Chloroplast microsatellite diversity of Pinus brutia Ten. and Pinus halepensis Mill. populations across the Mediterranean basin: Inferences of their distributions

Keywords: halepensis-complex, simple sequence repeats, tree genetics

Abstract

Aim of study: To characterize and compare the genetic resources and gain some insights into the evolutionary history of Aleppo pine (Pinus halepensis Mill.) and Brutia pine (Pinus brutia Ten.) species which are both distributed across more than 8 million hectares of area in the Mediterranean Basin.

Study area: Fifty-six populations from eight Mediterranean basin countries where P. halepensis and P. brutia species are located.

Materials and methods: We analyzed 1344 seeds belonging to 56 populations using five cpSSR primers (Pt15169, Pt30204, Pt41093, Pt87268, and Pt110048).

Main results: The analysis of molecular variance (AMOVA) revealed that the genetic diversity among the Brutia pine populations was slightly higher than that of Aleppo pine (27.06% and 24.27%, respectively). The Aleppo pine populations separately displayed a clear east-west differentiation across the Mediterranean Basin, confirming previous results using other markers. Although the Brutia pine populations showed no spatial genetic pattern, geographically close populations and/or populations from their continual distribution range were genetically closer than the fragmented and/or ecologically marginal populations.

Research highlights: The seven Aleppo pine populations from the eastern range (Türkiye, Greece, and Italy) were more than two-fold diverse than the 13 populations from the western range (Spain and Morocco). The eastern range of Aleppo pine and Brutia pine populations had similar levels of genetic diversity parameters. These results suggested that the Eastern Mediterranean Basin is a possible genetic diversity center for the two pine species.

Downloads

Download data is not yet available.

References

Bandelt HJ, Froster P, Roehl A, 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 161: 27-48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

Boydak M, 2004. Silvicultural characteristics and natural regeneration of Pinus brutia Ten.-A review. Plant Ecol 171: 153-163. https://doi.org/10.1023/B:VEGE.0000029373.54545.d2

Bucci G, Anzidei M, Madaghiele A, Vendramin GG, 1998. Detection of haplotypic variation and natural hybridization in halepensis-complex pine species using chloroplast simple sequence repeat (Ssr) markers. Mol Ecol 7: 1-11. https://doi.org/10.1046/j.1365-294x.1998.00466.x

Climent J, Alizoti P, Rodriguez-Quilón I, Kurt Y, Ducci F, Fady B, et al., 2021. Conservation and breeding of Mediterranean pines. In: Pines and their mixed forest ecosystems in the Mediterranean Basin; Ne'eman G, Osem Y (eds). Springer Nature Switzerland AG, 746 pp. https://doi.org/10.1007/978-3-030-63625-8_3

Conkle MT, Schiller G, Grunwald C, 1988. Electrophoretic analysis of diversity and phylogeny of Pinus brutia and closely related taxa. Syst Bot 13: 411-424. https://doi.org/10.2307/2419301

Corander J, Waldmann P, Sillanpaa MJ, 2003. Bayesian analysis of genetic differentiation between populations. Genetics 163: 367-374. https://doi.org/10.1093/genetics/163.1.367

Corander J, Sire'n J, Arjas E, 2008. Bayesian spatial modeling of genetic population structure. Comput Stat 23: 111-129. https://doi.org/10.1007/s00180-007-0072-x

Daskalakou EN, Thanos CA, 2010. Post-fire seedling dynamics and performance in Pinus halepensis Mill. populations. Acta Oecol 36: 446-453. https://doi.org/10.1016/j.actao.2010.05.001

Doyle JJ, Doyle JL, 1990. Isolation of plant DNA from fresh tissue. Focus 12: 13-15. https://doi.org/10.2307/2419362

Dzialuk A, Muchewicz E, Boratynski A, Montserrat JM, Boratynska K, Burczyk J, 2009. Genetic variation of Pinus uncinata (Pinaceae) in the Pyrenees determined with cpSSR markers. Plant Syst Evol 277: 197-205. https://doi.org/10.1007/s00606-008-0123-y

Earl DA, vonHoldt BM, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4: 359-361. https://doi.org/10.1007/s12686-011-9548-7

Eliades NG, Eliades DG, 2009. HAPLOTYPE ANALYSIS: software for analysis of haplotypes data. Distributed by the authors. Forest Genetics and Forest Tree Breeding, Georg-Augst University Goettingen, Germany.

Evanno G, Regnaut S, Goudet J, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611-2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x

Excoffier L, Laval G, Schneider S, 2005. Arlequin Ver 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47-50. https://doi.org/10.1177/117693430500100003

Fady B, 2005. Is there really more biodiversity in Mediterranean forest ecosystems? Taxon 54: 905-910. https://doi.org/10.2307/25065477

Fady B, 2012. Biogeography of neutral genes and recent evolutionary history of pines in the Mediterranean Basin. Ann Forest Sci 69: 421-428. https://doi.org/10.1007/s13595-012-0219-y

Fady B, Conord C, 2010. Macroecological patterns of species and genetic diversity in vascular plants of the Mediterranean basin. Divers Distrib 16: 53-64. https://doi.org/10.1111/j.1472-4642.2009.00621.x

Fady B, Semerci H, Vendramin GG, 2003. Euforgen technical guidelines for genetic conservation and use for Aleppo pine (Pinus halepensis) and Brutia pine (Pinus brutia). Int Plant Genet Resour Inst, Rome-Italy, 6 pp.

