A natural variant of NAL1, selected in high-yield rice breeding programs, pleiotropically increases photosynthesis rate

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Takai, Toshiyuki ^a,c   Adachi, Shunsuke ^b,c   Taguchi Shiobara, Fumio ^c   Sanoh Arai, Yumiko ^a   Iwasawa, Norio ^a   Yoshinaga, Satoshi ^a   Hirose, Sakiko ^a   Taniguchi, Yojiro ^a   Yamanouchi, Utako ^c   Wu, Jianzhong ^c   Matsumoto, Takashi ^c   Sugimoto, Kazuhiko ^c   Kondo, Katsuhiko ^c   Ikka, Takashi ^c   Ando, Tsuyu ^d   Kono, Izumi ^d   Ito, Sachie ^d   Shomura, Ayahiko ^d   Ookawa, Taiichiro ^b   Hirasawa, Tadashi ^b   Yano, Masahiro ^c   Kondo, Motohiko ^a   Yamamoto, Toshio ^c   more..

^a NATIONAL INSTITUTE OF CROP SCIENCE   (Japan)

^b TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^c NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^d NATIONAL VETERINARY ASSAY LABORATORY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE;

ALLELE; ARTICLE; BREEDING; CHROMOSOME MAP; GENE EXPRESSION REGULATION; GENE ORDER; GENETICS; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; MOLECULAR CLONING; PHENOTYPE; PHOTOSYNTHESIS; PLANT LEAF; QUANTITATIVE TRAIT LOCUS; RICE; SUNLIGHT;

ALLELES; BREEDING; CARBON DIOXIDE; CHROMOSOME MAPPING; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENE ORDER; KINETICS; ORYZA SATIVA; PHENOTYPE; PHOTOSYNTHESIS; PLANT LEAVES; QUANTITATIVE TRAIT LOCI; SUNLIGHT;

EID: 84893846644     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep02149     Document Type: Article

References (60)

