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Identification and fine mapping of lemma-distortion1, a single recessive gene playing an essential role in the development of lemma in rice

Published online by Cambridge University Press:  19 January 2016

D. W. YANG
Affiliation:
Rice Research Institute, Fujian Academy of Agricultural Sciences, Fujian High Quality Rice Research & Development Center, Fuzhou 350019, China
X. F. YE*
Affiliation:
Rice Research Institute, Fujian Academy of Agricultural Sciences, Fujian High Quality Rice Research & Development Center, Fuzhou 350019, China
X. H. ZHENG
Affiliation:
Rice Research Institute, Fujian Academy of Agricultural Sciences, Fujian High Quality Rice Research & Development Center, Fuzhou 350019, China
C. P. CHENG
Affiliation:
Rice Research Institute, Fujian Academy of Agricultural Sciences, Fujian High Quality Rice Research & Development Center, Fuzhou 350019, China
N. YE
Affiliation:
Rice Research Institute, Fujian Academy of Agricultural Sciences, Fujian High Quality Rice Research & Development Center, Fuzhou 350019, China
L. B. LU
Affiliation:
Rice Research Institute, Fujian Academy of Agricultural Sciences, Fujian High Quality Rice Research & Development Center, Fuzhou 350019, China
F. H. HUANG
Affiliation:
Rice Research Institute, Fujian Academy of Agricultural Sciences, Fujian High Quality Rice Research & Development Center, Fuzhou 350019, China
Q. Q. LI*
Affiliation:
Rice Research Institute, Fujian Academy of Agricultural Sciences, Fujian High Quality Rice Research & Development Center, Fuzhou 350019, China
*
*To whom all correspondence should be addressed. Emails: yexinfu@126.com; liqq@xmu.edu.cn
*To whom all correspondence should be addressed. Emails: yexinfu@126.com; liqq@xmu.edu.cn

Summary

Floral organ development influences plant reproduction and crop yield. The mechanism of floral organ specification is generally conserved in angiosperms as demonstrated by the ‘ABC’ model. However, mechanisms underlying the development of floral organs in specific groups of species such as grasses remain unclear. In the genus Oryza (rice), a spikelet consists of a fertile floret sub-tended by a lemma, a palea, two sterile lemmas and rudimentary glumes. To understand how the lemma is formed, a curve-shaped lemma-distortion1 (ld1) mutant was identified. Genetic analysis confirmed that the ld1 mutant phenotype was due to a single recessive gene mutation. Using a large F2 population, the LD1 gene was mapped between markers Indel-7-15 and Indel-7-18, which encompassed a region of 15·6 kilo base pairs (kbp). According to rice genome annotations, two putative genes, LOC_Os07g32510 and LOC_Os07g32520, were located in this candidate region. However, DNA sequencing results indicated only 1 base pair (bp) substitution (T⇨C) was found in LOC_Os07g32510 between the wild-type and the ld1 mutant. Thus LOC_Os07g32510, encoding a DNA binding with one zinc finger (DoF) containing protein, was the candidate gene for LD1. Further analysis showed that mutation of the amino acid cysteine (C) to arginine (R) was likely to lead to zinc finger protein deactivation. Phylogenetic and conservation analysis of the gene from different species revealed that cysteine was critical to LD1 function. As a new gene controlling lemma development, the study of LD1 could provide insights into rice floral organ formation mechanisms.

