Genetic diversity and phylogenetic relationships between and within wild Pistacia species populations and implications for its conservation

Abstract

Although cultivation and utilization of Pistacia are fully exploited, the evolutionary history of the Pistacia genus and the relationships among the species and accessions is still not well understood. The aim of this study was to analyze random amplified polymorphic DNA (RAPD) in a total of 50 accessions of wild pistachio species, which included five populations Pistacia vera, Pistacia khinjuk, Pistacia atlantica, Pistacia mutica, and Pistacia eurycarpa. High levels of genetic diversity were detected within wild pistachio accessions, as revealed by using the unweighted pair-group method with arithmetic averaging and supported via analysis of molecular variance. The objectives of this investigation were to estimate marker indices, polymorphic information contents (PICs), and genetic similarities (GS) for RAPD markers; assess the genetic diversity of Pistacia species, using GS estimated from RAPD fingerprints and molecular characterization; and facilitate the use of markers in inter-specific introgression and cultivar improvement. Out of the 149 polymerase chain reaction fragments that were scored, 146 (97.98 %) were polymorphic. Genetic similarities ranged from 0.3 to 0.86 %, marker indices ranged from 2.98 to 17.74 %, and PICs ranged from 0.80 to 0.99 %. Our results provided great molecular identification of all assayed genotypes, which have shown that there is large quantity of genetic diversity among the pistachio accessions. This finding might render striking information in breeding management strategies for genetic conservation and cultivar development.

Keywords

Pistachio / Pistacia / Phylogenetic / RAPD / Population structure / Genetic diversity

References

[1] Ahmad R, Ferguson L, Southwick SM. Identification of pistachio (Pistacia vera L.) nuts with microsatellite markers. J Am Soc Hortic Sci, 2003, 128: 898-903.

[2] Ahmad R, Struss D, Southwick SM. Development and characterization of microsatellite markers in citrus. J Am SocHorticSci, 2003, 128: 584-590.

[3] Ahmadi Afzadi M, SeyedTabatabaei BE, Mohammadi SA, Tajabadipur A. Comparison of genetic diversity in species and cultivars of pistachio (Pistacia vera L.) based on amplified fragment length polymorphism marker. Iran J Biotechnol, 2007, 5: 147-152.

[4] Allendorf FW. Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol, 1986, 5: 181-190.

[5] AL-Sousli M, Faory H, Nakar M, Zaid S, Al-Safadi B, Al-Saghir M. Genetic relationships among some Pistacia species (Anacardiaceae) in Syria. Middle-East J Sci Res, 2014, 21: 1487-1497.

[6] Badfar-Chaleshtori S, Shiran B, Kohgard M, Mommeni H, Hafizi A, Khodambashi M, Mirakhorli N, Sorkheh K. Assessment of genetic diversity and structure of Imperial Crown (Fritillaria imperialis L.) populations in the Zagros region of Iran using AFLP, ISSR and RAPD markers and implications for its conservation. Biochem Syst Ecol, 2012, 42: 35-48.

[7] Banihashemi Z (1995) The presence of pistachio gummosis in Iran. Paper presented at the 1st national workshop on the pistachio nut, Rafsanjan, Iran, 24–26 Sept 1995

[8] Barone E, Diamarco L, Marra FP, Sidari M (1993) Isozymes and multivariate analysis to discriminate male and female Sicilian germplasm of pistachio. IXth Groupe de Recherchesetd’EtudesMediterraneen pour le Pistachieretl’Amandier, Agrigento, pp 73–79

[9] Behboodi B. Ecological distribution study of wild pistachios for selection of rootstock. Options Mediterr Ser A, 2003, 63: 61-67.

[10] Brown-Guedira GL, Thompson JA, Nelson RL, Warburton ML. Evaluation of genetic diversity of soybean introductions and North American ancestors using RAPD and SSR markers. Crop Sci, 2000, 40: 815-823.

[11] Caicedo AL, Gaitan E, Duque MC, Chica OT, Tohma J. AFLP fingerprinting of Phaseolus lunatus L. and related wild species from South America. Crop Sci, 1999, 39: 1497-1507.

[12] Cruse-Sanders JM, Hamrick JL, Ahumada JA. Consequences of harvesting for genetic diversity in American ginseng (Panaxqu inquefolius L.): a simulation study. BiodiversConserv, 2005, 14: 493-504.

[13] Dollo L (1993) An isozyme study of Sicilian Pistacia species, varieties, and offspring from artificial pollination. IXth Groupe de Recherchesetd’EtudesMediterraneen pour le Pistachieretl’Amandier, Agrigento, pp 80–87

[14] Dollo L, Hormaza JI, Polito VS. RAPD polymorphism among pistachio (Pistacia vera) cultivars. Fruit Var J, 1995, 49: 147-152.

