Gene flow among wild and cultivated common walnut (Juglans regia) trees in the Qinling Mountains revealed by microsatellite markers

Huijuan Zhou , Peng Zhao , Keith Woeste , Shuoxin Zhang

Journal of Forestry Research ›› 2020, Vol. 32 ›› Issue (5) : 2189 -2201.

PDF
Journal of Forestry Research ›› 2020, Vol. 32 ›› Issue (5) : 2189 -2201. DOI: 10.1007/s11676-020-01254-z
Original Paper

Gene flow among wild and cultivated common walnut (Juglans regia) trees in the Qinling Mountains revealed by microsatellite markers

Author information +
History +
PDF

Abstract

Patterns of gene flow and gene introgression can be used to assess the risk of genetic pollution of wild forest trees from widespread cultivated trees. A comprehensive understanding of the genetic relationships and levels of gene flow among wild and cultivated common walnut (Juglans regia) has become an urgent issue. Using twelve microsatellite markers, we investigated the genetic diversity and gene flow between cultivated and wild trees of J. regia in the Qinling Mountains, China. A high level of genetic variation was detected in both cultivated and wild trees. The mean number of alleles per locus was 17.5. Observed heterozygosity (HO) and expected heterozygosity (HE) were 0.777 and 0.800, respectively. Pollination of mother trees was not by nearest neighbors, and a paternity of 60.7% of offspring evaluated could not be assigned to a local, sampled tree. Pollen flow from cultivated trees to wild trees was infrequent (5.4%), and selfing rates ranged from zero to 25.0%. Male parents were located from 0 to 1005 m from their female partners, with an average pollination distance of 285.1 m. These results are discussed in light of the cultivated species' diversity, outlining the frequent spontaneous genetic contributions from the wild to the cultivated compartment. In addition, the pollen flow parameters provide useful information about the dynamics of pollen movement within J. regia populations.

Keywords

Genetic diversity / Juglans regia / Mating patterns / Microsatellites / Pollen flow

Cite this article

Download citation ▾
Huijuan Zhou, Peng Zhao, Keith Woeste, Shuoxin Zhang. Gene flow among wild and cultivated common walnut (Juglans regia) trees in the Qinling Mountains revealed by microsatellite markers. Journal of Forestry Research, 2020, 32(5): 2189-2201 DOI:10.1007/s11676-020-01254-z

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Ahmed N, Mir JI, Mir RR, Rather NA, RashidR WSH, Mir H, Sheikh MA. SSR and RAPD analysis of genetic diversity in walnut (Juglans regia L.) genotypes from Jammu and Kashmir, India. Physiol Mol Biol Plants, 2012, 18(2): 149-160.

[2]

Aradhya M, Velasco D, Ibrahimov Z, Toktoraliev B, Maghradze D, Musayev M, Bobokashvili Z, Preece JE. Genetic and ecological insights into glacial refugia of walnut (Juglans regia L.). PLoS One, 2017 12 10

[3]

Bai WN, Zeng YF, Liao WJ, Zhang DY. Flowering phenology and wind-pollination efficacy of heterodichogamous Juglans mandshurica (Juglandaceae). Ann Bot, 2006, 98: 397-402.

[4]

Bai WN, Zeng YF, Zhang DY. Mating patterns and pollen dispersal in a heterodichogamous tree, Juglans mandshurica (Juglandaceae). New Phytol, 2007, 176(3): 699-707.

[5]

Barbour RC, Potts BM, Vaillancourt RE, Tibbits WN, Wiltshire RJ. Gene flow between introduced and native Eucalyptus species. New For, 2002, 23(3): 177-191.

[6]

Beer R, Kaiser F, Schmidt K, Ammann B, Carraro G, Grisa E, Tinner W. Vegetation history of the walnut forests in Kyrgyzstan (Central Asia): natural or anthropogenic origin?. Quat Sci Rev, 2008, 27(5–6): 621-632.

