Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Chloroplast and nuclear ribosomal cistron phylogenomics in a group of closely related sections in Salvia subg. Calosphace

  • 24 Accesses

Abstract

Sage phylogenies have not resolved many shallow level clades within problematic Salvia subgenus Calosphace, hindered by the difficulty in finding sufficiently variable loci. We assembled fifteen chloroplast genomes and nuclear ribosomal cistrons from non-target reads of a nuclear hybrid enrichment project to assess the phylogenetic utility for a closely related group of mainly Mexican sections. Chloroplast synteny is confirmed with 10 Lamiales chloroplasts, supporting a map to reference assembly. Salvia miltiorrhiza Bunge chloroplast was used as a reference for assemblies, averaging 25,970 reads with mean depth of 20.71 reads; genomes ranged from 141,451 to 150,339 bp. The S. carduacea Benth. nuclear ribosomal cistron (18S, ITS1, 5.8S, ITS2 and 26S) was used as a reference for assembly, averaging 66,387 reads and mean depth of 1508 reads. We evaluated several partitioning schemes for plastid, plastid and nrDNA and reduced sampling, to assess whether these would render the same phylogenetic inferences. Maximum likelihood inferences resulted with high bootstrap support and two main clades with interspersed species from Salvia sect. Scorodoniae: clade A with species from S. sects. Atratae and Mitratae and clade B from S. sects. Sigmoideae and Uricae. Only S. sect. Uricae is monophyletic in every analysis supporting its identity, not merged into S. sect. Scorodoniae; S. sect. Sigmoideae is inferred monophyletic only if the ribosomal DNA sequences are included. Greater resolution and higher branch support are obtained with the entire plastome and nrDNA, rather than subsampling highly variable regions; thus we recommend this approach with expanded taxon sampling, coupled with a morphological review to better solve sectional circumscription in closely related S. subgenus Calosphace species.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Álvarez 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

  2. Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Version 0.7.11. http://www.bioinformatics.babraham.ac.uk/projects/fastqc

  3. Ashworth V (2000) Phylogenetic relationships in Phoradendreae (Viscaceae) Inferred from three regions of the nuclear ribosomal cistron. II. The North American species of Phoradendron. Aliso. https://doi.org/10.5642/aliso.20001901.05

  4. Baldwin BG (1993) Molecular phylogenetics of Calycadenia (Compositae) based on ITS sequences of nuclear ribosomal DNA: chromosomal and morphological evolution reexamined. Am J Bot 80:222–238. https://doi.org/10.1002/j.1537-2197.1993.tb13792.x

  5. 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

  6. Bengtson A, Anderberg AA (2018) Species diversification in the Mediterranean genus Chiliadenus (Inuleae-Asteraceae). Plant Syst Evol 304:853–860. https://doi.org/10.1007/s00606-018-1515-2

  7. Bentham G, Hooker J (1876) Labiatae. In: Hooker J, Pamplin W (eds) Genera plantarum, vol 2. G. Bentham, London, pp 1160–1223

  8. Bozin B, Mimica-Dukic N, Samojlik I, Jovin E (2007) Antimicrobial and antioxidant properties of rosemary and sage (Rosmarinus officinalis L. and Salvia officinalis L., Lamiaceae) essential oils. J Agric Food Chem 55:7879–7885. https://doi.org/10.1021/jf0715323

  9. Bravo GA, Antonelli A, Bacon CD, Bartoszek K, Blom MPK, Huynh S, Jones G, Knowles LL, Lamichhaney S, Marcussen T, Morlon H, Nakhleh LK, Oxelman B, Pfeil B, Schliep A, Wahlberg N, Werneck FP, Wiedenhoeft J, Willows-Munro S, Edwards SV (2019) Embracing heterogeneity: coalescing the tree of life and the future of phylogenomics. PeerJ 7:e6399. https://doi.org/10.7717/peerj.6399

  10. Bult CJ, Sweere JA, Zimmer EA (1995) Cryptic sequence simplicity, nucleotide composition bias, and molecular coevolution in the large subunit of ribosomal DNA in plants: implications for phylogenetic analyses. Ann Mo Bot Gard 82:235–246. https://doi.org/10.2307/2399879