[15] Edwards KJ. Karp A, Issac PG, Ingram DE. Randomly amplified polymorphic DNAs (RAPDs). Molecular tools for screening biodiversity-plants and animals. 1998, London: Chapman and Hall, 171 179

[16] Esmail-pour A (2001) Distribution, use and conservation of pistachio in Iran. In: Padulosi S, Hadj-Hassan A (eds) In towards a comprehensive documentation and use of Pistacia genetic diversity in central and West Asia, North Africa and Europe. Report of the IPGRI workshop, 14–17 December 1998, Ibrid, Jordan. IPGRI, Rome, Italy

[17] Excoffier L, Smouse P, Quattro J. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 1992, 131: 479-491.

[18] Francisco-Ortega J, Santos-Guerra A, Kim SC, Crawford DJ. Plant genetic diversity in the Canary Islands: a conservation perspective. Am J Bot, 2000, 87: 909-919.

[19] Fu YM, Chen WH, Tsai WT, Lin YS, Chyou MS, Chen YH (1997) Phylogenetic studies of taxonomy and evolution among wild species of Phalaenopsis by Random Amplified DNA markers. Report of the Taiwan Sugar Research Institute 157:27–42

[20] Fu YB, Peterson G, Diederichsen A, Richards KW. RAPD analysis of genetic relationships of seven flax species in the genus Linum L. Genet Resour Crop Evol, 2002, 49: 253-259.

[21] Ghahreman A, Attar F. Biodiversity of plant species in Iran. 1999, Tehran: Publication of Tehran University

[22] Goh MWK, Kumar PP, Lim SH, Tan HTW. Random amplified polymorphic DNA analysis of the moth orchid, Phalaenopsis (Epidendroideae: Orchidaceae). Euphytica, 2005, 141: 11-22.

[23] Golan-Goldhirsh A, Barazani O, Wang ZS, Khadka DK, Saunders JA, Kostiukovsky V. Genetic relationships among Mediterranean Pistacia species evaluated by RAPD and AFLP markers. Plant SystEvol, 2004, 246: 9-18.

[24] Guilford P, Prakash S, Zhu JM, Rikkerink E, Gardiner S, Bassett H, Forster R. Microsatellite in Malus × domestica (apple). Abundance, polymorphism and cultivar identification. TheorAppl Genet, 1997, 94: 249-255.

[25] Hamrick JL, Godt MJW. Avise JC, Hamrick JL. Conservation genetics of endemic plant species. Conservation genetics: case histories from nature. 1996, New York: Chapman and Hall, 281 304

[26] Hormaza JI, Dollo L, Polito VS. Determination of relatedness and geographical movements of Pistacia vera L. (pistachio, Anacardiaceae) germplasm by RAPD analysis. Econ Bot, 1994, 48: 349-358.

[27] Hormaza JI, Pinney K, Polito VS. Genetic diversity of pistachio (Pistacia vera, Anacardiaceae) germplasm based on randomly amplified polymorphic DNA (RAPD) markers. Econ Bot, 1998, 52: 78-87.

[28] IPGRI (1998) Descriptors for Pistacia spp (excluding P. vera L.). International Plant Genetic Resources Institute, Rome

[29] Kafkas S. Phylogenetic analysis of the genus Pistacia by AFLP markers. Plant SystEvol, 2006, 262: 113-124.

[30] Kafkas S, Perl-Treves R. Morphological and molecular phylogeny of Pistacia species in Turkey. Theor Appl Genet, 2001, 102: 908-915.

[31] Kafkas S, Perl-Treves R. Interspecific relationship in the genus Pistacia L. (Anacardiaceae) based on RAPD fingerprinting. J Hort Sci, 2002, 37: 168-171.

[32] Kafkas S, Kafkas E, Perl-Treves R. Morphological diversity and germplasm survey of three wild Pistacia species in Turkey. Genet Resour Crop Evol, 2002, 49: 261-270.

[33] Kafkas S, Kaska A, Wassimi AN, Padulosi S. Molecular characterisation of Afghan pistachio accessions by amplified fragment length polymorphisms (AFLPs). J Hortic Sci Biotechnol, 2006, 81(5): 864-868.

[34] Kafkas S, Ozkan H, Ak BE, Acar I, Alti HS. Detecting DNA polymorphism and genetic diversity in a wide pistachio germplasm: comparison of AFLP, ISSR, and RAPD marker. J Am Soc Hortic Sci, 2006, 131: 522-529.

