Recent amplification of Osr4 LTR-retrotransposon caused rice D1 gene mutation and dwarf phenotype

doi:10.1016/j.pld.2017.01.003

Plant Diversity ›› 2017, Vol. 39 ›› Issue (02): 73-79.DOI: 10.1016/j.pld.2017.01.003

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Recent amplification of Osr4 LTR-retrotransposon caused rice D1 gene mutation and dwarf phenotype

Jie Chen^a,b, Hong Zhao^b, Xiujuan Zheng^a,b, Kangjing Liang^a,b, Yuchun Guo^a,b, Xinli Sun^a,b

a. Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Agriculture & Forestry University, Fuzhou, 350002, China;
b. College of Crop Science, Fujian Agriculture & Forestry University, Fuzhou, 350002, China

Received:2016-09-18 Revised:2017-01-19 Online:2021-11-05 Published:2017-04-25
Contact: Xinli Sun
Supported by:
This work was supported by National and Fujian Provincial Natural Science Foundation (No. 31371557 and K55NI921A), and Fujian Provincial Department of Education Project (K58MLV03A) and a startup fund from Fujian Agriculture and Forestry University (http://www.fafu.edu.cn/) to X.S.

Recent amplification of Osr4 LTR-retrotransposon caused rice D1 gene mutation and dwarf phenotype

Jie Chen^a,b, Hong Zhao^b, Xiujuan Zheng^a,b, Kangjing Liang^a,b, Yuchun Guo^a,b, Xinli Sun^a,b

a. Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Agriculture & Forestry University, Fuzhou, 350002, China;
b. College of Crop Science, Fujian Agriculture & Forestry University, Fuzhou, 350002, China

通讯作者: Xinli Sun
基金资助:
This work was supported by National and Fujian Provincial Natural Science Foundation (No. 31371557 and K55NI921A), and Fujian Provincial Department of Education Project (K58MLV03A) and a startup fund from Fujian Agriculture and Forestry University (http://www.fafu.edu.cn/) to X.S.

Abstract

Abstract: A novel rice d1 mutant was identified using map-based cloning and comparative analysis of known d1 mutants. The mutant (d1-a) shows a mild dwarf trait, which differs only slightly from the wildtype in plant height at the tillering stage. The d1-a mutant is different from other d1 mutants. We found that it was interrupted by an Osr4 long terminal repeat (LTR)-retrotransposon, which resulted in the loss of exon 7 in the mutant D1 mRNA. A paralog of the D1 gene, D1-like, was revealed. D1-like is a truncated gene that might have resulted from recombination between retrotransposons. We identified 65 Osr4 LTR-retrotransposons in Nipponbare, and found more LTR variants in contrast to coding DNA sequence (CDS) in the retrotransposons. We also identified five possible regulatory motifs in LTRs which may control the expression of the retrotransposons. In addition, we predicted six putative functional Osr4 retrotransposons that contain complete CDSs and all important elements. Osr4 retrotransposons were classified into 4 groups, and this type of retrotransposon only appears to be present in monocots. Members of group I-1, which included all putative functional retrotransposons, showed a high similarity with each other. The retrotransposons were expressed in all tissues, at especially higher levels in some leaves and seeds. These findings imply that transpositions of group I-1 members might have occurred frequently and recently.

Key words: Rice, Dwarf, Osr4 retrotransposon, D1 gene

摘要： A novel rice d1 mutant was identified using map-based cloning and comparative analysis of known d1 mutants. The mutant (d1-a) shows a mild dwarf trait, which differs only slightly from the wildtype in plant height at the tillering stage. The d1-a mutant is different from other d1 mutants. We found that it was interrupted by an Osr4 long terminal repeat (LTR)-retrotransposon, which resulted in the loss of exon 7 in the mutant D1 mRNA. A paralog of the D1 gene, D1-like, was revealed. D1-like is a truncated gene that might have resulted from recombination between retrotransposons. We identified 65 Osr4 LTR-retrotransposons in Nipponbare, and found more LTR variants in contrast to coding DNA sequence (CDS) in the retrotransposons. We also identified five possible regulatory motifs in LTRs which may control the expression of the retrotransposons. In addition, we predicted six putative functional Osr4 retrotransposons that contain complete CDSs and all important elements. Osr4 retrotransposons were classified into 4 groups, and this type of retrotransposon only appears to be present in monocots. Members of group I-1, which included all putative functional retrotransposons, showed a high similarity with each other. The retrotransposons were expressed in all tissues, at especially higher levels in some leaves and seeds. These findings imply that transpositions of group I-1 members might have occurred frequently and recently.

关键词: Rice, Dwarf, Osr4 retrotransposon, D1 gene

Jie Chen, Hong Zhao, Xiujuan Zheng, Kangjing Liang, Yuchun Guo, Xinli Sun. Recent amplification of Osr4 LTR-retrotransposon caused rice D1 gene mutation and dwarf phenotype[J]. Plant Diversity, 2017, 39(02): 73-79.

