The rice ALS3 encoding a novel pentatricopeptide repeat protein is required for chloroplast development and seedling growth

详细信息    查看全文

• 作者：Dongzhi Lin (1)
  Xiaodi Gong (1) (2)
  Quan Jiang (1)
  Kailun Zheng (1)
  Hua Zhou (1) (3)
  Jianlong Xu (4)
  Sheng Teng (5)
  Yanjun Dong (1)
  
  1. Development Center of Plant Germplasm Resources ; College of Life and Environment Sciences ; Shanghai Normal University ; Shanghai ; 200234 ; China
  2. Present address ; Institute of Genetics and Developmental Biology Chinese Academy of Sciences ; No.1 West Beichen Road ; Chaoyang District ; Beijing ; 100101 ; China
  3. Present address ; Agricultural Faculty ; Hokkaido University ; Sappro ; 060-0817 ; Japan
  4. Institute of Crop Science ; National Key Facility for Crop Gene Resources and Genetic Improvement ; Chinese Academy of Agricultural Sciences ; Beijing ; 10081 ; China
  5. Institute of Plant Physiology and Ecology ; Shanghai Institute for Biological Sciences ; Chinese Academy of Sciences ; Shanghai ; 200032 ; China
  
• 关键词：Albino ; Chloroplast development ; Lethality ; Rice ; Pentatricopeptide repeat (PPR) proteins
• 刊名：Rice
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：8
• 期：1
• 全文大小：2,486 KB
• 参考文献：1. Arnon, DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris Plant Physiol 24: pp. 1-15
  2. Asano, T, Miyao, A, Hirochika, H, Kikuchi, S, Kadowakia, K (2013) A pentatricopeptide repeat gene of rice is required for splicing of chloroplast transcripts and RNA editing of ndhA. Plant Biotechnol 30: pp. 57-64 CrossRef
  3. Cai, W, Ji, D, Peng, L, Guo, J, Ma, J, Zou, M, Lu, C, Zhang, L (2009) LPA66 is required for editing psbF chloroplast transcripts in Arabidopsis. Plant Physiol 150: pp. 1260-1271 CrossRef
  4. Chateigner-Boutin, AL, Ramos-Vega, M, Guevara-Garc鈥櫮盿, A, Andr鈥檈s, C, Luz Guti鈥檈rrez-Nava, M, Cantero, A, Delannoy, E, Jim鈥檈nez, LF, Lurin, C, Small, I, Le贸n, P (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J 56: pp. 590-602 CrossRef
  5. Cushing, DA, Nancy, RF, Daniel, RG, Vernon, DM (2005) Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis. Planta 221: pp. 424-436 CrossRef
  6. Longevialle, AF, Meyer, EH, Andr鈥檈s, C, Taylor, NL, Lurin, C, Millar, AH, Small, I (2007) The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 Intron 1 in Arabidopsis thaliana. Plant Cell 19: pp. 3256-3265 CrossRef
  7. Santis-Maciossek, G, Kofer, W, Bock, A, Schoch, S, Maier, RM, Wanner, G, Rudiger, W, Koop, HU, Herrmann, RG (1999) Targeted disruption of the plastid RNA polymerase genes rpoA, B and C1: Molecular biology, biochemistry and ultrastructure. Plant J 18: pp. 477-489 CrossRef
  8. Delannoy, E, Stanley, WA, Bond, CS, Small, ID (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem Soc Trans 35: pp. 1643-1647 CrossRef
  9. Goff, SA, Ricke, D, Lan, TH, Presting, G, Wang, R, Dunn, M, Glazebrook, J, Sessions, A, Oeller, P, Varma, H, Hadley, D, Hutchison, D, Martin, C, Katagiri, F, Lange, BM, Moughamer, T, Xia, Y, Budworth, P, Zhong, J, Miguel, T, Paszkowski, U, Zhang, S, Colbert, M, Sun, WL, Chen, L, Cooper, B, Park, S, Wood, TC, Mao, L, Quail, P (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: pp. 92-100 CrossRef
  10. Gong, X, Jiang, Q, Xu, J, Zhang, J, Teng, S, Lin, D, Dong, Y (2013) Disruption of the rice plastid ribosomal protein S20 leads to chloroplast developmental defects and seedling lethality. G3: Genes| Genomes|. Genetics 3: pp. 1769-1777
  11. Gong, X, Su, Q, Lin, D, Xu, J, Jiang, Q, Zhang, J, Teng, S, Dong, Y (2014) The rice OsV4 encoding a novel pentatricopeptide repeat protein is required for chloroplast development during the early leaf stage under cold stress. J Integr Plant Biol 56: pp. 400-410 CrossRef
  12. 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: pp. 421-433 CrossRef
  13. Hajdukiewicz, PT, Allison, LA, Maliga, P (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J 16: pp. 4041-4048 CrossRef
  14. Hattori, M, Miyake, H, Sugita, M (2007) A pentatricopeptide repeat protein is required for RNA processing of clpP Pre-mRNA in moss chloroplasts. J Biol Chem 282: pp. 10773-10782 CrossRef
  15. Hiei, Y, Ohta, S, Komari, T, Kumashiro, T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6: pp. 271-282 CrossRef
  16. Hiratsuka, J, Shimada, H, Whittier, R, Ishibashi, T, Sakamoto, M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217: pp. 185-194 CrossRef
  17. Ichinose, M, Tasaki, E, Sugita, C, Sugita, M (2012) A PPR-DYW protein is required for splicing of a group II intron of cox1 premRNA in physcomitrella patens. Plant J 70: pp. 271-278 CrossRef
  18. Karpenahalli, MR, Lupas, AN, S枚ding, J (2007) TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences. BMC Bioinformatics 8: pp. 2 CrossRef
  19. Kim, SR, Yang, JI, Moon, S, Ryu, CH, An, K, Kim, KM, Yim, J, An, G (2009) Rice OGR1 encodes a pentatricopeptide repeat-DYW protein and is essential for RNA editing in mitochondria. Plant J 59: pp. 738-749 CrossRef
  20. Kotera, E, Tasaka, M, Shikanai, T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433: pp. 326-330 CrossRef
  21. Kusumi, K, Chono, Y, Gotoh, E, Tsuyama, M, Iba, K (2010) Chloroplast biogenesis during the early stage of leaf development in rice. Plant Biotechnol 27: pp. 85-90 CrossRef