[7]

Beerli P. Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics, 2006, 22(3): 341-345.

[8]

Bernard A, Barreneche T, Lheureux F, Dirlewanger E. Analysis of genetic diversity and structure in a worldwide walnut (Juglans regia L.) germplasm using SSR markers. PLoS One, 2018 13 11

[9]

Breton C, Pinatel C, Médail F, Bonhomme F, Bervillé A. Comparison between classical and Bayesian methods to investigate the history of olive cultivars using SSR-polymorphisms. Plant Sci, 2008, 175(4): 524-532.

[10]

Cheng F, Peng X, Zhao P, Yuan J, Zhong C, Cheng Y, Cui C, Zhang S. Soil microbial biomass, basal respiration and enzyme activity of main forest types in the Qinling Mountains. PLoS One, 2013 8 6

[11]

Coart E, Van Glabeke S, De Loose M, Larsen AS, RoldánRuiz I. Chloroplast diversity in the genus Malus: new insights into the relationship between the European wild apple (Malus sylvestris (L.) Mill.) and the domesticated apple (Malus domestica Borkh.). Mol Ecol, 2006, 15(8): 2171-2182.

[12]

Cornille A, Gladieux P, Smulder MJ, Roldán-Ruiz I, Laurens F, Le Cam B, Nersesyan A, Clavel J, Olonova M, Feugey L, Gabrielyan I, Zhang X, Tenaillon ML, Giraud T. New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties. PLoS Genet, 2012 8 5

[13]

Cornille A, Giraud T, Bellard C, Tellier A, Cam BL, Smulders MJM, Kleinschmit J, Roldan-Ruiz I, Gladieux P. Post-glacial recolonization history of the European crabapple (Malus sylvestris Mill.), a wild contributor to the cultivated apple. Mol Ecol, 2013, 22(8): 2249-2263.

[14]

Dang M, Yue M, Zhang M, Zhao G, Zhao P. Gene introgression among closely related species in sympatric populations: a case study of three walnut (Juglans) species. Forests, 2019 10 11 965

[15]

Dangl GS, Woeste K, Aradhya MK, Koehmstedt A, Simon C, Potter D, Leslie CA, McGranahan G. Characterization of 14 microsatellite markers for genetic analysis and cultivar identification of walnut. J Am Soc Hortic Sci, 2005 130 3 348e354

[16]

Davies SJ, Cavers S, Finegan B, White A, Breed MF, Lowe AJ. Pollen flow in fragmented landscapes maintains genetic diversity following stand-replacing disturbance in a neotropical pioneer tree, Vochysia ferruginea Mart. J Hered, 2015, 115(2): 125-129.

[17]

De Andrés MT, Benito A, Pérez-Rivera G, Ocete R, Lopez MA, Gaforio L, MuozUÑOZ G, Cabello F, Martínez-Zapter JM, Arroyo-García R. Genetic diversity of wild grapevine populations in Spain and their genetic relationships with cultivated grapevines. Mol Ecol, 2012, 21(4): 800-816.

[18]

Delplancke M, Alvarez N, Espíndola A, Joly H, Benoit L, Brouck E, Arrigo N. Gene flow among wild and cultivated almond species: insights from chloroplast and nuclear markers. Evol Appl, 2012, 5(4): 317-329.

[19]

Delplancke M, Alvarez N, Benoit L, Espíndola AI, Joly H, Neuenschwander S, Arrigo N. Evolutionary history of almond tree domestication in the Mediterranean basin. Mol Ecol, 2013, 22(4): 1092-1104.

[20]

Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull, 1987, 19: 11-15.

[21]

Earl DA, Vonholdt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour, 2012, 4(2): 359-361.

[22]

ESRI. ArcGIS version 10.0, 2010, Redlands: Environmental Systems Research Institute.

[23]

Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol, 2005, 14(8): 2611-2620.

