Chin Bull Bot ›› 2012, Vol. 47 ›› Issue (6): 581-593.doi: 10.3724/SP.J.1259.2012.00581

Previous Articles     Next Articles

RNA Editing Sites in Chloroplast Protein-coding Genes in Leaf White Mutant of Triticum aestivum

Likun Deng, Yan Li, Jianing Yu*   

  1. College of Life Sciences, Shaanxi Normal University, Xi’an 710062, China
  • Received:2012-01-16 Revised:2012-04-11 Online:2012-09-04 Published:2012-11-01
  • Contact: Jianing Yu E-mail:jianingyucn@yahoo.com.cn
  • Supported by:

    National key basic research development program

Abstract: RNA editing is a post-transcriptional process and mainly occurs in higher plant organelles. Lacking RNA editing in some plants can cause albino or yellow leaves. We investigated RNA editing in 14 protein-coding genes from the chloroplast genome of Triticum aestivum Aibian 1 and the wheat leaf-stage albino mutant FA85. We found 26 editing sites in these genes. The two plants significantly differed in editing efficiency of 5 partial editing events. The 5 sites include the phosphoenylpyruvate (PEP) genes rpoC2, rpoA and rpoB, and 3 of them are predicted to change the secondary protein structure. We further analyzed the transcriptional pattern of chloroplast genes that depend on PEP, on nuclear export protein (NEP) and on both PEP and NEP. The mRNA levels of chloroplast genes, except for psbA and clpP, were lower in the mutant than wild-type leaves. The wheat leaf-stage albino phenotype may be attributed to a decrease in efficiency of the 5 editing sites and alteration of transcript level of some chloroplast genes.

