. Wissuwa, M. Combining a modeling with a genetic approach in establishing associations between genetic and physiological effects in relation to phosphorus uptake. Plant Soil 269, 57–68 (2005)

    Article  CAS  Google Scholar 

  5. Pariasca-Tanaka, J., Satoh, K., Rose, T., Mauleon, R. & Wissuwa, M. Stress response versus stress tolerance: a transcriptome analysis of two rice lines contrasting in tolerance to phosphorus deficiency. Rice 2, 167–185 (2009)

    Article  Google Scholar 

  6. Heuer, S. et al. Comparative sequence analyses of the major quantitative trait locus Phosphorus uptake 1 (Pup1) reveal a complex genetic structure. Plant Biotechnol. J. 7, 456–471 (2009)

    Article  CAS  PubMed  Google Scholar 

  7. Chin, J. H. et al. Development and application of gene-based markers for the major rice QTL Phosphorus uptake 1. Theor. Appl. Genet. 120, 1073–1086 (2010)

    Article  CAS  PubMed  Google Scholar 

  8. Chin, J. H. et al. Developing rice with high yield under phosphorus deficiency: Pup1 sequence to application. Plant Physiol. 156, 1202–1216 (2011)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  9. Haefele, S. M. & Hijmans, R. J. In Science, Technology, and Trade for Peace and Prosperity: Proceedings of the 26th International Rice Research Conference, New Delhi, India. (eds Aggarwal, P. K., Ladha, J. K., Singh, R. K., Devakumar, C. & Hardy, B. ) International Rice Research Institute, Indian Council of Agricultural Research, and National Academy of Agricultural Sciences, Los Baños, Philippines, and New Delhi, India. 297–308 (2007)

    Google Scholar 

  10. Haefele, S. M. & Hijmans, R. J. Soil quality in rainfed lowland rice. Rice Today 8, 30–31 (2009)

    Google Scholar 

  11. Dawe, D., Pandey, S. & Nelson, A. In Rice in the Global Economy. Strategic Research and Policy Issues for Food Security (eds Pandey, S. et al.) 5–35 (International Rice Research Institute, 2010)

    Google Scholar 

  12. Cordell, D., Drangert, J. O. & White, S. The story of phosphorus: global food security and food for thought. Glob. Environ. Change 19, 292–305 (2009)

    Article  Google Scholar 

  13. Londo, J. P., Chiang, Y. C., Hung, K. H., Chiang, T. Y. & Schaal, B. A. Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc. Natl Acad. Sci. USA 103, 9578–9583 (2006)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  14. Xu, K. et al. Sub1A is an ethylene-responsive-factor-like gene that confers submergence tolerance to rice. Nature 442, 705–708 (2006)

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Manzanilla, D. O. et al. Submergence risks and farmers’ preferences: implications for breeding Sub1 rice in Southeast Asia. Agric. Syst. 104, 335–347 (2011)

    Article  Google Scholar 

  16. Gowda, V. R. P. et al. Water uptake dynamics under progressive drought stress in diverse accessions of the OryzaSNP panel of rice (Oryza sativa). Func. Plant Bio. 39, 402–411 (2012)

    Article  Google Scholar 

  17. Wissuwa, M., Wegner, J., Ae, N. & Yano, M. Substitution mapping of Pup1: a major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theor. Appl. Genet. 105, 890–897 (2002)

    Article  CAS  PubMed  Google Scholar 

  18. Gregory, P. D., Barbari, S. & Hörz, W. Transcriptional control of phosphate-regulated genes. Food Technol. Biotechnol. 38, 295–303 (2000)

    CAS  Google Scholar 

  19. Yang, X. J. & Finnegan, P. M. Regulation of phosphate starvation responses in higher plants. Ann. Bot. (Lond.) 105, 513–526 (2010)

    Article  CAS  Google Scholar 

  20. Dardick, C., Chen, J., Richter, T., Ouyang, S. & Ronald, P. The rice kinase database. A phylogenomic database for the rice kinome. Plant Physiol. 143, 579–586 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Vij, S., Giri, J., Dansana, P. K., Kapoor, S. & Tyagi, A. K. The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress. Mol. Plant 1, 732–750 (2008)

    Article  CAS  PubMed  Google Scholar 

  22. Wang, X., Zafian, P., Choudhary, M. & Lawton, M. The PR5K receptor protein kinase from Arabidopsis thaliana is structurally related to a family of plant defense proteins. Proc. Natl Acad. Sci. USA 93, 2598–2602 (1996)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bi, D., Cheng, Y. T., Li, X. & Zhang, Y. Activation of plant immune responses by a gain-of-function mutation in an atypical receptor-like kinase. Plant Physiol. 153, 1771–1779 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bonardi, V. et al. Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437, 1179–1182 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  25. Inukai, Y. et al. Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17, 1387–1396 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhao, Y., Hu, Y., Dai, M., Huang, L. & Zhou, D.-X. The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell 21, 736–748 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lohrmann, J. & Harter, K. Plant two-component signaling systems and the role of response regulators. Plant Physiol. 128, 363–369 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Scarpella, E., Simons, E. J. & Meijer, A. J. Multiple regulatory elements contribute to the vascular-specific expression of the rice HD-Zip gene Oshox1 in Arabidopsis. Plant Cell Physiol. 46, 1400–1410 (2005)