[35] Kafkas S, Dogan Y, Zaloglu S (2009) Phylogenetic analysis in the genus Pistacia by simple sequence repeat markers. In: 5th international symposium on pistachios and almonds. Abstract book, p. 84, October 6–10, Sanliurfa, Turkey

[36] Karimi HR, Kafkas S. Genetic relationships among Pistacia species studied by SAMPL markers. Plant Syst Evol, 2011, 297: 207-212.

[37] Karimi HR, Kafkas S, Zamani Z, Ebadi A, Fatahi MR. Genetic relationships among species and cultivars of Pistacia using AFLP marker. Plant Syst Evol, 2009, 279: 21-28.

[38] Karimi HR, Zamani Z, Ebadi A, Fatahi MR. Morphological diversity of Pistacia species in Iran. Genet Resour Crop Evol, 2009, 56: 561-571.

[39] Karimi HR, Zamani Z, Ebadi A, Fatahi MR. Genetic relationship of some Pistacia species using RAPD and AFLP markers. Hort Environ Biotechnol, 2009, 50: 519-524.

[40] Karimi HR, HajizadehHossinAbadi M, MalekiKohbanani A. Genetic diversity of Pistacia khinjuk Stocks. using RAPD markers and leaf morphological characters. Plant Syst Evol, 2012, 298: 963-968.

[41] Katsiotis A, Hagidimitriou M, Drossou A, Pontikis C, Loukas M. Genetic relationships among species and cultivars of Pistacia using RAPDs and AFLPs. Euphytica, 2003, 132: 279-286.

[42] Macpherson JM, Eckstein PE, Scoles GJ, Gajadhar AA. Variability of the random amplified polymorphic assay among thermal cyclers and effects of primer and DNA concentration. Mol Cell Probe, 1993, 7: 293-299.

[43] Maggs DH. Genetic resources in pistachio. Plant Genet Resour Newsl, 1973, 29: 7-15.

[44] Mantel N. The detection of disease clustering and generalized regression approach. Cancer Res, 1967, 27: 209-220.

[45] Milligan BG, Leebens-Mack J, Strand AE. Conservation genetics: beyond the maintenance of marker diversity. MolEcol, 1994, 12: 844-855.

[46] Mirzaei S, Bahar M, Sharifnabi B. A phylogenetic study of Iranian wild pistachio species and some cultivars using RAPD marker. Acta Hortic, 2005, 726: 39-43.

[47] Muralidharan K, Wakeland EK. Concentration of primer and template qualitatively affects products in random amplified polymorphic DNA PCR. Biotechniques, 1993, 14: 362-364.

[48] Nahum S, Inbar M, Nèeman G, Ben-Shlomo R. Phenotypic plasticity and gene diversity in Pistacia lentiscus L. along environmental gradients in Israel. Tree Genet Geno, 2009, 4: 777-785.

[49] Nei M. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci (USA), 1973, 70: 3321-3323.

[50] Niknejad A, Kadir MA, Kadzimin SB, Abdullah NAP, Sorkheh K. Molecular characterization and phylogenetic relationships among and within species of Phalaenopsis (Epidendroideae: Orchidaceae) based on RAPD analysis. Afr J Biotechnol, 2009, 8: 5225-5240.

[51] Noroozi S, Baghizadeh A, JalaliJavaran M. The genetic diversity of Iranian pistachio (Pistacia vera L.) cultivars revealed by ISSR markers. Biol Diver Conserv, 2009, 2: 50-56.

[52] Ozden-Tokatli Y, Akdemir H, Tilkat E, Onay A. Current status and conservation of Pistacia germplasm. Biotechnol Adv, 2010, 28: 130-141.

[53] Parfitt DE, Badenes ML. Molecular phylogenetic analysis of the genus Pistacia. Acta Hortic, 1998, 470: 143-151.

[54] Parfitt D, Badens ML. Phylogeny of the genus Pistacia as determined from analysis of the chloroplast genome. Proc Natl Acad Sci USA, 1997, 94: 7987-7992.

[55] Pazouki L, SalehiShanjani P, Hagidimitrion M, Pirseyedi SM, Naghavi MR, Avanzato D, Quarta R, Kafkas S, Ghareyazie B, Ghaffari MR, KhayamNekoui SM, Mardi M (2009) Genetic diversity and relationships among Pistacia species and cultivar. 5th international symposium on Pistachio and Almonds. Abstract book. Saliurfa, Turkey, p 81

[56] Pazouki L, Mardi M, SalehiShanjani P, Hagidimitriou M, Pirseyedi SM, Naghavi MR, Avanzato D, Vendramin E, Kafkas S, Ghareyazie B, Ghaffari MR, KhayamNekoui SM. Genetic diversity and relationships among Pistacia species and cultivars. Conserv Genet, 2010, 11: 311-318.

