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Genetic diversity and population structure analysis of Pistacia species revealed by phenylalanine ammonia-lyase gene markers and implications for conservation

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Abstract

Information on population genetic structure and crop genetic diversity is important for genetically improving crop species and conserving threatened species. The PAL gene sequence is part of a multigene family that can be utilized to design DNA marker systems for genetic diversity and population structure investigation. In the current study, genetic diversity and population structure of 100 accessions of wild Pistacia species were investigated with 78 PAL markers. A protocol for using PAL sequences as DNA markers was developed. A total of 313 PAL loci were recognized, showing 100% polymorphism for PAL markers. The PAL markers produced relatively more observed and effective alleles in Pistacia falcata and Pistacia atlantica, with a higher Shannon’s information index and expected heterozygosity in P. atlantica, Pistacia vera and Pistacia mutica. Pairwise assessment of Nei’s genetic distance and genetic identity between populations revealed a close association between geographically isolated populations of Pistacia khinjuk and Pistacia chinensis. The accessions of wild Pistacia species had more genetic relationship among studied groups of species. Analysis of molecular variance indicated 19% among-population variation and 81% within-population variation for the PAL gene based DNA marker. Population structure analysis based on PAL revealed four groups with high genetic admixture among populations. The results establish PAL markers as a functional DNA marker system and provide important genetic information about accessions from wild populations of Pistacia species.

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Abbreviations

PAL:

Phenylalanine ammonia-lyase

PCRs:

Polymerase chain reactions

PAGE:

Polyacrylamide gel electrophoresis

PIC:

Polymorphism information content

RP:

Resolving power

SI:

Shannon’s information index

AMOVA:

Analysis of molecular variance

CCC:

Cophenetic correlation coefficient

UPGMA:

Unweighted pair group method arithmetic

PCA:

Principal component analysis

PCoA:

Principal coordinate analysis

NTSYS:

Numerical taxonomy multivariate analysis system

MCMC:

Markov chain Monte Carlo

SCoT:

Start codon targeted

IRAP:

Inter-retrotransposon amplified polymorphism

MI:

Marker index

PP:

Percentage polymorphism

UTR:

Untranslated region

References

  • Anderson JA, Churchill GA, Autrique JE, Tanksley SD, Sorrells ME (1993) Optimizing parental selection for genetic linkage maps. Genome 36:181–186. https://doi.org/10.1139/g93-024

    Article  PubMed  CAS  Google Scholar 

  • Bagal UR, Leebens-Mack JH, Lorenz WW, Dean JF (2012) The phenylalanine ammonia lyase (PAL) gene family shows a gymnosperm-specific lineage. BMC Genom 13(Suppl. 3):S1

    CAS  Google Scholar 

  • Basha SA, Chatterjee SC (2007) Activation of phenylalanine ammonia lyase contributes to non-host resistance in Triticum aestivum against Sclerotinia sclerotiorum. Indian Phytopathol 60:442–449

    Google Scholar 

  • Campos R, Nonogaki H, Suslow T, Saltveit ME (2004) Isolation and characterization of a wound inducible phenylalanine ammonia-lyase gene (LsPAL1) from Romaine lettuce leaves. Physiol Plant 121:429–438. https://doi.org/10.1111/j.1399-3054.2004.00336.x

    Article  CAS  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang A, Lim MH, Lee SW, Robb EJ, Nazar RN (2008) Tomato phenylalanine ammonia-lyase gene family, highly redundant but strongly underutilized. J Biol Chem 283:33591–33601. https://doi.org/10.1074/jbc.M804428200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Creste S, Neto AT, Figueira A (2001) Detection of single sequence repeat polymorphisms in denaturing polyacrylamide sequencing gels by silver staining. Plant Mol Biol Rep 19:299–306. https://doi.org/10.1007/BF02772828

    Article  CAS  Google Scholar 

  • Cui Y, Magill J, Frederiksen R, Magill C (1996) Chalcone synthase and phenylalanine ammonia lyase mRNA following exposure of sorghum seedlings to three fungal pathogens. Physiol Mol Plant Pathol 49:187–199. https://doi.org/10.1006/pmpp.1996.0048

