Abstract
Sage (Salvia officinalis L.) is not found in Turkey's natural flora; however, its cultivation has been increasing in recent years. The species is widely cultivated in many provinces of the Aegean and the Mediterranean regions. There has been no information regarding genetic characteristics and the intra-individual phylogeny of cultivated sage. The levels of genetic relatedness of 19 Salvia samples from Izmir were determined by molecular tools. The sequences from the internal transcriber spacer (ITS) region of 18S–28S nuclear ribosomal DNA (nrDNA) locus were amplified by PCR and sequenced. Approximately, a 710 bp single amplified product was obtained in all genotypes. Of the nineteen Salvia specimens, six were identified as Salvia x sylvestris L. and the remaining 13 specimens were S. officinalis. The sequences of both species shared no similar secondary structures. The ITS region of all specimens contains several indels and substitutions. In the phylogenetic dendrogram, three major clusters (I, II, and III) and two independent branches (IV and V) were observed. Ninety-seven percent of local Salvia specimens were clustered in two branches (I and II), indicating a high diversity of genetic relatedness. Sequence divergence was higher among the specimens of S. officinalis than the specimens of Salvia x sylvestris.
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References
Alvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434. https://doi.org/10.1016/S1055-7903(03)00208-2
Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ (1995) The ITS region of nuclear ribosomal DNA: A valuable source of evidence on Angiosperm phylogeny. Ann Mo Bot Gard 82:247–277. https://doi.org/10.2307/2399880
Bezić N, Samanić I, Dunkić V, Besendorfer V, Puizina J (2009) Essential oil composition and internal transcribed spacer (ITS) sequence variability of four South-Croatian Satureja species (Lamiaceae). Molecules 14(3):925–938
Ceylan A, Kaya N, Çelik N (1990) Studies on the Culture of Medicinal Sage (Salvia officinalis L.). Ege University Faculty of Agriculture J 26:127–141
DePamphilis CW, Young ND, Wolfe AD (1997) Evolution of plastid gene rps2 in a lineage of hemiparasitic and holoparasitic plants: Many losses of photosynthesis and complex patterns of rate variation. Proc Natl Acad Sci USA 94:7367–7372. https://doi.org/10.1073/pnas.94.14.7367
Drew BT, Sytsma KJ (2011) Testing the monophyly and placement of Lepechinia in the tribe Mentheae (Lamiaceae). Syst Bot 36:1038–1049. https://doi.org/10.1600/036364411X605047
Dweck A (2000) The Folklore and Cosmetic Use of Various Salvia Species. In Sage: The Genus Salvia (Edited by Spiridon E. Kintzios). Harwood Academic Publishers, The Netherlands, 1–26
Edger PP, Tang M, Bird KA, Mayfield DR, Conant G, Mummenhoff K, Koch MA, Pires JC (2014) Secondary structure analyses of the nuclear rRNA internal transcribed spacers and assessment of its phylogenetic utility across the Brassicaceae (Mustards). PLoS ONE 9:e101341. https://doi.org/10.1371/journal.pone.0101341
Fabriki-Ourang S (2017) Investigation in the intergenic transcribed sequences to determination of genetic variation for Iranian species of Salvia. J Biodivers Environ Sci 11:92–100
Grajales A, Aguilar C, Sanchez JA (2007) Phylogenetic reconstruction using secondary structures of Internal Transcribed Spacer 2 (ITS2, rDNA): finding the molecular and morphological gap in Caribbean gorgonian corals. BMC Evol Biol 7:90. https://doi.org/10.1186/1471-2148-7-90
Grdiša M, JUG-Dujaković M, Lončarić M, Carović-Stanko K, Ninčević T, Liber Z, Radosavljević I, Šatović Z (2015) Dalmatian Sage (Salvia officinalis L.): A review of biochemical contents, medical properties and genetic diversity. Agric Conspec Sci 80:69–78
