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Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions

Nature Genetics volume 45, pages 1097–1102 (2013)Cite this article

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Abstract

The genetic improvement of drought resistance is essential for stable and adequate crop production in drought-prone areas1. Here we demonstrate that alteration of root system architecture improves drought avoidance through the cloning and characterization of DEEPER ROOTING 1 (DRO1), a rice quantitative trait locus controlling root growth angle. DRO1 is negatively regulated by auxin and is involved in cell elongation in the root tip that causes asymmetric root growth and downward bending of the root in response to gravity. Higher expression of DRO1 increases the root growth angle, whereby roots grow in a more downward direction. Introducing DRO1 into a shallow-rooting rice cultivar by backcrossing enabled the resulting line to avoid drought by increasing deep rooting, which maintained high yield performance under drought conditions relative to the recipient cultivar. Our experiments suggest that control of root system architecture will contribute to drought avoidance in crops.

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Figure 1: Phenotypic characterization and cloning of DRO1.
Figure 2: Effect of DRO1 on root growth angle and root gravitropic curvature.
Figure 3: Expression analysis of DRO1.
Figure 4: Molecular characterization of DRO1.
Figure 5: Effect of DRO1 on the response to drought-induced stress.

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DDBJ/GenBank/EMBL

Gene Expression Omnibus

References

  1. Pennisi, E. The Blue Revolution, drop by drop, gene by gene. Science 320, 171–173 (2008).

    Article  CAS  PubMed  Google Scholar 

  2. Kondo, M., Murty, M.V.R. & Aragones, D.V. Characteristics of root growth and water uptake from soil in upland rice and maize under water stress. Soil Sci. Plant Nutr. 46, 721–732 (2000).

    Article  Google Scholar 

  3. Yoshida, S. & Hasegawa, S. The rice root system: its development and function. in Drought Resistance in Crops with Emphasis on Rice 97–114 (International Rice Research Institute, Los Baños, Philippines, 1982).

  4. Fukai, S. & Cooper, M. Development of drought-resistant cultivars using physio-morphological traits in rice. Field Crops Res. 40, 67–86 (1995).

    Article  Google Scholar 

  5. Gowda, V.R.P., Henry, A., Yamauchi, A., Shashidhar, H.E. & Serraj, R. Root biology and genetic improvement for drought avoidance in rice. Field Crops Res. 122, 1–13 (2011).

    Article  Google Scholar 

  6. Rebouillat, J. et al. Molecular genetics of rice root development. Rice 2, 15–34 (2009).

    Article  Google Scholar 

  7. Coudert, Y., Périn, C., Courtois, B., Khong, N.G. & Gantet, P. Genetic control of root development in rice, the model cereal. Trends Plant Sci. 15, 219–226 (2010).

    Article  CAS  PubMed  Google Scholar 

  8. Obara, M. et al. Fine-mapping of qRL6.1, a major QTL for root length of rice seedlings grown under a wide range of NH4+ concentrations in hydroponic conditions. Theor. Appl. Genet. 121, 535–547 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Uga, Y., Okuno, K. & Yano, M. Fine mapping of Sta1, a quantitative trait locus determining stele transversal area, on rice chromosome 9. Mol. Breed. 26, 533–538 (2010).

    Article  Google Scholar 

  10. Uga, Y., Okuno, K. & Yano, M. Dro1, a major QTL involved in deep rooting of rice under upland field conditions. J. Exp. Bot. 62, 2485–2494 (2011).

    Article  CAS  PubMed  Google Scholar 

  11. Ding, X., Li, X. & Xiong, L. Evaluation of near-isogenic lines for drought resistance QTL and fine mapping of a locus affecting flag leaf width, spikelet number, and root volume in rice. Theor. Appl. Genet. 123, 815–826 (2011).

    Article  PubMed  Google Scholar 

  12. Uga, Y. et al. Identification of qSOR1, a major rice QTL involved in soil-surface rooting in paddy fields. Theor. Appl. Genet. 124, 75–86 (2012).

    Article  PubMed  Google Scholar 

  13. Uga, Y. et al. Variation in root morphology and anatomy among accessions of cultivated rice (Oryza sativa L.) with different genetic backgrounds. Breed. Sci. 59, 87–93 (2009).

    Article  Google Scholar 

  14. Araki, H., Morita, S., Tatsumi, J. & Iijima, M. Physio-morphological analysis on axile root growth in upland rice. Plant Prod. Sci. 5, 286–293 (2002).