  11. Cahill JP (2003) Ethnobotany of chia, Salvia hispanica L. (Lamiaceae). Econ Bot 57:604–618. https://doi.org/10.1016/0378-8741(94)90116-3

  12. Calonje M, Martín-Bravo S, Dobeš C, Gong W, Jordon-Thaden I, Kiefer C, Kiefer M, Paule J, Schmick R, Koch MA (2009) Non-coding nuclear DNA markers in phylogenetic reconstruction. Plant Syst Evol 282:257–280. https://doi.org/10.1007/s00606-008-0031-1

  13. Campbell V, Legendre P, Lapointe FJ (2011) The performance of the congruence among distance matrices (CADM) test in phylogenetic analysis. BMC Evol Biol 8:11–15. https://doi.org/10.1186/1471-2148-11-64

  14. Carbonell-Caballero J, Alonso R, Ibañez V, Terol J, Talon M, Dopazo J (2015) A phylogenetic analysis of 34 chloroplast genomes elucidates the relationships between wild and domestic species within the genus Citrus. Mol Biol Evol 32:2015–2035. https://doi.org/10.1093/molbev/msv082

  15. Chang-Li Z, Guang-Yong W, Jian-Bo W, Gui-Xin Y, Bi-Yun CH, Kun X, Jun L, Gui-Zhen G, Xiao-Ming W, Zhao B, Lei L (2012) High-Throughput discovery of chloroplast and mitochondrial DNA polymorphisms in Brassicaceae species by ORG-EcoTILLING. PLoS ONE 7:1–22. https://doi.org/10.1371/journal.pone.0047284

  16. Clebsch B (2003) The new book of Salvias: a sage for every garden, 2nd edn. Tiber Press, London, pp 1–344

  17. Cruz F, Turchetto-Zolet AC, Veto N, Mondin CA, Sobral M, Almerão M, Margis R (2013) Phylogenetic analysis of the genus Hexachlamys (Myrtaceae) based on plastid and nuclear DNA sequences and their taxonomic implications. Bot J Linn Soc 172:532–543. https://doi.org/10.1111/boj.12036

  18. Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403. https://doi.org/10.1101/gr.2289704

  19. Deng T, Chen Y, Wang H, Zhang X, Volis S, Yusupov Z, Qian H, Sun H (2018) Molecular phylogeny and biogeography of Adenocaulon highlight the biogeographic links between new world and old world. Front Ecol Evol. https://doi.org/10.3389/fevo.2017.00162

  20. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hart C, Philippakis AA, del Angel G, Rivas MA, Hanna M, Mckenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491–498. https://doi.org/10.1038/ng.806

  21. Devi RJ, Chrungoo NK (2017) Evolutionary divergence in Chenopodium and validation of SNPs in chloroplast rbcL and matk genes by allele-specific PCR for development of Chenopodium quinoa-specific markers. Crop J 5:32–42. https://doi.org/10.1016/j.cj.2016.06.019

  22. Doyle J, Doyle JL (1987) Genomic plant DNA preparation from fresh tissue-CTAB method. Phytochem Bull 19:11–15

  23. 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

  24. Drew BT, Sytsma KJ (2012) Phylogenetics, biogeography, and staminal evolution in the tribe Mentheae (Lamiaceae). Am J Bot 99:933–953. https://doi.org/10.3732/ajb.1100549

  25. Duvall MR, Fisher AE, Columbus JT, Ingram AL, Wysocki WP, Burke SV, Clark LG, Kelchner SA (2016) Phylogenomics and plastome evolution of the Chloridoid grasses (Chloridoideae: Poaceae). Int J Plant Sci 177:235–246. https://doi.org/10.1086/684526