Han JP, Shi LC, Chen XC, Lin YL (2012) Comparison of four DNA barcodes in identifying certain medicinal plants of Lamiaceae. J Syst Evol 50:227–234. https://doi.org/10.1111/j.1759-6831.2012.00184.x
Hughes CE, Eastwood RJ, Bailey CD (2006) From famine to feast? Selecting nuclear DNA sequence loci for plant species-level phylogeny reconstruction. Phil Trans Biol Sci 361:211–225. https://doi.org/10.1098/rstb.2005.1735
Ipek A, Gurbuz B (2010) Salvia species in flora of Turkey and their status in danger. J Field Crops Central Res Institute 19:30–35
Jenks AA, Walker JB (2011) Kim SC (2011) Evolution and origins of the Mazatec hallucinogenic sage, Salvia divinorum (Lamiaceae): a molecular phylogenetic approach. J Plant Res 124:593–600. https://doi.org/10.1007/s10265-010-0394-6
Karik U, Cinar O, Tunçturk M, Sekeroglu N, Gezici S (2018) Essential oil composition of some Sage (Salvia spp.) species cultivated in Izmir (Turkey) ecological conditions. Indian J Pharm Educ Res 52:102–107. https://doi.org/10.5530/ijper.52.4s.83
Keskin F, Kaya I, Usta M, Demir I, Sipahioglu HM, Nemli Y (2017) Molecular cloning and sequence analysis of the its region of nuclear ribosomal DNA for species identification in dodders (Cuscuta; Convolvulaceae). Int J Agric Biol 19:1447–1451
Kirici S, Ozguven M, Yenikalaycı A (1996) Investigations on medicinal sage in Cukurova region. Workshop of Medicinal and Aromatic Plants, 25–26, Izmir, 39–40
Koehler-Santos P, Lorenz-Lemke AP, Muschner VC, Bonatto SL, Salzano FM, Freitas LB (2006) Molecular genetic variation in Passiflora alata (Passifloraceae), an invasive species in southern Brazil. Biol J Linn Soc 88:611–630. https://doi.org/10.1111/j.1095-8312.2006.00647.x
Kusaksız G (2019) Rare and endemic taxa of Lamiaceae in Turkey and their threat categories. J Sci Perspect 3:69–84. https://doi.org/10.26900/jsp.3.008
Li QQ, Li MH, Yuan QJ, Cui ZH, Huang LQ, Xiao PG (2013) Phylogenetic relationships of Salvia (Lamiaceae) in China: evidence from DNA sequence datasets. J Syst Evol 51:184–195
Liao BS, Chen XC, Han J, Dan Y, Wang L, Jiao W, Song J, Chen S (2015) Identification of commercial Ganoderma (Lingzhi) species by ITS2 sequences. Chin Med 10:22. https://doi.org/10.1186/s13020-015-0056-7
Lorenz-Lemke AP, Muschner VC, Bonatto SL, Cervi AC, Salzano FM, Freitas LB (2005) Phylogeographic inferences concerning evolution of Brazilian Passiflora actinia and P. elegans (Passifloraceae) based on ITS (nr DNA) variation. Ann Bot 95:799–806. https://doi.org/10.1093/aob/mci079
Mäder G, Zamberlan PM, Nelson JR, Fagundes NJR, Magnus T, Salzano FM, Bonatto SL, Freitas LB (2010) The use and limits of ITS data in the analysis of intraspecific variation in Passiflora L. (Passifloraceae). Genet Mol Biol 33:99–108. https://doi.org/10.1590/S1415-47572009005000101
Mąkol J, Saboori A, Felska M (2019) Inter-and intraspecific variability of morphological and molecular characters in Allothrombium species, with special reference to Allothrombium fuliginosum. Exp Appl Acarol 78:485–504. https://doi.org/10.1007/s10493-019-00400-5
Manos P, Doyle JJ, Nixon KC (1999) Phylogeny, biogeography and processes of molecular differantion in Quercus subgenus Quercus (Fagaceae). Mol Phylogenetics Evol 12:333–349. https://doi.org/10.1006/mpev.1999.0614
Mayr E (1954) Change of genetic environment and evolution. In: Huxley J, Hardy AC, Ford EB (eds) Evolution as a Process. Allen and Unwin, London, pp 157–180
Muschner VC, Lorenz AP, Cervi AC, Bonatto SL, SouzaChies TT, Salzano FM, Freitas LB (2003) A first molecular phylogenetic analysis of Passiflora (Passifloraceae). Am J Bot 90:1229–1238. https://doi.org/10.3732/ajb.90.8.1229
Pillmann A, Woolcott GW, Olsen JL, Stam WT, King RJ (1997) Inter- and intraspecific genetic variation in Caulerpa (Chlorophyta) based on nuclear rDNA ITS sequences. Eur J Phycol 32:379–386. https://doi.org/10.1080/09670269710001737319