    Article  Google Scholar 

  15. Morita, M.T. & Tasaka, M. Gravity sensing and signaling. Curr. Opin. Plant Biol. 7, 712–718 (2004).

    Article  CAS  PubMed  Google Scholar 

  16. Vanneste, S. & Friml, J. Auxin: a trigger for change in plant development. Cell 136, 1005–1016 (2009).

    Article  CAS  PubMed  Google Scholar 

  17. Brunoud, G. et al. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482, 103–106 (2012).

    Article  CAS  PubMed  Google Scholar 

  18. Song, Y., Wang, L. & Xiong, L. Comprehensive expression profiling analysis of OsIAA gene family in developmental processes and in response to phytohormone and stress treatments. Planta 229, 577–591 (2009).

    Article  CAS  PubMed  Google Scholar 

  19. Hagen, G. & Guilfoyle, T. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol. 49, 373–385 (2002).

    Article  CAS  PubMed  Google Scholar 

  20. Ulmasov, T., Murfett, J., Hagen, G. & Guilfoyle, T.J. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963–1971 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Waller, F., Furuya, M. & Nick, P. OsARF1, an auxin response factor from rice, is auxin-regulated and classifies as a primary auxin responsive gene. Plant Mol. Biol. 50, 415–425 (2002).

    Article  CAS  PubMed  Google Scholar 

  22. Wang, D. et al. Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394, 13–24 (2007).

    Article  CAS  PubMed  Google Scholar 

  23. Swarup, R. et al. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7, 1057–1065 (2005).

    Article  CAS  PubMed  Google Scholar 

  24. Mullen, J.L., Ishikawa, H. & Evans, M.L. Analysis of changes in relative elemental growth rate patterns in the elongation zone of Arabidopsis roots upon gravistimulation. Planta 206, 598–603 (1991).

    Article  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. Liu, H. et al. ARL1, a LOB domain protein required for adventitious root formation in rice. Plant J. 43, 47–56 (2005).

    Article  PubMed  Google Scholar 

  27. Kitomi, Y. et al. The auxin responsive AP2/ERF transcription factor CROWN ROOTLESS5 is involved in crown root initiation in rice through the induction of OsRR1, a type-A response regulator of cytokinin signaling. Plant J. 67, 472–484 (2011).

    Article  CAS  PubMed  Google Scholar 

  28. Morita, Y. & Kyozuka, J. Characterization of OsPID, the rice ortholog of PINOID, and its possible involvement in the control of polar auxin transport. Plant Cell Physiol. 48, 540–549 (2007).

    Article  CAS  PubMed  Google Scholar 

  29. Kitomi, Y., Ogawa, A., Kitano, H. & Inukai, Y. CRL4 regulates crown root formation through auxin transport in rice. Plant Root 2, 19–28 (2008).

    Article  CAS  Google Scholar 

  30. Liu, S. et al. Adventitious root formation in rice requires OsGNOM1 and is mediated by the OsPINs family. Cell Res. 19, 1110–1119 (2009).

    Article  CAS  PubMed  Google Scholar 

  31. Garrity, D.P. & O'Toole, J.C. Selection for reproductive stage drought avoidance in rice, using infrared thermometry. Agron. J. 87, 773–779 (1995).

    Article  Google Scholar 

  32. Nemoto, H., Suga, R., Ishihara, M. & Okutsu, Y. Deep rooted rice varieties detected through the observation of root characteristics using the trench method. Breed. Sci. 48, 321–324 (1998).

    Google Scholar 

  33. Oyanagi, A., Nakamoto, T. & Wada, M. Relationship between root growth angle of seedlings and vertical distribution of roots in the field in wheat cultivars. Jpn. J. Crop. Sci. 62, 565–570 (1993).

    Article  Google Scholar 

  34. Hattori, Y. et al. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460, 1026–1030 (2009).

    Article  CAS  PubMed  Google Scholar 

  35. Fuse, T., Sasaki, T. & Yano, M. Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol. 18, 219–222 (2001).

    Article  CAS  Google Scholar 

  36. Hiei, Y. & Komari, T. Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat. Protoc. 3, 824–834 (2008).

    Article  CAS  PubMed  Google Scholar 

  37. Matsubara, K. et al. Ehd3, encoding a plant homeodomain finger–containing protein, is a critical promoter of rice flowering. Plant J. 66, 603–612 (2011).

    Article  CAS  PubMed  Google Scholar 

  38. Kawakatsu, T., Yamamoto, M.P., Touno, S.M., Yasuda, H. & Takaiwa, F. Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. Plant J. 59, 908–920 (2009).

    Article  CAS  PubMed  Google Scholar 

  39. Matsushita, A. et al. The nuclear ubiquitin proteasome degradation affects WRKY45 function in the rice defense program. Plant J. 73, 302–313 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  40. 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 

  41. Kojima, S. et al. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. 43, 1096–1105 (2002).

    Article  CAS  PubMed  Google Scholar 

  42. Takehisa, H. et al. Genome-wide transcriptome dissection of the rice root system: implications for developmental and physiological functions. Plant J. 69, 126–140 (2012).