Type
Crops and Soils Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Bommert, P., Satoh-Nagasawa, N., Jackson, D. & Hirano, H. Y. (2005). Genetics and evolution of inflorescence and flower development in grasses. Plant and Cell Physiology 46, 6978.Google Scholar
Clayton, W. D. & Renvoize, S. A. (1986). Genera Graminum, Grasses of the World. Kew Bulletin Additional Series 13. London: HMSO.Google Scholar
Coen, E. S. & Meyerowitz, E. M. (1991). The war of the whorls: genetic interactions controlling flower development. Nature 353, 3137.Google Scholar
Dreni, L., Jacchia, S., Fornara, F., Fornari, M., Ouwerkerk, P. B., An, G., Colombo, L. & Kater, M. M. (2007). The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice. Plant Journal 52, 690699.Google Scholar
Duan, Y. L., Diao, Z. J., Liu, H. Q., Cai, M. S., Wang, F., Lan, T. & Wu, W. R. (2010). Molecular cloning and functional characterization of OsJAG gene based on a complete-deletion mutant in rice (Oryza sativa L.). Plant Molecular Biology 74, 605615.CrossRefGoogle ScholarPubMed
Duan, Y. L., Xing, Z., Diao, Z. J., Xu, W. Y., Li, S. P., Du, X. Q., Wu, G. H., Wang, C. L., Lan, T., Meng, Z., Liu, H. Q., Wang, F., Wu, W. R. & Xue, Y. B. (2012). Characterization of Osmads6-5, a null allele, reveals that OsMADS6 is a critical regulator for early flower development in rice (Oryza sativa L.). Plant Molecular Biology 80, 429442.CrossRefGoogle Scholar
Feng, M., Fu, D. Z., Liang, H. X. & Lu, A. M. (1995). Floral morphogenesis of Aquilegia L. (Ranunculaceae). Acta Botanica Sinica 37, 791794.Google Scholar
Goff, S. A., Ricke, D., Lan, T. H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., Varma, H., Hadley, D., Hutchison, D., Martin, C., Katagiri, F., Lange, B. M., Moughamer, T., Xia, Y., Budworth, P., Zhong, J., Miguel, T., Paszkowski, U., Zhang, S., Colbert, M., Sun, W. L., Chen, L., Cooper, B., Park, S., Wood, T. C., Mao, L., Quail, P., Wing, R., Dean, R., Yu, Y., Zharkikh, A., Shen, R., Sahasrabudhe, S., Thomas, A., Cannings, R., Gutin, A., Pruss, D., Reid, J., Tavtigian, S., Mitchell, J., Eldredge, G., Scholl, T., Miller, R. M., Bhatnagar, S., Adey, N., Rubano, T., Tusneem, N., Robinson, R., Feldhaus, J., Macalma, T., Oliphant, A. & Briggs, S. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp. Japonica). Science 296, 920–100.Google Scholar
Hou, Y. L., Hong, C. Y. & Chen, K. Y. (2014). Functional characterization of the stunt lemma palea 1 mutant allele in rice. Plant Growth Regulation 73, 257265.Google Scholar
Hu, L. F., Liang, W. Q., Yin, C. S., Cui, X., Zong, J., Wang, X., Hu, J. P. & Zhang, D. B. (2011). Rice MADS3 regulates ROS homeostasis during late anther development. The Plant Cell 23, 515533.CrossRefGoogle ScholarPubMed
Itoh, J. I., Nonomura, K. I., Ikeda, K., Yamaki, S., Inukai, Y., Yamagishi, H., Kitano, H. & Nagato, Y. (2005). Rice plant development: from zygote to spikelet. Plant & Cell Physiology 46, 2347.CrossRefGoogle ScholarPubMed
Jeon, J. S., Jang, S., Lee, S., Nam, J., Kim, C., Lee, S. H., Chung, Y. Y., Kim, S. R., Lee, Y. H., Cho, Y. G. & An, G. (2000). leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. The Plant Cell 12, 871884.Google Scholar
Jin, Y., Luo, Q., Tong, H. N., Wang, A. J., Cheng, Z. J., Tang, J. F., Li, D. Y., Zhao, X. F., Li, X. B., Wan, J. M., Jiao, Y. L., Chu, C. C. & Zhu, L. H. (2011). An AT-hook gene is required for palea formation and floral organ number control in rice. Developmental Biology 359, 277288.CrossRefGoogle ScholarPubMed
Keck, E., McSteen, P., Carpenter, R. & Coen, E. (2003). Separation of genetic functions controlling organ identity in flowers. EMBO Journal 22, 10581066.Google Scholar