Goldstein DB, Ruiz LA, Cavalli-Sforza LL, Feldman MW, 1995. An evolution of genetic distances for use with microsatellite loci. Genetics 139: 463-471. https://doi.org/10.1093/genetics/139.1.463

Grivet D, Sebastiani F, González-Martínez SC, Vendramin GG, 2009. Patterns of polymorphism resulting from long-range colonization in the Mediterranean conifer Aleppo pine. New Phytol 184: 1016-1028. https://doi.org/10.1111/j.1469-8137.2009.03015.x

Grivet D, Sebastiani F, Alia R, Bataillon T, Torre S, Zabal-Aguirre M, et al., 2011. Molecular footprints of local adaptation in two Mediterranean conifers. Mol Biol Evol 28(1): 101-116. https://doi.org/10.1093/molbev/msq190

Heuertz M, Teufel J, Gonzalez-Martinez SC, Soto A, Fady B, Alia R, et al., 2010. Geography determines genetic relationships between species of mountain pine (Pinus mugo complex) in western Europe. J Biogeogr 37: 541-556. https://doi.org/10.1111/j.1365-2699.2009.02223.x

Hohn M, Abran P, Vendramin GG, 2005. Genetic analysis of Swiss stone pine populations (Pinus cembra L. subsp cembra) from the Carpathians using chloroplast microsatellite. Acta Silv Lignaria Hung 1: 39-47.

Isik F, Isik K, Lee SJ, 1999. Genetic variation in Pinus brutia Ten. in Turkey: I. Growth, biomass and stem quality traits. Forest Genet 6(2): 89-99.

Isik K, Isik F, 1999. Genetic variation in Pinus brutia Ten. in Turkey II. Branching and crown traits. Silvae Genet 48(6): 293-302.

İçgen Y, Kaya Z, Çengel B, Velioğlu E, Öztürk H, Önde S, 2006. Potential impact of forest management and tree improvement on genetic diversity of Brutia pine (Pinus brutia Ten.) plantations in Turkey. Forest Ecol and Manag 225: 328-336. https://doi.org/10.1016/j.foreco.2006.01.009

Jakobsson M, Rosenberg NA, 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801-1806. https://doi.org/10.1093/bioinformatics/btm233

Kandemir GE, Kandemir I, Kaya Z, 2004. Genetic variation in Turkish red pine (Pinus brutia Ten.) seed stands as determined by Rapd markers. Silvae Genet 53(4): 169-175. https://doi.org/10.1515/sg-2004-0031

Kaya N, Isik K, Adams WT, 2006. Mating system and pollen contamination in a Pinus brutia seed orchard. New Forest 31: 409-416. https://doi.org/10.1007/s11056-005-0876-x

Korol L, Madmony A, Riov Y, Schiller G, 1995. Pinus halepensis x Pinus brutia subsp. brutia hybrids? Identification using morphological and biochemical traits. Silvae Genet 44: 186-190.

Korol L, Shklar G, Schiller G, 2002a. Diversity among circum-Mediterranean populations of Aleppo pine and differentiation from Brutia pine in their isoenzymes: additional results. Silvae Genet 51(1): 35-41.

Korol L, Shklar G, Schiller G, 2002b. Genetic variation within and among Pinus brutia Ten. seed stands in Turkey in their isoenzymes. Forest Genet 9(3): 233-242.

Kremer A, Kleinschmit J, Cottrell J, Cundall EP, Deans JD, Ducousso A, et al., 2002. Is there a correlation between chloroplastic and nuclear divergence, or what are the roles of history and selection on genetic diversity in European oaks? For Ecol Manag 156: 75-87. https://doi.org/10.1016/S0378-1127(01)00635-1

Kremer A, Ronce O, Robledo-Arnuncio JJ, Guillaume F, Bohrer G, Nathan R, et al., 2012. Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecol Lett 15(4): 378-392. https://doi.org/10.1111/j.1461-0248.2012.01746.x

Kurt Y, González-Martínez SC, Isik K, Alia R, 2012. Genetic differentiation in Pinus brutia Ten. using molecular markers and quantitative traits: the role of altitude. Ann For Sci 69: 345-351. https://doi.org/10.1007/s13595-011-0169-9

Lise Y, Kaya Z, Isik F, Sabuncu R, Kandemir I, Onde S, 2007. The impact of over-exploitation on the genetic structure of Turkish red pine (Pinus brutia Ten.) populations determined by RAPD markers. Silva Fenn 41(2): 211-220. https://doi.org/10.14214/sf.291

Mauri A, Di Leo M, de Rigo D, Caudullo G, 2016. Pinus halepensis and Pinus brutia in Europe: distribution, habitat, usage and threats. In: European Atlas of Forest Tree Species; San-Miguel-Ayanz J, et al. (eds),. Publ. Off. EU, Luxembourg, pp. e0166b8.

