Abstract
Chlorophyll is an important photosynthetic pigment in the process of photosynthesis in plants and photosynthetic bacteria. Genes involved in chlorophyll biosynthesis in Arabidopsis and photosynthetic bacteria have been well documented. In rice, however, these genes have not been fully annotated. In this paper, a yellow-green leaf gene, yellow green leaf3 (ygl3) was cloned and analyzed. ygl3 encodes magnesium chelation ChlD (D) subunit, a key enzyme for chlorophyll synthesis, resulting in a yellow-green leaf phenotype in all growth stages in rice. Expression content of ygl3 is highest in the leaf blades, followed by the leaf sheaths, while there is virtually no expression of the gene in the stems and seeds. The sub-cellular structure and protein content of the photosynthetic system of the ygl3 mutant were revealed by transmission electron microscopy, BN-PAGE, and western blotting. The results show that the mutation of the ygl3 gene indirectly leads to a decrease in the protein content of the photosynthetic system and severely obstructs the formation of granum thylakoids.
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Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace, a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201
Bollivar DW (2006) Recent advances in chlorophyll biosynthesis. Photosynth Res 90:173–194
Cazzonelli CI, Pogson BJ (2010) Source to sink, regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15:266–274
Davison PA, Schubert HL, Reid JD, Iorg CD, Heroux A, Hill CP, Hunter CN (2005) Structural and biochemical characterization of Gun4 suggests a mechanism for its role in chlorophyll biosynthesis. Biochemistry 44:7603–7612
Du P, Ling YH, Sang XC, Zhao FM, Xie R, Yang ZL, He GH (2009) Gene mapping related to yellow green leaf in a mutant line in rice (Oryza sativa L.). Genes Genomics 31:165–171
Eckhardt U, Grimm B, Hortensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 56:1–14
Gadjieva R, Axelsson E, Olsson U, Hansson M (2005) Analysis of gun phenotype in barley magnesium chelatase and Mg-protoporphyrin IX monomethyl ester cyclase mutants. Plant Physiol Biochem 43:901–908
Gothandam KM, Kim ES, Cho H, Chung YY (2005) OsPPR1, a pentatricopeptide repeat protein of rice is essential for the chloroplast biogenesis. Plant Mol Biol 58:421–433
Grafe S, Saluz HP, Grimm BF (1999) Mg-chelatase of tobacco: the role of the subunit CHL D in the chelation step of protoporphyrin IX. Proc Natl Acad Sci USA 96:1941–1946
Hansson A, Willows R, Roberts T, Hansson M (2002) Three semidominant barley mutants with single amino acid substitutions in the smallest magnesium chelatase subunit form defective AAA + hexamers. Proc Natl Acad Sci USA 99:13944–13949
Jensen PE, Reid JD, Hunter CN (2000) Modification of cysteine residues in the ChlI and ChlH subunits of magnesium chelatase results in enzyme inactivation. Biochem J 352:435–441
Jung KH, Hur J, Ryu CH, Choi Y, Chung YY, Miyao A, Hirochika H, An GH (2003) Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system. Plant Cell Physiol 44:463–472
Kannangara CG, Vothknecht UC, Hansson M, VonWettstein D (1997) Magnesium chelatase: association with ribosomes and mutant complementation studies identify barley subunit Xantha-G as a functional counterpart of Rhodobacter subunit BchD. Mol Gen Genet 254:85–92
Kobayashi Y, Kanesakib Y, Tanaka A, Kuroiwa H, Kuroiwa T, Tanaka K (2009) Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells. Proc Natl Acad Sci USA 106:803–807
Luo ZK, Yang ZL, Zhong BQ, Li YF, Xie R, Zhao FM, Ling YH, He GH (2007) Genetic analysis and fine mapping of a dynamic rolled leaf gene, RL10(t), in rice (Oryza sativa L.). Genome 50:811–817
Morita R, Kusaba M, Yamaguchi H, Amano E, Miyao A, Hirochika H, Nishimura M (2005) Characterization of Chlorophyllide a oxygenase (CAO) in rice. Breed Sci 55:361–364
