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The Chloroplast and Mitochondrial Genomes of Salvia miltiorrhiza

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The Salvia miltiorrhiza Genome

Part of the book series: Compendium of Plant Genomes ((CPG))

Abstract

Salvia miltiorrhiza is one of the most widely used medicinal plants. Here, we discuss research progresses made on its chloroplast and mitochondrial genomes. In these studies, strand-specific RNA-Seq and single-molecule real-time (SMRT) sequencing analyses were conducted. Then, the RNA-Seq reads were mapped to the genome assembly to determine the relative expression levels of genes, DNA modifications and RNA editing events. For the chloroplast, the expression levels of all 80 protein-coding genes and 136 putative antisense and intergenic noncoding RNA (ncRNA) genes were detected. A total of 2687 putative modification sites were identified. Further analysis identified two DNA modification motifs: “TATANNNATNA” and “WNYANTGAW”. For the mitochondrial genome, the assembled genome has been validated extensively. A pipeline was developed to predict the RNA editing events using REDItools. A total of 1123 editing sites were identified, including 225 “C” to “U” sites in the protein-coding regions. The nucleotides on both strands at 115 of the 225 sites had undergone RNA editing, which were called symmetrical RNA editing (SRE). Taken together, a complex interplay among DNA transcriptome, modifications in S. miltiorrhiza plastome has been reported. In addition, symmetrical RNA editing events have been identified in its mitochondrial genome.

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References

  • Brennicke A, Marchfelder A, Binder S (1999) RNA editing. FEMS Microbiol Rev 23:297–316

    Article  CAS  Google Scholar 

  • Castandet B, Choury D, Begu D, Jordana X, Araya A (2010) Intron RNA editing is essential for splicing in plant mitochondria. Nucleic Acids Res 38(20):7112–7121

    Article  CAS  Google Scholar 

  • Chan E, Tan M, Xin J, Sudarsanam S, Johnson DE (2010) Interactions between traditional Chinese medicines and Western therapeutics. Curr Opin Drug Discov Dev 13(1):50–65

    CAS  Google Scholar 

  • Chen H, Wu B, Nelson DR, Wu K, Liu C (2014a) Computational identification and systematic classification of novel cytochrome P450 genes in Salvia miltiorrhiza. PLoS ONE 9(12):e115149

    Article  Google Scholar 

  • Chen H, Zhang J, Yuan G, Liu C (2014b) Complex interplay among DNA modification, noncoding RNA expression and protein-coding RNA expression in Salvia miltiorrhiza plastome. PLoS ONE 9(6):e99314

    Article  Google Scholar 

  • Cheng T (2007) Cardiovascular effects of Danshen. Int J Cardiol 121(1):9–22

    Article  Google Scholar 

  • Clark TA, Murray IA, Morgan RD, Kislyuk AO, Spittle KE, Boitano M, Fomenkov A, Roberts RJ, Koriach J (2012) Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing. Nucleic Acids Res 40(4):e29

    Article  CAS  Google Scholar 

  • Georg J, Honsel A, Voss B, Rennenberg H, Hess WR (2010) A long antisense RNA in plant chloroplasts. New Phytol 186(3):615–622

    Article  CAS  Google Scholar 

  • Giege P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci USA 96(26):15324–15329

    Article  CAS  Google Scholar 

  • Gott JM (2003) Expanding genome capacity via RNA editing. C R Biol 326(10–11):901–908

    Article  CAS  Google Scholar 

  • Gott JM, Emeson RB (2000) Functions and mechanisms of RNA editing. Annu Rev Genet 34:499–531

    Article  CAS  Google Scholar 

  • Grewe F, Viehoever P, Weisshaar B, Knoop V (2009) A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res 37(15):5093–5104

    Article  CAS  Google Scholar 

  • Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 31(20):5907–5916

    Google Scholar 

  • He G, Elling AA, Deng XW (2011) The epigenome and plant development. Annu Rev Plant Biol 62:411–435

    Article  CAS  Google Scholar 

  • Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447:418–424

    Article  CAS  Google Scholar 

  • Henze K, Martin W (2003) Evolutionary biology: essence of mitochondria. Nature 426:127–128

    Article  CAS  Google Scholar 

  • Hoch B, Maier RM, Appel K, Igloi GL, Kossel H (1991) Editing of a chloroplast mRNA by creation of an initiation codon. Nature 353(6340):178–180

    Article  CAS  Google Scholar 

  • Lee CY, Agrawal DC, Wang CS, Yu SM, Chen JJ, Tsay HS (2008) T-DNA activation tagging as a tool to isolate Salvia miltiorrhiza transgenic lines for higher yields of tanshinones. Planta Med 74(7):780–786

    Article  CAS  Google Scholar 

  • Li M, Chen J, Peng Y, Wu Q, Xiao P (2008) Investigation of Danshen and related medicinal plants in China. J Ethnopharmacol 120(3):419–426

    Article  Google Scholar 

  • Li Y, Song L, Liu M, Hu Z, Wang Z (2009) Advancement in analysis of Salviae miltiorrhizae Radix et Rhizoma (Danshen). J Chromatogr A 1216(11):1941–1953

    Article  CAS  Google Scholar 

  • Ma Y, Yuan L, Wu B, Li X, Chen S, Lu S (2012) Genome-wide identification and characterization of novel genes involved in terpenoid biosynthesis in Salvia miltiorrhiza. J Exp Bot 63(7):2809–2823

