Next generation haplotyping to decipher nuclear genomic interspecific admixture in Citrus species: analysis of chromosome 2

BMC Genetics

Patrick Ollitrault³  Luis Navarro²  Jean-Pierre Jacquemoud-Collet³  Xavier Perrier³  François Luro¹  Andres Garcia-Lor²  Gema Ancillo²  Franck Curk² 

[1] UMR AGAP, Institut National de la Recherche Agronomique (Inra), Centre Inra de Corse, San Giuliano, F-20230, France;Centro de Protección Vegetal y Biotecnología, Instituto Valenciano de Investigaciones Agrarias (IVIA), Moncada, 46113, Valencia, Spain;UMR AGAP, Centre de coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), TA A-108/02, Montpellier, 34398, Cedex 5, France

关键词: Genome admixture;    NGS;    SNP;    Evolution;    Haplotype;    Phylogeny;   

Others  :  1121345
DOI  :  10.1186/s12863-014-0152-1

 received in 2014-08-21, accepted in 2014-12-11,  发布年份 2014

【 摘 要 】

Background

The most economically important Citrus species originated by natural interspecific hybridization between four ancestral taxa (Citrus reticulata, Citrus maxima, Citrus medica, and Citrus micrantha) and from limited subsequent interspecific recombination as a result of apomixis and vegetative propagation. Such reticulate evolution coupled with vegetative propagation results in mosaic genomes with large chromosome fragments from the basic taxa in frequent interspecific heterozygosity. Modern breeding of these species is hampered by their complex heterozygous genomic structures that determine species phenotype and are broken by sexual hybridisation. Nevertheless, a large amount of diversity is present in the citrus gene pool, and breeding to allow inclusion of desirable traits is of paramount importance. However, the efficient mobilization of citrus biodiversity in innovative breeding schemes requires previous understanding of Citrus origins and genomic structures. Haplotyping of multiple gene fragments along the whole genome is a powerful approach to reveal the admixture genomic structure of current species and to resolve the evolutionary history of the gene pools. In this study, the efficiency of parallel sequencing with 454 methodology to decipher the hybrid structure of modern citrus species was assessed by analysis of 16 gene fragments on chromosome 2.

Results

454 amplicon libraries were established using the Fluidigm array system for 48 genotypes and 16 gene fragments from chromosome 2. Haplotypes were established from the reads of each accession and phylogenetic analyses were performed using the haplotypic data for each gene fragment. The length of 454 reads and the level of differentiation between the ancestral taxa of modern citrus allowed efficient haplotype phylogenetic assignations for 12 of the 16 gene fragments. The analysis of the mixed genomic structure of modern species and cultivars (i) revealed C. maxima introgressions in modern mandarins, (ii) was consistent with previous hypotheses regarding the origin of secondary species, and (iii) provided a new picture of the evolution of chromosome 2.

Conclusions

454 sequencing was an efficient strategy to establish haplotypes with significant phylogenetic assignations in Citrus, providing a new picture of the mixed structure on chromosome 2 in 48 citrus genotypes.

