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Genome-wide identification of serine acetyltransferase (SAT) gene family in rice (Oryza sativa) and their expressions under salt stress

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Abstract

Background

Assimilation of sulfur to cysteine (Cys) occurs in presence of serine acetyltransferase (SAT). Drought and salt stresses are known to be regulated by abscisic acid, whose biosynthesis is limited by Cys. Cys is formed by cysteine synthase complex depending on SAT and OASTL enzymes. Functions of some SAT genes were identified in Arabidopsis; however, it is not known how SAT genes are regulated in rice (Oryza sativa) under salt stress.

Methods and results

Sequence, protein domain, gene structure, nucleotide, phylogenetic, selection, gene duplication, motif, synteny, digital expression and co-expression, secondary and tertiary protein structures, and binding site analyses were conducted. The wet-lab expressions of OsSAT genes were also tested under salt stress. OsSATs have underwent purifying selection. Segmental and tandem duplications may be driving force of structural and functional divergences of OsSATs. The digital expression analyses of OsSATs showed that jasmonic acid (JA) was the only hormone inducing the expressions of OsSAT1;1, OsSAT2;1, and OsSAT2;2 whereas auxin and ABA only triggered OsSAT1;1 expression. Leaf blade is the only plant organ where all OsSATs but OsSAT1;1 were expressed. Wet-lab expressions of OsSATs indicated that OsSAT1;1, OsSAT1;2 and OsSAT1;3 genes were upregulated at different exposure times of salt stress.

Conclusions

OsSAT1;1, expressed highly in rice roots, may be a hub gene regulated by cross-talk of JA, ABA and auxin hormones. The cross-talk of the mentioned hormones and the structural variations of OsSAT proteins may also explain the different responses of OsSATs to salt stress.

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References

  1. Leustek T (2002) Sulfate metabolism. Arabidopsis Book 1:e0017. https://doi.org/10.1199/tab.0017

    Article  PubMed  PubMed Central  Google Scholar 

  2. Droux M (2003) Plant serine acetyltransferase: new insights for regulation of sulphur metabolism in plant cells. Plant Physiol Biochem 41:619–627. https://doi.org/10.1016/s0981-9428(03)00083-4

    Article  CAS  Google Scholar 

  3. Haas FH, Heeg C, Queiroz R et al (2008) Mitochondrial serine acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells. Plant Physiol 148:1055–1067. https://doi.org/10.1104/pp.108.125237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Droux M, Ruffet M-L, Douce R, Job D (1998) Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants. Structural and kinetic properties of the free and bound enzymes. Eur J Biochem 255:235–245. https://doi.org/10.1046/j.1432-1327.1998.2550235.x

    Article  CAS  PubMed  Google Scholar 

  5. Wirtz M, Hell R (2006) Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J Plant Physiol 163:273–286. https://doi.org/10.1016/j.jplph.2005.11.013

    Article  CAS  PubMed  Google Scholar 

  6. Romero LC, Aroca MÁ, Laureano-Marín AM et al (2014) Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Mol Plant 7:264–276. https://doi.org/10.1093/mp/sst168

    Article  CAS  PubMed  Google Scholar 

  7. Kopriva S, Patron N, Keeling P, Leustek T (2008) Phylogenetic analysis of sulfate assimilation and cysteine biosynthesis in phototrophic organisms. In: Hell R, Dahl C, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer, Dordrecht, The Netherlands, pp 33–60

  8. Hell R, Jost R, Berkowitz O, Wirtz M (2002) Molecular and biochemical analysis of the enzymes of cysteine biosynthesis in the plant Arabidopsis thaliana. Amino Acids 22:245–257. https://doi.org/10.1007/s007260200012

    Article  CAS  PubMed  Google Scholar 

  9. Kawashima CG, Berkowitz O, Hell R et al (2005) Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol 137:220–230. https://doi.org/10.1104/pp.104.045377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Xiang X, Wu Y, Planta J et al (2018) Overexpression of serine acetyltransferase in maize leaves increases seed-specific methionine-rich zeins. Plant Biotechnol J 16:1057–1067. https://doi.org/10.1111/pbi.12851

    Article  CAS  PubMed  Google Scholar 

  11. Cao MJ, Wang Z, Zhao Q et al (2014) Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana. Plant J 77:604–615. https://doi.org/10.1111/tpj.12407

    Article  CAS  PubMed  Google Scholar 

  12. Dominguez-Solis JR, He Z, Lima A et al (2008) A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts. Proc Natl Acad Sci USA 105:16386–16391. https://doi.org/10.1073/pnas.0808204105

    Article  PubMed  PubMed Central  Google Scholar 

  13. Goodstein DM, Shu S, Howson R et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186. https://doi.org/10.1093/nar/gkr944