1. Hargrove, T. R. & Cabanilla, V. L. The impact of semidwarf varieties on Asian rice-breeding programs. Bioscience 29, 731-735 (1979).
2. Khush, G. S. Green revolution: the way forward. Nat. Rev. Genet. 2, 815-822 (2001).
3. Tester, M. & Langridge, P. Breeding technologies to increase crop production in a changing world. Science 327, 818-822 (2010).
4. Foley, J. A. et al. Solutions for a cultivated planet. Nature 478, 337-342 (2011).
5. Ashikari, M. et al. Cytokinin oxidase regulates rice grain production. Science 309, 741-745 (2005).
6. Terao, T., Nagata, K., Morino, K. & Hirose, T. A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice. Theor. Appl. Genet. 120, 875-893 (2010).
7. Miura, K. et al. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545-549 (2010).
8. Song, X. J., Huang, W., Shi, M., Zhu, M. Z. & Lin, H. X. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39, 623-630 (2007).
9. Fan, C. et al. GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor. Appl. Genet. 112, 1164-1171 (2006).
10. Shomura, A. et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nat. Genet. 40, 1023-1028 (2008).
11. Li, Y. et al. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat. Genet. 43, 1266-1269 (2011).
12. Ohsumi, A. et al. Evaluation of yield performance in rice near-isogenic lines with increased spikelet number. Field Crops Res. 120, 68-75 (2011).
13. Yoshida, H., Horie, T. & Shiraiwa, T. A model for explaining genotypic and environmental variation in vegetative biomass growth in rice based on observed LAI and leaf nitrogen content. Field Crops Res. 108, 222-230 (2008).
14. Yoshida, H. & Horie, T. A process model for explaining genotypic and environmental variation in growth and yield of rice based on measured plant N accumulation. Field Crops Res. 113, 227-237 (2009).
15. Sasaki, H. & Ishii, R. Cultivar differences in leaf photosynthesis of rice bred in Japan. Photosynthesis Res. 32, 139-146 (1992).
16. Hubbart, S., Peng, S., Horton, P., Chen, Y. & Murchie, E. H. Trends in leaf photosynthesis in historical rice varieties developed in the Philippines since 1966. J. Exp. Bot. 58, 3429-3438 (2007).
17. Farquhar, G. D. & Sharkey, T. D. Stomatal conductance and photosynthesis. Annu. Rev. Plant Physiol. 33, 317-345 (1982).
18. Lambers, H., Chapin III, F. S. & Pons, T. L. Plant Physiological Ecology. (Springer Verlag, 1998).
19. 3 plants. Oecologia 78, 9-19 (1989).
20. Makino, A. Rubisco and nitrogen relationships in rice: Leaf photosynthesis and plant growth. Soil Sci. Plant Nutr. 49, 319-327 (2003).
21. Kanemura, T., Homma, K., Ohsumi, A., Shiraiwa, T. & Horie, T. Evaluation of genotypic variation in leaf photosynthetic rate and its associated factors by using rice diversity research set of germplasm. Photosynthesis Res. 94, 23-30 (2007).
22. Ohsumi, A. et al. A model explaining genotypic and ontogenetic variation of leaf photosynthetic rate in rice (Oryza sativa) based on leaf nitrogen content and stomatal conductance. Ann. Bot. 99, 265-273 (2007).
23. Xing, Y. Z. & Zhang, Q. F. Genetic and molecular bases of rice yield. Annu. Rev. Plant Biol. 61, 421-442 (2010).
24. Flood, P. J., Harbinson, J. & Aarts, M. G. Natural genetic variation in plant photosynthesis. Trends Plant Sci. 16, 327-335 (2011).
25. Taylaran, R. D., Adachi, S., Ookawa, T., Usuda, H. & Hirasawa, T. Hydraulic conductance as well as nitrogen accumulation plays a role in the higher rate of leaf photosynthesis of the most productive variety of rice in Japan. J. Exp. Bot. 62, 4067-4077.
26. Takai, T. et al. Comparative mapping suggests repeated selection of the same quantitative trait locus for high leaf photosynthesis rate in rice high-yield breeding programs. Crop Sci. 52, 2649-2658 (2012).
27. Takai, T., Kondo, M., Yano, M. & Yamamoto, T. A quantitative trait locus for chlorophyll content and its association with leaf photosynthesis in rice. Rice 3, 172-180 (2010).
28. Adachi, S. et al. Identification and characterization of genomic regions on chromosomes 4 and 8 that control the rate of photosynthesis in rice leaves. J. Exp. Bot. 62, 1927-1938 (2011).
29. 3 species. Planta 149, 78-90 (1980).
30. Rice Annotation Project. The Rice Annotation Project Database (RAP-DB): 2008 update. Nucleic Acids Res. 36, D1028-1033 (2008).
31. Yamamoto, T. et al. Fine definition of the pedigree haplotypes of closely related rice cultivars by means of genome-wide discovery of single-nucleotide polymorphisms. BMC Genomics 11, 267 (2010).
32. Qi, J. et al. Mutation of the rice Narrow leaf1 gene, which encodes a novel protein, affects vein patterning and polar auxin transport. Plant Physiol. 147, 1947-1959 (2008).
33. Chen, M. et al. Fine mapping of a major QTL for flag leaf width in rice, qFLW4, which might be caused by alternative splicing of NAL1. Plant Cell Rep. 31, 863-872 (2011).
34. Boardman, N. K. Comparative photosynthesisofsun and shade plants. Annu. Rev. Plant Physiol. 28, 355-377 (1977).
35. Niinemets, U. Components of leaf dry mass per area - thickness and density - alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol. 144, 35-47 (1999).
36. Vile, D. et al. Specific leaf area and dry matter content estimate thickness in laminar leaves. Ann. Bot. 96, 1129-1136 (2005).
37. Chung, G. S. & Heu, M. H. Innovative Approaches to Rice Breeding, 135-152 (IRRI, 1980).
38. Ishihara, K. & Saito, K. Diurnal courses of photosynthesis, transpiration, and diffusive conductance in the single-leaf of the rice plants grown in the paddy field under submerged condition. Japan. J. Crop Sci. 56, 8-17 (1987).
39. 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).
40. Ishikawa, C., Hatanaka, T., Misoo, S., Miyake, C. & Fukayama, H. Functional incorporation of sorghum small subunit increases the catalytic turnover rate of Rubisco in transgenic rice. Plant Physiol. 156, 1603-1611 (2011).
41. 4 catalytic switch that increases ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) carboxylation rate in Flaveria. Proc. Natl. Acad. Sci. USA 108, 14688-14693 (2011).
42. Yamori, W., Masumoto, C., Fukayama, H. & Makino, A. Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthesis at high temperature. Plant J. 71, 871-880 (2012).
43. 2 diffusion. J. Exp. Bot. 57, 343-354 (2006).
44. Pearce, R. B., and Carlson., G. E., Barnes, D. K., Hart, R. H. & Hanson, C. H. Specific leaf weight and photosynthesis in Alfalfa. Crop Sci. 9, 423-426 (1969).
45. Masle, J., Gilmore, S. R. & Farquhar, G. D. The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436, 866-870 (2005).
46. Torii, K. U. et al. The arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8, 735-746 (1996).
47. Smillie, I. R., Pyke, K. A. & Murchie, E. H. Variation in vein density and mesophyll cell architecture in a rice deletion mutant population. J. Exp. Bot. 63, 4563-4570 (2012).
48. Smillie, I. R. A. Analysis of leaf morphology and photosynthesis in deletion mutants of rice (Oryza sativa L.) Ph.D. thesis available at http://etheses.nottingham.ac.uk/2569/ (University of Nottingham, 2012).
49. Takeda, S. & Matsuoka, M. Genetic approaches tocrop improvement: responding to environmental and population changes. Nat. Rev. Genet. 9, 444-457 (2008).
50. Ikeda-Kawakatsu, K. et al. Expression level of ABERRANT PANICLE ORGANIZATION1 determines rice inflorescence form through control of cell proliferation in the meristem. Plant Physiol. 150, 736-747 (2009).
51. Ookawa, T. et al. New approach for rice improvement using a pleiotropic QTL gene for lodging resistance and yield. Nat. Commun. 1, 132 (2010).
52. Sasaki, A. et al. A mutant gibberellin-synthesis gene in rice. Nature 416, 701-702 (2002).
53. Peng, S., and Cassman., K. G., Virmani, S. S., Sheehy, J. & Khush, G. S. Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential. Crop Sci. 39, 1552-1559 (1999).
54. Lander, E. S. et al. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1, 174-181 (1987).
55. QTL Cartographer. Version 1.16. A Reference Manual and Tutorial for QTL Mapping (North Carolina State University, 2002).
56. Bernacchi, C. J., and Singsaas., E. L., Pimentel, C., Portis, J. R. & Long, S. P. Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ. 24, 253-259 (2001).
57. Porra, R. J., Thompson, W. A. & Kriedemann, P. E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384-394 (1989).
58. Kuroda, M., Kimizu, M. & Mikami, C.A simple set of plasmids for the production of transgenic plants. Biosci. Biotechnol. Biochem. 74, 2348-2351 (2010).
59. Ozawa, K. Establishment of a high efficiency Agrobacterium-mediated transformation system of rice (Oryza sativa L.). Plant Sci. 176, 522-527 (2009).
60. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 (1976).