Kellogg, E. A. (2009). The evolutionary history of Ehrhartoideae, Oryzeae, and Oryza . Rice 2, 114.Google Scholar
Lancashire, P. D., Bleiholder, H., Van Den Boom, T., Langelüddecke, P., Stauss, R., Weber, E. & Witzenberger, A. (1991). A uniform decimal code for growth stages of crops and weeds. Annals of Applied Biology 119, 561601.Google Scholar
Lander, E. S., Green, P., Abrahamson, J., Barlow, A., Daly, M. J., Lincoln, S. E. & Newberg, L. A. (1987). Mapmaker: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1, 174181.Google Scholar
Liao, L., Shi, C. H., Zeng, D. D., Jin, X. L. & Wu, J. G. (2015). Morphogenesis and molecular basis on the unclosed glumes, a novel mutation related to the floral organ of rice. Plant Molecular Biology Reporter 33, 480489.CrossRefGoogle Scholar
Linder, H. P. & Rudall, P. J. (2005). Evolutionary history of poales. Annual Review of Ecology, Evolution and Systematics 36, 107124.Google Scholar
Liu, H. R. & Meng, J. L. (2003). MapDraw: a Microsoft Excel macro for drawing genetic linkage maps based on given genetic linkage data. Hereditas (Beijing) 25, 317321.Google Scholar
Luo, Q., Zhou, K. D., Zhao, X. F., Zeng, Q. C., Xia, H. G., Zhai, W. X., Xu, J. C., Wu, X. J., Yang, H. S. & Zhu, L. H. (2005). Identification and fine mapping of a mutant gene for palealess spikelet in rice. Planta 221, 222230.CrossRefGoogle ScholarPubMed
Ma, X. D., Cheng, Z. J., Wu, F. Q., Jin, M. G., Zhang, L. G., Zhou, F., Wang, J. L., Zhou, K. N., Ma, J., Lin, Q. B., Lei, C. L. & Wan, J. M. (2013). BEAK LIKE SPIKELET1 is required for lateral development of lemma and palea in rice. Plant Molecular Biology Reporter 31, 98108.Google Scholar
Malcomber, S. T. & Kellogg, E. A. (2004). Heterogeneous expression patterns and separate roles of the SEPALLATA gene LEAFY HULL STERILE1 in grasses. The Plant Cell 16, 16921706.CrossRefGoogle ScholarPubMed
McCouch, S. R., Teytelman, L., Xu, Y. B., Lobos, K. B., Clare, K., Walton, M., Fu, B. Y., Maghirang, R., Li, Z. K., Xing, Y. Z., Zhang, Q. F., Kono, I., Yano, M., Fjellstrom, R., DeClerck, G., Schneider, D., Cartinhour, S., Ware, D. & Stein, L. (2002). Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). DNA Research 9, 199207.Google Scholar
Mizukami, Y. & Ma, H. (1992). Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71, 119131.CrossRefGoogle ScholarPubMed
Murray, M. G. & Thompson, W. F. (1980). Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 43214326.Google Scholar
Nagasawa, N., Miyoshi, M., Sano, Y., Satoh, H., Hirano, H., Sakai, H. & Nagato, Y. (2003). SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130, 705718.CrossRefGoogle ScholarPubMed
Panaud, O., Chen, X. & McCouch, S. R. (1996). Development of microsatellite markers and characterization of simple sequence length polymorphism (SSLP) in rice (Oryza sativa L.). Molecular and General Genetics 252, 597607.Google Scholar
Prasad, K., Parameswaran, S. & Vijayraghavan, U. (2005). OsMADS1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. Plant Journal 43, 915928.Google Scholar
Preston, J. C., Christensen, A., Malcomber, S. T. & Kellogg, E. A. (2009). MADS-box gene expression and implications for developmental origins of the grass spikelet. American Journal of Botany 96, 14191429.Google Scholar
Rahman, M. L., Chu, S. H., Choi, M. S., Qiao, Y. L., Jiang, W. Z., Piao, R. H., Khanam, S., Cho, Y. I., Jeung, J. U., Jena, K. K. & Koh, H. J. (2007). Identification of QTLs for some agronomic traits in rice using an introgression line from Oryza minuta . Molecules and Cells 24, 1626.Google Scholar