  22. Kyozuka, J, McElroy, D, Hayakawa, T, Xie, Y, Wu, R, Shimamoto, K (1993) Light-regulated and cell-specific expression of tomato rbcS-gusA and rice rbcS-gusA fusion genes in transgenic rice. Plant Physiol 102: pp. 991-1000 CrossRef
  23. Leister, D (2003) Chloroplast research in the genomic age. Trends Genet 19: pp. 47-56 CrossRef
  24. Livak, KJ, Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-螖螖CT method. Methods 25: pp. 402-408 CrossRef
  25. Lurin, C, Andr茅sa, C, Aubourga, S, Bellaouia, M, Bittona, F, Bruy猫reb, C, Cabochea, M, Debastc, C, Gualbertod, J, Hoffmanna, B, Lecharnyb, A, Retd, M, Martin-Magnietteae, M, Mireauc, H, Peetersc, N, Renoua, J, Szureka, B, Taconnata, L, Smalla, I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repear proteins reveals their essential role in organelle biogenesis. Plant Cell 16: pp. 2089-2103 CrossRef
  26. McCouch, SR, Teytelman, L, Xu, Y, Lobos, KB, Clare, K, Walton, M, Fu, B, Maghirang, R, Li, Z, Xing, Y, Zhang, Q, Kono, I, Yano, M, Fjellstrom, M, 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 Res 9: pp. 199-207 CrossRef
  27. Meierhoff, K, Felder, S, Nakamura, T, Bechtold, N, Schuster, G (2003) HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein, involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs. Plant Cell 15: pp. 1480-1495 CrossRef
  28. Mullet, JE (1993) Dynamic regulation of chloroplast transcription. Plant Physiol 103: pp. 309-313 CrossRef
  29. O鈥橳oole, N, Hattori, M, Andres, C, Iida, K, Lurin, C, Schmitz-Linneweber, C, Sugita, M, Small, I (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 25: pp. 1120-1128 CrossRef
  30. Okuda, K, Myouga, F, Motohashi, R, Shinozaki, K, Shikanai, T (2007) Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc Natl Acad Sci U S A 104: pp. 8178-8183 CrossRef
  31. Pfalz, J, Bayraktar, OA, Prikryl, J, Barkan, A (2009) Site-specific binding of a PPR protein defines and stabilizes 5鈥?and 3鈥?mRNA termini in chloroplasts. EMBO J 28: pp. 2042-2052 CrossRef
  32. Schmitz-Linneweber, C, Small, I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13: pp. 663-670 CrossRef
  33. Schmitz-Linneweber, C, Williams-Carrier, RE, Williams-Voelker, PM, Kroeger, TS, Vichas, A, Barkan, A (2006) A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18: pp. 2650-2663 CrossRef
  34. Small, ID, Peeters, N (2000) The PPR motif鈥揳 TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25: pp. 46-47 CrossRef
  35. Sosso, D, Mbelo, S, Vernoud, V, Gendrot, G, Dedieu, A, Chambrier, P, Dauzat, M, Heurtevin, L, Guyon, V, Takenaka, M, Rogowsky, PM (2012) PPR2263, a DYW-subgroup pentatricopeptide repeat protein, is required for mitochondrial nad5 and cob transcript editing, mitochondrion biogenesis, and maize growth. Plant Cell 24: pp. 676-691 CrossRef
  36. Su, N, Hu, ML, Wu, DX, Wu, FQ, Fei, GL, Lan, Y, Chen, XL, Shu, XL, Zhang, X, Guo, XP, Cheng, ZJ, Lei, CL, Qi, CK, Jiang, L, Wang, HY, Wan, JM (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 Physiol 159: pp. 227-238 CrossRef
  37. Sugimoto, H, Kusumi, K, Tozawa, Y, Yazaki, J, Kishimoto, N, Kikuchi, S, Iba, K (2004) The virescent-2 mutation inhibits translation of plastid transcripts for the plastid genetic system at an early stage of chloroplast differentiation. Plant Cell Physiol 45: pp. 985-996 CrossRef
  38. Takeuchi, R, Kimura, S, Saotome, A, Sakaguchi, K (2007) Biochemical properties of a plastidial DNA polymerase of rice. Plant Mol Biol 64: pp. 601-611 CrossRef
  39. Tavares-Carre贸n, F, Camacho-Villasana, Y, Zamudio-Ochoa, A, Shing煤-V谩zquez, M, Torres-Larios, A, P茅rez-Mart铆nez, X (2008) The pentatricopeptide repeats present in Pet309 are necessary for translation but not for stability of the mitochondrial COX1 mRNA in yeast. J Biol Chem 283: pp. 1472-1479 CrossRef
  40. Tseng, CC, Sung, TY, Li, YC, Hsu, SJ, Lin, CL, Hsieh, MH (2010) Editing of accD and ndhF chloroplast transcripts is partially affected in the Arabidopsis vanilla cream1 mutant. Plant Mol Biol 73: pp. 309-323 CrossRef
  41. Wang, Z, Chen, C, Xu, Y, Jiang, R, Han, Y, Xu, Z, Chong, K (2004) A practical vector for efficient knockdown of gene expression in rice (Oryza sativa L.). Plant Molecular Biology Reporter 22: pp. 409-417 CrossRef
  42. Williams, PM, Barkan, A (2003) A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J 36: pp. 675-686 CrossRef
  43. Yamazaki, H, Tasaka, M, Shikanai, T (2004) PPR motifs of the nucleusencoded factor, PGR3, function in the selective and distinct steps of chloroplast gene expression in Arabidopsis. Plant J 38: pp. 152-163 CrossRef
  44. Yin, QQ, Cui, YL, Zhang, GR, Zhang, HD, Wang, XM, Yang, ZN (2012) The Arabidopsis pentatricopeptide repeat protein PDM1 is associated with the intergenic sequence of S11-rpoA for rpoA monocistronic RNA cleavage. Chin Sci Bull 57: pp. 3452-3459 CrossRef
  45. Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J,Han Y, Li L, Li W, Hu G, Huang X, Li W, Li J, Liu Z, Li L et al (2002) A draft sequence of the rice genome ( / Oryza sativa L. ssp. / indica). Science 296:79鈥?2
  46. Yu, QB, JiangY, CK, 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: pp. 1011-1023 CrossRef
  47. Zhou, W, Cheng, Y, Yap, A, Chateigner-Boutin, AL, Delannoy, E, Hammani, K, Small, I, Huang, J (2009) The Arabidopsis gene YS1 encoding a DYW protein is required for editing of rpoB transcripts and the rapid development of chloroplasts during early growth. Plant J 58: pp. 82-96 CrossRef
  
