Plastid ribosomal protein S5 is involved in photosynthesis, plant development, and cold stress tolerance in Arabidopsis

Journal of Experimental Botany

Volumn 67, Issue 9, 2016, Pages 2731-2744

  Zhang, Junxiang ^a,b,c   Yuan, Hui ^b   Yang, Yong ^b   Fish, Tara ^b   Lyi, Sangbom M ^b   Thannhauser, Theodore W ^b   Zhang, Lugang ^a   Li, Li ^b  

^a NORTHWEST A F UNIVERSITY   (China)

^b Cornell University ^*  (United States)

^c SHENYANG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Arabidopsis; cold stress tolerance; photosynthesis; plastid ribosomal protein; proteomics; RPS5

Indexed keywords

ARABIDOPSIS PROTEIN; RNA 16S; RPS5 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; COLD; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MISSENSE MUTATION; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLASTID; REAL TIME POLYMERASE CHAIN REACTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; COLD TEMPERATURE; MUTATION, MISSENSE; PHOTOSYNTHESIS; PLASTIDS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; STRESS, PHYSIOLOGICAL;

EID: 84969972373     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erw106     Document Type: Article

References (52)

1. Bryant N, Lloyd J, Sweeney C, Myouga F, Meinke D. 2011. Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis. Plant Physiology 155, 1678-1689.
2. Byrne ME. 2009. A role for the ribosome in development. Trends in Plant Science 14, 512-519.
3. Carroll AJ. 2013. The Arabidopsis cytosolic ribosomal proteome: from form to function. Frontiers in Plant Science 4, 1-14.
4. Chi W, Sun X, Zhang L. 2013. Intracellular signaling from plastid to nucleus. Annual Review of Plant Biology 64, 559-582.
5. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2, 953-971.
6. Fleischmann TT, Scharff LB, Alkatib S, Hasdorf S, Schottler MA, Bock R. 2011. Nonessential plastid-encoded ribosomal proteins in tobacco: A developmental role for plastid translation and implications for reductive genome evolution. The Plant Cell 23, 3137-3155.
7. Friso G, Giacomelli L, Ytterberg AJ, Peltier JB, Rudella A, Sun Q, Wijk KJ. 2004. In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. The Plant Cell 16, 478-499.
8. Fristedt R, Scharff LB, Clarke CA, Wang Q, Lin CT, Merchant SS, Bock R. 2014. RBF1, a plant homolog of the bacterial ribosome-binding factor RbfA, acts in processing of the chloroplast 16S ribosomal RNA. Plant physiology , 164, 201-215.
9. 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 10, 1769-1777.
10. Harris EH, Boynton JE, Gillham NW. 1994. Chloroplast ribosomes and protein synthesis. Microbiological Reviews 58, 700-754.
11. Horiguchi G, Van Lijsebettens M, Candela H, Micol JL, Tsukaya H. 2012. Ribosomes and translation in plant developmental control. Plant Science 191, 24-34.
12. Inskeep WP, Bloom PR. 1985. Extinction coefficients of chlorophyll a and b in N, N-dimethylformamide and 80% acetone. Plant Physiology 77, 483-485.
13. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: A case study using the Phyre server. Nature Protocols 4, 363-371.
14. Kleinknecht L, Wang F, Stube R, Philippar K, Nickelsen J, Bohne AV. 2014. RAP, the sole octotricopeptide repeat protein in Arabidopsis, is required for chloroplast 16S rRNA maturation. The Plant Cell 26, 777-787.
15. Li L, Yang Y, Xu Q, Owsiany K, Welsch R, Chitchumroonchokchai C, Lu S, Van Eck J, Deng X-X, Failla M. 2012. The Or gene enhances carotenoid accumulation and stability during post-harvest storage of potato tubers. Molecular plant 5, 339-352.