    Article  CAS  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dong CJ, Shang QM (2013) Genome-wide characterization of phenylalanine ammonia-lyase gene family in watermelon (Citrullus lanatus). Planta 238:35–49. https://doi.org/10.1007/s00425-013-1869-1

    Article  PubMed  CAS  Google Scholar 

  • Duroux L, Welinder KG (2003) The peroxidase gene family in plants: a phylogenetic overview. J Mol Evol 57:397–407. https://doi.org/10.1007/s00239-003-2489-3

    Article  PubMed  CAS  Google Scholar 

  • Esmail-pour A (2001) Distribution, use and conservation of pistachio in Iran. In: Padulosi S, Hadj-Hassan A (eds), Towards a comprehensive documentation and use of Pistacia genetic diversity in central and West Asia, North Africa and Europe, 16–26. Report of the IPGRI Workshop, 14–17 Dec 1998, Ibrid, Jordan. International Plant Genetic Resources Institute (IPGRI), Rome, Italy

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  PubMed Central  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null allele. Mol Ecol 7:574–578. https://doi.org/10.1111/j.1471-8286.2007.01758.x

    Article  CAS  Google Scholar 

  • FAO (2006) FAOSTAT database. www.fao.org/faostat/

  • Fraser CM, Chapple C (2011) The phenylpropanoid pathway in Arabidopsis. Arabidopsis Book 9:e152

    Article  Google Scholar 

  • Fukasawa-Akada T, Kung SD, Watson JC (1996) Phenylalanine ammonia-lyase gene structure, expression, and evolution in Nicotiana. Plant Mol Biol 30:711–722

    Article  PubMed  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez AM, Marcel TC, Kohutova Z, Stam P, van der Linden CG, Niks RE (2010) Peroxidase profiling reveals genetic linkage between peroxidase gene clusters and basal host and nonhost resistance to rusts and mildew in barley. PLoS ONE 5(8):e10495. https://doi.org/10.1371/journal.pone.0010495

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gulsen O, Shearman RC, Heng-Moss TM, Mutlu N, Lee DJ, Sarath G (2007) Peroxidase gene polymorphism in buffalograss and other grasses. Crop Sci 47:767–774. https://doi.org/10.2135/cropsci2006.07.0496

    Article  CAS  Google Scholar 

  • Gulsen O, Kaymak S, Ozongun S, Uzun A (2010) Genetic analysis of Turkish apple germplasm using peroxidase gene-based markers. Sci Hortic 125:368–373

    Article  CAS  Google Scholar 

  • Hamberger B, Ellis M, Friedmann M, de Azevedo Sousa C, Barbazuk B, Douglas C (2007) Genome-wide analyses of phenylpropanoid- related genes in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families. Can J Bot 85:1182–1201

    Article  CAS  Google Scholar 

  • Herrero J, Esteban-Carrasco A, Zapata JM (2013) Looking for Arabidopsis thaliana peroxidases involved in lignin biosynthesis. Plant Physiol Biochem 67:77–86. https://doi.org/10.1016/j.plaphy.2013.02.019

    Article  PubMed  CAS  Google Scholar 

  • Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidase. Plant Cell Physiol 42:462–468. https://doi.org/10.1093/pcp/pce061

    Article  PubMed  CAS  Google Scholar 

  • Iranjo P, Nabati Ahmadi D, Sorkheh K, Rajabi Memeari H, Ercisli S (2016) Genetic diversity and phylogenetic relationships between and within wild Pistacia species populations and implications for its conservation. J For Res 27:685–697. https://doi.org/10.1007/s11676-015-0098-9

    Article  Google Scholar 

  • Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bulletin de la Société Vaudoise des Sciences Naturelles 44:223–270

    Google Scholar 

  • Jeong MJ, Choi BS, Bae DW, Shin SC, Park SU, Lim HS, Kim J, Kim JB, Cho BK, Bae H (2012) Differential expression of kenaf phenylalanine ammonia-lyase (PAL) ortholog during developmental stages and in response to abiotic stresses. Plant Omics J 5:392–399

