RBCS1A and RBCS3B, two major members within the Arabidopsis RBCS multigene family, function to yield sufficient Rubisco content for leaf photosynthetic capacity

Journal of Experimental Botany

Volumn 63, Issue 5, 2012, Pages 2159-2170

  Izumi, Masanori ^a   Tsunoda, Honami ^a   Suzuki, Yuji ^a   Makino, Amane ^a   Ishida, Hiroyuki ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Arabidopsis; RbcL; RBCS multigene family; Rubisco

Indexed keywords

ARABIDOPSIS PROTEIN; BACTERIAL DNA; MESSENGER RNA; PLANT RNA; RIBULOSEBISPHOSPHATE CARBOXYLASE; T DNA; T-DNA;

ARABIDOPSIS; ARTICLE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MULTIGENE FAMILY; PHENOTYPE; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; PHENOTYPE; PHOTOSYNTHESIS; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; RIBULOSE-BISPHOSPHATE CARBOXYLASE; RNA, MESSENGER; RNA, PLANT;

ARABIDOPSIS;

EID: 84858049305     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err434     Document Type: Article

References (55)

1. Andersson I. 1996. Large structures at high resolution: the 1.6 angstrom crystal structure of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase complexed with 2-carboxyarabinitol bisphosphate. Journal of Molecular Biology 259, 160-174.
2. Arnon DI. 1949. Copper enzymes in isolated chloroplasts-polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1-15.
3. Boulouis A, Raynaud C, Bujaldon S, Aznar A, Wollman FA, Choquet Y. 2011. The nucleus-encoded trans-acting factor MCA1 plays a critical role in the regulation of cytochrome f synthesis in Chlamydomonas chloroplasts. The Plant Cell 23, 333-349.
4. Cheng SH, Moore BD, Seemann JR. 1998. Effects of short-and long-term elevated CO2 on the expression of ribulose-1,5-bisphosphate carboxylase/ oxygenase genes and carbohydrate accumulation in leaves of Arabidopsis thaliana (L.) Heynh. Plant Physiology 116, 715-723. (Pubitemid 128482300)
5. Dean C, Pichersky E, Dunsmuir P. 1989. Structure, evolution, and regulation of rbcS genes in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 40, 415-439.
6. Dedonder A, Rethy R, Fredericq H, Vanmontagu M, Krebbers E. 1993. Arabidopsis rbcS genes are differentially regulated by light. Plant Physiology 101, 801-808.
7. Evans JR. 1986. The relationship between carbon-dioxide-limited photosynthetic rate and ribulose-1,5-bisphosphate-carboxylase content in two nuclear-cytoplasm substitution lines of wheat, and the coordination of ribulose-bisphosphate-carboxylation and electrontransport capacities. Planta 167, 351-358.
8. Evans JR. 1989. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9-19.
9. Ewing RM, Jenkins GI, Langdale JA. 1998. Transcripts of maize RbcS genes accumulate differentially in C-3 and C-4 tissues. Plant Molecular Biology 36, 593-599. (Pubitemid 28139558)
10. Farquhar GD, von Caemmerer S, Berry JA. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78-90.
11. Friedrich JW, Huffaker RC. 1980. Photosynthesis, leaf resistances, and ribulose-1,5-bisphosphate carboxylase degradation in senescing barley leaves. Plant Physiology 65, 1103-1107.
12. Galili S, Avivi Y, Feldman M. 1998. Differential expression of three RbcS subfamilies in wheat. Plant Science 139, 185-193. (Pubitemid 29048406)
13. Genkov T, Meyer M, Griffiths H, Spreitzer RJ. 2010. Functional hybrid Rubisco enzymes with plant small subunits and algal large subunits: engineered rbcS cDNA for expression in Chlamydomonas. Journal of Biological Chemistry 285, 19833-19841.
14. Getzoff TP, Zhu GH, Bohnert HJ, Jensen RG. 1998. Chimeric Arabidopsis thaliana ribulose-1,5-bisphosphate carboxylase/oxygenase containing a pea small subunit protein is compromised in carbamylation. Plant Physiology 116, 695-702. (Pubitemid 128482297)
15. Grimm R, Grimm M, Eckerskorn C, Pohlmeyer K, Rohl T, Soll J. 1997. Postimport methylation of the small subunit of ribulose-1,5-bisphosphate carboxylase in chloroplasts. FEBS Letters 408, 350-354. (Pubitemid 27227031)
16. Hahnen S, Joeris T, Kreuzaler F, Peterhansel C. 2003. Quantification of photosynthetic gene expression in maize C-3 and C-4 tissues by real-time PCR. Photosynthesis Research 75, 183-192. (Pubitemid 36391717)