• 刊物主题：Plant Sciences; Plant Genetics & Genomics; Plant Breeding/Biotechnology; Agriculture; Plant Ecology;
• 出版者：Springer US
• ISSN：1939-8433

文摘

Background Pentatricopeptide repeat (PPR) proteins play essential roles in modulating the expression of organelle genes and have expanded greatly in higher plants. However, molecular mechanisms of most rice PPR genes remain unclear. Results In this study, a new rice PPR mutant, asl3 (albino seedling lethality3) exhibits an albino lethal phenotype at the seedling stage. This albino phenotype was associated with altered photosynthetic-pigment and chloroplast development. Map-based cloning showed that ASL3 encodes a novel rice PPR protein with 10 tandem PPR motifs, which localizes to the chloroplast. ASL3 showed tissue-specific expression, as it was highly expressed in the chlorenchyma, but expressed at much lower levels in roots and panicles. RNAi of ASL3 confirmed that ASL3 plays an essential role in the early development and chloroplast development in rice. Moreover, expression analysis revealed that the asl3 mutation severely affected the transcriptional levels of important genes associated with plastid translation machinery and photosynthesis, which may impair photosynthesis and finally led to the seedling death in asl3 mutant. These results evidenced the important role of ASL3 in the early development of rice, especially chloroplast development. Conclusions The ASL3 gene encoded a novel chloroplast-targeted PPR protein with 10 tandem PPR motifs in rice. Disruption of the ASL3 would lead to a defective chloroplast and seedling lethality, and affected expression levels of genes associated with chloroplast development and photosynthesis at early leaf stage of rice.