|
Special Issue:
水稻遗传育种Rice Genetics · Breeding · Germplasm Resources
|
|
|
|
| OsDXR interacts with OsMORF1 to regulate chloroplast development and the RNA editing of chloroplast genes in rice |
CAO Peng-hui1*, WANG Di2*, GAO Su3*, LIU Xi3, 4#, QIAO Zhong-ying1, XIE Yu-lin1, DONG Ming-hui1, DU Tan-xiao3, ZHANG Xian3, ZHANG Rui3, JI Jian-hui3, 4#
|
1 Institute of Agricultural Sciences in Taihu Area of Jiangsu, Suzhou 215155, P.R.China
2 Huaiyin Institute of Agricultural Sciences of Xuhuai Region in Jiangsu, Huai’an 223001, P.R.China
3 School of Life Sciences, Huaiyin Normal University, Huai’an 223300, P.R.China
4 Key Laboratory of Eco-Agricultural Biotechnology around Hongze Lake, Regional Cooperative Innovation Center for Modern Agriculture and Environmental Protection, Huaiyin Normal University, Huai’an 223300, P.R.China
|
|
|
|
|
摘要
植物叶绿素生物合成和叶绿体发育是两个受外源和内源因子调控的极其复杂过程。在本研究中，我们鉴定了一个正调控水稻叶绿素生物合成和叶绿体发育的还原异构酶基因OsDXR。OsDXR基因敲除突变体表现为白化致死表型，不能完成整个生命周期。OsDXR在水稻叶片中高表达，亚细胞定位表明OsDXR是一种叶绿体蛋白。与野生型相比，在OsDXR敲除突变体中许多参与叶绿素生物合成和叶绿体发育的基因表达存在差异。我们发现在OsDXR敲除突变体中叶绿体基因ndhA-1019和rpl2-1的RNA编辑效率显著降低。此外，酵母双杂交和双分子荧光互补实验证实，OsDXR与RNA编辑因子OsMORF1有相互作用。我们证实质体2-C-甲基-去甲三醇-4-磷酸途径的破坏导致叶绿体发育和叶绿体基因的RNA编辑存在缺陷。
Abstract
Plant chlorophyll biosynthesis and chloroplast development are two complex processes that are regulated by exogenous and endogenous factors. In this study, we identified OsDXR, a gene encoding a reductoisomerase that positively regulates chlorophyll biosynthesis and chloroplast development in rice. OsDXR knock-out lines displayed the albino phenotype and could not complete the whole life cycle process. OsDXR was highly expressed in rice leaves, and subcellular localization indicated that OsDXR is a chloroplast protein. Many genes involved in chlorophyll biosynthesis and chloroplast development were differentially expressed in the OsDXR knock-out lines compared to the wild type. Moreover, we found that the RNA editing efficiencies of ndhA-1019 and rpl2-1 were significantly reduced in the OsDXR knock-out lines. Furthermore, OsDXR interacted with the RNA editing factor OsMORF1 in a yeast two-hybrid screen and bimolecular fluorescence complementation assay. Finally, disruption of the plastidial 2-C-methyl-derythritol-4-phosphate pathway resulted in defects in chloroplast development and the RNA editing of chloroplast genes.
|
|
Received: 23 November 2022
Accepted: 16 February 2022
|
| Fund:
This study was supported by the Program for Subsidized Project of Suzhou Academy of Agricultural Sciences, China (20028), the Science and Technology Foundation of Suzhou (SNG2020048), the Huaishang Talents, China, the National Natural Science Foundation of China (32070345), the Huai’an Academy of Agricultural Sciences Initiation and Development of Scientific Research Fund for High-level Introduced Talents, China (0062019016B), the Six Talents Summit Project of Jiangsu Province, China (NY-129), and the Natural Science Foundation of Jiangsu Province, China (BK20190239 and BK20180107).
|
| About author: #Correspondence LIU Xi, E-mail: 1240623244@qq.com; JI Jian-hui, E-mail: jijianhui@hytc.edu.cn
* These authors contributed equally to this work. |
Cite this article:
CAO Peng-hui, WANG Di, GAO Su, LIU Xi, QIAO Zhong-ying, XIE Yu-lin, DONG Ming-hui, DU Tan-xiao, ZHANG Xian, ZHANG Rui, JI Jian-hui.
2023.
OsDXR interacts with OsMORF1 to regulate chloroplast development and the RNA editing of chloroplast genes in rice. Journal of Integrative Agriculture, 22(3): 669-678.
|
Barkan A, Goldschmidt-Clermont M. 2000. Participation of nuclear genes in chloroplast gene expression. Biochimie, 82, 559–572.
Carretero-Paulet L, Ahumada I, Cunillera N, Rodríguez-Concepción M, Ferrer A, Boronat A, Campos N. 2002. Expression and molecular analysis of the Arabidopsis DXR gene encoding 1-deoxy-D-xylulose 5-phosphate reductoisomerase, the first committed enzyme of the 2-C-methyl-D-erythritol 4-phosphate pathway. Plant Physiology, 129, 1581–1591.