Semerdjieva IB, Zheljazkov VD (2019) Chemical constituents, biological properties, and uses of Tribulus terrestris: A Review. Nat Prod Commun 1:26. https://doi.org/10.1177/1934578X19868394
Shiran B, Alian M, Kharazian N (Unpublished) Phylogenetic analysis of Salvia species from Iran based on morphological and nuclear ribosomal internal transcribed spacer and chloroplast trnL-F sequences. Unpublished
Smith BJ, Sivasithamparam K (2000) Internal transcribed spacer ribosomal DNA sequence of five species of Ganoderma from Australia. Mycol Res 104:943–951
Stefanović S, Olmastead RG (2004) Testing the phylogenetic position of a parasitic plant (Cuscuta, Convolvulaceae, Asteridae): Bayesian inference and the parametric bootstrap on data drawn from three genomes. Syst Biol 53:384–399. https://doi.org/10.1080/10635150490445896
Thornhill DJ, Lajeunesse TC, Santos SR (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16:5326–5340. https://doi.org/10.1111/j.1365-294X.2007.03576.x
Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (1972) Flora Europaea, 3. Cambridge University Press
Walker JB, Sytsma KJ (2007) Staminal evolution in the genus Salvia (Lamiaceae): molecular phylogenetic evidence for multiple origins of the staminal lever. Ann Bot 100:375–391. https://doi.org/10.1093/aob/mcl176
Wang M, Zhao HX, Wang L, Wang T, Yang RW, Wang XL, Zhou YH, Ding CB, Zhang L (2013) Potential use of DNA barcoding for the identification of Salvia based on cpDNA and nrDNA sequences. Gene 528:206–215. https://doi.org/10.1016/j.gene.2013.07.009
Wang X, Ma T, Yun Y, Li Y, Zhang J, Liang H, Yang X (2021) Distinct phylogeographic structures and evolutionary histories of wild medicinal Salvia miltiorrhiza Bunge plant populations in the mountains of Central China. Genet Resour Crop Evol. https://doi.org/10.1007/s10722-021-01189-2
Wheeler WC, Honeycutt RL (1988) Paired sequence difference in ribosomal RNAs: evolutionary and phylogenetic implication. Mol Biol Evol 5:90–96. https://doi.org/10.1093/oxfordjournals.molbev.a040480
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press Inc., New York, pp 315–322
Will M, Claßen-Bockhoff R (2017) Time to split Salvia s.l. (Lamiaceae): new insights from Old World Salvia phylogeny. Mol Phylogenet Evol 109:33–58. https://doi.org/10.1016/j.ympev.2016.12.041
Wolfe AD, dePamphilis CW (1995) Systematic implications of relaxed functional constraints on the RUBISCO large subunit in parasitic plants of the Scrophulariaceae and Orobanchaceae. Am J Bot (abst) 82:6
Yilmaz D, Gokduman ME (2015) Determination of Physico-Mechanical Properties of Sage (Salvia officinalis l.) at Different Moisture Contents. Suleyman Demirel University J Facul Agricul 10:73–82
Young ND, Steiner KE, dePamphilis CW (1999) The evolution of parasitism in Scrophulariaceae/Orobanchaceae: Plastid gene sequences refute an evolutionary transition series. Ann Mo Bot Gard 4:876–893. https://doi.org/10.2307/2666173
Zhang Y, Li X, Wang Z (2013) Diversity evaluation of Salvia miltiorrhiza using ISSR markers. Biochem Genet 51:707–721. https://doi.org/10.1007/s10528-013-9600-2
Zhang X, Xu Z, Pei H, Chen Z, Tan X, Hu J, Yang B, Sun J (2017) Intraspecific variation and phylogenetic relationships are revealed by ITS1 secondary structure analysis and single nucleotide polymorphism in Ganoderma lucidum. PLoS ONE. https://doi.org/10.1371/journal.pone.0169042
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Tursun, A.O., Sipahioglu, H.M. & Telci, I. Genetic relationships and diversity within cultivated accessions of Salvia officinalis L. in Turkey. Plant Biotechnol Rep 15, 663–672 (2021). https://doi.org/10.1007/s11816-021-00712-2
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DOI: https://doi.org/10.1007/s11816-021-00712-2