  26. Epling C (1939) A revision of Salvia subgenus Calosphace. Repert Specierum Nov Regni Veg 110:1–383

  27. Epling C (1940) Supplementary notes on American Labiatae. Bull Torrey Bot Club 67:509–534

  28. Epling C (1941) Supplementary notes on American Labiatae II. Bull Torrey Bot Club 68:552–568

  29. Epling C (1944) Supplementary notes on American Labiatae III. Bull Torrey Bot Club 71:484–497

  30. Epling C (1947) Supplementary notes on American Labiatae IV. Bull Torrey Bot Club 74:512–518

  31. Epling C (1951) Supplementary notes on American Labiatae V. Brittonia 7:129–142

  32. Epling C, Mathias ME (1957) Supplementary notes on American Labiatae VI. Brittonia 8:297–313

  33. Espejo-Serna A, Ramamoorthy TP (1993) Revisión taxonómica de Salvia sección Sigmoideae (Lamiaceae). Acta Bot Mex 23:65–102

  34. Fan C, Xiang Q-YJ (2003) Phylogenetic analyses of Cornales based on 26S rRNA and combined 26S rDNA-matK -rbcL sequence data. Am J Bot 90:1357–1372. https://doi.org/10.3732/ajb.90.9.1357

  35. Feliner GN, Rosselló JA (2007) Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Mol Phylogenet Evol 44:911–919. https://doi.org/10.1016/j.ympev.2007.01.013

  36. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/BF01734359

  37. Fragoso-Martínez I, Salazar GA, Martínez-Gordillo M, Magallón S, Sánchez-Reyes L, Lemmon EM, Lemmon AR, Sazatornil F, Granados-Mendoza C (2017) A pilot study applying the plant anchored hybrid enrichment method to new world sages (Salvia subgenus Calosphace; Lamiaceae). Mol Phylogenet Evol 117:124–134. https://doi.org/10.1016/j.ympev.2017.02.006

  38. Fragoso-Martínez I, Martínez-Gordillo M, Salazar GA, Sazatornil F, Jenks AA, García-Peña MR, Barrera-Aveleida G, Benitez-Vieyra S, Magallón S, Cornejo-Tenorio G, Granados-Mendoza C (2018) Phylogeny of the neotropical sages (Salvia subg. Calosphace; Lamiaceae) and insights into pollinator and area shifts. Plant Syst Evol 304:43–55. https://doi.org/10.1007/s00606-017-1445-4

  39. Godden GT, Jordon-Thaden IE, Chamala S, Crowl AA, García N, Germain-Aubrey C, Heaney JM, Latvis M, Qi X, Gitzendanner MA (2012) Making next-generation sequencing work for you: approaches and practical considerations for marker development and phylogenetics. Plant Ecol Divers 5:427–450. https://doi.org/10.1080/17550874.2012.745909

  40. Ha Y-H, Choi KS, Choi K (2018) Characterization of complete chloroplast genome of endemic species of Korea Peninsular, Salvia chanryoenica (Lamiaceae). Mitochondrial DNA Part B 3:992–993. https://doi.org/10.1080/23802359.2018.1495115

  41. He Y, Shen S, Shen Z (2017) Cloning and application of the complete nuclear ribosomal DNA (nrDNA) cistron sequence of Pyropia haitanensis (Bangiales, Rhodophyta). Bot Mar 60:327–337. https://doi.org/10.1515/bot-2016-0079

  42. Hebert PDN, Ratnasingham S, de Waard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B Biol Sci. https://doi.org/10.1098/rsbl.2003.0025

  43. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281

  44. Hu G-X, Takano A, Drew BT, Liu ED, Soltis DE, Soltis PS, Peng H, Xiang CH-L (2018) Phylogeny and staminal evolution of Salvia (Lamiaceae, Nepetoideae) in East Asia. Ann Bot 122:649–668. https://doi.org/10.1093/aob/mcy104

  45. Jansen RK, Kaittanis C, Saski C, Le S-B, Tomkins J, Alverson A, Daniell H (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol 6:32. https://doi.org/10.1186/1471-2148-6-32

  46. Jenks AA, Kim S-C (2013) Medicinal plant complexes of Salvia subgenus Calosphace: an ethnobotanical study of new world sages. J Ethnopharmacol 146:214–224. https://doi.org/10.1016/j.jep.2012.12.035

  47. Jenks AA, Walker JB, Kim S-C (2013) Phylogeny of new world Salvia subgenus Calosphace (Lamiaceae) based on cpDNA (psbA-trnH) and nrDNA (ITS) sequence data. J Plant Res 126:483–496. https://doi.org/10.1007/s10265-012-0543-1