Chen N, Wang P, Li C, Wang Q, Pan J, Xiao F, Wang Y, Zhang K, Li C, Yang B, Sun C, Deng X. 2018. A single nucleotide mutation of the IspE gene participating in the MEP pathway for isoprenoid biosynthesis causes a green-revertible yellow leaf phenotype in rice. Plant Cell Physiology, 59, 1905–1917.
Cui X, Wang Y, Wu J, Han X, Gu X, Lu T, Zhang Z. 2019. The RNA editing factor DUA1 is crucial to chloroplast development at low temperature in rice. New Phytologist, 221, 834–849.
Dong H, Fei G L, Wu C Y, Wu F Q, Sun Y Y, Chen M J, Ren Y L, Zhou K N, Cheng Z J, Wang J L, Jiang L, Zhang X, Guo X P, Lei C L, Su N, Wang H, Wan J M. 2013. A rice virescent-yellow leaf mutant reveals new insights into the role and assembly of plastid caseinolytic protease in higher plants. Plant Physiology, 162, 1867–1880.
García-Alcázar M, Giménez E, Pineda B, Capel C, García-Sogo B, Sánchez S, Yuste-Lisbona F J, Angosto T, Capel J, Moreno V, Lozano R. 2017. Albino T-DNA tomato mutant reveals a key function of 1-deoxy-D-xylulose-5-phosphate synthase (DXS1) in plant development and survival. Scientific Reports, 7, 45333.
García-Andrade J, Ramírez V, López A, Vera P. 2013. Mediated plastid RNA editing in plant immunity. PLoS Pathogens, 9, e1003713.
Hsieh M H, Chang C Y, Hsu S J, Chen J J. 2008. Chloroplast localization of methylerythritol 4-phosphate pathway enzymes and regulation of mitochondrial genes in ispD and ispE albino mutants in Arabidopsis. Plant Molecular Biology, 66, 663–673.
Hsieh M H, Goodman H M. 2005. The Arabidopsis IspH homolog is involved in the plastid nonmevalonate pathway of isoprenoid biosynthesis. Plant Physiology, 138, 641–653.
Hsieh M H, Goodman H M. 2006. Functional evidence for the involvement of Arabidopsis IspF homolog in the nonmevalonate pathway of plastid isoprenoid biosynthesis. Planta, 223, 779–784.
Huang R, Wang Y, Wang P, Li C, Xiao F, Chen N, Li N, Li C, Sun C, Li L, Chen R, Xu Z, Zhu J, Deng X. 2018. A single nucleotide mutation of IspF gene involved in the MEP pathway for isoprenoid biosynthesis causes yellow-green leaf phenotype in rice. Plant Molecular Biology, 96, 5–16.
Huang W, Zhang Y, Shen L, Fang Q, Liu Q, Gong C, Zhang C, Zhou Y, Mao C, Zhu Y, Zhang J, Chen H, Zhang Y, Lin Y, Bock R, Zhou F. 2020. Accumulation of the RNA polymerase subunit RpoB depends on RNA editing by OsPPR16 and affects chloroplast development during early leaf development in rice. New Phytologist, 228, 1401–1416.
Karcher D, Bock R. 2002. Temperature sensitivity of RNA editing and intron splicing reactions in the plastid ndhB transcript. Current Genetics, 41, 48–52.
Lange B M, Croteau R. 1999. Isoprenoid biosynthesis via a mevalonate-independent pathway in plants: Cloning and heterologous expression of 1-deoxy-D-xylulose-5-phosphate reductoisomerase from peppermint. Archives of Biochemistry and Biophysics, 365, 170–174.
Lin C S, Chen J J W, Chiu C C, Hsiao H C W, Yang C J, Jin X H, Leebens-Mack J, de Pamphilis C W, Huang Y T, Yang L H, Chang W J, Kui L, Wong G K, Hu J M, Wang W, Shih M C. 2017. Concomitant loss of NDH complex-related genes within chloroplast and nuclear genomes in some orchids. Plant Journal, 90, 994–1006.
Liu X, Cao P H, Huang Q Q, Yang Y R, Tao D D. 2020. Disruption of a rice chloroplast-targeted gene OsHMBPP causes a seedling-lethal albino phenotype. Rice, 13, 51.
Liu X, Yi X, Yang Y R, Huang Q Q. 2021. A rice geranylgeranyl reductase is essential for chloroplast development. Journal of Integrative Agriculture, 20, 2592–2600.
Lu Y, Ye X, Guo R, Huang J, Wang W, Tang J Y, Tan L T, Zhu J K, Chu C C, Qian Y W. 2017. Genome-wide targeted mutagenesis in rice using the CRISPR/Cas9 system. Molecular Plant, 10, 1242–1245.
Mahmoud S S, Croteau R B. 2001. Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase. Proceedings of the National Academy of Sciences of the United States of America, 98, 8915–8920.
Nierhaus K H. 1982. Structure, assembly, and function of ribosomes. Current Topics in Microbiology and Immunology, 97, 81–155.