    Article  CAS  PubMed  Google Scholar 

  14. Finn RD, Coggill P, Eberhardt RY et al (2015) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285. https://doi.org/10.1093/nar/gkv1344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Finn RD, Clements J, Arndt W et al (2015) HMMER web server: 2015 update. Nucleic Acids Res 43:W30–W38. https://doi.org/10.1093/nar/gkv397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hall TATA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98. https://doi.org/10.1088/1751-8113/44/8/085201

    Article  CAS  Google Scholar 

  17. Hu B, Jin J, Guo A-Y et al (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297. https://doi.org/10.1093/bioinformatics/btu817

    Article  PubMed  Google Scholar 

  18. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, pp 571–607

  19. Törönen P, Medlar A, Holm L (2018) PANNZER2: a rapid functional annotation web server. Nucleic Acids Res 46:W84–W88. https://doi.org/10.1093/nar/gky350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME Suite. Nucleic Acids Res 43:W39–W49. https://doi.org/10.1093/nar/gkv416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/bf01731581

    Article  CAS  PubMed  Google Scholar 

  22. Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC et al (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248

    Article  CAS  PubMed  Google Scholar 

  23. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8:275–282. https://doi.org/10.1093/bioinformatics/8.3.275

    Article  CAS  Google Scholar 

  24. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Tajima F, Misawa K, Innan H (1998) The amount and pattern of DNA polymorphism under the neutral mutation hypothesis. Genetica 102–103(1–6):103–107

  26. Yang S, Zhang X, Yue J-X et al (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics 280:187–198. https://doi.org/10.1007/s00438-008-0355-0

    Article  CAS  PubMed  Google Scholar 

  27. Darzentas N (2010) Circoletto: visualizing sequence similarity with Circos. Bioinformatics 26:2620–2621. https://doi.org/10.1093/bioinformatics/btq484

    Article  CAS  PubMed  Google Scholar 

  28. Lee T-H, Tang H, Wang X, Paterson AH (2012) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res 41:D1152–D1158. https://doi.org/10.1093/nar/gks1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Sato Y, Takehisa H, Kamatsuki K et al (2013) RiceXPro version 3.0: expanding the informatics resource for rice transcriptome. Nucleic Acids Res 41:D1206–D1213. https://doi.org/10.1093/nar/gks1125

    Article  CAS  PubMed  Google Scholar 

  30. Sato Y, Namiki N, Takehisa H et al (2013) RiceFREND: a platform for retrieving coexpressed gene networks in rice. Nucleic Acids Res 41:D1214–D1221. https://doi.org/10.1093/nar/gks1122

    Article  CAS  PubMed  Google Scholar 

  31. Geourjon C, Deléage G (1995) SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Bioinformatics 11:681–684. https://doi.org/10.1093/bioinformatics/11.6.681

    Article  CAS  Google Scholar 

  32. Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371. https://doi.org/10.1038/nprot.2009.2

    Article  CAS  PubMed  Google Scholar 

  33. Guex N, Peitsch MC, Schwede T (2009) Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis 30:S162–S173. https://doi.org/10.1002/elps.200900140

    Article  PubMed  Google Scholar 

  34. Nguyen MN, Tan KP, Madhusudhan MS (2011) CLICK—topology-independent comparison of biomolecular 3D structures. Nucleic acids Res 39(Web Server issue):W24–W28. https://doi.org/10.1093/nar/gkr393

  35. Jones P, Binns D, Chang H-Y et al (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240. https://doi.org/10.1093/bioinformatics/btu031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622. https://doi.org/10.1373/clinchem.2008.112797

  37. Kim JH, Lim SD, Jang CS (2020) Oryza sativa drought-, heat-, and salt-induced RING finger protein 1 (OsDHSRP1) negatively regulates abiotic stress-responsive gene expression. Plant Mol Biol 103:235–252. https://doi.org/10.1007/s11103-020-00989-x

    Article  CAS  PubMed  Google Scholar 

  38. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

  39. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40:1–12. https://doi.org/10.1093/nar/gks596

  40. Rademacher EH, Offringa R (2012) Evolutionary adaptations of plant AGC kinases: from light signaling to cell polarity regulation. Front Plant Sci. https://doi.org/10.3389/fpls.2012.00250

    Article  PubMed  PubMed Central  Google Scholar 

  41. Xu C, Luo F, Hochholdinger F (2016) LOB domain proteins: beyond lateral organ boundaries. Trends Plant Sci 21:159–167. https://doi.org/10.1016/j.tplants.2015.10.010

    Article  CAS  PubMed  Google Scholar 

  42. Chen Y-C, Li C-L, Hsiao Y-Y et al (2014) Structure and function of TatD exonuclease in DNA repair. Nucleic Acids Res 42:10776–10785. https://doi.org/10.1093/nar/gku732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Bækgaard L, Mikkelsen MD, Sørensen DM et al (2010) A combined zinc/cadmium sensor and zinc/cadmium export regulator in a heavy metal pump. J Biol Chem 285:31243–31252. https://doi.org/10.1074/jbc.m110.111260