  48. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285

  49. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

  50. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

  51. Kelchner SA (2000) The Evolution of non-coding chloroplast DNA and Its application in plant systematics. Ann Mo Bot Gard 87:482–498. https://doi.org/10.2307/2666142

  52. Klitgaard BB (2012) Salvia L. Flora Mesoamericana 4:396–424

  53. Kress WJ, Erickson DL (2008) DNA barcoding-a windfall for tropical biology? Commentary. Biotropica 40:405–408. https://doi.org/10.1111/j.1744-7429.2008.00426.x

  54. Kriebel R, Drew BT, Drummond CP, González-Gallegos J, Celep F, Mahdjoub MM, Rose JP, Xiang C-L, Hu G-X, Walker JB, Lemmon EM, Lemmon AR, Sytsma KJ (2019) Tracking temporal shifts in area, biomes, and pollinators in the radiation of Salvia (sages) across continents: leveraging anchored hybrid enrichment and targeted sequence data. Am J Bot 106:573–597. https://doi.org/10.1002/ajb2.1268

  55. Kuritzin A, Kischka T, Schmitz J, Churakov G (2016) Incomplete lineage sorting and hybridization statistics for large-scale retroposon insertion data. PLoS Comput Biol 12:e1004812. https://doi.org/10.1371/journal.pcbi.1004812

  56. Lee D-S, Lee S-H, Noh J-G, Hong S-D (1999) Antibacterial activities of cryptotanshinone and dihydrotanshinone I from a medicinal herb, Salvia miltiorrhiza Bunge. Biosci Biotechnol Biochem 63:2236–2239. https://doi.org/10.1271/bbb.63.2236

  57. Legendre P, Lapointe F-J (2004) Assessing congruence among distance matrices: single-malt scotch whiskies revisited. Aust N Z J Stat 46:615–629. https://doi.org/10.1111/j.1467-842X.2004.00357.x

  58. Lei Y-X, Liu J, Fan X, Sha L-N, Wang Y, Kang H-Y, Zhou YH (2018) Phylogeny and maternal donor of Roegneria and its affinitive genera (Poaceae: Triticeae) based on sequence data for two chloroplast DNA regions (ndhF and trnH–psbA). J Syst Evol 56:105–119. https://doi.org/10.1111/jse.12291

  59. Lemmon AR, Lemmon EM (2012) High-throughput identification of informative nuclear loci for shallow-scale phylogenetics and phylogeography. Syst Biol 61:745–761. https://doi.org/10.1093/sysbio/sys051

  60. Li Q-Q, Li M-H, Yuan Q-J, Cui ZH, Huang L-Q, Xiao P-G (2013) Phylogenetic relationships of Salvia (Lamiaceae) in China: evidence from DNA sequence datasets. J Syst Evol 51:184–195. https://doi.org/10.1111/j.1759-6831.2012.00232.x

  61. Li X, Xu J, He Y, Shen Y, Zhu J, Shen Z (2016) The complete nuclear ribosomal DNA (nrDNA) cistron sequence of Pyropia yezoensis (Bangiales, Rhodophyta). J Appl Phycol 28:663–669. https://doi.org/10.1007/s10811-015-0522-8

  62. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187

  63. Logacheva MD, Schelkunov MI, Shtratnikova VY, Matveeva MV, Penin AA (2016) Comparative analysis of plastid genomes of non-photosynthetic Ericaceae and their photosynthetic relatives. Sci Rep 6:30042. https://doi.org/10.1038/srep30042

  64. Lohse M, Drechsel O, Bock R (2007) OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 52:267–274. https://doi.org/10.1007/s00294-007-0161-y

  65. Lukas B, Novak J (2013) The complete chloroplast genome of Origanum vulgare L. (Lamiaceae). Gene 528:163–169. https://doi.org/10.1016/j.gene.2013.07.026

  66. Luo J, Hou B-W, Niu Z-T, Liu W, Xue Q-Y, Ding X-Y (2014) Comparative chloroplast genomes of photosynthetic orchids: insights into evolution of the orchidaceae and development of molecular markers for phylogenetic applications. PLoS ONE 9:1–15. https://doi.org/10.1371/journal.pone.0099016