Morgante M, Felice N, Vendramin GG, 1998. Analysis of hypervariable chloroplast microsatellites in Pinus halepensis reveals a dramatic genetic bottleneck. In: Molecular tools for screening biodiversity; Karp A, Isaac PG, Ingram DS (eds). Chapman & Hall, London. pp: 407-412. https://doi.org/10.1007/978-94-009-0019-6_73

Nei M, 1987. Molecular evolutionary genetics. Columbia University Press, New York, 512 pp. https://doi.org/10.7312/nei-92038

Olsson S, Lorenzo Z, Zabal-Aguirre M, Andrea Piotti A, Vendramin GG, González-Martínez SC, et al., 2021. Evolutionary history of the Mediterranean Pinus halepensis-brutia species complex using gene-resequencing and transcriptomic approaches. Plant Mol Biol 106: 367-380. https://doi.org/10.1007/s11103-021-01155-7

Panetsos KP, Scaltsoyiannes A, Aravanopoulos FA, Dounavi K, Demetrakopoulos A, 1997. Identification of Pinus brutia Ten, P. halepensis Mill. and their putative hybrids". Silvae Genet 46: 253-257.

Petit RJ, Hampe A, Cheddadi R, 2005. Climate changes and tree phylogeography in the Mediterranean. Taxon 54: 877-885. https://doi.org/10.2307/25065568

Pritchard JK, Stephens M, Donnelly P, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959. https://doi.org/10.1093/genetics/155.2.945

Rambaut A, 2018. Figtree v1.4.4. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/

Ribeiro MM, Plomion C, Petit R, Vendramin GG, Szmidt AE, 2001. Variation in chloroplast single-sequence repeats in Portuguese maritime pine (Pinus pinaster Ait.). Theor App Genet 102: 97-103. DOI:10.1007/s001220051623 https://doi.org/10.1007/s001220051623

Richardson DM, Rundel PW, Jackson ST, Teskey RO, Aronson J, Bytnerowicz A, et al., 2007. Human impacts in pine forests: past, present and future. Annu Rev Ecol Evol Syst 38: 275-297. https://doi.org/10.1146/annurev.ecolsys.38.091206.095650

Robledo-Arnuncio JJ, Collada C, Alía R, Gil L, 2005. Genetic structure of montane isolates of Pinus sylvestris L. in a Mediterranean refugial area. J Biogeogr 32: 595-605. https://doi.org/10.1111/j.1365-2699.2004.01196.x

Ruiz Daniels R, Taylor RS, Serra-Varela MJ, Vendramin GG, Gonzalez-Martinez SC, Grivet D, 2018. Inferring selection in instances of long-range colonization: The Aleppo pine (Pinus halepensis) in the Mediterranean Basin. Mol Ecol 27: 3331-3345. https://doi.org/10.1111/mec.14786

Schiller G, Conkle MT, Grunwald C, 1986. Local differentiation among Mediterranean populations of Aleppo pine in their isozymes. Silvae Genet 35: 11-18.

StClair JB, Howe GT, 2011. Strategies for conserving forest genetic resources in the face of climate change. Turk J Bot 35: 403-409. https://doi.org/10.3906/bot-1012-98

Tozkar CO, Onde S, Kaya Z, 2009. The phylogenetic relationship between populations of marginally and sympatrically located Pinus halepensis Mill. and Pinus brutia Ten. in Turkey, based on the ITS-2 region. Turk J Agric For 33: 363-373. https://doi.org/10.3906/tar-0811-26

Tzedakis PC, Lawson IT, Frogley MR, Hewitt GM, Preece RC, 2002. Buffered tree population changes in a Quaternary refugium: Evolutionary implications. Science 297: 2044-2047. https://doi.org/10.1126/science.1073083

Vendramin GG, Lelli L, Rossi P, Morgante M, 1996. A set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae. Mol Ecol 5: 595-598. https://doi.org/10.1111/j.1365-294X.1996.tb00353.x

Vendramin GG, Anzidei M, Madaghiele A, Bucci G, 1998. Distribution of genetic diversity in Pinus pinaster Ait. as revealed by chloroplast microsatellites. Theor Appl Genet 97: 456-463. https://doi.org/10.1007/s001220050917

Published
2023-06-08
How to Cite
KURT, Y., CENGEL, B., VELIOGLU, E., GONZALEZ-MARTINEZ, S. C., GRIVET, D., & KAYA, N. (2023). Chloroplast microsatellite diversity of Pinus brutia Ten. and Pinus halepensis Mill. populations across the Mediterranean basin: Inferences of their distributions. Forest Systems, 32(2), e008. https://doi.org/10.5424/fs/2023322-19729
Section
Research Articles