    CAS  Google Scholar 

  • Jolliffe IT (2002) Principal component analysis, 2nd edn. Springer, New York

    Google Scholar 

  • Jones DH (1984) Phenylalanine ammonia-lyase: regulation of its induction, and its role in plant development. Phytochemistry 23:1349–1359. https://doi.org/10.1016/S0031-9422(00)80465-3

    Article  CAS  Google Scholar 

  • Kao YY, Harding SA, Tsai CJ (2002) Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiol 130:796–807

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan MSY, Bano S, Javed K, Mueed MA (2006) A comprehensive review of the chemistry and pharmacology of Corchorus species—A source of cardiac glycosides, triterpenoids, ionones, flavonoids, coumarins, steroids and some other compounds. J Sci Ind Res 65:283–298

    CAS  Google Scholar 

  • Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738

    PubMed  PubMed Central  CAS  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology, 2nd English edn. Elsevier, Amsterdam

    Google Scholar 

  • Lewontin RC (1972) The apportionment of human diversity. In: Dobzhansky T, Hecht M, Steere WC (eds) Springer book archive, evolutionary biology, pp 381–398. 10.1007/978-1-4684-9063-3_14

  • Mantel N (1967) The detection of disease clustering and generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • McDermott JM, McDonald BA (1993) Gene flow in plant pathosystems. Annu Rev Phytopathol 31:353–373. https://doi.org/10.1146/annurev.py.31.090193.002033

    Article  Google Scholar 

  • Milligan BG, Leebens-Mack J, Strand AE (1994) Conservation genetics: beyond the maintenance of marker diversity. Mol Ecol 12:844–855

    Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Breusegem FW (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009

    Article  PubMed  CAS  Google Scholar 

  • Mizutani M, Ohta D, Sato R (1997) Isolation of a cDNA and a genomic clone encoding cinnamate 4-hydroxylase from Arabidopsis and its expression manner in plant. Plant Physiol 113:755–763

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci (USA) 70:3321–3323

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Olsen KM, Lea US, Slimestad R, Verheul M, Lillo C (2008) Differential expression of four Arabidopsis PAL genes; PAL1 and PAL2 have functional specialization in abiotic environmental-triggered flavonoid synthesis. J Plant Physiol 165:1491–1499

    Article  PubMed  CAS  Google Scholar 

  • Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265. https://doi.org/10.1007/s00299-005-0972-6

    Article  PubMed  CAS  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  • Prevost A, Wilkinson MJ (1999) A new system of comprising PCR primers applied to ISSR fingerprinting of potato accessions. Theor Appl Genet 98:107–112. https://doi.org/10.1007/s001220051046

    Article  CAS  Google Scholar 

  • Pritchard JK, Stevens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pritchard JK, Wen XQ, Falush D (2010) Documentation for structure software: Version 2.3. http://pritch.bsd.uchicago.edu/software/structure_v.2.3.1/documentation.pdf. Accessed 15 Sept 2012

  • Raes J, Rohde A, Christensen JH, Van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramakrishnan M, Antony Ceasar S, Duraipandiyan V, Al-Dhabi NA, Ignacimuthu S (2016) Using molecular markers to assess the genetic diversity and population structure of finger millet (Eleusine coracana (L.) Gaertn.) from various geographical regions. Genet Resour Crop Evol 63:361–376. https://doi.org/10.1007/s10722-015-0255-1

    Article  Google Scholar 

  • Rawal HC, Singh NK, Sharma TR (2013) Conservation, divergence, and genome-wide distribution of PAL and POX A gene families in plants. Int J Genomics. Article ID 678969, p 10. http://dx.doi.org/10.1155/2013/678969

  • Razavi S (2006) Pistachio production, Iran vs. the world. Acta Hortic 726:689–694