  67. Ma L (2018) The complete chloroplast genome sequence of the fragrant plant Lavandula angustifolia (Lamiaceae). Mitochondrial DNA Part B 3:135–136. https://doi.org/10.1080/23802359.2018.1431067

  68. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12. https://doi.org/10.14806/ej.17.1.200

  69. Martin W, Deusch O, Stawski N, Grünheit N, Goremykin V (2005) Chloroplast genome phylogenetics: why we need independent approaches to plant molecular evolution. Trends Plant Sci 10:203–209. https://doi.org/10.1016/j.tplants.2005.03.007

  70. Martínez-Gordillo M, Fragoso-Martínez I, del García-Peña M, Montiel O (2013) Géneros de Lamiaceae de México, diversidad y endemismo. Rev Mex Biodivers 84:30–86. https://doi.org/10.7550/rmb.30158

  71. Mayer C (2010) Phobos Version 3.3. 12. Tandem repeat search program 20

  72. Moore MJ, Hassan N, Gitzendanner MA, Bruenn RA, Croley M, Vandeventer A, Horn JW, Dhingra A, Brockington SF, Latvis M, Ramdial J, Alexandre R, Piedrahita A, Xi Z, Davis CC, Soltis PS, Soltis DE (2011) Phylogenetic analysis of the plastid inverted repeat for 244 species: insights into deeper-level angiosperm relationships from a long, slowly evolving sequence region. Int J Plant Sci 172:541–558. https://doi.org/10.1086/658923

  73. Mort ME, Archibald JK, Randle CP, Levsen ND, O’Leary TR, Topalov K, Wiegand CM, Crawford DJ (2007) Inferring phylogeny at low taxonomic levels: utility of rapidly evolving cpDNA and nuclear ITS loci. Am J Bot 94:173–183. https://doi.org/10.3732/ajb.94.2.173

  74. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, p 512

  75. Nei M, Li W-H (1976) The transient distribution of allele frequencies under mutation pressure. Genet Res 28:205–214

  76. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152. https://doi.org/10.1146/annurev.genet.39.073003.112240

  77. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300

  78. Nickrent DL, Soltis DE (1995) A comparison of angiosperm phylogenies from nuclear 18S rDNA and rbcL sequences. Ann Mo Bot Gard 82:208–234. https://doi.org/10.2307/2399878

  79. Olvera-Mendoza EI, Bedolla-García BY, Lara-Cabrera SI (2017) Revisión taxonómica de Salvia subgénero Calosphace sección Scorodoniae (Lamiaceae), endémica de México. Acta Bot Mex 118:7–40. https://doi.org/10.21829/abm118.2017.1198

  80. Paradis E, Bolker B, Claude J (2012) Package ape. Analyses of phylogenetics and evolution. R package version 2012.04-04

  81. Parks M, Cronn R, Liston A (2009) Increasing phylogenetic resolution at low taxonomic levels using massively parallel sequencing of chloroplast genomes. BMC Biol 7:84

  82. Patil RG, Jadhao KR, Samal KC, Rout GR (2015) Molecular phylogeny of Indian indigenous aromatic rice based on sequence diversity of the chloroplast-encoded matK Gene. Rice Genom Genet. https://doi.org/10.5376/rgg.2015.06.0008

  83. Pham KK, Hipp AL, Manos PS, Cronn RC (2017) A time and a place for everything: phylogenetic history and geography as joint predictors of oak plastome phylogeny. Genome 60:720–732. https://doi.org/10.1139/gen-2016-0191

  84. Potts AJ, Hedderson TA, Grimm GW (2014) Constructing phylogenies in the presence of intra-individual site polymorphisms (2ISPs) with a focus on the nuclear ribosomal cistron. Syst Biol 63:1–16. https://doi.org/10.1093/sysbio/syt052

  85. Qian J, Song J, Gao H, Zhu Y, Xu J, Pang X, Yao H, Sun C, Li X, Li C, Liu J, Xu H, Chen S, Wu K (2013) The complete chloroplast genome sequence of the medicinal plant Salvia miltiorrhiza. PLoS ONE 8(2):e57607

