OsNOA1/RIF1 is a functional homolog of AtNOA1/RIF1: implication for a highly conserved plant cGTPase essential for chloroplast function.
*The bacterial protein YqeH is a circularly permuted GTPase with homologs encoded by plant nuclear genomes. The rice homolog OsNOA1/RIF1 is encoded by the single-copy gene Os02g01440. OsNOA1/RIF1 is expressed in different tissues and is light-inducible. The OsNOA1/RIF1-EYFP fusion protein was targeted to chloroplasts in transgenic Arabidopsis plants. In addition, the rice homolog was able to rescue most of the growth phenotypes in an Arabidopsis rif1 mutant. *Rice (Oryza sativa) OsNOA1/RIF1 RNAi mutant seedlings were chlorotic with reduced pigment contents and lower photosystem II (PSII) efficiency. However, the expressions of the chloroplast-encoded genes rbcL, atpB, psaA and psbA were not affected. By contrast, reduced abundance of the chloroplast 16S rRNA was observed in the mutant. *Quantitative iTRAQ-LC-MS/MS proteomics investigations revealed proteome changes in the rice mutant consistent with the expected functional role of OsNOA1/RIF1 in chloroplast translation. The RNAi mutant showed significantly decreased expression levels of chloroplast-encoded proteins as well as nuclear-encoded components of chloroplast enzyme complexes. Conversely, upregulation of some classes of nonchloroplastic proteins, such as glycolytic and phenylpropanoid pathway enzymes, was detected. *Our work provides independent indications that a highly conserved nuclear-encoded cGTPase of likely prokaryotic origin is essential for proper chloroplast ribosome assembly and/or translation in plants.
Liu
Hongjia
H
Crop Molecular Breeding Center, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, China.|School of Biological Sciences.
Lau
Edward
E
Department of Chemistry, The University of Hong Kong, Pokfulam Road, Hong Kong, China.
Lam
Maggie P Y
MPY
Department of Chemistry, The University of Hong Kong, Pokfulam Road, Hong Kong, China.
Chu
Hung
H
School of Biological Sciences.
Li
Sujuan
S
Crop Molecular Breeding Center, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, China.
Huang
Guo
G
Crop Molecular Breeding Center, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, China.
Guo
Peng
P
Crop Molecular Breeding Center, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, China.
Wang
Junqi
J
Department of Biology, The Chinese University of Hong Kong, Shatin, Hong Kong, China.
Jiang
Liwen
L
Department of Biology, The Chinese University of Hong Kong, Shatin, Hong Kong, China.
Chu
Ivan K
IK
Department of Chemistry, The University of Hong Kong, Pokfulam Road, Hong Kong, China.
Lo
Clive
C
School of Biological Sciences.
Tao
Yuezhi
Y
Crop Molecular Breeding Center, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, China.
D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000201:enzymology*; D029681:Arabidopsis Proteins / Q000737:chemistry*; D002736:Chloroplasts / Q000201:enzymology*; D017124:Conserved Sequence / Q000235:genetics*; D020558:GTP Phosphohydrolases / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D005816:Genetic Complementation Test; D005838:Genotype; D008969:Molecular Sequence Data; D009154:Mutation / Q000235:genetics; D019001:Nitric Oxide Synthase / Q000737:chemistry*; D012275:Oryza / Q000201:enzymology* / Q000235:genetics; D010940:Plant Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D021381:Protein Transport; D034622:RNA Interference; D011993:Recombinant Fusion Proteins / Q000378:metabolism; D016415:Sequence Alignment; D017386:Sequence Homology, Amino Acid; D013489:Suppression, Genetic
D029681:Arabidopsis Proteins; D010940:Plant Proteins; D011993:Recombinant Fusion Proteins; C521947:NOA1 protein, Arabidopsis; D019001:Nitric Oxide Synthase; D020558:GTP Phosphohydrolases
Abdallah F, Salamini F, Leister D. 2000. A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends in Plant Science 5: 141-142.
Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16: 735-743.
Crawford NM, Gally M, Tischner R, Heimer YM, Okamoto M, Mack A. 2006. Plant nitric oxide synthase: back to square one. Trends in Plant Science 11: 526-527.
Dyall SD, Brown MT, Johnson PJ. 2004. Ancient invasions: from endosymbionts to organelles. Science 304: 253-257.
Fernández AP, Strand A. 2008. Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Current Opinions in Plant Biology 11: 509-513.
Flores-Pérez Ú, Sauret-Güeto S, Gas E, Jarvis P, Rodríguez-Concepción M. 2008. A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell 20: 1303-1315.
