Species-diagnostic markers in the genus Pinus: evaluation of the chloroplast regions matK and ycf1

Sanna Olsson, Delphine Grivet, Jeronimo Cid-Vian

Abstract


Aim of study: The identification of material of forest tree species using genetic markers was carried out. Two promising chloroplast barcode markers, matK and ycf1, were tested for species identification and reconstruction of phylogenetic relationships in pines.

Area of study: The present study included worldwide Pinus species, with a wide representation of European taxa.

Material and methods: All matK sequences longer than 1600 base pairs and ycf1 sequences for the same species were downloaded from GenBank, aligned and subsequently analyzed to estimate alignment statistics, phylogenetic trees and substitution saturation signals.

Main results: We confirm the usefulness of the ycf1 marker for barcoding purposes and phylogenetic studies in pines, especially in studies focusing at the within-genus level relationships, but caution in the use of the matK marker is recommended.

Research highlights: Incongruent phylogenetic signals between these two chloroplast markers are demonstrated in pines for the first time.

Keywords: barcoding, conifers, phylogeny.

Abbreviations: posterior probabilities (PP), bootstrap (BS).


Keywords


barcoding, conifers, phylogeny

Full Text:

PDF HTML XML

References


Alfaro ME, Zoller S, Lutzoni F, 2003. Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov Chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol Biol Evol 20: 255-266. https://doi.org/10.1093/molbev/msg028

Álvarez-Álvarez P, Pizarro C, Barrio-Anta M, Cámara-Obregón A, Bueno JLM, Álvarez A, Gutiérrez I, Burslem DFRP, 2018. Evaluation of tree species for biomass energy production in Northwest Spain. Forests 9(4): 160. https://doi.org/10.3390/f9040160

Aragonés A, Barrena I, Espinel S, Herrán A, Ritter E, 1997. Origin of Basque populations of radiata pine inferred from RAPD data. Ann Sci For 54(8): 697-703. https://doi.org/10.1051/forest:19970801

Baker SC, Steel D, Choi Y, Lee H, Kim KS, Choi SK, Ma Y-U, Hambleton C, Psihoyos L, Brownell RL, Funahashi N, 2010. Genetic evidence of illegal trade in protected whales links Japan with the US and South Korea. Biol Lett 6(5): 647-650. https://doi.org/10.1098/rsbl.2010.0239

Bruni I, De Mattia F, Martellos S, Galimberti A, Savadori P, Casiraghi M, Nimis PL, Labra M, 2012. DNA Barcoding as an effective tool in improving a digital plant identification system: a case study for the area of Mt. Valerio, Trieste (NE Italy). PLoS ONE 7(9): e43256. https://doi.org/10.1371/journal.pone.0043256

Businský R, Frantik T, Vit P, 2014. Morphological evaluation of the Pinus kesiya complex (Pinaceae). Plant Syst Evol. 300: 273-285. https://doi.org/10.1007/s00606-013-0880-0

Celinski K, Kijak H, Wojnicka-Półtorak A, Buczkowska-Chmielewska K, Sokołowska J, Chudzińska E, 2017. Effectiveness of the DNA barcoding approach for closely related conifers discrimination: A case study of the Pinus mugo complex. C R Biol 340(6-7): 339-348. https://doi.org/10.1016/j.crvi.2017.06.002

Christensen KI, 1987. Taxonomic revision of the Pinus mugo complex and P. rhaetica (P. mugo sylvestris) (Pinaceae). Nord J Bot 7 383-408. https://doi.org/10.1111/j.1756-1051.1987.tb00958.x

Darriba D, Taboada GL, Doallo R, Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8): 772-772.