  86. Ramamoorthy TP, Elliott M (1998) Lamiaceae de México, diversidad, distribución, endemismo y evolución. Diversidad biológica. Orígenes y distribución. Universidad Nacional Autónoma de México, TP Ramamoorthy, Bye RP, Lot AFa J, pp 501–526

  87. Raubeson LA, Peery R, Chumley TW, Dziubek C, Fourcade HM, Boore JL, Jansen RK (2007) Comparative chloroplast genomics: analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genom 8:174. https://doi.org/10.1186/1471-2164-8-174

  88. Reisfield AS (1993) The botany of Salvia divinorum (Labiatae). SIDA Contrib Bot 15:349–366

  89. Reyes-Caudillo E, Tecante A, Valdivia-López MA (2008) Dietary fibre content and antioxidant activity of phenolic compounds present in Mexican chia (Salvia hispanica L.) seeds. Food Chem 107:656–663. https://doi.org/10.1016/j.foodchem.2007.08.062

  90. Rodriguez-Hahn L (1992) The distribution of diterpenoids in Salvia. In: Harley RM, Reynolds T (eds) Advances in Labiatae science. Royal Botanic Gardens, Kew, pp 335–345

  91. RStudio Team (2015) RStudio: integrated development environment for R (Version 1.0. 153). RStudio, Inc., Boston. https://www.rstudio.com

  92. R Core Team (2014) R: a language and environment for statistical computing. R Foundation For Statistical Computing, Vienna, Austria. http://www.R-project.org/

  93. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci 74:5463–5467. https://doi.org/10.1073/pnas.74.12.5463

  94. Satoh K, Shutoh K, Kurosawa T, Hayasaka E, Kaneko S (2018) Genetic analysis of Japanese and American specimens of Scirpus hattorianus suggests its introduction from North America. J Plant Res 131:91–97. https://doi.org/10.1007/s10265-017-0976-7

  95. Siebert DJ (1994) Salvia divinorum and salvinorin A new pharmacologic findings. J Ethnopharmacol 43:53–56. https://doi.org/10.1016/0378-8741(94)90116-3

  96. Smith SA, Beaulieu JM, Stamatakis A, Donoghue MJ (2011) Understanding angiosperm diversification using small and large phylogenetic trees. Am J Bot 98:404–414. https://doi.org/10.3732/ajb.1000481

  97. Soltis DE, Soltis PS, Nickrent DL, Johnson LA, Hahn WJ, Hoot SB, Sweere JA, Kuzoff RK, Kron KA, Chase MW, Swensen SM (1997a) Angiosperm phylogeny inferred from 18S ribosomal DNA sequences. Ann Mo Bot Gard 1:1–49

  98. Soltis DE, Soltis PS, Nickrent DL, Johnson LA, Hahn WJ, Hoot SB, Sweere JA, Kuzoff RK, Kron KA, Chase MW, Swensen SM (1997b) Angiosperm phylogeny inferred from 18S ribosomal DNA sequences. Ann Mo Botanical Garden 1:1–49

  99. Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M, Swensen SM, Prince LM, Kress WJ, Nixon KC, Farris JS (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133:381–461. https://doi.org/10.1111/j.1095-8339.2000.tb01588.x

  100. Soltis DE, Albert VA, Savolainen V, Hilu K, Qiu Y-L, Chase MW, Farris JS, Stefanović S, Rice DW, Palmer JD, Soltis PS, Less S (2004) Genome-scale data, angiosperm relationships, and ‘ending incongruence’: a cautionary tale in phylogenetics. Trends Plant Sci 9:477–483. https://doi.org/10.1016/j.tplants.2004.08.008

  101. Soltis DE, Gitzendanner MA, Stull G, Chanderbali A, Chamala S, Jordon-Thaden I, Soltis PS, Schnable PS, Barbazuk WB (2013) The potential of genomics in plant systematics. Taxon 62:886–898. https://doi.org/10.12705/625.13

  102. Song Y, Wang S, Ding Y, Xu J, Li MF, Zhu S, Chen N (2017) Chloroplast genomic resource of Paris for species discrimination. Sci Rep 7:3427. https://doi.org/10.1038/s41598-017-02083-7