[24]

Excoffier L, Lischer HEL. Arlequin suite version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour, 2010, 10(3): 564-567.

[25]

Felber F, Kozlowski G, Arrigo N, Guadagnuolo R. Genetic and ecological consequences of transgene flow to the wild flora. Adv Biochem Eng Biotechnol, 2007, 107(1): 173-205.

[26]

Feng X, Zhou H, Zulfiqar S, Luo X, Hu Y, Feng L, Malvolti ME, Woeste K, Zhao P. The phytogeographic history of common walnut in China. Front Plant Sci, 2018, 9: 1399.

[27]

Gepts P, Papa P. Possible effects to (trans) gene flow from crops on the genetic diversity from landraces and wild relatives. Environ Biosaf Res, 2003, 2(2): 89-103.

[28]

Goodnight KF, Queller DC. Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol, 1999, 8(7): 1231-1234.

[29]

Gunn BF, Aradhya M, Salick JM, Miller AJ, Yang Y, Lin L, Xian H. Genetic variation in walnuts (Juglans regia and J. sigillata; Juglandaceae): species distinctions, human impacts, and the conservation of agrobiodiversity in Yunan, China. Am J Bot, 2010, 97(4): 660-671.

[30]

Guo Y, Li G, Hu Y, Kang D, Wang D, Yang G. Regeneration of Betula albosinensis in strip clearcut and uncut forests of the Qinling Mountains in China. PLoS One, 2013 8 3

[31]

Härdling R, Bergsten J. Nonrandom mating preserves intrasexual polymorphism and stops population differentiation in sexual conflict. Am Nat, 2006, 167: 401-409.

[32]

Hardy OJ, Vekemans X. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes, 2002, 2(4): 618-620.

[33]

Jolivet C, Höltken AM, Liesebach H, Steiner W, Degen B. Mating patterns and pollen dispersal in four contrasting wild cherry populations (Prunus avium L.). Eur J For Res, 2012, 131(4): 1055-1069.

[34]

Jones ME, Shepherd M, Henry R, Delves A. Pollen flow in Eucalyptus grandis determined by paternity analysis using microsatellite markers. Tree Genet Genomes, 2008, 4(1): 37-47.

[35]

Kalinowski ST, Taper ML, Marshall TC. Revising How the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol, 2007, 16(5): 1099-1006.

[36]

Kery M, Matthies D, Schmid B. Demographic stochasticity in population fragments of the declining distylous perennial Primula veris (Primulaceae). Basic Appl Ecol, 2003, 4(3): 197-206.

[37]

Kimura MK, Goto S, Suyama Y, Matsui M, Woeste K, Seiwa K. Morph-specific mating patterns in a low-density population of a heterodichogamous tree, Juglans ailantifolia. Plant Ecol, 2012, 213(9): 1477-1487.

[38]

Manning WE. The classification within the Juglandaceae. Ann Mo Bot Gard, 1978, 65(4): 1058-1087.

[39]

Matsuoka Y, Yamazaki Y, Ogihara Y, Tsunewaki K. Whole chloroplast genome comparison of rice, maize, and wheat: implications for chloroplast gene diversification and phylogeny of cereals. Mol Evol, 2002, 19(12): 2084-2091.

[40]

McGranahan G, Leslie C (2009) Breeding Walnuts (Juglans Regia). In: Jain SM, Priyadarshan PM (eds) Breeding plantation tree crops: temperate species. Springer Sciencet Business Media, LLC, pp 268–270

[41]

McGranahan GH, Hansen J, Shaw DV. Inter- and intraspecific variation in California black walnuts. J Am Soc Hortic Sci, 1988, 83(5): 210-215.

[42]

Miller AJ, Gross BL. From forest to field: perennial fruit crop domestication. Am J Bot, 2011, 98(9): 1389-1414.

