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Identification, evolution and expression analyses of Ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit gene family in wheat (Triticum aestivum L.)

  • Lingyue Qin
  • Yuanxia Xue
  • Ying Fei
  • Lingfeng Zeng
  • Shushen Yang
  • Xiping Deng
Original Article

Abstract

Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) serves as a plentiful leaf protein which functions in both eukaryote and prokaryote photosynthesis. The small subunits of Rubisco (RBCS) exist as a multigene family which regulates the catalytic efficiency of holoenzyme. Here, 20 RBCS family genes were identified in Triticum aestivum genome, and were clustered into 4 clades according to phylogenetic analysis. On the basis of the identified 9 and 8 RBCSs in Triticum urartu and Aegilops tauschii, homology analysis revealed some TaRBCS genes were orthologous to TuRBCSs and AetRBCSs, and the number of in-paralog pairs between RBCSs in wheat were much more than that in T. urartu or A. tauschii. Gene structure, protein motif and cis-acting element analysis exhibited that TaRBCSs in each clade shared some identity. The in silico expression of RBCS genes showed that RBCSs mainly expressed in leaf, flower and caryopsis. Quantitative real-time PCR analysis showed that TaRBCSs were remarkably responsive to drought, salt, ABA and darkness stresses. The work comprehensively studies the RBCS family genes in wheat, and lays the foundation for subsequent functional research of TaRBCSs.

Keywords

RBCS Wheat Phylogenetic analysis Gene expression Abiotic stress 

Notes

Acknowledgments

This work was supported by The National Nature Science Foundation of China (No. 31671609 and No. 51479189), The State Key Laboratory of Soil Erosion and Dryland Farming on Loess Plateau, Institute of Soil and Water Conversation, Chinese Academy of Science (No. 10502), and The National Basic Research Program of China (No. 2015CB150402).

Supplementary material

11738_2018_2658_MOESM1_ESM.pdf (1.9 mb)
Fig. S1 Distribution of RBCSs throughout all clades. RBCSs in wheat, T. urartu, Ae. tauschii, B. distachyon, rice, poplar, and Arabidopsis were divided into 5 clades. Sum of RBCSs in particular genome was presented by number in the bracket (PDF 1989 kb)
11738_2018_2658_MOESM2_ESM.pdf (4.8 mb)
Fig. S2 The number of ortholog pairs between T. urartu or Ae. tauschii genome and wheat sub-genomes. Numbers besides straight line indicate the sum of ortholog pairs between particular genome and sub-genome (PDF 4882 kb)
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Fig. S3 Orthologs between RBCS genes in T. urartu and Ae. tauschi (PDF 2048 kb)
11738_2018_2658_MOESM4_ESM.pdf (1.1 mb)
Fig. S4 Multiple alignment of Rubisco_small domain sequences in moss, gymnosperm, monocot or dicot. Conserved residues across all sequences are displayed in blue. The protein secondary structure α-helix A, B, and β-strands A to D are colored in green and yellow. The accession numbers of these RBCSs are BAA83481.1, BAR94274.1, EFJ27478.1, EFJ07320.1, XP_012074043.1, ABK25403.1, XP_010450913.1, CDX74532.1, AIF75325.1, AED94314.1, BAB19812.1, EMS44969.1, EMT21848.1, AAF07946.1 (PDF 1092 kb)
11738_2018_2658_MOESM5_ESM.pdf (4.8 mb)
Fig. S5 Details (width and site) for conserved motifs among RBCS family members detected by MEME. The maximum motif was set as 50 (PDF 4928 kb)
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Supplementary material 6 (PDF 135 kb)
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Supplementary material 11 (XLSX 17 kb)