[57] Powell W, Morgante M, Andre C, Hanafey Mm Vogel J, Tingey S, Rafalski A. The comparison of RFLP, RAPD, AFLP and SSR (microsatellite) markers for germplasm analysis. Mol Breed, 1996, 2: 225-238.

[58] Rohlf M (1998) NTSYSpc. Numerical taxonomy and multivariate analysis system. Version 2.02i. Department of Ecology and Evolution. State University of New York

[59] Rovira M, Batlle I, Romero M, Vargas FJ. Isoenzymic identification of Pistacia species. Acta Hortic, 1995, 419: 265-271.

[60] SalehiShanjani P, Mardi M, Pazouki L, Hagidimitriou M, Avanzato D, MostafaPirseyedi S, Ghaffari MR, KhayamNekoui SM. Analysis of the molecular variation between and within cultivated and wild Pistacia species using AFLPs. Tree Genet Genome, 2009, 5: 447-458.

[61] Schneider S, Roessli D, Excoffier L (2001) Arlequin: a software for population genetics data analysis. Version 2.000. Genetics and Biometry Lab, Dep. of Athropology, University of Geneva, Geneva

[62] Sorkheh K, Shiran B, Gradziel TM, Epperson BK, Martinez-Gomez P, Asadi E. Amplified fragment length polymorphism as a tool for molecular characterization of almond germplasm: genetic diversity among cultivated genotypes and related wild species of almond, and its relationships with agronomic traits. Euphytica, 2007, 156: 237-344.

[63] Sorkheh K, Shiran B, Rouhi V, Asadi E, Jahanbazi H, Moradi H, Gradziel TM, Martinez-Gomez P. Phenotypic diversity within native Iranian almond (Prunus sp.) species and their breeding potential. Gen Resour Crop Evol, 2009, 56: 947-961.

[64] Struss D, Ahmad R, Southwick SM. Analysis of sweet cherry (Prunusavium L.) cultivars using SSR and AFLP markers. J Am Soc Hortic Sci, 2003, 128: 904-909.

[65] Talebi M, Kazemi M, EbrahimSayed-Tabatabaei B. Molecular diversity and phylogenetic relationships of Pistacia vera, Pistacia atlantica subsp. mutica and Pistacia khinjuk using SRAP markers. Biochem Syst Ecol, 2012, 44: 179-185.

[66] Tanksley SD, Young ND, Paterson AH, Bonierbale MW. RFLP in plant breeding: new tools for an old science. Biotech, 1989, 7: 257-264.

[67] TayefehAliakbarkhany S, Talaie AR, Fatahi Moghadam MR. Investigation of genetic diversity among Pistacia Vera In the Khorasan by using molecular. Mod Genet, 2013, 8: 169-176.

[68] Tsai C-C, Chou C-H. Molecular phylogenetics of Phalaenopsis taxa: an updated review. Orchid Sci Biotechnol, 2007, 1: 44-50.

[69] Van de Peer Y, De Wachter R. TREECON for Windows: as software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. ComputApplBiosci, 1994, 10: 569-570.

[70] Vendramin E, Dettori MT, Verde I, Micali S, Giovinazzi J, Mardi M. Molecular characterization of Pistacia genus by microsatellite markers. Acta Hortic, 2009, 825: 55-61.

[71] Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucl Acids Res, 1990, 18: 6531-6535.

[72] Wishart D. CLASTAN user manual, 1987 3 Edinburgh: Program Library Unit, Univ. of Edinburgh

[73] Yeh FC, Yang RC (1999) POPGENE Version 1.31. University of Albert and Tim Boyle, Center for International Research

[74] Zografou P, Linos A, Hagidimitriou M (2010) Genetic diversity among different genotypes of Pistacia lentiscus var. chia (mastic tree). In: Zakynth in os G. (ed.). XIV GREMPA Meetingon Pistachios and Almonds. Zaragoza: CIHEAM/FAO/AUA/TEI Kalamatas/NAGREF, Options Méditerranéennes: Série A. Séminaires Méditerranéens 94:159–163

[75] Zohary M. A monographic study of the genus Pistacia. Palest J Bot Jerus Ser, 1952, 5: 187-228.

[76] Zohary D. Padulosi S, Caruso T, Barone E. The genus Pistacia L. Taxonomy, distribution, conservation and uses of Pistacia genetic resources. 1996, Rome: IPGRI, 1 11