Nagata N, Tanaka R, Satoh S, Tanaka A (2005) Identification of a vinyl reductase gene for chlorophyll synthesis in Arabidopsis thaliana and implications for the evolution of Prochlorococcus species. Plant Cell 17:233–240
Reinbothe C, Bartsch S, Eggink LL, Hoober JK, Brusslan J, Andrade-Paz R, Monnet J, Reinbothe S (2006) A role for chlorophyllide a oxygenase in the regulated import and stabilization of light-harvesting chlorophyll a/b proteins. Proc Natl Acad Sci USA 103:4777–4782
Schmid VH (2008) Light-harvesting complexes of vascular plants. Cell Mol Life Sci 65:3619–3639
Soldatova O, Apchelimov A, Radukina N, Ezhova T, Shestakov S, Ziemann V, Hedtke B, Grimm B (2005) An Arabidopsis mutant that is resistant to the protoporphyrinogen oxidase inhibitor acifluorfen shows regulatory changes in tetrapyrrole biosynthesis. Mol Genet Genomics 273:311–318
Strand A, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83
Sugimoto H, Kusumi K, Noguchi K, Yano M, Yoshimura A, Iba K (2007) The rice nuclear gene, VIRESCENT 2, is essential for chloroplast development and encodes a novel type of guanylate kinase targeted to plastids and mitochondria. Plant J 52:512–527
Suzuki JY, Bollivar DW, Bauer CE (1997) Genetic analysis of chlorophyll biosynthesis. Annu Rev Genet 31:61–89
Vavilin DV, Vermaas WF (2002) Regulation of the tetrapyrrole biosynthetic pathway leading to heme and chlorophyll in plants and cyanobacteria. Physiol Plant 115:9–24
Walker CJ, Willows RD (1997) Mechanism and regulation of Mg-chelatase. Biochem J 327:321–333
Wang P, Gao J, Wan C, Zhang F, Xu Z, Huang X, Sun X, Deng X (2010) Divinyl chlorophyll(ide) a can be converted to monovinyl chlorophyll(ide) a by a divinyl reductase in rice. Plant Physiol 153:994–1003
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Plant Physiol 144:307–313
Wu ZM, Zhang X, He B, Diao LP, Sheng S, Wang JL, Guo XP, Su N, Wang LF, Jiang L, Wang CM, Zhai HQ, Wan JM (2007) A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. Plant Physiol 145:29–40
Xiao H, Tang JF, Li YF, Wang WM, Li XB, Jin L, Xie R, Luo HF, Zhao XF, Meng Z, He GH, Zhu LH (2009) STAMENLESS 1, encoding a single C2H2 zinc finger protein, regulates floral organ identity in rice. Plant J 59:789–801
Yoo SC, Cho SH, Sugimoto H, Li JJ, Kusumi K, Koh HJ, Iba K, Paek NC (2009) Rice virescent3 and stripe1 encoding the large and small subunits of ribonucleotide reductase are required for chloroplast biogenesis during early leaf development. Plant Physiol 150:388–401
Yu QB, Jiang Y, Chong K, Yang ZN (2009) AtECB2, a pentatricopeptide repeat protein, is required for chloroplast transcript accD RNA editing and early chloroplast biogenesis in Arabidopsis thaliana. Plant J 59:1011–1023
Zhang HT, Li JJ, Yoo JH, Yoo SC, Cho SH, Koh HJ, Seo HS, Paek NC (2006) Rice chlorina-1 and chlorina-9 encode ChlD and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development. Plant Mol Biol 62:325–337
Acknowledgments
This research was supported by the National Natural Science Foundation (30800598), the Outstanding Youth Foundation of Chongqing (CSTC, 2008BA1033), the Natural Science Foundation of Chongqing (CSTC, 2008BB1258), and the Fundamental Research Funds for the Central Universities (XDJK2012C073).
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Xiaoqing Tian and Yinghua Ling contributed equally to this study.
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Tian, X., Ling, Y., Fang, L. et al. Gene cloning and functional analysis of yellow green leaf3 (ygl3) gene during the whole-plant growth stage in rice. Genes Genom 35, 87–93 (2013). https://doi.org/10.1007/s13258-013-0069-5
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DOI: https://doi.org/10.1007/s13258-013-0069-5