References

Ashikari, M., Wu, J., Yano, M., Sasaki, T., Yoshimura, A., 1999. Rice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the alpha-subunit of GTP-binding protein. Proc. Natl. Acad. Sci. U.S.A. 96. 10284-10289.
Bilgin, D.D., DeLucia, E.H., Clough, S.J., 2009. A robust plant RNA isolation method suitable for Affymetrix GeneChip analysis and quantitative real-time RT-PCR. Nat. Protoc. 4. 333-340.
Chen, H.-X., Zhou, C.-B., Xing, Y.-Z., 2011. A new rice dwarf1 mutant caused by a frame-shift mutation. Hered. (Beijing) 33. 397-403.
Daviere, J.M., Achard, P., 2013. Gibberellin signaling in plants. Development 140. 1147-1151.
Dhadi, S.R., Xu, Z., Shaik, R., Driscoll, K., Ramakrishna, W., 2015. Differential regulation of genes by retrotransposons in rice promoters. Plant Mol. Biol. 87. 603-613.
Fujisawa, Y., Kato, H., Iwasaki, Y., 2001. Structure and function of heterotrimeric G proteins in plants. Plant Cell Physiol. 42. 789-794.
Fujisawa, Y., Kato, T., Ohki, S., Ishikawa, A., Kitano, H., Sasaki, T., Asahi, T., Iwasaki, Y., 1999. Suppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice. Proc. Natl. Acad. Sci. U.S.A. 96. 7575-7580.
Grandbastien, M.A., 2015. LTR retrotransposons, handy hitchhikers of plant regulation and stress response. Biochim. Biophys. Acta 1849. 403-416.
Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H., Kanda, M., 1996. Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Natl. Acad. Sci. U.S.A. 93. 7783-7788.
Ishikawa, A., Tsubouchi, H., Iwasaki, Y., Asahi, T., 1995. Molecular cloning and characterization of a cDNA for the alpha subunit of a G protein from rice. Plant Cell Physiol. 36. 353-359.
Kimple, R.J., Kimple, M.E., Betts, L., Sondek, J., Siderovski, D.P., 2002. Structural determinants for GoLoco-induced inhibition of nucleotide release by Galpha subunits. Nature 416. 878-881.
Kumar, A., Bennetzen, J.L., 1999. Plant retrotransposons. Annu. Rev. Genet. 33. 479-532.
Ma, J., Devos, K.M., Bennetzen, J.L., 2004. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res. 14. 860-869.
McCarthy, E.M., Liu, J., Lizhi, G., McDonald, J.F., 2002. Long terminal repeat retrotransposons of Oryza sativa. Genome Biol. 3. 1-11.
Michelmore, R.W., Paran, I., Kesseli, R.V., 1991. Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl. Acad. Sci. U.S.A. 88. 9828-9832.
Miura, K., Agetsuma, M., Kitano, H., Yoshimura, A., Matsuoka, M., Jacobsen, S.E., Ashikari, M., 2009. A metastable DWARF1 epigenetic mutant affecting plant stature in rice. Proc. Natl. Acad. Sci. U.S.A. 106. 11218-11223.
Oki, K., Kitagawa, K., Fujisawa, Y., Kato, H., Iwasaki, Y., 2009. Function of alpha subunit of heterotrimeric G protein in brassinosteroid response of rice plants. Plant Signal Behav. 4. 126-128.
Oki, K., Inaba, N., Kitano, H., Takahashi, S., Fujisawa, Y., Kato, H., Iwasaki, Y., 2009. Study of novel d1 alleles, defective mutants of the alpha subunit of heterotrimeric G-protein in rice. Genes Genet. Syst. 84. 35-42.
Oki, K., Inaba, N., Kitagawa, K., Fujioka, S., Kitano, H., Fujisawa, Y., Kato, H., Iwasaki, Y., 2009. Function of the alpha subunit of rice heterotrimeric G protein in brassinosteroid signaling. Plant Cell Physiol. 50. 161-172.
Suharsono, U., Fujisawa, Y., Kawasaki, T., Iwasaki, Y., Satoh, H., Shimamoto, K., 2002. The heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proc. Natl. Acad. Sci. U.S.A. 99. 13307-13312.
Takeda, S., Sugimoto, K., Otsuki, H., Hirochika, H., 1999. A 13-bp cis-regulatory element in the LTR promoter of the tobacco retrotransposon Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. Plant J. 18. 383-393.
Ueguchi-Tanaka, M., Fujisawa, Y., Kobayashi, M., Ashikari, M., Iwasaki, Y., Kitano, H., Matsuoka, M., 2000. Rice dwarf mutant d1, which is defective in the alpha subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc. Natl. Acad. Sci. U.S.A. 97. 11638-11643.
Urano, D., Jones, A.M., 2014. Heterotrimeric G protein-coupled signaling in plants. Annu. Rev. Plant Biol. 65. 365-384.
Vitte, C., Panaud, O., Quesneville, H., 2007. LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics 8. 218.
Waldie, T., McCulloch, H., Leyser, O., 2014. Strigolactones and the control of plant development: lessons from shoot branching. Plant J. 79. 607-622.
Wang, Z., Ye, S., Li, J., Zheng, B., Bao, M., Ning, G., 2011. Fusion primer and nested integrated PCR (FPNI-PCR): a new high-efficiency strategy for rapid chromosome walking or flanking sequence cloning. BMC Biotechnol. 11. 109.
Zhang, C., Bai, M.Y., Chong, K., 2014. Brassinosteroid-mediated regulation of agronomic traits in rice. Plant Cell Rep. 33. 683-696.
Zheng, K., Subudhi, P.K., Domingo, J., Maopantay, G., Huang, N., 1995. Rapid DNA isolation for marker assisted selection in rice breeding. Rice Genet. Newslett. 12. 48.

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Recent amplification of Osr4 LTR-retrotransposon caused rice D1 gene mutation and dwarf phenotype

Recent amplification of Osr4 LTR-retrotransposon caused rice D1 gene mutation and dwarf phenotype

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