References

  1. Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59:1555–1568.  https://doi.org/10.1093/jxb/ern091 CrossRefPubMedGoogle Scholar
  2. Bolser DM, Kerhornou A, Walts B, Kersey P (2015) Triticeae resources in ensembl plants. Plant Cell Physiol 56:e3.  https://doi.org/10.1093/pcp/pcu183 CrossRefPubMedGoogle Scholar
  3. Bolser D, Staines DM, Pritchard E, Kersey P (2016) Ensembl Plants: integrating tools for visualizing, mining, and analyzing plant genomics data. Methods Mol Biol 1374:115–140.  https://doi.org/10.1007/978-1-4939-3167-5_6 CrossRefPubMedGoogle Scholar
  4. Bota J, Medrano H, Flexas J (2004) Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytol 162:671–681.  https://doi.org/10.1111/j.1469-8137.2004.01056.x CrossRefGoogle Scholar
  5. Brenchley R et al (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491:705–710.  https://doi.org/10.1038/nature11650 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cai Z, Liu G, Zhang J, Li Y (2014) Development of an activity-directed selection system enabled significant improvement of the carboxylation efficiency of Rubisco. Protein Cell 5:552–562.  https://doi.org/10.1007/s13238-014-0072-x CrossRefPubMedPubMedCentralGoogle Scholar
  7. Castresana C, Garcia-Luque I, Alonso E, Malik VS, Cashmore AR (1988) Both positive and negative regulatory elements mediate expression of a photoregulated CAB gene from Nicotiana plumbaginifolia. EMBO J 7:1929–1936PubMedPubMedCentralGoogle Scholar
  8. Chen ZJ, Ha M, Soltis D (2007) Polyploidy: genome obesity and its consequences. New Phytol 174:717–720.  https://doi.org/10.1111/j.1469-8137.2007.02084.x CrossRefPubMedPubMedCentralGoogle Scholar
  9. Curmi PM, Cascio D, Sweet RM, Eisenberg D, Schreuder H (1992) Crystal structure of the unactivated form of ribulose-1,5-bisphosphate carboxylase/oxygenase from tobacco refined at 2.0-A resolution. J Biol Chem 267:16980–16989PubMedGoogle Scholar
  10. Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA (2012) PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Res 40:D1194–D1201.  https://doi.org/10.1093/nar/gkr938 CrossRefPubMedGoogle Scholar
  11. Dias MC, Brüggemann W (2007) Differential inhibition of photosynthesis under drought stress in Flaveria species with different degrees of development of the C4 syndrome. Photosynthetica 45:75–84.  https://doi.org/10.1007/s11099-007-0012-6 CrossRefGoogle Scholar
  12. Eversole K, Feuillet C, Mayer KF, Rogers J (2014) Slicing the wheat genome. Introduction. Science 345:285–287.  https://doi.org/10.1126/science.1257983 CrossRefPubMedGoogle Scholar
  13. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37.  https://doi.org/10.1093/nar/gkr367 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Finn RD et al (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230.  https://doi.org/10.1093/nar/gkt1223 CrossRefPubMedGoogle Scholar
  15. Flachmann R, Bohnert HJ (1992) Replacement of a conserved arginine in the assembly domain of Ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit interferes with holoenzyme formation. J Biol Chem 267:10576–11058PubMedGoogle Scholar
  16. Fluhr R, Moses P, Morelli G, Coruzzi G, Chua N-H (1986) Expression dynamics of the pea rbcS multigene family and organ distribution of the transcripts. EMBO J 5:2063–2071PubMedPubMedCentralGoogle Scholar
  17. Genkov T, Spreitzer RJ (2009) Highly conserved small subunit residues influence rubisco large subunit catalysis. J Biol Chem 284:30105–30112.  https://doi.org/10.1074/jbc.M109.044081 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gill BS et al (2004) A workshop report on wheat genome sequencing: international genome research on wheat consortium. Genetics 168:1087–1096.  https://doi.org/10.1534/genetics.104.034769 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Giménez MJ, Pistón F, Atienza SG (2011) Identification of suitable reference genes for normalization of qPCR data in comparative transcriptomics analyses in the Triticeae. Planta 233:163–173.  https://doi.org/10.1007/s00425-010-1290-y CrossRefPubMedGoogle Scholar
  20. Gutteridgel S, Gatenby AA (1995) Rubisco synthesis, assembly, mechanism, and regulation. Plant Cell 7:809–819CrossRefGoogle Scholar
  21. Hauser T, Bhat JY, Milicic G, Wendler P, Hartl FU, Bracher A (2015) Structure and mechanism of the Rubisco-assembly chaperone Raf1. Nat Struct Mol Biol 22:720–728.  https://doi.org/10.1038/nsmb.3062 CrossRefPubMedGoogle Scholar
  22. Hudson GS, Evans JR, von Caemmerer S, Arvidsson YB, Andrews TJ (1992) Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. Plant Physiol 98:294–302CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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 Physiol 156:1603–1611.  https://doi.org/10.1104/pp.111.177030 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Keegstra K, Olsen LJ (1989) Chloroplastic precursors and their transport across the envelope membranes. Annu Rev Plant Phys 40:471–501CrossRefGoogle Scholar
  25. 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 Mol Biol 11:745–759.  https://doi.org/10.1007/bf00019515 CrossRefPubMedGoogle Scholar