    Article  PubMed  PubMed Central  Google Scholar 

  44. Sankararaman S, Sha F, Kirsch JF et al (2010) Active site prediction using evolutionary and structural information. Bioinformatics 26:617–624. https://doi.org/10.1093/bioinformatics/btq008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Cvijović I, Good BH, Desai MM (2018) The effect of strong purifying selection on genetic diversity. Genetics 209:1235–1278. https://doi.org/10.1534/genetics.118.301058

    Article  PubMed  PubMed Central  Google Scholar 

  46. Yang Z, Yoder AD (1999) Estimation of the transition/transversion rate bias and species sampling. J Mol Evol 48:274–283. https://doi.org/10.1007/pl00006470

    Article  CAS  PubMed  Google Scholar 

  47. Šmarda P, Bureš P, Horová L et al (2014) Ecological and evolutionary significance of genomic GC content diversity in monocots. Proc Natl Acad Sci 111:E4096–E4102. https://doi.org/10.1073/pnas.1321152111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Panchy N, Lehti-Shiu M, Shiu SH (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316. https://doi.org/10.1104/pp.16.00523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Kuo Y-T, Chao Y-T, Chen W-C et al (2019) Segmental and tandem chromosome duplications led to divergent evolution of the chalcone synthase gene family in Phalaenopsis orchids. Ann Bot 123:69–77. https://doi.org/10.1093/aob/mcy136

    Article  CAS  PubMed  Google Scholar 

  50. Watanabe M, Mochida K, Kato T et al (2008) Comparative genomics and reverse genetics analysis reveal indispensable functions of the serine acetyltransferase gene family in Arabidopsis. Plant Cell 20:2484–2496. https://doi.org/10.1105/tpc.108.060335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ben-Hur A, Brutlag D (2006) Sequence motifs: highly predictive features of protein function. In: Guyon I, Nikravesh M, Gunn S, Zadeh LA (eds) Feature extraction. Studies in fuzziness and soft xomputing, vol 207. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-35488-8_32

  52. Marks DS, Colwell LJ, Sheridan R et al (2011) Protein 3D structure computed from evolutionary sequence variation. PLoS One 6:e28766. https://doi.org/10.1371/journal.pone.0028766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Yi H, Dey S, Kumaran S et al (2013) Structure of soybean serine acetyltransferase and formation of the cysteine regulatory complex as a molecular chaperone. J Biol Chem 288:36463–36472. https://doi.org/10.1074/jbc.m113.527143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Wirtz M, Droux M (2005) Synthesis of the sulfur amino acids: cysteine and methionine. Photosynth Res 86:345–362. https://doi.org/10.1007/s11120-005-8810-9

    Article  CAS  PubMed  Google Scholar 

  55. Wang Y, Hou Y, Qiu J et al (2020) Abscisic acid promotes jasmonic acid biosynthesis via a ‘SAPK10-bZIP72-AOC’ pathway to synergistically inhibit seed germination in rice (Oryza sativa). New Phytol 228:1336–1353. https://doi.org/10.1111/nph.16774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Wang J, Song L, Gong X et al (2020) Functions of jasmonic acid in plant regulation and response to abiotic stress. Int J Mol Sci. https://doi.org/10.3390/ijms21041446

    Article  PubMed  PubMed Central  Google Scholar 

  57. Yang J, Duan G, Li C et al (2019) The crosstalks between jasmonic acid and other plant hormone signaling highlight the involvement of jasmonic acid as a core component in plant response to biotic and abiotic stresses. Front Plant Sci 10:1–12. https://doi.org/10.3389/fpls.2019.01349

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Plant Production and Technologies, Faculty of Applied Sciences, Mus Alparslan University, Mus, Turkey

    Fırat Kurt

  2. Department of Crop and Animal Production, Cilimli Vocational School, Duzce University, Cilimli, Duzce, Turkey

    Ertugrul Filiz

  3. Department of Agricultural Biotechnology, Faculty of Agriculture, Iğdır University, Iğdır, Turkey

    Adnan Aydın

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  1. Fırat Kurt
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EF and FK designed the study. EF, FK and AA conducted the experiments and analyzed the data. All authors contributed to writing and editing the manuscript.

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Correspondence to Ertugrul Filiz.

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Kurt, F., Filiz, E. & Aydın, A. Genome-wide identification of serine acetyltransferase (SAT) gene family in rice (Oryza sativa) and their expressions under salt stress. Mol Biol Rep 48, 6277–6290 (2021). https://doi.org/10.1007/s11033-021-06620-6

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