    Article  CAS  PubMed  Google Scholar 

  29. Kong, Z., Li, M., Yang, W., Xu, W. & Xue, Y. A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol. 141, 1376–1388 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ouyang, J. et al. Identification and analysis of eight peptide transporter homologs in rice. Plant Sci. 179, 374–382 (2010)

    Article  CAS  Google Scholar 

  31. Haldrup, A., Naver, H. & Scheller, H. V. The interaction between plastocyanin and photosystem I is inefficient in transgenic Arabidopsis plants lacking the PSI-N subunit of photosystem I. Plant J. 17, 689–698 (1999)

    Article  CAS  PubMed  Google Scholar 

  32. Pribil, M., Pesaresi, P., Hertle, A., Barbato, R. & Leister, D. Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol. 8, e1000288 (2010)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Curtis, M. D. & Grossniklaus, U. A Gateway cloning vector set for high throughput functional analysis of genes in planta. Plant Physiol. 133, 462–469 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hiei, Y., Ishida, Y., Kasaoka, K. & Komari, T. Improved frequency of transformation in rice and maize by treatment of immature embryos with centrifugation and heat prior to infection with Agrobacterium tumefaciens. Plant Cell Tiss. Org. 87, 233–243 (2006)

    Article  Google Scholar 

  35. Yoshida, S., Forno, D. A., Cock, J. H. & Gomez, K. A. Laboratory Manual for Physiological Studies of Rice 2nd edn 1–70 (International Rice Research Institute, 1972)

    Google Scholar 

  36. Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907 (1987)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Bernier, J., Kumar, A., Ramaiah, V., Spaner, D. & Atlin, G. A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice. Crop Sci. 47, 507–518 (2007)

    Article  Google Scholar 

  38. Bimpong, I. K. et al. Determination of genetic variability for physiological traits related to drought tolerance in African rice (Oryza glaberrima). J. Plant Breed. Crop. Sci. 3, 60–67 (2011)

    Google Scholar 

  39. Courtois, B. et al. Rice root architecture: meta-analysis from a drought QTL database. Rice 2, 115–128 (2009)

    Article  Google Scholar 

  40. Gomez, M. S. et al. Mapping QTLs linked to physio-morphological and plant production traits under drought stress in rice (Oryza sativa L.) in the target environment. Am. J. Biochem. Biotechnol. 2, 161–169 (2006)

    Article  Google Scholar 

  41. Lanceras, J. C., Pantuwan, G., Jongdee, B. & Toojinda, T. Quantitative trait loci associated with drought tolerance at reproductive stage in rice. Plant Physiol. 135, 384–399 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ni, J. J., Wu, P., Senadhira, D. & Huang, N. Mapping QTLs for phosphorus deficiency tolerance in rice (Oryza sativa L.). Theor. Appl. Genet. 97, 1361–1369 (1998)

    Article  CAS  Google Scholar 

  43. Thomson, M. J. et al. High-throughput single nucleotide polymorphism genotyping for breeding applications in rice using the BeadXpress platform. Mol. Breed. 29, 875–886 (2011)

    Article  CAS  Google Scholar 

  44. Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000)

    Article  CAS  PubMed  Google Scholar 

  45. Falush, D., Stephens, M. & Pritchard, J. K. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Bradbury, P. J. et al. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23, 2633–2635 (2007)

    Article  CAS  PubMed  Google Scholar 

  47. Miki, D. & Shimamoto, K. Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol. 45, 490–495 (2004)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank A. Cruz, E. Ramos and L. Olivo for technical and secretarial support, the staff at the transformation laboratory, F. Rossi for help with the Pstol1 kinase assay, M. Akutsu for help with the analysis of transgenic plants, and S. Haefele and his team for their support. We thank J. Prasetiyono, M. Bustamam and S. Moeljopawiro for their long-term collaboration. This project has been primarily funded by the Generation Challenge Program (GCP) since 2005.

Author information

Authors and Affiliations

Authors

Contributions

R.G. cloned and transformed the PSTOL1 gene into IR64 and Nipponbare. R.G., J.P.T. and M.W. performed the phenotyping of transgenic plants. J.H.C. conducted the root meta-QTL analysis and J.H.C. and C.D. developed the IR64-Pup1 and IR74-Pup1 NILs. P.P. carried out the Pstol1 kinase assay. S.C. conducted the expression analysis of putative PSTOL1 downstream genes. E.M.T.M. provided advice about the experiments and I.S.-L. provided technical support and infrastructure for rice transformation. R.G., M.W. and S.H. designed the experiments and wrote the manuscript.

Corresponding author

Correspondence to Sigrid Heuer.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Figures

This file contains Supplementary Figures 1-9. (PDF 1264 kb)

Supplementary Data 1

This file contains Supplementary Table 1, which shows a summary of P starvation responsive genes. (XLS 224 kb)

Supplementary Data 2

This file contains Supplementary Table 2 showing a list of genes with constitutively altered expression in 35S::OsPSTOL1 roots. (XLS 40 kb)

Supplementary Data 3

This file contains Supplementary Table 3, which shows a list of primers used in this study. (XLS 26 kb)

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Gamuyao, R., Chin, J., Pariasca-Tanaka, J. et al. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488, 535–539 (2012). https://doi.org/10.1038/nature11346

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