Okada K, Kawaide H, Kuzuyama T, Seto H, Curtis I S, Kamiya Y. 2002. Antisense and chemical suppression of the nonmevalonate pathway affects ent-kaurene biosynthesis in Arabidopsis. Planta, 215, 339–344.
Porra R J, Thompson W A, Kriedemann P E. 1989. 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. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 975, 384–394.
Rodrigues N F, Fonseca G C, Kulcheski F R, Margis R. 2017. Salt stress affects mRNA editing in soybean chloroplasts. Genetics and Molecular Biology, 40, 200–208.
Rodríguez-Concepción M. 2014. Plant isoprenoids: A general overview. Methods in Molecular Biology, 1153, 1–5.
Rohdich F, Kis K, Bacher A, Eisenreich W. 2001. The non-mevalonate pathway of isoprenoids: Genes, enzymes and intermediates. Current Opinion Chemical Biology, 5, 535–540.
Su N, Hu M L, Wu D X, Wu F Q, Fei G L, Lan Y, Chen X L, Shu X L, Zhang X, Guo X P, Cheng Z J, Lei C L, Qi C K, Jiang L, Wang H, Wan J M. 2012. Disruption of a rice pentatricopeptide repeat protein causes a seedling-specific albino phenotype and its utilization to enhance seed purity in hybrid rice production. Plant Physiology, 159, 227–238.
Takenaka M, Zehrmann A, Verbitskiy D, Kugelmann M, Härtel B, Brennicke A. 2012. Multiple organellar RNA editing factor (MORF) family proteins are required for RNA editing in mitochondria and plastids of plants. Proceedings of the National Academy of Sciences of the United States of America, 109, 5104–5109.
Tang J, Zhang W, Wen K, Chen G, Sun J, Tian Y, Tang W, Yu J, An H, Wu T, Kong F, Terzaghi W, Wang C, Wan J M. 2017. OsPPR6, a pentatricopeptide repeat protein involved in editing and splicing chloroplast RNA, is required for chloroplast biogenesis in rice. Plant Molecular Biology, 95, 345–357.
Tarkowská D, Strnad M. 2018. Isoprenoid-derived plant signaling molecules: biosynthesis and biological importance. Planta, 247, 1051–1066.
Waadt R, Schmidt L K, Lohse M, Hashimoto K, Bock R, Kudla J. 2008. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. The Plant Journal, 56, 505–516.
Wang Y, Ren Y, Zhou K, Liu L, Wang J, Xu Y, Zhang H, Zhang L, Feng Z, Wang L, Ma W, Wang Y, Guo X, Zhang, X, Lei C, Cheng Z, Wan J M. 2017. WHITE STRIPE LEAF4 encodes a novel P-type PPR protein required for chloroplast biogenesis during early leaf development. Frontiers in Plant Science, 8, 1116.
Wang Y, Wang Y, Ren Y, Duan E, Zhu X, Hao Y, Zhu J, Chen R, Lei J, Teng X, Zhang Y, Wang D, Zhang X, Guo X, Jiang L, Liu S, Tian Y, Liu X, Chen L, Wang H, Wan J M. 2021. White panicle2 encoding thioredoxin z, regulates plastid RNA editing by interacting with multiple organellar RNA editing factors in rice. New Phytologist, 229, 2693–2706.
Xiao H, Xu Y, Ni C, Zhang Q, Zhong F, Huang J, Liu W, Peng L, Zhu Y, Hu J. 2018. A rice dual-localized pentatricopeptide repeat protein is involved in organellar RNA editing together with OsMORFs. Journal of Experimental Botany, 69, 2923–2936.
Xing S, Miao J, Li S, Qin G, Tang S, Li H, Gu H, Qu L J. 2010. Disruption of the 1-deoxy-D-xylulose-5-phosphate reductoisomerase (DXR) gene results in albino, dwarf and defects in trichome initiation and stomata closure in Arabidopsis. Cell Research, 20, 688–700.
Zhang Q, Shen L, Wang Z, Hu G, Ren D, Hu J, Zhu L, Gao Z, Zhang G, Guo L, Zeng D, Qian Q. 2019. OsCAF1, a CRM domain containing protein, influences chloroplast development. International Journal of Molecular Science, 20, 4386.
Zheng H, Wang Z, Tian Y, Liu L, Lv F, Kong W, Bai W, Wang P, Wang C, Yu X, Liu X, Jiang L, Zhao Z, Wan J M. 2019. Rice albino 1, encoding a glycyl-tRNA synthetase, is involved in chloroplast development and establishment of the plastidic ribosome system in rice. Plant Physiology and Biochemistry, 139, 495–503.
Zeng Z Q, Lin T Z, Zhao J Y, Zheng T H, Xu L F, Wang Y H, Liu L L, Jiang L, Chen S H, Wan J M. 2020. OsHemA gene,encoding glutamyl-trna reductase (GluTR) is essential for chlorophyll biosynthesis in rice (Oryza sativa). Journal of Integrative Agriculture, 19, 612–623.
|
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