  26. Larkin MA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948.  https://doi.org/10.1093/bioinformatics/btm404 CrossRefPubMedGoogle Scholar
  27. Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell Environ 25:275–294CrossRefGoogle Scholar
  28. Lescot M et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327CrossRefPubMedPubMedCentralGoogle Scholar
  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  30. Marcussen T et al (2014) Ancient hybridizations among the ancestral genomes of bread wheat. Science 345:1250092.  https://doi.org/10.1126/science.1250092 CrossRefPubMedGoogle Scholar
  31. Paritosh K, Pental D, Burma PK (2013) Structural and transcriptional characterization of rbcS genes of cotton (Gossypium hirsutum). Plant Mol Biol Rep 31:1176–1183.  https://doi.org/10.1007/s11105-013-0576-1 CrossRefGoogle Scholar
  32. Patel M, Berry JO (2008) Rubisco gene expression in C4 plants. J Exp Bot 59:1625–1634.  https://doi.org/10.1093/jxb/erm368 CrossRefPubMedGoogle Scholar
  33. Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882.  https://doi.org/10.1093/jxb/erq340 CrossRefPubMedGoogle Scholar
  34. Rodermel SR, Abbott MS, Bogorad L (1988) Nuclear-organelle interactions: nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell 55:673–681CrossRefPubMedGoogle Scholar
  35. Rodermel S, Haley J, Jiang C-Z, Tsai C-H, Bogorad L (1996) A mechanism for intergenomic integration: abundance of ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large-subunit mRNA. P Natl Acad Sci USA 93:3881–3885CrossRefGoogle Scholar
  36. Spreitzer RJ (2003) Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. Arch Biochem Biophys 414:141–149CrossRefPubMedGoogle Scholar
  37. Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53:449–475.  https://doi.org/10.1146/annurev.arplant.53.100301.135233 CrossRefPubMedGoogle Scholar
  38. Spreitzer RJ, Esquivel MG, Du Y-C, McLaughlin PD (2001) Alanine-scanning mutagenesis of the small-subunit βA–βB loop of chloroplast Ribulose-1,5-bisphosphate carboxylase/oxygenase: substitution at Arg-71 affects thermal stability and CO2/O2 specificity. Biochemistry 40:5615–5621CrossRefPubMedGoogle Scholar
  39. Su N, Wu Q, Shen Z, Xia K, Cui J (2014) Effects of light quality on the chloroplastic ultrastructure and photosynthetic characteristics of cucumber seedlings. Plant Growth Regul 73:227–235.  https://doi.org/10.1007/s10725-013-9883-7 CrossRefGoogle Scholar
  40. Sugita M, Manzara T, Pichersky E, Cashmore A, Gruissem W (1987) Genomic organization, sequence analysis and expression of all five genes encoding the small subunit of ribulose-l,5-bisphosphate carboxylase/oxygenase from tomato. Mol Genet Genom 209:247–256CrossRefGoogle Scholar
  41. Suzuki Y, Nakabayashi K, Yoshizawa R, Mae T, Makino A (2009) Differences in expression of the RBCS multigene family and Rubisco protein content in various rice plant tissues at different growth stages. Plant Cell Physiol 50:1851–1855.  https://doi.org/10.1093/pcp/pcp120 CrossRefPubMedGoogle Scholar
  42. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739.  https://doi.org/10.1093/molbev/msr121 CrossRefPubMedPubMedCentralGoogle Scholar
  43. van Lun M, Hub JS, van der Spoel D, Andersson I (2014) CO2 and O2 distribution in Rubisco suggests the small subunit functions as a CO2 reservoir. J Am Chem Soc 136:3165–3171.  https://doi.org/10.1021/ja411579b CrossRefPubMedGoogle Scholar
  44. Vandesompele J, Preter KD, Pattyn F, Poppe B, Roy NV, Paepe AD, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:7CrossRefGoogle Scholar
  45. Vassileva V, Demirevska K, Simova-Stoilova L, Petrova T, Tsenov N, Feller U (2012) Long-term field drought affects leaf protein pattern and chloroplast ultrastructure of winter wheat in a cultivar-specific manner. J Agron Crop Sci 198:104–117.  https://doi.org/10.1111/j.1439-037X.2011.00492.x CrossRefGoogle Scholar
  46. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249CrossRefPubMedGoogle Scholar
  47. Whitmore AP, Whalley WR (2009) Physical effects of soil drying on roots and crop growth. J Exp Bot 60:2845–2857.  https://doi.org/10.1093/jxb/erp200 CrossRefPubMedGoogle Scholar
  48. Wostrikoff K, Stern D (2007) Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts. Proc Natl Acad Sci USA 104:6466–6471.  https://doi.org/10.1073/pnas.0610586104 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Zhang L, Zhang L, Sun J, Zhang Z, Ren H, Sui X (2013) Rubisco gene expression and photosynthetic characteristics of cucumber seedlings in response to water deficit. Sci Hortic 161:81–87.  https://doi.org/10.1016/j.scienta.2013.06.029 CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2018

Authors and Affiliations

  1. 1.College of Life ScienceNorthwest A&F UniversityYanglingPeople’s Republic of China
  2. 2.Yangling Vocational and Technical CollegeYanglingPeople’s Republic of China
  3. 3.Institute of Soil and Water ConservationChinese Academy of SciencesYanglingPeople’s Republic of China

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