    Article  CAS  PubMed  Google Scholar 

  43. Komatsuda, T. et al. Six-rowed barley originated from a mutation in a homeodomain–leucine zipper I–class homeobox gene. Proc. Natl. Acad. Sci. USA 104, 1424–1429 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Rice Annotation Project. The Rice Annotation Project Database (RAP-DB): 2008 update. Nucleic Acids Res. 36, D1028–D1033 (2008).

  45. Sato, Y. et al. Field transcriptome revealed critical developmental and physiological transitions involved in the expression of growth potential in japonica rice. BMC Plant Biol. 11, 10 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hirano, K. et al. Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol. 49, 1429–1450 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Miyashita, Y., Takasugi, T. & Ito, Y. Identification and expression analysis of PIN genes in rice. Plant Sci. 178, 424–428 (2010).

    Article  CAS  Google Scholar 

  48. Takai, T., Yano, M. & Yamamoto, T. Canopy temperature on clear and cloudy days can be used to estimate varietal differences in stomatal conductance in rice. Field Crops Res. 115, 165–170 (2010).

    Article  Google Scholar 

  49. Hirayama, M. & Suga, R. Drought resistance. in Rice Breeding Manual 152–155 (Yokendo, Tokyo, 1996).

  50. Cabuslay, G.S., Ito, O. & Alejar, A.A. Physiological evaluation of responses of rice (Oryza sativa L.) to water deficit. Plant Sci. 163, 815–827 (2002).

    Article  CAS  Google Scholar 

  51. Kato, Y., Hirotsu, S., Nemoto, K. & Yamagishi, J. Identification of QTLs controlling rice drought tolerance at seedling stage in hydroponic culture. Euphytica 160, 423–430 (2008).

    Article  Google Scholar 

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Acknowledgements

We thank K. Shimamoto (NAra Institute of Science and Technology, NAIST) and E.E. Hood (Arkansas State University) for kindly providing the pANDA vector and Agrobacterium (EHA101), respectively. Full-length cDNAs for use as controls in the quantitative RT-PCR experiments were provided by the Rice Genome Resource Center of NIAS. We thank N. Hattori, T. Tanaka, M. Yamanouchi, K. Matsubara, S. Mochizuki, N. Yokotani, T. Mizubayashi, T. Ando, N. Sentoku and A. Tagiri for technical support and advice on molecular analysis; T. Nishikawa, Y. Itai, M. Takimoto, E. Nakao, H. Oode, R. Matsushita and the staff of the technical support section of NIAS for technical assistance during field evaluation; M. Kondo, A. Oyanagi, T. Izawa, E. Yamamoto, T. Hoshino, J. Tohme, C.P. Martinez, N.T. Perea and A. Fernando for valuable discussion; and K. Shinozaki for critical reading of the manuscript. This work was supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (QTL-4003 and RBS-2009).

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Author notes

  1. Jagadish Rane, Yuka Kitomi & Kazutoshi Okuno

    Present address: Present addresses: National Institute of Abiotic Stress Management, Malegaon, Baramati, India (J.R.), Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan (Y.K.) and Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan (K. Okuno).,

Authors and Affiliations

  1. National Institute of Agrobiological Sciences (NIAS), Tsukuba, Japan

    Yusaku Uga, Kazuhiko Sugimoto, Naho Hara, Kazuko Ono, Noriko Kanno, Haruhiko Inoue, Hinako Takehisa, Ritsuko Motoyama, Yoshiaki Nagamura, Jianzhong Wu, Takashi Matsumoto, Kazutoshi Okuno & Masahiro Yano

  2. International Center for Tropical Agriculture (CIAT), Cali, Colombia

    Satoshi Ogawa, Jagadish Rane & Manabu Ishitani

  3. Faculty of Science, University of Valle, Cali, Colombia

    Satoshi Ogawa

  4. Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan

    Yuka Kitomi & Yoshiaki Inukai

  5. National Institute of Crop Science, Tsukuba, Japan

    Toshiyuki Takai

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Contributions

Y.U. designed the experiments, cloned the DRO1 gene and wrote the manuscript. Y.U., K.S., Y.K., N.H., H.I., H.T. and R.M. performed molecular analysis of DRO1. Y.U., K. Ono and N.K. generated transgenic plants. J.W. and T.M. performed BAC analysis. Y.U., S.O., J.R. and T.T. performed field experiments. K.S., M.I., Y.I., Y.N., K. Okuno and M.Y. provided advice on the experiments.

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Correspondence to Yusaku Uga.

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Uga, Y., Sugimoto, K., Ogawa, S. et al. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45, 1097–1102 (2013). https://doi.org/10.1038/ng.2725

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