16. Lyi SM, Heller LI, Rutzke M, Welch RM, Kochian LV, Li L. 2005. Molecular and biochemical characterization of the selenocysteine Se-methyltransferase gene and Se-methylselenocysteine synthesis in broccoli. Plant Physiology 138, 409-420.
17. Lyi SM, Zhou X, Kochian LV, Li L. 2007. Biochemical and molecular characterization of the homocysteine S-methyltransferase from broccoli (Brassica oleracea var. italica). Phytochemistry 68, 1112-1119.
18. Morita-Yamamuro C, Tsutsui T, Tanaka A, Yamaguchi J. 2004. Knock-out of the plastid ribosomal protein S21 causes impaired photosynthesis and sugar-response during germination and seedling development in Arabidopsis thaliana. Plant and Cell Physiology 45, 781-788.
19. 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. The Plant Journal 27, 179-189.
20. Ramakrishnan V. 2002. Ribosome structure and the mechanism of translation. Cell 108, 557-572.
21. Ramakrishnan V, White SW. 1992. The structure of ribosomal protein S5 reveals sites of interaction with 16S rRNA. Nature 358, 768-771.
22. Rogalski M, Ruf S, Bock R. 2006. Tobacco plastid ribosomal protein S18 is essential for cell survival. Nucleic Acids Research 34, 4537-4545.
23. Rogalski M, Schottler MA, Thiele W, Schulze WX, Bock R. 2008. Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions. The Plant Cell 20, 2221-2237.
24. Rolland N, Curien G, Finazzi G, Kuntz M, Marechal E, Matringe M, Ravanel S, Seigneurin-Berny D. 2012. The biosynthetic capacities of the plastids and integration between cytoplasmic and chloroplast processes. Annual Review of Genetics 46, 233-264.
25. Romani I, Tadini L, Rossi F, Masiero S, Pribil M, Jahns P, Kater M, Leister D, Pesaresi P. 2012. Versatile roles of Arabidopsis plastid ribosomal proteins in plant growth and development. The Plant Journal 72, 922-934.
26. Schippers JH, Mueller-Roeber B. 2010. Ribosomal composition and control of leaf development. Plant Science 179, 307-315.
27. Shajani Z, Sykes MT, Williamson JR. 2011. Assembly of bacterial ribosomes. Annual Review of Biochemistry 80, 501-526.
28. Shumskaya M, Bradbury LM, Monaco RR, Wurtzel ET. 2012. Plastid localization of the key carotenoid enzyme phytoene synthase is altered by isozyme, allelic variation, and activity. The Plant Cell 24, 3725-3741.
29. Stern S, Powers T, Changchien L-M, Noller HF. 1989. RNA-protein interactions in 30S ribosomal subunits: folding and function of 16S rRNA. Science 244, 783-790.
30. Takano S, Niihama M, Smith HM, Tasaka M, Aida M. 2010. gorgon, a novel missense mutation in the SHOOT MERISTEMLESS gene, impairs shoot meristem homeostasis in Arabidopsis. Plant and Cell Physiology 51, 621-634.
31. Thomashow MF. 1998. Role of cold-responsive genes in plant freezing tolerance. Plant Physiology 118, 1-8.
32. Tiller N, Bock R. 2014. The translational apparatus of plastids and its role in plant development. Molecular plant 7, 1105-1120.
33. Tiller N, Weingartner M, Thiele W, Maximova E, Schottler MA, Bock R. 2012. The plastid-specific ribosomal proteins of Arabidopsis thaliana can be divided into non-essential proteins and genuine ribosomal proteins. The Plant Journal 69, 302-316.
34. Vaidya AT, Top D, Manahan CC, Tokuda JM, Zhang S, Pollack L, Young MW, Crane BR. 2013. Flavin reduction activates Drosophila cryptochrome. Proceedings of the National Academy of Sciences of the United States of America 110, 20455-20460.
35. Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C. 2004. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. The Plant Journal 40, 428-438
