Abstract
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Breakage of the tight linkage between rice seed lipoxygenase - 3 and easy preharvest sprouting trait led to breeding of lines with few stale flavors after long storage and desirable preharvest sprouting resistance.
Abstract
Lipoxygenase-3 (LOX-3) is involved in the production of volatile constituents in stored rice, and the development of stale flavor is delayed in LOX-3 null rice. In the process of breeding new LOX-3-null lines with long storability, we found a close association between LOX-3 and preharvest sprouting resistance. To determine whether this relationship was due to the tight linkage of two genes or the pleiotropic effect of LOX-3, we performed marker-assisted selection using a BC3F3 population derived from crosses between LOX-3-present/preharvest sprouting-resistant lines and LOX-3-null/preharvest susceptible lines. In one individual, a recombination event occurred 13 kb downstream of LOX-3 (RM15750) and a significant quantitative trait locus, namely qPHS3, for easy preharvest sprouting trait (LOD = 10.4) was detected in an 842-kb region between RM15711 and RM15768. Using BC3F4 and BC3F5 populations, we succeeded in selecting LOX-3-absent and preharvest sprouting-resistant lines with only a 393-kb introgressed chromosome segment from the donor line for LOX-3-null at the LOX-3 locus on chromosome 3. This result indicated that the LOX-3 gene and the locus affecting preharvest sprouting are distinct. The selected line was named ‘Hokuriku 244’. Sensory testing of rice grains with and without LOX-3 confirmed that stale flavor production in LOX-3-null rice during storage was lower than in normal LOX-3 rice. These results indicated that rice varieties with little stale flavor after long storage and preharvest sprouting resistance had been selected.
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References
Dong Y, Tsuzuki E, Kamiunten H, Terao H, Lin D, Matsuo M, Zheng Y (2003) Identification of quantitative trait loci associated with pre-harvest sprouting resistance in rice (Oryza sativa L.). Field Crops Res 81:133–139
Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297
Frank G, Millar AA, Jacobsen JV (2005) Dormancy release, ABA and pre-harvest sprouting. Curr Opin Plant Biol 8:183–187
Gardner HW (1988) Lipoxygenase pathway in cereals. Adv Cereal Sci Technol 9:161–215
Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJJ (2012) Molecular mechanism of seed dormancy. Plant Cell Environ 35:1769–1786
Groos C, Gay G, Perretant M-R, Gervais L, Bernard M, Dedryver F, Charmet G (2002) Study of the relationship between pre-harvest sprouting and grain color by quantitative trait loci analysis in a white × red grain bread-wheat cross. Theor Appl Genet 104:39–47
Gu XY, Foley ME, Horvath DP, Anderson JV, Feng J, Zhang L, Mowry CR, Ye H, Suttle JC, Kadowaki K, Chen Z (2011) Association between seed dormancy and pericarp color is controlled by a pleiotropic gene that regulates abscisic acid and flavonoid synthesis in weedy red rice. Genetics 189:1515–1524
Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54
Horiuchi H (1996) Sprouting. In: Yamamoto T, Horisue N, Ikeda R (eds) Rice breeding manual. Yokendo, Tokyo, pp 147–150 (in Japanese)
Ida S, Masaki Y, Morita Y (1983) The isolation of multiple forms and product specificity of rice lipoxygenase. Agric Biol Chem 47:637–641
Ideta O, Kono I, Takeuchi Y, Hirabayashi H, Hirayama M, Ohta H, Sato H, Ando I, Kato H, Nemoto H, Yano M, Imbe T, Yamasaki M, Yoshida T (2012) Diversity and relationships between coefficient of parentage and genetic distance estimated by SSR markers in Japanese rice cultivars. Breed Res 14:106–113
International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:4
Lincoln SE, Daly MJ, Lander ES (1993) Constructing genetic linkage maps with MAPMAKER, version 3: a tutorial and reference manual. Whitehead Institute for Biomedical Research, Cambridge
McCouch SR, CGSNL (Committee on Gene Symbolization, Nomenclature and Linkage, Rice Genetics Cooperative) (2008) Gene nomenclature system for rice. Rice 1:72–84
McCouch SR, McNally KL, Wang W, Hamilton RS (2012) Genomics of gene banks: a case study in rice. Am J Bot 99:407–423
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T, Utsugi S, Ogawa T, Handa H, Ishida H, Mori M, Kawaura K, Ogihara Y, Miura H (2011) A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell 23:3215–3229
Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, Wakimoto H, Yang CC, Iwamoto M, Abe T, Yamada Y, Muto A, Inokuchi H, Ikemura T, Matsumoto T, Sasaki T, Itoh T (2013) Rice Annotation Project Database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54:e6
Sato Y, Antonio BA, Namiki N, Takehisa H, Minami H, Kamatsuki K, Sugimoto K, Shimizu Y, Hirochika H, Nagamura Y (2011) RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucleic Acids Res 39:D1141–D1148
Shirasawa K, Takeuchi Y, Ebitani T, Suzuki Y (2008) Identification of gene for rice (Oryza sativa) seed lipoxygenase-3 involved in the generation of stale flavor and development of SNP markers for lipoxygenase-3 deficiency. Breed Sci 58:169–176
Sugimoto K, Marzougi S, Yano M (2009) Genetic control of seed dormancy in rice. Gamma Field Symp 48:53–60
Sugimoto K, Takeuchi Y, Ebana K, Miyao A, Hirochika H, Hara N, Ishiyama K, Kobayashi M, Ban Y, Hattori T, Yano M (2010) Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. Proc Natl Acad Sci USA 107:5792–5797
Suzuki Y (1995) Screening and mode of inheritance of a rice variety lacking lipoxygenase-3. Gamma Field Symp 33:51–62
Suzuki Y (2011) Isolation and characterization of a rice (Oryza sativa L.) Mutant deficient in seed phospholipase D, an enzyme involved in the degradation of oil-body membranes. Crop Sci 51:567–573
Suzuki Y, Nagamine T, Kobayashi A, Ohtsubo K (1993) Detection of a new rice variety lacking lipoxygenase-3 by monoclonal antibodies. Japan J Breed 43:405–409
Suzuki Y, Nagamine T, Okuno K (1996a) Genetic analysis of a null-allele for lipoxygenase-3 in rice seeds. Euphytica 91:99–101
Suzuki Y, Yasui T, Matsukura U, Terao J (1996b) Oxidative stability of bran lipids from rice variety [Oryza sativa (L.)] lacking lipoxygenase-3 in seeds. J Agric Food Chem 44:3479–3483
Suzuki Y, Ise K, Li C, Honda I, Iwai Y, Matsukura U (1999) Volatile components in stored rice [Oryza sativa (L.)] of varieties with and without lipoxygenase-3 in seeds. J Agric Food Chem 47:1119–1124
Suzuki Y, Ise K, Nagamine T (2000) Geographical variation of the gene (lox-3 (t)), causing lipoxygenase-3 deficiency in Asian rice varieties. Rice Genet Newslett 17:13–14
Suzuki M, Latshaw S, Sato Y, Settles AM, Koch KE, Hannah LC, Kojima M, Sakakibara H, McCarty DR (2008) The maize viviparous8 locus, encoding a putative ALTERED MERISTEM PROGRAM1-like peptidase, regulates abscisic acid accumulation and coordinates embryo and endosperm development. Plant Physiol 146:1193–1206
Suzuki Y, Takeuchi Y, Shirasawa K (2011) Identification of a seed phospholipase D null allee in rice (Oryza sativa L.) and development of SNP markers for phospholipase D deficiency. Crop Sci 51:2113–2118
Takahashi N (1997) Inheritance of seed germination and dormancy. In: Science of the rice plant. 3. Genetics. Food and Agriculture Policy Research Center, Tokyo, pp 348–359
Takano K (1993) Advances in cereal chemistry and technology in Japan. Cereal Foods World 38:695–698
Tsugita T, Ohta T, Kato H (1983) Cooking flavor and texture of rice stored under different conditions. Agric Biol Chem 47:543–549
Wang S, Basten C, Zeng Z (2007) Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh
Yamamoto A, Fujii Y, Yasumoto K, Mitsuda H (1980) Product specificity of rice germ lipoxygenase. Lipids 15:1–5
Yasumatsu K, Moritaka S (1964) Fatty acid compositions of rice lipid and their changes during storage. Agric Biol Chem 28:257–264
Zhou Z, Robards K, Helliwella S, Blanchard C (2002) Ageing of stored rice: changes in chemical and physical attributes. J Cereal Sci 35:65–78
Acknowledgments
We thank Ms. Chika Hashimoto and Sumiko Sakurai for technical assistance, Dr. Tsuyu Ando of the STAFF Institute for genotyping and Dr. Ikuo Ashikawa (NARO Inst. Crop Sci.) for helpful discussions of an early version of this manuscript. This work was supported in part by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (the research project; Development of New rice Varieties using Genomic Breeding Technology). We would like to thank Enago (www.enago.jp) for the English language review.
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Communicated by L. Xiong.
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Suzuki, Y., Miura, K., Shigemune, A. et al. Marker-assisted breeding of a LOX-3-null rice line with improved storability and resistance to preharvest sprouting. Theor Appl Genet 128, 1421–1430 (2015). https://doi.org/10.1007/s00122-015-2516-y
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DOI: https://doi.org/10.1007/s00122-015-2516-y