[43]

Myles S, Boyko AR, Owens CL, Brown PJ, Grassi F, Aradhya MK, Prins B, Reynolds A, Chia J, Ware D, Bustamante CD, Buckler ES. Genetic structure and domestication history of the grape. Proc Natl Acad Sci USA, 2011, 108(9): 3530-3535.

[44]

Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics, 2012, 28(19): 2537-2539.

[45]

Pollegioni P, Woeste KE, Chiocchini F, Del Lungo S, Olimpieri I, Tortolano V, Clark J, Hemery GE, Mapelli S, Malvolti ME. Ancient humans influenced the current spatial genetic structure of common walnut populations in Asia. PLoS One, 2015 10 9

[46]

Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics, 2000, 155(2): 945-959.

[47]

Raymond M, Rousset F. GENEPOP (Version 1.22): population genetics software for exact tests and ecumenicism. J Hered, 1995, 86(3): 248-249.

[48]

Rogers R. Temperate ecosystems, Juglandaceae, 2004, Amsterdam, Holland: Elsevier Ltd 1427 1430

[49]

Rosenberg NA. DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes, 2004, 4(1): 137-138.

[50]

Ross-Davis A, Huang Z, Mckenna J, Ostry M, Woeste K. Morphological and molecular methods to identify butternut (Juglans cinerea) and butternut hybrids: relevance to butternut conservation. Tree Physiol, 2008, 28(7): 1127-1133.

[51]

Sánchez-de León Y, Johnson-Maynard J. Dominance of an invasive earthworm in native and non-native grassland ecosystems. Biol Invasions, 2009, 11(6): 1393-1401.

[52]

Sun Y, Hou N, Woeste K, Zhang C, Yue M, Yuan X, Zhao P. Population genetic structure and adaptive differentiation of iron walnut Juglans regia subsp. sigillata in southwestern China. Ecol Evol, 2019, 9: 14154-14166.

[53]

Trucco F, Tatum T, Rayburn AL, Tranel PJ. Out of the swamp: unidirectional hybridization with weedy species may explain the prevalence of Amaranthus tuberculatus as a weed. New Phytol, 2009, 184(4): 819-827.

[54]

Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Resour, 2004, 4(3): 535-538.

[55]

Victory ER, Glaubitz JC, Rhodes OE, Woeste KE. Genetic Homogeneity in Juglans nigra (Juglandaceae) at nuclear microsatellites. Am J Bot, 2006, 93(1): 118-126.

[56]

Woeste K, Burns R, Rhodes O, Michler C. Thirty polymorphic nuclear microsatellite loci from black walnut. J Hered, 2002, 93(1): 58-60.

[57]

Wolf DE, Takebayashi N, Riesberg LH. Predicting the risk of extinction through hybridization. Conserv Biol, 2001, 15(4): 1039-1053.

[58]

Yeh FC, Boyle TB. Population genetic analysis of codominant and dominant markers and quantitative traits. Belg J Bot, 1996, 129: 157.

[59]

Yuan X, Sun Y, Bai X, Dang M, Feng X, Zulfiqar S, Zhao P. Population structure, genetic diversity, and gene introgression of two closely related walnuts (Juglans regia and J. sigillata) in southwestern China revealed by EST-SSR markers. Forests, 2018 9 10 646

[60]

Zhao P, Woeste K. DNA markers identify hybrids between butternut (Juglans cinerea L.), and Japanese walnut (Juglans ailantifolia Carr.). Tree Genet Genomes, 2011, 7(3): 511-533.

[61]

Zhao P, Zhou HJ, Potter D, Hu YH, Feng XJ, Dang M, Feng L, Zulfiqar S, Liu WZ, Zhao GF, Woeste K. Population genetics, phylogenomics and hybrid speciation of Juglans in China determined from whole chloroplast genomes, transcriptomes, and genotyping-by-sequencing (GBS). Mol Phylogenet Evol, 2018, 126: 250-265.

AI Summary AI Mindmap
PDF

129

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/