36. Walter M, Piepenburg K, Schöttler MA, Petersen K, Kahlau S, Tiller N, Drechsel O, Weingartner M, Kudla J, Bock R. 2010. Knockout of the plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency. The Plant Journal 64, 851-863.
37. Wang S, Yang X, Xu M, Lin X, Lin T, Qi J, Shao G, Tian N, Yang Q, Zhang Z, Huang S. 2015. A rare SNP identified a TCP transcription factor essential for tendril development in cucumber. Molecular Plant 8, 1795-1808.
38. Wang YQ, Yang Y, Fei Z, Yuan H, Fish T, Thannhauser TW, Mazourek M, Kochian LV, Wang X, Li L. 2013. Proteomic analysis of chromoplasts from six crop species reveals insights into chromoplast function and development. Journal of experimental botany 64, 949-961.
39. Wimberly BT, Brodersen DE, Clemons WM, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V. 2000. Structure of the 30S ribosomal subunit. Nature 407, 327-339.
40. Woo HR, Goh CH, Park JH, de la Serve BT, Kim JH, Park YI, Nam HG. 2002. Extended leaf longevity in the ore4-1 mutant of Arabidopsis with a reduced expression of a plastid ribosomal protein gene. The Plant Journal 31, 331-340.
41. Yamaguchi K, Subramanian AR. 2000. The plastid ribosomal proteins identification of all the proteins in the 50S subunit of an organelle ribosome (chloroplast). Journal of Biological Chemistry 275, 28466-28482.
42. Yamaguchi K, von Knoblauch K, Subramanian AR. 2000. The plastid ribosomal proteins identification of all the proteins in the 30S subunit of an organelle ribosome (chloroplast). Journal of Biological Chemistry 275, 28455-28465.
43. Yang Y, Qiang X, Owsiany K, Zhang S, Thannhauser TW, Li L. 2011. Evaluation of different multidimensional LC-MS/MS pipelines for isobaric tags for relative and absolute quantitation (iTRAQ)-based proteomic analysis of potato tubers in response to cold storage. Journal of Proteome Research 10, 4647-4660.
44. Yang Y, Thannhauser TW, Li L, Zhang S. 2007. Development of an integrated approach for evaluation of 2-D gel image analysis: Impact of multiple proteins in single spots on comparative proteomics in conventional 2-D gel/MALDI workflow. Electrophoresis 28, 2080-2094.
45. Yin T, Pan G, Liu H, Wu J, Li Y, Zhao Z, Fu T, Zhou Y. 2012. The chloroplast ribosomal protein L21 gene is essential for plastid development and embryogenesis in Arabidopsis. Planta 235, 907-921.
46. Yu F, Liu X, Alsheikh M, Park S, Rodermel S. 2008. Mutations in SUPPRESSOR OF VARIEGATION1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis. The Plant Cell 20, 1786-1804.
47. Yu HD, Yang X-F, Chen S-T, Wang Y-T, Li J-K, Shen Q, Liu X-L, Guo F-Q. 2012. Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis. PLoS Genetics 8, e1002669.
48. Yuan H, Owsiany K, Sheeja TE, et al. 2015. A single amino acid substitution of the ORANGE protein causes carotenoid accumulation in Arabidopsis. Plant Physiology 169, 421-431.
49. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate J, Noller HF. 2001. Crystal structure of the ribosome at 5.5 A resolution. Science 292, 883-896.
50. Zhang JX, Yuan H, Fei ZJ, Pogson BJ, Zhang LG, Li L. 2015. Molecular characterization and transcriptome analysis of orange head Chinese cabbage (Brassica rapa L. ssp. pekinensis). Planta 241, 1381-1394.
51. Zhou X, Sun TH, Wang N, Ling HQ, Lu S, Li L. 2011. The cauliflower Orange gene enhances petiole elongation by suppressing expression of eukaryotic release factor 1. New Phytologist 190, 89-100.
52. Zhou X, Welsch R, Yang Y, Álvarez D, Riediger M, Yuan H, Fish T, Liu J, Thannhauser TW, Li L. 2015. Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. Proceedings of the National Academy of Sciences of the United States of America 112, 3558-3563.