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

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.

Keywords

Genetic relationship / Classification / Genetic resources / PAL / Phenylalanine ammonia-lyase gene

References

[1] Anderson JA, Churchill GA, Autrique JE, Tanksley SD, Sorrells ME. Optimizing parental selection for genetic linkage maps. Genome, 1993, 36: 181-186.

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

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

[4] Campos R, Nonogaki H, Suslow T, Saltveit ME. Isolation and characterization of a wound inducible phenylalanine ammonia-lyase gene (LsPAL1) from Romaine lettuce leaves. Physiol Plant, 2004, 121: 429-438.

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

[6] Chang A, Lim MH, Lee SW, Robb EJ, Nazar RN. Tomato phenylalanine ammonia-lyase gene family, highly redundant but strongly underutilized. J Biol Chem, 2008, 283: 33591-33601.

[7] Creste S, Neto AT, Figueira A. Detection of single sequence repeat polymorphisms in denaturing polyacrylamide sequencing gels by silver staining. Plant Mol Biol Rep, 2001, 19: 299-306.

[8] Cui Y, Magill J, Frederiksen R, Magill C. Chalcone synthase and phenylalanine ammonia lyase mRNA following exposure of sorghum seedlings to three fungal pathogens. Physiol Mol Plant Pathol, 1996, 49: 187-199.

[9] Dixon RA, Paiva NL. Stress-induced phenylpropanoid metabolism. Plant Cell, 1995, 7: 1085-1097.

[10] Dong CJ, Shang QM. Genome-wide characterization of phenylalanine ammonia-lyase gene family in watermelon (Citrullus lanatus). Planta, 2013, 238: 35-49.

[11] Duroux L, Welinder KG. The peroxidase gene family in plants: a phylogenetic overview. J Mol Evol, 2003, 57: 397-407.

[12] 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

[13] Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol, 2005, 14: 2611-2620.

[14] 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.

[15] Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: dominant markers and null allele. Mol Ecol, 2007, 7: 574-578.

[16] FAO (2006) FAOSTAT database. www.fao.org/faostat/

[17] Fraser CM, Chapple C. The phenylpropanoid pathway in Arabidopsis. Arabidopsis Book, 2011, 9: e152.

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

[19] Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem, 2010, 48: 909-930.

[20] Gonzalez AM, Marcel TC, Kohutova Z, Stam P, van der Linden CG, Niks RE. Peroxidase profiling reveals genetic linkage between peroxidase gene clusters and basal host and nonhost resistance to rusts and mildew in barley. PLoS ONE, 2010 5 8 e10495

[21] Gulsen O, Shearman RC, Heng-Moss TM, Mutlu N, Lee DJ, Sarath G. Peroxidase gene polymorphism in buffalograss and other grasses. Crop Sci, 2007, 47: 767-774.

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

[23] Hamberger B, Ellis M, Friedmann M, de Azevedo Sousa C, Barbazuk B, Douglas C. 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, 2007, 85: 1182-1201.

[24] Herrero J, Esteban-Carrasco A, Zapata JM. Looking for Arabidopsis thaliana peroxidases involved in lignin biosynthesis. Plant Physiol Biochem, 2013, 67: 77-86.

[25] Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H. A large family of class III plant peroxidase. Plant Cell Physiol, 2001, 42: 462-468.

[26] Iranjo P, Nabati Ahmadi D, Sorkheh K, Rajabi Memeari H, Ercisli S. Genetic diversity and phylogenetic relationships between and within wild Pistacia species populations and implications for its conservation. J For Res, 2016, 27: 685-697.

[27] Jaccard P. Nouvelles recherches sur la distribution florale. Bulletin de la Société Vaudoise des Sciences Naturelles, 1908, 44: 223-270.

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

[29] Jolliffe IT. Principal component analysis, 2002 2 New York: Springer.

[30] Jones DH. Phenylalanine ammonia-lyase: regulation of its induction, and its role in plant development. Phytochemistry, 1984, 23: 1349-1359.

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

[32] Khan MSY, Bano S, Javed K, Mueed MA. 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, 2006, 65: 283-298.

[33] Kimura M, Crow JF. The number of alleles that can be maintained in a finite population. Genetics, 1964, 49: 725-738.

[34] Legendre P, Legendre L. Numerical ecology , 1998 2 English Amsterdam: Elsevier.

[35] 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

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

[37] McDermott JM, McDonald BA. Gene flow in plant pathosystems. Annu Rev Phytopathol, 1993, 31: 353-373.

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

[39] Mittler R, Vanderauwera S, Gollery M, Breusegem FW. Reactive oxygen gene network of plants. Trends Plant Sci, 2004, 9: 490-498.

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

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

[42] Nei M. Molecular evolutionary genetics, 1987, New York: Columbia University Press.

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

[44] Passardi F, Cosio C, Penel C, Dunand C. Peroxidases have more functions than a Swiss army knife. Plant Cell Rep, 2005, 24: 255-265.

[45] Peakall R, Smouse PE. GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes, 2006, 6: 288-295.

[46] Prevost A, Wilkinson MJ. A new system of comprising PCR primers applied to ISSR fingerprinting of potato accessions. Theor Appl Genet, 1999, 98: 107-112.

[47] Pritchard JK, Stevens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics, 2000, 155: 945-959.

[48] 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

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

[50] Ramakrishnan M, Antony Ceasar S, Duraipandiyan V, Al-Dhabi NA, Ignacimuthu S. 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, 2016, 63: 361-376.

[51] 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

[52] Razavi S. Pistachio production, Iran vs. the world. Acta Hortic, 2006, 726: 689-694.

[53] Reichert AI, He XZ, Dixon RA. Phenylalanine ammonia-lyase (PAL) from tobacco (Nicotiana tabacum): characterization of the four tobacco PAL genes and active heterotetrameric enzymes. Biochem J, 2009, 424: 233-242.

[54] 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. Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell, 2004, 16: 2749-2771.

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

[56] Satya P, Banerjee R, Biswas C, Karan M, Ghosh S, Ali N. 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, 2014, 54: 1609-1620.

[57] Schopfer P. Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J, 2001, 28: 679-688.

[58] Shang QM, Li L, Dong CJ. Multiple tandem duplication of the phenylalanine ammonia-lyase genes in Cucumis sativus L. Planta, 2012, 236: 1093-1105.

[59] 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.

[60] Sorkheh K, Amirbakhtiar N, Ercislie S. 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, 2016, 54: 368-387.

[61] 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

[62] Zhang ZG, Zhang Q, Wu JX, Zheng X, Zheng S, Sun XH, Qiu QS, Lu TG. 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, 2013 8 2 E57472

[63] 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