Duplication History and Molecular Evolution of the RbcS Multigene Family in Angiosperms

Overview

Journal J Exp Bot

Publisher Oxford University Press

Specialty Biology

Date 2019 Sep 10

PMID 31498865

Citations 8

Authors

Kana Yamada

Iakov I Davydov

Guillaume Besnard

Nicolas Salamin

Affiliations

Soon will be listed here.

Abstract

Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) is considered to be the main enzyme determining the rate of photosynthesis. The small subunit of the protein, encoded by the rbcS gene, has been shown to influence the catalytic efficiency, CO2 specificity, assembly, activity, and stability of RuBisCO. However, the evolution of the rbcS gene remains poorly studied. We inferred the phylogenetic tree of the rbcS gene in angiosperms using the nucleotide sequences and found that it is composed of two lineages that may have existed before the divergence of land plants. Although almost all species sampled carry at least one copy of lineage 1, genes of lineage 2 were lost in most angiosperm species. We found the specific residues that have undergone positive selection during the evolution of the rbcS gene. We detected intensive coevolution between each rbcS gene copy and the rbcL gene encoding the large subunit of RuBisCO. We tested the role played by each rbcS gene copy on the stability of the RuBisCO protein through homology modelling. Our results showed that this evolutionary constraint could limit the level of divergence seen in the rbcS gene, which leads to the similarity among the rbcS gene copies of lineage 1 within species.

Citing Articles

Transcriptomic responses to shifts in light and nitrogen in two congeneric diatom species.

Ma X, Qin Z, Johnson K, Sweat L, Dai S, Li G Front Microbiol. 2024; 15:1437274.

PMID: 39206371 PMC: 11349689. DOI: 10.3389/fmicb.2024.1437274.

Insights on the enhancement of chilling tolerance in Rice through over-expression and knock-out studies of OsRBCS3.

Hu Y, Tian C, Song S, Li R Plant Signal Behav. 2024; 19(1):2318514.

PMID: 38375792 PMC: 10880504. DOI: 10.1080/15592324.2024.2318514.

A temporal gradient of cytonuclear coordination of chaperonins and chaperones during RuBisCo biogenesis in allopolyploid plants.

Li C, Ding B, Ma X, Yang X, Wang H, Dong Y Proc Natl Acad Sci U S A. 2022; 119(34):e2200106119.

PMID: 35969751 PMC: 9407610. DOI: 10.1073/pnas.2200106119.

The small subunit of Rubisco and its potential as an engineering target.

Mao Y, Catherall E, Diaz-Ramos A, Greiff G, Azinas S, Gunn L J Exp Bot. 2022; 74(2):543-561.

PMID: 35849331 PMC: 9833052. DOI: 10.1093/jxb/erac309.

Rubiscosome gene expression is balanced across the hexaploid wheat genome.

Caruana L, Orr D, Carmo-Silva E Photosynth Res. 2022; 152(1):1-11.

PMID: 35083631 PMC: 9090852. DOI: 10.1007/s11120-022-00897-9.

References

Rensing S . Gene duplication as a driver of plant morphogenetic evolution. Curr Opin Plant Biol. 2014; 17:43-8. DOI: 10.1016/j.pbi.2013.11.002. View

Schymkowitz J, Borg J, Stricher F, Nys R, Rousseau F, Serrano L . The FoldX web server: an online force field. Nucleic Acids Res. 2005; 33(Web Server issue):W382-8. PMC: 1160148. DOI: 10.1093/nar/gki387. View

Ohta T . Time for acquiring a new gene by duplication. Proc Natl Acad Sci U S A. 1988; 85(10):3509-12. PMC: 280241. DOI: 10.1073/pnas.85.10.3509. View

Sugita M, Manzara T, Pichersky E, Cashmore A, Gruissem W . Genomic organization, sequence analysis and expression of all five genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from tomato. Mol Gen Genet. 1987; 209(2):247-56. DOI: 10.1007/BF00329650. View