    Article  Google Scholar 

  • Reichert AI, He XZ, Dixon RA (2009) Phenylalanine ammonia-lyase (PAL) from tobacco (Nicotiana tabacum): characterization of the four tobacco PAL genes and active heterotetrameric enzymes. Biochem J 424:233–242. https://doi.org/10.1042/BJ20090620

    Article  PubMed  CAS  Google Scholar 

  • Rohde A, Morreel K, Ralph J, Goeminne G, Hostyn V, De Rycke R, Kushnir S, Van Doorsselaere J, Joseleau JP, Vuylsteke M, Van Driessche G, Van Beeumen J, Messens E, Boerjan W (2004) Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell 16:2749–2771

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

  • Satya P, Banerjee R, Biswas C, Karan M, Ghosh S, Ali N (2014) Genetic analysis of population structure using peroxidase gene and phenylalanine ammonia-lyase gene-based DNA markers: a case study in Jute (Corchorus spp.). Crop Sci 54:1609–1620. https://doi.org/10.2135/cropsci2013.08.0518

    Article  CAS  Google Scholar 

  • Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J 28:679–688. https://doi.org/10.1046/j.1365-313x.2001.01187.x

    Article  PubMed  CAS  Google Scholar 

  • Shang QM, Li L, Dong CJ (2012) Multiple tandem duplication of the phenylalanine ammonia-lyase genes in Cucumis sativus L. Planta 236:1093–1105

    Article  PubMed  CAS  Google Scholar 

  • Sorkheh K, Shiran B, Gradziel TM, Epperson BK, Martinez-Gomez P, Asadi E (2007) 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 156:237–344

    Article  CAS  Google Scholar 

  • Sorkheh K, Amirbakhtiar N, Ercislie S (2016) Potential start codon targeted (SCoT) and inter-retrotransposon amplified polymorphism (IRAP) markers for evaluation of genetic diversity and conservation of wild Pistacia species population. Bioch Genet 54:368–387. https://doi.org/10.1007/s10528-016-9725-1

    Article  CAS  Google Scholar 

  • Yeh FC, Yang R, Boyle TJ, Ye Z, Xiyan JM (2000) PopGene32, microsoft windows-based freeware for population genetic analysis. Version 1.32. Molecular Biology and Biotechnology Centre, University of Alberta, Edmonton

  • Zhang ZG, Zhang Q, Wu JX, Zheng X, Zheng S, Sun XH, Qiu QS, Lu TG (2013) Gene knockout study reveals that cytosolic Ascorbate Peroxidase 2(OsAPX2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses. PLoS ONE 8(2):E57472. https://doi.org/10.1371/journal.pone.0057472

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zohary D (1996) The genus Pistacia L. In: Padulosi S, Caruso T, Barone E (eds) Taxonomy, distribution, conservation and uses of Pistacia genetic resources. IPGRI, Palermo, Italy, pp 1–11

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Acknowledgements

We thank the Iranian Pistachio Research Institute, Rafsanjan, Iran for providing some samples of the accessions of wild Pistacia species. We also thank two anonymous reviewers for constructive suggestions that greatly helped to improve the manuscript.

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Authors and Affiliations

  1. Department of Agronomy and Plant Breeding, Faculty of Agriculture, Shahid Chamran University of Ahvaz, P. O. Box 61355/144, Ahvaz, Iran

    Setareh Mirzavand, Karim Sorkheh & Mohammad Reza Siahpoosh

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  1. Setareh Mirzavand
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  2. Karim Sorkheh
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  3. Mohammad Reza Siahpoosh
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All authors contributed equally to this work.

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Correspondence to Karim Sorkheh.

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Project funding: This study was supported by Shahid Chamran University of Ahvaz Fund (SHCUF) under Project No. SHCH_AGF_Grant 1394.

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Corresponding editor: Tao Xu.

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Mirzavand, S., Sorkheh, K. & Siahpoosh, M.R. Genetic diversity and population structure analysis of Pistacia species revealed by phenylalanine ammonia-lyase gene markers and implications for conservation. J. For. Res. 29, 991–1001 (2018). https://doi.org/10.1007/s11676-017-0508-2

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