Degen B, Höltken A, Rogge M, 2010. Use of DNA-fingerprints to control the origin of forest reproductive material. Silvae Genet 59(6): 268-273. https://doi.org/10.1515/sg-2010-0038

Deguilloux M-F, Pemonge M-H, Petit RJ, 2004. DNA-based control of oak wood geographic origin in the context of the cooperage industry. Ann For Sci 61(1): 97-104. https://doi.org/10.1051/forest:2003089

Dong W, Xu C, Li C, Sun J, Zuo Y, Shi S, Cheng T, Guo J, Zhou S, 2015. ycf1, the most promising plastid DNA barcode of land plants. Sci Rep 5(1): 8348. https://doi.org/10.1038/srep08348

Eckert A, Hall B, 2006. Phylogeny, historical biogeography, and patterns of diversification for Pinus (Pinaceae): Phylogenetic tests of fossil-based hypotheses. Mol Phylogenet Evol 40(1): 166-182. https://doi.org/10.1016/j.ympev.2006.03.009

Fidler F, Burgman MA, Cumming G, Buttrose R, Thomason N, 2006. Impact of criticism of null-hypothesis significance testing on statistical reporting practices in conservation biology. Conserv Biol 20(5): 1539-1544. https://doi.org/10.1111/j.1523-1739.2006.00525.x

Finkeldey R, Leinemann L, Gailing O, 2010. Molecular genetic tools to infer the origin of forest plants and wood. Appl Microbiol Biotechnol 85: 1251-1258. https://doi.org/10.1007/s00253-009-2328-6

Geada López G, Kamiya K, Harada K, 2002. Phylogenetic relationships of Diploxylon pines (Subgenus Pinus) based on plastid sequence data. Int J Plant Sci 163(5): 737-747. https://doi.org/10.1086/342213

Gernandt D, Liston A, Piñero D, 2003. Phylogenetics of Pinus Subsections Cembroides and Nelsoniae Inferred from cpDNA Sequences. Syst Bot 28(4): 657-673.

Gernandt DS, López GG, García SO, Liston A, 2005. Phylogeny and classification of Pinus. Taxon 54: 29-42. https://doi.org/10.2307/25065300

Gernandt D, Magallón S, Geada López G, Zerón Flores O, Willyard A, Liston A, 2008. Use of simultaneous analyses to guide fossil‐based calibrations of Pinaceae Phylogeny. Int J Plant Sci: 169(8): 1086-1099. https://doi.org/10.1086/590472

Gernandt DS, Aguirre Dugua X, Vázquez-Lobo A, Willyard A, Moreno Letelier A, Pérez de la Rosa JA, Piñero D, Liston A, 2018. Multi-locus phylogenetics, lineage sorting, and reticulation in Pinus subsection Australes. Am J Bot 105: 1-15. https://doi.org/10.1002/ajb2.1052

Ghorbani A, Gravendeel B, Selliah S, Zarré S, de Boer H, 2017. DNA barcoding of tuberous Orchidoideae: a resource for identification of orchids used in Salep. Mol Ecol Res 17(2): 342-352. https://doi.org/10.1111/1755-0998.12615

Grivet D, Climent J, Zabal-Aguirre M, Neale D, 2013. Adaptive evolution of Mediterranean pines. Mol Phylogenet Evol 68(3): 555-566. https://doi.org/10.1016/j.ympev.2013.03.032

Hernández-León S, Gernandt D, Pérez de la Rosa J, Jardón-Barbolla L, 2013. Phylogenetic relationships and species delineation in Pinus Section Trifoliae inferred from plastid DNA. PLoS ONE 8(7): e70501. https://doi.org/10.1371/journal.pone.0070501

Hernández-Tecles, de las Heras J, Lorenzo Z, Navascués M, Alia R, 2017. Identification of gene pools used in restoration and conservation by chloroplast microsatellite markers in Iberian pine species. For Syst 26(2): e058.

Hollingsworth PM, Forrest L, Spouge J, Hajibabaei M, Ratnasingham S, van der Bank M, Chase MW, Cowan RS, Erickson DL, Fazekas AJ, et al., 2009a. A DNA barcode for land plants. Proc Natl Acad Sci, 106(31): 12794-12797. https://doi.org/10.1073/pnas.0905845106

Hollingsworth ML, Clark AA, Forrest LL, Richardson J, Pennington RT, Long DG, Cowan R, Chase MW, Gaudeul M, Hollingsworth PM, 2009b. Selecting barcoding loci for plants: evaluation of seven candidate loci with species-level sampling in three divergent groups of land plants. Mol Ecol Resour 9: 439-457. https://doi.org/10.1111/j.1755-0998.2008.02439.x