17. Hudson GS, Evans JR, von Caemmerer S, Arvidsson YBC, Andrews TJ. 1992. Reduction of ribulose-1,5-bisphosphate carboxylase oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. Plant Physiology 98, 294-302.
18. Ichikawa K, Miyake C, Iwano M, Sekine M, Shinmyo A, Kato K. 2008. Ribulose 1,5-bisphosphate carboxylase/oxygenase large subunit translation is regulated in a small subunit-independent manner in the expanded leaves of tobacco. Plant and Cell Physiology 49, 214-225. (Pubitemid 351231587)
19. Imai K, Suzuki Y, Mae T, Makino A. 2008. Changes in the synthesis of Rubisco in rice leaves in relation to senescence and N influx. Annals of Botany 101, 135-144. (Pubitemid 350274507)
20. Ishida H, Nishimori Y, Sugisawa M, Makino A, Mae T. 1997. The large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is fragmented into 37-kDa and 16-kDa polypeptides by active oxygen in the lysates of chloroplasts from primary leaves of wheat. Plant and Cell Physiology 38, 471-479. (Pubitemid 127467263)
21. Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T. 2008. Mobilization of Rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiology 148, 142-155. (Pubitemid 352847588)
22. Ishikawa C, Hatanaka T, Misoo S, Miyake C, Fukayama H. 2011. Functional incorporation of sorghum small subunit increases the catalytic turnover rate of Rubisco in transgenic rice. Plant Physiology 156, 1603-1611.
23. Izumi M, Wada S, Makino A, Ishida H. 2010. The autophagic degradation of chloroplasts via Rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiology 154, 1196-1209.
24. Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch HJ, Rosenkranz R, Stabler N, Schonfeld B, Kreuzaler F, Peterhansel C. 2007. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nature Biotechnology 25, 593-599. (Pubitemid 46834840)
25. Knight MR, Jenkins GI. 1992. Genes encoding the small subunit of ribulose 1,5-bisphosphate carboxylase oxygenase in Phaseolus vulgaris L.: nucleotide sequence of cDNA clones and initial studies of expression. Plant Molecular Biology 18, 567-579.
26. Krebbers E, Seurinck J, Herdies L, Cashmore AR, Timko MP. 1988. Four genes in two diverged subfamilies encode the ribulose-1,5-bisphosphate carboxylase small subunit polypeptides of Arabidopsis thaliana. Plant Molecular Biology 11, 745-759.
27. Loiselay C, Gumpel NJ, Girard-Bascou J, Watson AT, Purton S, Wollman FA, Choquet Y. 2008. Molecular identification and function of cis-and trans-acting determinants for petA transcript stability in Chlamydomonas reinhardtii chloroplasts. Molecular and Cellular Biology 28, 5529-5542.
28. Mae T, Makino A, Ohira K. 1983. Changes in the amounts of ribulose bisphosphate carboxylase synthesized and degraded during the life-span of rice leaf (Oryza sativa L.). Plant and Cell Physiology 24, 1079-1086.
29. Makino A, Mae T, Ohira K. 1988. Differences between wheat and rice in the enzymic properties of ribulose-1,5-bisphosphate carboxylase oxygenase and the relationship to photosynthetic gas exchange. Planta 174, 30-38.
30. Makino A, Nakano H, Mae T, Shimada T, Yamamoto N. 2000. Photosynthesis, plant growth and N allocation in transgenic rice plants with decreased Rubisco under CO2 enrichment. Journal of Experimental Botany 51, 383-389. (Pubitemid 30104765)
31. Makino A, Osmond B. 1991. Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat. Plant Physiology 96, 355-362. (Pubitemid 21914020)
32. Makino A, Sakuma H, Sudo E, Mae T. 2003. Differences between maize and rice in N-use efficiency for photosynthesis and protein allocation. Plant and Cell Physiology 44, 952-956. (Pubitemid 37231837)
33. Makino A, Shimada T, Takumi S, Kaneko K, Matsuoka M, Shimamoto K, Nakano H, Miyao-Tokutomi M, Mae T, Yamamoto N. 1997. Does decrease in ribulose-1,5-bisphosphate carboxylase by antisense RbcS lead to a higher N-use efficiency of photosynthesis under conditions of saturating CO2 and light in rice plants̈Plant Physiology 114, 483-491. (Pubitemid 28381802)
34. Meier I, Callan KL, Fleming AJ, Gruissem W. 1995. Organ-specific differential regulation of a promoter subfamily for the ribulose-1,5-biphosphate carboxylase oxygenase small-subunit genes in tomato. Plant Physiology 107, 1105-1118.