Theiβen, G. & Saedler, H. (2001). Plant biology: floral quartets. Nature 409, 469471.Google Scholar
Thompson, B. E. & Hake, S. (2009). Translational biology: from Arabidopsis flowers to grass inflorescence architecture. Plant Physiology 149, 3845.Google Scholar
Whipple, C. J., Ciceri, P., Padilla, C. M., Ambrose, B. A., Bandong, S. L. & Schmidt, R. J. (2004). Conservation of B-class floral homeotic gene function between maize and Arabidopsis . Development 131, 60836091.CrossRefGoogle ScholarPubMed
Xiao, H., Tang, J. F., Li, Y. F., Wang, W. M., Li, X. B., Jin, L., Xie, R. B., Luo, H. F., Zhao, X. F., Meng, Z., He, G. H. & Zhu, L. H. (2009). STAMENLESS 1, encoding a single C2H2 zinc finger protein, regulates floral organ identity in rice. Plant Journal 59, 789801.Google Scholar
Xie, S. Y., Chen, M., Pei, R., Ouyang, Y. & Yao, J. L. (2015). OsEMF2b acts as a regulator of flowering transition and floral organ identity by mediating H3K27me3 deposition at OsLFL1 and OsMADS4 in rice. Plant Molecular Biology Reporter 33, 121132.CrossRefGoogle Scholar
Yamaguchi, T., Nagasawa, N., Kawasaki, S., Matsuoka, M., Nagato, Y. & Hirano, H. Y. (2004). The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa . The Plant Cell 16, 500509.Google Scholar
Yamaguchi, T., Lee, D. Y., Miyao, A., Hirochika, H., An, G. & Hirano, H. Y. (2006). Functional diversification of the two C-class MADS box genes OSMADS 3 and OSMADS 58 in Oryza sativa . The Plant Cell 18, 1528.CrossRefGoogle Scholar
Yanagisawa, M., Liour, S. S. & Yu, R. K. (2004). Involvement of gangliosides in proliferation of immortalized neural progenitor cells. Journal of Neurochemistry 91, 804812.Google Scholar
Yang, D. W., Lu, L. B., Chen, C. P., Zeng, M. J., Zheng, X. H., Ye, N., Liu, C. D. & Ye, X. F. (2012). Morphological characteristics and gene mapping of a palea degradation (pd2) mutant in rice. Hereditas (Beijing) 34, 10641072 (in Chinese with English summary).Google Scholar
Yoshida, A., Suzaki, T., Tanaka, W. & Hirano, H. Y. (2009). The homeotic gene long sterile lemma (G1) specifies sterile lemma identity in the rice spikelet. Proceedings of the National Academy of Sciences of the United States of America 106, 2010320108.Google Scholar
Yu, J., Hu, S. N., Wang, J., Wong, G. K. S., Li, S. G., Liu, B., Deng, Y. J., Dai, L., Zhou, Y., Zhang, X. Q., Cao, M. L., Liu, J., Sun, J. D., Tang, J. B., Chen, Y. J., Huang, X. B., Lin, W., Ye, C., Tong, W., Cong, L. J., Geng, J. N., Han, Y. J., Li, L., Li, W., Hu, G. Q., Huang, X. G., Li, W. J., Li, J., Liu, Z. W., Li, L., Liu, J. P., Qi, Q. H., Liu, J. S., Li, L., Li, T., Wang, X. G., Lu, H., Wu, T. T., Zhu, M., Ni, P. X., Han, H., Dong, W., Ren, X. Y., Feng, X. L., Cui, P., Li, X. R., Wang, H., Xu, X., Zhai, W. X., Xu, Z., Zhang, J. S., He, S. J., Zhang, J. G., Xu, J. C., Zhang, K. L., Zheng, X. W., Dong, J. H., Zeng, W. Y., Tao, L., Ye, J., Tan, J., Ren, X. D., Chen, X. W., He, J., Liu, D. F., Tian, W., Tian, C. G., Xia, H. G., Bao, Q. Y., Li, G., Gao, H., Cao, T., Wang, J., Zhao, W. M., Li, P., Chen, W., Wang, X. D., Zhang, Y., Hu, J. F., Wang, J., Liu, S., Yang, J., Zhang, G. Y., Xiong, Y. Q., Li, Z. J., Mao, L., Zhou, C. S., Zhu, Z., Chen, R. S., Hao, B. L., Zheng, W. M., Chen, S. Y., Guo, W., Li, G. J., Liu, S. Q., Tao, M., Wang, J., Zhu, L. H., Yuan, L. P. & Yang, H. M. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296, 7992.CrossRefGoogle ScholarPubMed
Yuan, Z., Gao, S., Xue, D. W., Luo, D., Li, L. T., Ding, S. Y., Yao, X., Wilson, Z. A., Qian, Q. & Zhang, D. B. (2009). RETARDED PALEA 1 controls palea development and floral zygomorphy in rice. Plant Physiology 149, 235244.Google Scholar