Dib L, Silvestro D, Salamin N . Evolutionary footprint of coevolving positions in genes. Bioinformatics. 2014; 30(9):1241-9. DOI: 10.1093/bioinformatics/btu012. View

Studer R, Christin P, Williams M, Orengo C . Stability-activity tradeoffs constrain the adaptive evolution of RubisCO. Proc Natl Acad Sci U S A. 2014; 111(6):2223-8. PMC: 3926066. DOI: 10.1073/pnas.1310811111. View

Lu A, Guindon S . Performance of standard and stochastic branch-site models for detecting positive selection among coding sequences. Mol Biol Evol. 2013; 31(2):484-95. DOI: 10.1093/molbev/mst198. View

Sen L, Fares M, Liang B, Gao L, Wang B, Wang T . Molecular evolution of rbcL in three gymnosperm families: identifying adaptive and coevolutionary patterns. Biol Direct. 2011; 6:29. PMC: 3129321. DOI: 10.1186/1745-6150-6-29. View

Flagel L, Wendel J . Gene duplication and evolutionary novelty in plants. New Phytol. 2009; 183(3):557-564. DOI: 10.1111/j.1469-8137.2009.02923.x. View

10.

Thomas-Hall S, Campbell P, Carlens K, Kawanishi E, Swennen R, Sagi L . Phylogenetic and molecular analysis of the ribulose-1,5-bisphosphate carboxylase small subunit gene family in banana. J Exp Bot. 2007; 58(10):2685-97. DOI: 10.1093/jxb/erm129. View

11.

Nei M, Gu X, Sitnikova T . Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci U S A. 1997; 94(15):7799-806. PMC: 33709. DOI: 10.1073/pnas.94.15.7799. View

12.

Kokubun N, Ishida H, Makino A, Mae T . The degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase into the 44-kDa fragment in the lysates of chloroplasts incubated in darkness. Plant Cell Physiol. 2002; 43(11):1390-5. DOI: 10.1093/pcp/pcf159. View

13.

Moore R, Purugganan M . The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol. 2005; 8(2):122-8. DOI: 10.1016/j.pbi.2004.12.001. View

14.

Kubien D, Whitney S, Moore P, Jesson L . The biochemistry of Rubisco in Flaveria. J Exp Bot. 2008; 59(7):1767-77. DOI: 10.1093/jxb/erm283. View

15.

Ogihara Y, Shimizu H, Hasegawa K, Tsujimoto H, Sasakuma T . Chromosome assignment of four photosynthesis-related genes and their variability in wheat species. Theor Appl Genet. 2013; 88(3-4):383-94. DOI: 10.1007/BF00223649. View

16.

Cantsilieris S, Baird P, White S . Molecular methods for genotyping complex copy number polymorphisms. Genomics. 2012; 101(2):86-93. DOI: 10.1016/j.ygeno.2012.10.004. View

17.

Hatch M, Slack C . A new enzyme for the interconversion of pyruvate and phosphopyruvate and its role in the C4 dicarboxylic acid pathway of photosynthesis. Biochem J. 1968; 106(1):141-6. PMC: 1198479. DOI: 10.1042/bj1060141. View

18.

Roulin A, Auer P, Libault M, Schlueter J, Farmer A, May G . The fate of duplicated genes in a polyploid plant genome. Plant J. 2012; 73(1):143-53. DOI: 10.1111/tpj.12026. View

19.

Matsumura H, Mizohata E, Ishida H, Kogami A, Ueno T, Makino A . Crystal structure of rice Rubisco and implications for activation induced by positive effectors NADPH and 6-phosphogluconate. J Mol Biol. 2012; 422(1):75-86. DOI: 10.1016/j.jmb.2012.05.014. View

20.

Lynch M, Force A . The probability of duplicate gene preservation by subfunctionalization. Genetics. 2000; 154(1):459-73. PMC: 1460895. DOI: 10.1093/genetics/154.1.459. View