Katoh K, Standley D, 2013. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in performance and usability. Mol Biol Evol 30(4): 772-780. https://doi.org/10.1093/molbev/mst010

Kress W, 2017. Plant DNA barcodes: Applications today and in the future. JSE IBC Special Issue on Frontiers in Plant Systematics and Evolution. J Syst Evol 55(4): 291-307. https://doi.org/10.1111/jse.12254

Kress W, Erickson D, Jones F, Swenson N, Perez Sanjur O, Bermingham E, 2009. Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama. Proc Natl Acad Sci 106(44): 18621-18626. https://doi.org/10.1073/pnas.0909820106

Lidder P, Sonnino A, 2011. Background study paper no. 52. Biotechnologies for the management of genetic resources for food and agricuture. Commission on Genetic Resources for Food and Agriculture.

Liston A, Gernandt DS, Vining TF, Campbell CS, Piñero D, 2003. Molecular phylogeny of Pinaceae and Pinus. Acta Hort 615: 107-114. https://doi.org/10.17660/ActaHortic.2003.615.7

Liston A, Parker-Defeniks M, Syring JV, Willyard A, Cronn R, 2007. Interspecific phylogenetic analysis enhances intraspecific phylogeographical inference: a case study in Pinus lambertiana. Mol Ecol 16: 3926-3937. https://doi.org/10.1111/j.1365-294X.2007.03461.x

Miller MA, Pfeiffer W, Schwartz T, 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14th November, 2010, New Orleans, LA, 1-8. https://doi.org/10.1109/GCE.2010.5676129

Moreira X, Sampedro L, Zas R, Pearse I, 2016. Defensive traits in young pine trees cluster into two divergent syndromes related to early growth rate. PLOS ONE: 11(3): e0152537. https://doi.org/10.1371/journal.pone.0152537

Müller KF, Quandt D, Müller J, Neinhuis C, 2005. PhyDE ® 0.995: Phylogenetic Data Editor. http://www.phyde.de.

Nanson A, 2001. The new OECD scheme for the certification of forest reproductive materials. Silvae Genet 50(5-6): 181-187.

Nielsen LR, Dahl KE, 2008. Tracing Timber from Forest to Consumer with DNA Markers. Copenhagen: Danish Ministry of the Environment, Forest and Nature Agency. Available from http://www.skovognatur.dk/udgivelser

Ortiz-Martínez, Gernandt DS, 2016. Species diversity and plastid DNA haplotype distributions of Pinus subsection Australes (Pinaceae) in Guerrero and Oaxaca. TIP Rev Esp Cienc Quím Biol 19(2): 92-101.

Palmé AE, Pyhäjärvi T, Wachowiak W, Savolainen O, 2009. Selection on nuclear genes in a Pinus phylogeny. Mol Biol Evol 26(4): 893-905. https://doi.org/10.1093/molbev/msp010

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. https://doi.org/10.1186/1741-7007-7-84

Parks M, Liston A, Cronn R, 2011. Newly developed primers for complete ycf1 amplification in Pinus (Pinaceae) chloroplasts with possible family-wide utility. Am J Bot 98(7): e185-188. https://doi.org/10.3732/ajb.1100088

Price RA, Liston A, Strauss SH, 1998. Phylogeny and systematics of Pinus. In: Ecology and Biogeography of Pinus; Richardson DM (ed.). pp. 49-68. Cambridge University Press, NY, USA.

Rambaut A, Suchard MA, Xie D, Drummond AJ, 2014. Tracer v1.6. Available from http://beast.bio.ed.ac.uk/Tracer

Ran JH, Wang PP, Zhao HJ, Wang XQ, 2010. A test of seven candidate barcode regions from the plastome in Picea (Pinaceae). J Integr Plant Biol 52: 1109-1126. https://doi.org/10.1111/j.1744-7909.2010.00995.x

Ribeiro MM, Le-Provost G, Gerber S, Vendramin GG, Anzidei M, Decroocq S, Marpeau A, Mariette S, Plomion C, 2002. Origin identification of maritime pine stands in France using chloroplast simple-sequence repeats. Ann Forest Sci. 59(1): 53-62. https://doi.org/10.1051/forest:2002100

Richardson DM, Rundel, 1998. Pine ecology and biogeography – An introduction. In: Ecology and Biogeography of Pinus; Richardson DM (ed.). pp. 49-68. Cambridge University Press, NY, USA. pp 3-46. Cambridge University Press, NY, USA.

Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP, 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539-542. https://doi.org/10.1093/sysbio/sys029

Schoch W, Heller I, Schweingruber FH, Kienast F, 2004. Wood anatomy of central European Species. Online version http:www.woodanatomy.ch

Soltis D, Soltis P, 1998. Molecular systematics of plants II. DNA sequencing. Kluwer Academic Publishers, NY, USA. 42 pp. https://doi.org/10.1007/978-1-4615-5419-6

Stamatakis A, Hoover P and Rougemont J, 2008. A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57(5): 758-771. https://doi.org/10.1080/10635150802429642

Stöver BC, Müller KF, 2010. TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11: 7. https://doi.org/10.1186/1471-2105-11-7

Swofford DL, 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0. Sinauer Assoc, Sunderland, MA, USA.

Syring J, Willyard A, Cronn R, Liston A, 2005. Evolutionary relationships among Pinus (Pinaceae) subsections inferred from multiple low-copy nuclear loci. Am J Bot 92(12): 2086-2100. https://doi.org/10.3732/ajb.92.12.2086

Tigabu M, Oden PC, Lindgren D, 2005. Identification of seed sources and parents of Pinus sylvestris L. using visible-near infrared reflectance spectra and multivariate analysis. Trees-Struct Funct 19: 468-476. https://doi.org/10.1007/s00468-005-0408-5

Tnah LH 2009, Lee SL, Ng KKS, Tani N, Bhassu S, Othman RY, 2009. Geographical traceability of an important tropical timber (Neobalanocarpus heimii) inferred from chloroplast DNA. Forest Ecol Manag 258(9): 1918-1923. https://doi.org/10.1016/j.foreco.2009.07.029

Tnah LH, Lee Soon LL, Ng KKS, Zaman FQ, Faridah-Hanum I, 2010. Forensic DNA profiling of tropical timber species in Peninsular Malaysia. Forest Ecol Manag 259(8): 1436-1446. https://doi.org/10.1016/j.foreco.2010.01.017

Tsitrone A, Kirkpatrick M, Levin D, 2003. A model for chloroplast capture. Evolution 57(8): 1776. https://doi.org/10.1111/j.0014-3820.2003.tb00585.x

Volkmann L, Martyn I, Moulton V, Spillner A, Mooers AO, 2014. Prioritizing populations for conservation using phylogenetic networks. PLoS ONE 9(2): e88945. https://doi.org/10.1371/journal.pone.0088945

Wang XR, Tsumura Y, Yoshimaru H, Nagasaka K, Szmidt AE, 1999. Phylogenetic relationships of Eurasian pines (Pinus, Pinaceae) based on chloroplast rbcL, MATK, RPL20-RPS18 spacer, and TRNV intron sequences. Am J Bot 86(12): 1742-53. https://doi.org/10.2307/2656672

Willyard A, Cronn R, Liston A, 2009. Reticulate evolution and incomplete lineage sorting among the ponderosa pines. Mol Phylogenet Evol 52: 498-511. https://doi.org/10.1016/j.ympev.2009.02.011

Xu J-H, Liu Q, Hu W, Wang T, Xue Q, Messing J, 2015. Dynamics of chloroplast genomes in green plants. Genomics 106(4): 221-231. https://doi.org/10.1016/j.ygeno.2015.07.004

Yang RC, Yeh FC, Ye TZ, 2007. Multilocus structure in the Pinus contorta-Pinus banksiana complex. Can J Bot 85: 774-784. https://doi.org/10.1139/B07-054

Zeng L, Zhang Q, Sun R, Kong H, Zhang N, Ma H, 2014. Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nat Commun 5:4956. https://doi.org/10.1038/ncomms5956




DOI: 10.5424/fs/2018273-13688

Webpage: www.inia.es/Forestsystems