江媛, 何筠, 范术丽, 俞嘉宁, 宋美珍 (2011a) 棉花芽黄突变体十个叶绿体蛋白编码基因RNA编辑位点的测定及分析. 棉花学报 23, 3-9.
江媛, 范术丽, 宋美珍, 俞嘉宁, 喻树迅 (2011b) 棉花叶绿体基因RNA编辑位点的测定及分析. 植物学报 46, 386-395.
Bock R, Hagemann R, Kossel H, Kudla J (1993) Tissue- and stage-specific modulation of RNA editing of the psbF and psbL transcript from spinach plastids--a new regulatory mechanism? Mol Gen Genet 240, 238-244.
Bock R, Kossel H, Maliga P (1994) Introduction of a heterologous editing site into the tobacco plastid genome: the lack of RNA editing leads to a mutant phenotype. EMBO J 13, 4623-4628.
Calsa Junior T, Carraro DM, Benatti MR, Barbosa AC, Kitajima JP, Carrer H (2004) Structural features and transcript-editing analysis of sugarcane (Saccharum officinarum L.) chloroplast genome. Curr Genet 46, 366-373.
Castandet B, Choury D, Begu D, Jordana X, Araya A (2010) Intron RNA editing is essential for splicing in plant mitochondria. Nucleic Acids Res 38, 7112-7121.
Chateigner-Boutin AL, Hanson MR (2002) Cross-competition in transgenic chloroplasts expressing single editing sites reveals shared cis elements. Mol Cell Biol 22, 8448-8456.
Chateigner-Boutin AL, Hanson MR (2003) Developmental co-variation of RNA editing extent of plastid editing sites exhibiting similar cis-elements. Nucleic Acids Res 31, 2586-2594.
Chateigner-Boutin AL, Ramos-Vega M, Guevara-Garcia A, Andres C, de la Luz Gutierrez-Nava M, Cantero A, Delannoy E, Jimenez LF, Lurin C, Small I, Leon P (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J 56, 590-602.
Chateigner-Boutin AL, Small I (2010) Plant RNA editing. RNA Biol 7, 213-219.
Chaudhuri S, Carrer H, Maliga P (1995) Site-specific factor involved in the editing of the psbL mRNA in tobacco plastids. EMBO J 14, 2951-2957.
Chi W, Mao J, Li Q, Ji D, Zou M, Lu C, Zhang L (2010) Interaction of the pentatricopeptide-repeat protein DELAYED GREENING 1 with sigma factor SIG6 in the regulation of chloroplast gene expression in Arabidopsis cotyledons. Plant J 64, 14-25.
Corneille S, Lutz K, Maliga P (2000) Conservation of RNA editing between rice and maize plastids: are most editing events dispensable? Mol Gen Genet 264, 419-424.
Fiebig A, Stegemann S, Bock R (2004) Rapid evolution of RNA editing sites in a small non-essential plastid gene. Nucleic Acids Res 32, 3615-3622.
Giege P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci U S A 96, 15324-15329.
Gott JM, Emeson RB (2000) Functions and mechanisms of RNA editing. Annu Rev Genet 34, 499-531.
Grewe F, Viehoever P, Weisshaar B, Knoop V (2009) A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res 37, 5093-5104.
Groth-Malonek M, Wahrmund U, Polsakiewicz M, Knoop V (2007) Evolution of a pseudogene: exclusive survival of a functional mitochondrial nad7 gene supports Haplomitrium as the earliest liverwort lineage and proposes a secondary loss of RNA editing in Marchantiidae. Mol Biol Evol 24, 1068-1074.
Guzowska-Nowowiejska M, Fiedorowicz E, Plader W (2009) Cucumber, melon, pumpkin, and squash: are rules of editing in flowering plants chloroplast genes so well known indeed? Gene 434, 1-8.
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, 4041-4048.
Hammani K, Okuda K, Tanz SK, Chateigner-Boutin AL, Shikanai T, Small I (2009) A study of new Arabidopsis chloroplast RNA editing mutants reveals general features of editing factors and their target sites. Plant Cell 21, 3686-3699.
Hedtke B, Borner T, Weihe A (1997) Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science 277, 809-811.
Hirose T, Kusumegi T, Tsudzuki T, Sugiura M (1999) RNA editing sites in tobacco chloroplast transcripts: editing as a possible regulator of chloroplast RNA polymerase activity. Mol Gen Genet 262, 462-467.
Hou DY, Xu H, Du GY, Lin JT, Duan M, Guo AG (2009) Proteome analysis of chloroplast proteins in stage albinism line of winter wheat (triticum aestivum) FA85. BMB Rep 42, 450-455.
Inada M, Sasaki T, Yukawa M, Tsudzuki T, Sugiura M (2004) A systematic search for RNA editing sites in pea chloroplasts: an editing event causes diversification from the evolutionarily conserved amino acid sequence. Plant Cell Physiol 45, 1615-1622.
Kahlau S, Aspinall S, Gray JC, Bock R (2006) Sequence of the tomato chloroplast DNA and evolutionary comparison of solanaceous plastid genomes. J Mol Evol 63, 194-207.
Kapoor S, Suzuki JY, Sugiura M (1997) Identification and functional significance of a new class of non-consensus-type plastid promoters. Plant J 11, 327-337.
Karcher D, Bock R (2002) The amino acid sequence of a plastid protein is developmentally regulated by RNA editing. J Biol Chem 277, 5570-5574.
Kobayashi Y, Matsuo M, Sakamoto K, Wakasugi T, Yamada K, Obokata J (2008) Two RNA editing sites with cis-acting elements of moderate sequence identity are recognized by an identical site-recognition protein in tobacco chloroplasts. Nucleic Acids Res 36, 311-318.
Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K (2003) RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res 31, 2417-2423.
Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299, 902-906.
Liere K, Maliga P (1999) In vitro characterization of the tobacco rpoB promoter reveals a core sequence motif conserved between phage-type plastid and plant mitochondrial promoters. EMBO J 18, 249-257.
Maier RM, Neckermann K, Igloi GL, Kossel H (1995) Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J Mol Biol 251, 614-628.
Maier RM, Zeltz P, Kossel H, Bonnard G, Gualberto JM, Grienenberger JM (1996) RNA editing in plant mitochondria and chloroplasts. Plant Mol Biol 32, 343-365.
Maier UG, Bozarth A, Funk HT, Zauner S, Rensing SA, Schmitz-Linneweber C, Borner T, Tillich M (2008) Complex chloroplast RNA metabolism: just debugging the genetic programme? BMC Biol 6, 36.
Ogihara Y, Isono K, Kojima T, Endo A, Hanaoka M, Shiina T, Terachi T, Utsugi S, Murata M, Mori N (2000) Chinese spring wheat (Triticum aestivum L.) chloroplast genome: complete sequence and contig clones. Plant Molecular Biology Reporter 18, 243-253.
Robbins JC, Heller WP, Hanson MR (2009) A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of the Arabidopsis chloroplast accD transcript. RNA 15, 1142-1153.
Salone V, Rudinger M, Polsakiewicz M, Hoffmann B, Groth-Malonek M, Szurek B, Small I, Knoop V, Lurin C (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett 581, 4132-4138.
Sasaki Y, Kozaki A, Ohmori A, Iguchi H, Nagano Y (2001) Chloroplast RNA editing required for functional acetyl-CoA carboxylase in plants. J Biol Chem 276, 3937-3940.
Schmitz-Linneweber C, Regel R, Du TG, Hupfer H, Herrmann RG, Maier RM (2002) The plastid chromosome of Atropa belladonna and its comparison with that of Nicotiana tabacum: the role of RNA editing in generating divergence in the process of plant speciation. Mol Biol Evol 19, 1602-1612.
Shikanai T (2006) RNA editing in plant organelles: machinery, physiological function and evolution. Cell Mol Life Sci 63, 698-708.
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, 309-323.
Tsudzuki T, Wakasugi T, Sugiura M (2001) Comparative analysis of RNA editing sites in higher plant chloroplasts. J Mol Evol 53, 327-332.
Wakasugi T, Hirose T, Horihata M, Tsudzuki T, Kossel H, Sugiura M (1996) Creation of a novel protein-coding region at the RNA level in black pine chloroplasts: the pattern of RNA editing in the gymnosperm chloroplast is different from that in angiosperms. Proc Natl Acad Sci U S A 93, 8766-8770.
Wolf PG, Rowe CA, Hasebe M (2004) High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. Gene 339, 89-97.
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.
Yura K, Sulaiman S, Hatta Y, Shionyu M, Go M (2009) RESOPS: a database for analyzing the correspondence of RNA editing sites to protein three-dimensional structures. Plant Cell Physiol 50, 1865-1873.
Zeng WH, Liao SC, Chang CC (2007) Identification of RNA editing sites in chloroplast transcripts of Phalaenopsis aphrodite and comparative analysis with those of other seed plants. Plant Cell Physiol 48, 362-368.
Zito F, Kuras R, Choquet Y, Kossel H, Wollman FA (1997) Mutations of cytochrome b6 in Chlamydomonas reinhardtii disclose the functional significance for a proline to leucine conversion by petB editing in maize and tobacco. Plant Mol Biol 33, 79-86.
No related articles found!
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] . [J]. Chin Bull Bot, 1994, 11(专辑): 91 .
[2] QIAN Ying-Qian. Some Issues in Biodiversity[J]. Chin Bull Bot, 1998, 15(06): 1 -18 .
[3] ZHANG Xiu-Juan MEI Li WANG Zheng-Quan HAN You-Zhi. Advances in Studying Fine Root Decomposition in Forests[J]. Chin Bull Bot, 2005, 22(02): 246 -254 .
[4] CHENG Long-Jun GUO De-Ping GE Hong-Juan. The Special Proteins in Sweet Potato Tuber—Sporamin[J]. Chin Bull Bot, 2001, 18(06): 672 -677 .
[5] Tang Yancheng. A Short Guide to the International Code of Botanical Nomenclature[J]. Chin Bull Bot, 1984, 2(06): 49 -54 .
[6] Chuanyuan Deng, Guiliang Xin, Wanchao Zhang, Suzhi Guo, Qiuhua Xue, Zhongxiong Lai, Luying Ye. SEM Observations and Measurements of Vestured Pits of the Secondary Xylem in the Tribe Rhizophoreae[J]. Chin Bull Bot, 2015, 50(1): 90 -99 .
[7] YANG Xiao-Lin, ZHANG Xi-Ming, LI Yi-Ling, LI Shao-Cai, SUN Hai-Long. ANALYSIS OF ROOT ARCHITECTURE AND ROOT ADAPTIVE STRATEGY IN THE TAKLIMAKAN DESERT AREA OF CHINA[J]. Chin J Plan Ecolo, 2008, 32(6): 1268 -1276 .
[8] Zhang Jintun, Pickett S. T. A. Gradient Analysis of Forest Vegetation Along an Urban-Rural Transect in New York[J]. Chin J Plan Ecolo, 1998, 22(5): 392 -397 .
[9] JI Fang, MA Ying-Jie, FAN Zi-Li. Soil Water Regime in Populus euphratica Forest on the Tarim River Alluvial Plain[J]. Chin J Plan Ecolo, 2001, 25(1): 17 -21 .
[10] JIANG Fu-Wei, JIANG Hong, LI Wei, YU Shu-Quan, ZENG Bo, WANG Yan-Hong. PHOTOSYNTHETIC AND PHYSIOLOGICAL CHARACTERISTICS OF THREE ANGIOSPERMS OF DIFFERENT EVOLUTIONARY AGES UNDER ACID RAIN STRESS[J]. Chin J Plan Ecolo, 2009, 33(1): 125 -133 .