Gas E, Flores-Pérez U, Sauret-Güeto S, Rodríguez-Concepción M. 2009. Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 21: 18-23.
Gray J, Janick-Buckner D, Buckner B, Close PS, Johal GS. 2002. Light-dependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiology 130: 1894-1907.
Gray JC, Sullivan JA, Wang JH, Jerome CA, MacLean D. 2003. Coordination of plastid and nuclear gene expression. Philosophical Transactions of the Royal Society B: Biological Sciences 358: 135-144.
Guo FQ, Crawford NM. 2005. Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17: 3436-3450.
Guo FQ, Okamoto M, Crawford NM. 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302: 100-103.
He Y, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM, Jing L, Yang Z, Chen L, Guo F et al. 2004. Nitric oxide represses the Arabidopsis floral transition. Science 305: 1968-1971.
Hess WR, Müller A, Nagy F, Börner T. 1994. Ribosome-deficient plastids affect transcription of light-induced nuclear genes: genetic evidence for a plastid-derived signal. Molecular and General Genetics 242: 305-312.
Hess WR, Schendel R, Börner T, Rüdiger W. 1991. Reduction of mRNA level for two nuclear encoded light regulated genes in the barley mutant albostrians is not correlated with phytochrome content and activity. Journal of Plant Physiology 138: 292-298.
Huang J, Takano T, Akita S. 2000. Expression of a-expansin genes in young seedlings of rice (Oryza sativa L.). Planta 211: 467-473.
Jenkins BD, Kulhanek DJ, Barkan A. 1997. Nuclear mutations that block group II RNA splicing in maize chloroplasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell 9: 283-296.
Kim J, Rudella A, Ramirez Rodriguez V, Zybailov B, Olinares PD, van Wijk KJ. 2009. Subunits of the plastid ClpPR protease complex have differential contributions to embryogenesis, plastid biogenesis, and plant development in Arabidopsis. Plant Cell 21: 1669-1692.
Kumar S, Tamura K, Nei M. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinformatics 5: 150-163.
Lee SC, Jeon JS, Jung KH, An G. 1999. Binary vectors for efficient transformation of rice. Journal of Plant Biology 42: 310-316.
Leipe DD, Wolf YI, Koonin EV, Aravind L. 2002. Classification and evolution of P-loop GTPases and related ATPases. Journal of Molecular Biology 317: 41-72.
Marín-Navarro J, Manuell AL, Wu Joann, Mayfield SP. 2007. Chloroplast translation regulation. Photosynthesis Research 94: 359-374.
Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF. 2008. AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. Journal of Biological Chemistry 283: 32957-32967.
Pesaresi P, Masiero S, Eubel H, Braun HP, Bhushan S, Glaser E, Salamini F, Leister D. 2006. Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. Plant Cell 18: 970-991.
Pesaresi P, Varotto C, Meurer J, Jahns P, Salamini F, Leister D. 2001. Knock-out of the plastid ribosomal protein L11 in Arabidopsis: effects on mRNA translation and photosynthesis. Plant Journal 27: 179-189.
Subramanian AR. 1993. Molecular genetics of chloroplast ribosomal proteins. Trends in Biochemical Science 18: 177-181.
Sudhamsu J, Lee GI, Klessig DF, Crane BR. 2008. The structure of YqeH: an AtNOS1/AtNOA1 ortholog that couples GTP hydrolysis to molecular recognition. Journal of Biological Chemistry 283: 32968-32976.
Uicker WC, Schaefer L, Koenigsknecht M, Britton RA. 2007. The essential GTPase YqeH is required for proper ribosome assembly in Bacillus subtilis. Journal of Bacteriology 189: 2926-2929.
Williams PM, Barkan A. 2003. A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant Journal 36: 675-686.
Woodson JD, Chory J. 2008. Coordination of gene expression between organellar and nuclear genomes. Nature Reviews Genetics 9: 383-395.
Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J. 2004. Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proceedings of the National Academy of Sciences, USA 101: 15811-15816.
Zemojtel T, Frohlich A, Palmieri MC, Kolanczyk M, Mikula I, Wyrwicz LS, Wanker EE, Mundlos S, Vingron M, Martasek P et al. 2006. Plant nitric oxide synthase: a never-ending story? Trends in Plant Science 11: 524-525.
Zhao MG, Tian QY, Zhang WH. 2007. Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiology 144: 206-217.
Zybailov B, Friso G, Kim J, Rudella A, Rodríguez VR, Asakura Y, Sun Q, van Wijk KJ. 2009. Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Molecular & Cellular Proteomics 8: 1789-1810.