    Article  CAS  Google Scholar 

  • Mallela A, Nishikura K (2012) A-to-I editing of protein coding and noncoding RNAs. Crit Rev Biochem Mol Biol 47(6):493–501

    Article  CAS  Google Scholar 

  • Martienssen RA, Colot V (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293(5532):1070–1074

    Article  CAS  Google Scholar 

  • Martin JA, Wang Z (2011) Next-generation transcriptome assembly. Nat Rev Genet 12:671–682

    Article  CAS  Google Scholar 

  • Mower JP, Palmer JD (2006) Patterns of partial RNA editing in mitochondrial genes of Beta vulgaris. Mol Genet Genomics 276(3):285–293

    Article  CAS  Google Scholar 

  • Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268(4):434–445

    Google Scholar 

  • Picardi E, Horner DS, Chiara M, Schiavon Valle G, Pesole G (2010) Large-scale detection and analysis of RNA editing in grape mtDNA by RNA deep-sequencing. Nucleic Acids Res 38(14):4755–4767

    Article  CAS  Google Scholar 

  • Stern DS, Higgs DC, Yang J (1997) Transcription and translation in chloroplasts. Trends Plant Sci 2(8):308–315

    Article  Google Scholar 

  • Sultan M, Dokel S, Amstislavskiy V, Wuttig D, Sultmann H, Lehrach H, Yaspo ML (2012) A simple strand-specific RNA-Seq library preparation protocol combining the Illumina TruSeq RNA and the dUTP methods. Biochem Biophys Res Commun 422(4):643–646

    Article  CAS  Google Scholar 

  • Takenaka M, Verbitskiy D, van der Merwe JA, Zehrmann A, Brennicke A (2008) The process of RNA editing in plant mitochondria. Mitochondrion 8(1):35–46

    Article  CAS  Google Scholar 

  • Takenaka M, Zehrmann A, Verbitskiy D, Hartel B, Brennicke A (2013) RNA editing in plants and its evolution. Annu Rev Genet 47:335–352

    Article  CAS  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562–578

    Article  CAS  Google Scholar 

  • Verma D, Daniell H (2007) Chloroplast vector systems for biotechnology applications. Plant Physiol 145(4):1129–1143

    Article  CAS  Google Scholar 

  • Wang B (2010) Salvia miltiorrhiza: chemical and pharmacological review of a medicinal plant. J Med Plants Res 4(25):2813–2820

    CAS  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63

    Article  CAS  Google Scholar 

  • Wu B, Chen H, Shao J, Zhang H, Wu K, Liu C (2017) Identification of symmetrical RNA editing events in the mitochondria of Salvia miltiorrhiza by strand-specific RNA sequencing. Sci Rep 7:42250

    Article  CAS  Google Scholar 

  • Xiao Y, Zhang L, Gao S, Saechao S, Di P, Chen J, Chen W (2011) The c4h, tat, hppr and hppd genes prompted engineering of rosmarinic acid biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. PLoS ONE 6(12):e29713

    Article  CAS  Google Scholar 

  • Xu H, Song J, Luo H, Zhang Y, Li Q, Zhu Y, Xu J, Li Y, Song C, Wang B, Sun W, Shen G, Zhang X, Qian J, Ji A, Xu Z, Luo X, He L, Li C, Sun C, Yan H, Cui G, Li X, Wei J, Liu J, Wang Y, Hayward A, Nelson D, Ning Z, Peters RJ, Qi X, Chen S (2016) Analysis of the genome sequence of the medicinal plant Salvia miltiorrhiza. Mol Plant 9(6):949–952

    Article  CAS  Google Scholar 

  • Yan Y, Wang Z (2007) Genetic transformation of the medicinal plant Salvia miltiorrhiza by Agrobacterium tumefaciens-mediated method. Plant Cell Tissue Organ Cult 88(2):175–184

    Article  CAS  Google Scholar 

  • Zghidi-Abouzid O, Merendino L, Buhr F, Malik Ghulam M, Lerbs-Mache S (2011) Characterization of plastid psbT sense and antisense RNAs. Nucleic Acids Res 39(13):5379–5387

    Article  CAS  Google Scholar 

  • Zhang G, Tian Y, Zhang J, Shu L, Yang S, Wang W, Sheng J, Dong Y, Chen W (2015) Hybrid de novo genome assembly of the Chinese herbal plant Danshen (Salvia miltiorrhiza Bunge). Gigascience 4:62

    Article  Google Scholar 

  • Zhong G, Li P, Zeng L, Guan J, Li D, Li S (2009) Chemical characteristics of Salvia miltiorrhiza (Danshen) collected from different locations in China. J Agric Food Chem 57(15):6879–6887

    Article  CAS  Google Scholar 

  • Zhou L, Zuo Z, Chow MS (2005) Danshen: an overview of its chemistry, pharmacology, pharmacokinetics, and clinical use. J Clin Pharmacol 45(12):1345–1359

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work has been supported by Chinese Academy of Medical Sciences, Innovation Funds for Medical Sciences (CIFMS) (2016-I2M-3-016, 2017-I2M-1-013); National Natural Science Foundation of China (81872966).

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Correspondence to Chang Liu .

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Chen, H., Liu, C. (2019). The Chloroplast and Mitochondrial Genomes of Salvia miltiorrhiza. In: Lu, S. (eds) The Salvia miltiorrhiza Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-030-24716-4_5

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