35. Ogawa S, Suzuki Y, Yoshizawa R, Kanno K, Makino A. 2011. Effect of individual suppression of RBCS multigene family on Rubisco contents in rice leaves. Plant, Cell and Environment (in press).
36. Quick WP, Schurr U, Fichtner K, Schulze ED, Rodermel SR, Bogorad L, Stitt M. 1991a. The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS. The Plant Journal 1, 51-58. (Pubitemid 121001032)
37. Quick WP, Schurr U, Scheibe R, Schulze ED, Rodermel SR, Bogorad L, Stitt M. 1991b. Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with antisense rbcS. 1. Impact on photosynthesis in ambient growth conditions. Planta 183, 542-554.
38. Rodermel S, Haley J, Jiang CZ, Tsai CH, Bogorad L. 1996. A mechanism for intergenomic integration: abundance of ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large-subunit mRNA. Proceedings of the National Academy of Sciences, USA 93, 3881-3885. (Pubitemid 26144216)
39. Sasanuma T. 2001. Characterization of the rbcS multigene family in wheat: subfamily classification, determination of chromosomal location and evolutionary analysis. Molecular Genetics and Genomics 265, 161-171.
40. Sawbridge TI, Knight MR, Jenkins GI. 1996. Ontogenetic regulation and photoregulation of members of the Phaseolus vulgaris L. rbcS gene family. Planta 198, 31-38.
41. Schwarte S, Tiedemann R. 2011. A gene duplication/loss event in the ribulose-1,5-bisphosphate-carboxylase/oxygenase (Rubisco) small subunit gene family among accessions of Arabidopsis thaliana. Molecular Biology and Evolution 28, 1861-1876.
42. Sharkey TD. 1985. Photosynthesis in intact leaves of C3 plants-physics, physiology and rate limitations. Botanical Review 51, 53-105.
43. Silverthorne J, Tobin EM. 1990. Posttranscriptional regulation of organ-specific expression of individual rbcS mRNAs in Lemna gibba. The Plant Cell 2, 1181-1190. (Pubitemid 120015468)
44. Silverthorne J, Wimpee CF, Yamada T, Rolfe SA, Tobin EM. 1990. Differential expression of individual genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in Lemna gibba. Plant Molecular Biology 15, 49-58.
45. Spreitzer RJ. 2003. Role of the small subunit in ribulose-1,5- bisphosphate carboxylase/oxygenase. Archives of Biochemistry and Biophysics 414, 141-149. (Pubitemid 36627346)
46. Suzuki Y, Kihara-Doi T, Kawazu T, Miyake C, Makino A. 2010. Differences in Rubisco content and its synthesis in leaves at different positions in Eucalyptus globulus seedlings. Plant, Cell and Environment 33, 1314-1323.
47. Suzuki Y, Makino A, Mae T. 2001. Changes in the turnover of Rubisco and levels of mRNAs of rbcL and rbcS in rice leaves from emergence to senescence. Plant, Cell and Environment 24, 1353-1360. (Pubitemid 34002002)
48. Suzuki Y, Miyamoto T, Yoshizawa R, Mae T, Makino A. 2009a. Rubisco content and photosynthesis of leaves at different positions in transgenic rice with an overexpression of RBCS. Plant, Cell and Environment 32, 417-427.
49. Suzuki Y, Nakabayashi K, Yoshizawa R, Mae T, Makino A. 2009b. Differences in expression of the RBCS multigene family and Rubisco protein content in various rice plant tissues at different growth stages. Plant and Cell Physiology 50, 1851-1855.
50. Suzuki Y, Ohkubo M, Hatakeyama H, Ohashi K, Yoshizawa R, Kojima S, Hayakawa T, Yamaya T, Mae T, Makino A. 2007. Increased Rubisco content in transgenic rice transformed with the 'sense' rbcS gene. Plant and Cell Physiology 48, 626-637. (Pubitemid 47356115)
51. von Caemmerer S, Farquhar GD. 1981. Some relationships between the biochemistry of photosynthesis and the gas-exchange of leaves. Planta 153, 376-387.
52. Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A. 2009. Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiology 149, 885-893.
53. Wanner LA, Gruissem W. 1991. Expression dynamics of the tomato rbcS gene family during development. The Plant Cell 3, 1289-1303. (Pubitemid 21913673)
54. Wostrikoff K, Stern D. 2007. Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts. Proceedings of the National Academy of Sciences, USA 104, 6466-6471. (Pubitemid 47186117)
55. Yoon M, Putterill JJ, Ross GS, Laing WA. 2001. Determination of the relative expression levels of Rubisco small subunit genes in Arabidopsis by rapid amplification of cDNA ends. Analytical Biochemistry 291, 237-244. (Pubitemid 32373158)