  103. Srikulnath K, Sawasdichai S, Jantapanon TK, Pongtongkam P, Peyachoknagul S (2015) Phylogenetic relationship of Dendrobium species in Thailand inferred from chloroplast matK Gene and Nuclear rDNA ITS Region. Hortic J 84:243–252. https://doi.org/10.2503/hortj.MI-028

  104. Sullivan AR, Schiffthaler B, Thompson SL, Street NR, Wang X-R (2017) Interspecific plastome recombination reflects ancient reticulate evolution in Picea (Pinaceae). Mol Biol Evol 34:1689–1701. https://doi.org/10.1093/molbev/msx111

  105. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109. https://doi.org/10.1007/BF00037152

  106. Takano A (2017) Taxonomic study on Japanese Salvia (Lamiaceae): phylogenetic position of S. akiensis, and polyphyletic nature of S. lutescens var. intermedia. PhytoKeys. https://doi.org/10.3897/phytokeys.80.11611

  107. Troitsky AV, Melekhovets YF, Rakhimova GM, Bobrova VK, Valiejo-Roman KM, Antonov AS (1991) Angiosperm origin and early stages of seed plant evolution deduced from rRNA sequence comparisons. J Mol Evol 32:253–261. https://doi.org/10.1007/BF02342748

  108. Turner BL (2009) Recension of the Mexican species of Salvia (Lamiaceae), section Scorodonia. Phytologia 91:256–269

  109. Uchoi A, Malik SK, Choudhary R, Kumar S, Rohini MR, Pal D, Ercisli S, Chaudhury R (2016) Inferring phylogenetic relationships of Indian citron (Citrus medica L.) based on rbcL and matK Sequences of Chloroplast DNA. Biochem Genet 54:249–269. https://doi.org/10.1007/s10528-016-9716-2

  110. Veranso-Libalah MC, Kadereit G, Stone RD, Couvreur TLP (2018) Multiple shifts to open habitats in Melastomateae (Melastomataceae) congruent with the increase of African Neogene climatic aridity. J Biogeogr 45:1420–1431. https://doi.org/10.1111/jbi.13210

  111. Walker JB (2007) A preliminary phylogenetic analysis of Salvia subgenus Calosphace. Ph.D. thesis, University of Wisconsin, Madison

  112. 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

  113. Walker JB, Sytsma KJ, Treutlein J, Wink M (2004) Salvia (Lamiaceae) is not monophyletic: implications for the systematics, radiation, and ecological specializations of Salvia and tribe Mentheae. Am J Bot 91:1115–1125. https://doi.org/10.3732/ajb.91.7.1115

  114. Walker JB, Drew BT, Sytsma KJ (2015) Unravelling species relationships and diversification within the iconic California floristic province sages (Salvia Subgenus Audibertia, Lamiaceae). Syst Bot 40:826–844. https://doi.org/10.1600/036364415X689285

  115. Welch AJ, Collins K, Ratan A, Daniela I, Drautz-Moses DI, Schuster SC, CharlotteLindqvist C (2016) Data characterizing the chloroplast genomes of extinct and endangered Hawaiian endemic mints (Lamiaceae) and their close relatives. Data Brief 7:900–922. https://doi.org/10.1016/j.dib.2016.03.037

  116. Weng M-L, Ruhlman TA, Jansen RK (2017) Expansion of inverted repeat does not decrease substitution rates in Pelargonium plastid genomes. New Phytol 214:842–851. https://doi.org/10.1111/nph.14375

  117. Wester P, Claßen-Bockhoff R (2011) Pollination syndromes of new world Salvia species with special reference to bird pollination. Ann Mo Bot Gard 98:101–155. https://doi.org/10.3417/2007035

  118. Will M, Claßen-Bockhoff R (2014) Why Africa matters: evolution of old world Salvia (Lamiaceae) in Africa. Ann Bot 114:61–83. https://doi.org/10.1093/aob/mcu081

  119. 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

  120. Will M, Schmalz N, Classen-Bockhoff R (2015) Towards a new classification of Salvia s.l.: (re)establishing the genus Pleudia Raf. Turk J Bot 39:693–707. https://doi.org/10.3906/bot-1405-34

  121. Wu YB, Ni ZY, Shi QW, Dong M, Kiyota H, Gu YC, Cong B (2012) Constituents from Salvia species and their biological activities. Chem Rev 112:5967–6026. https://doi.org/10.1021/cr200058f

  122. Xu J, Jiang B, Chai S, He Y, Zhu J, Shen Z, Shen S (2016) Complete nuclear ribosomal DNA sequence amplification and molecular analyses of Bangia (Bangiales, Rhodophyta) from China. Chin J Oceanol Limnol 34:1044–1053. https://doi.org/10.1007/s00343-016-5033-1

  123. Yan L, Lai X, Li X, Wei C, Tan X, Zhang Y (2015) Analyses of the complete genome and gene expression of chloroplast of sweet potato (Ipomoea batata). PLoS ONE 10:e0124083. https://doi.org/10.1371/journal.pone.0124083

  124. Yang J-B, Yang S-X, Li H-T, Yang J, Li D-Z (2013) Comparative chloroplast genomes of Camellia species. PLoS ONE 8:e73053. https://doi.org/10.1371/journal.pone.0073053

  125. Yi D-K, Kim K-J (2012) Complete chloroplast genome sequences of important oilseed crop Sesamum indicum L. PLoS ONE 7:e35872. https://doi.org/10.1371/journal.pone.0035872

  126. Yu X-Q, Drew BT, Yang J-B, Gao L-M, Li D-Z (2017) Comparative chloroplast genomes of eleven Schima (Theaceae) species: insights into DNA barcoding and phylogeny. PLoS ONE 12:e0178026. https://doi.org/10.1371/journal.pone.0178026

  127. Zhang Z-Y, Li D-Z (2004) Molecular phylogeny of section Parrya of Pinus (Pinaceae) based on chloroplast matK gene sequence data. Acta Bot Sin 46:171–179

  128. Zimmer EA, Wen J (2015) Using nuclear gene data for plant phylogenetics: progress and prospects II. Next-gen approaches. J Syst Evol 53:371–379. https://doi.org/10.1111/jse.12174

Download references

Acknowledgements

The results here presented are part of the Ph.D. thesis of EIOM under the advisory of SILC. We thank the financial support of the following: CONACyT graduate studies scholarship 290575 to EIOM, CONACyT sabbatical scholarship 232839 to SILC, Coordinación de la Investigación Científica (UMSNH), Project 8.16. NSF award number 1120080 to JMP. Curators from herbaria RSA, BIGU, EBUM, ENCB, IEB, MEXU and UAMIZ. We are thankful for the collection assistance of Arnulfo Blanco, Anna Paizanni, Brenda Bedolla, Cesar Alfaro, Justino Olvera, Manuel Ramírez, Sergio Zamudio and Mario Veliz (BIGU) for aiding in the Guatemala collection. Mario Hernández for allowing collection of fresh leaf material at the Botanical Garden “Charco del Ingenio” in San Miguel de Allende, Guanajuato. And Heather Blume for facilitating collections at the Cabrillo College Environmental Horticulture Center & Botanic Gardens.

Author information

Grant T. Godden, J. Mark Porter, and Sabina I. Lara-Cabrera were involved in conceptualization of the study; Grant T. Godden, J. Mark Porter, and Sabina I. Lara-Cabrera contributed to methodology; material preparation and data collection were performed by Grant T. Godden, J. Mark Porter, Sabina I. Lara-Cabrera and Edgar I. Olvera-Mendoza. All authors contributed to analysis, investigation and writing, review and editing of the manuscript. All authors read and approved the final manuscript.

Correspondence to Sabina I. Lara-Cabrera.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 3549 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Olvera-Mendoza, E.I., Godden, G.T., Montero-Castro, J.C. et al. Chloroplast and nuclear ribosomal cistron phylogenomics in a group of closely related sections in Salvia subg. Calosphace. Braz. J. Bot (2020). https://doi.org/10.1007/s40415-019-00572-9

Download citation

Keywords

  • Lamiaceae
  • Lamiales
  • Nuclear ribosomal cistron
  • Nucleotide diversity
  • Plastid genome