【 授权许可】

   
2014 Curk et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]FAO: FAOSTAThttp://faostat3.fao.org/home/E. 2014,
• [2]Ollitrault P, Navarro L: Citrus. In Fruit Breeding. Edited by Badenes M, Byrne D. Springer New York, London; 2012:623-662.
• [3]Wang N, Trivedi P: Citrus Huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology 2013, 103(7):652-665.
• [4]Grosser JW, Dutt M, Omar A, Orbovic V, Barthe G: Progress towards the development of transgenic disease resistance in citrus. Acta Hort (ISHS) 2011, 892(101):107.
• [5]Texeira DC, Ayres J, Kitajima EW, Danet L, Jagoueix-Eveillard S, Saillard C, Bové JM: First Report of a Huanglongbing-Like Disease of Citrus in Sao Paulo State, Brazil and Association of a New Liberibacter Species, “Candidatus Liberibacter americanus”, with the Disease. Plant Dis 2005, 89(1):107.
• [6]Grosser JW, Deng XX, Goodrich RM: Somaclonal variation in sweet orange: practical applications for variety improvement and possible causes. In Citrus genetics, breeding and biotechnology. Edited by Kham IA. Wallingford: CAB International; 2007:219–233.
• [7]Krueger RR, Navarro L: Citrus germplasm resources. In Citrus Genetics, Breeding and Biotechnology. CAB International, Anonymous Wallingford, UK; 2007:45-140.
• [8]Scora RW: On the history and origin of Citrus. Bull Torrey Bot Club 1975, 102:369-375.
• [9]Swingle WT, Reece PC: The botany of Citrus and its wild relatives. In The citrus industry. Volume 1. 2nd edition. Edited by Reuther W, Webber HJ, Batchelor LD. University of California Press, Berkeley, California, USA; 1967:190-430.
• [10]Tanaka T: Citologia: Semi-centennial Commemoration Papers on Citrus Studies. Citologia Supporting Foundation, Osaka; 1961.
• [11]Mabberley DJ: A classification for edible Citrus (Rutaceae). Telopea 1997, 7(2):167-172.
• [12]Federici CT, Fang DQ, Scora RW, Roose ML: Phylogenetic relationships within the genus Citrus (Rutaceae) and related genera as revealed by RFLP and RAPD analysis. Theor Appl Genet 1998, 96(6/7):812-822.
• [13]Nicolosi E, Deng ZN, Gentile A, La Malfa S, Continella G, Tribulato E: Citrus phylogeny and genetic origin of important species as investigated by molecular markers. Theor Appl Genet 2000, 100:1155-1166.
• [14]Barkley NA, Roose ML, Krueger RR, Federici CT: Assessing genetic diversity and population structure in a citrus germplasm collection utilizing simple sequence repeat markers (SSRs). Theor Appl Genet 2006, 112(8):1519-1531.
• [15]Garcia-Lor A, Luro F, Navarro L, Ollitrault P: Comparative use of InDel and SSR markers in deciphering the interspecific structure of cultivated citrus genetic diversity: a perspective for genetic association studies. Mol Genet Genomics 2012, 287(1):77-94.
• [16]Garcia-Lor A, Curk F, Snoussi-Trifa H, Morillon R, Ancillo G, Luro F, Navarro L, Ollitrault P: A nuclear phylogenetic analysis: SNPs, indels and SSRs deliver new insights into the relationships in the ‘true citrus fruit trees’ group (Citrinae, Rutaceae) and the origin of cultivated species. Ann Bot 2013, 111(1):1-19.
• [17]Ollitrault P, Terol J, Chen C, Federici CT, Lotfy S, Hippolyte I, Ollitrault F, Berard A, Chauveau A, Cuenca J, Costantino G, Kacar Y, Mu L, Garcia-Lor A, Froelicher Y, Aleza P, Boland A, Billot C, Navarro L, Luro F, Roose ML, Gmitter FG, Talon M, Brunel D: A reference genetic map of C. clementina hort. ex Tan.; citrus evolution inferences from comparative mapping. BMC Genomics 2012, 13:593-2164-13-593.
• [18]Ollitrault P, Terol J, Garcia-Lor A, Berard A, Chauveau A, Froelicher Y, Belzile C, Morillon R, Navarro L, Brunel D, Talon M: SNP mining in C. clementina BAC end sequences; transferability in the Citrus genus (Rutaceae), phylogenetic inferences and perspectives for genetic mapping. BMC Genomics 2012, 13:13-2164-13-13.
• [19]Webber HJ, Reuther W, Lawton HW, et al.: istory and development of the Citrus industry. In The Citrus Industry. Edited by Reuther W. University of California, Division of Agricultural Sciences, Berkeley; 1967:1-39.
• [20]Barrett HC, Rhodes AM: A numerical taxonomic study ofaffinity relationships in cultivated Citrus and its close relatives. Syst Bot 1976, 1:105-136.
• [21]Ollitrault P, Jacquemond C, Dubois C, Luro F: Citrus. In Genetic diversity of cultivated tropical plants. Edited by Hamon P, Seguin M, Perrier X, Glaszmann J-C. Cirad, Montpellier; 2003:193-217.
• [22]Luro F, Gatto J, Costantino G, Pailly O: Analysis of genetic diversity in Citrus. Plant Genetic Resources 2011, 9:218-221.
• [23]Fanciullino AL, Dhuique-Mayer C, Luro F, Casanova J, Morillon R, Ollitrault P: Carotenoid diversity in cultivated citrus is highly influenced by genetic factors. J Agric Food Chem 2006, 54(12):4397-4406.
• [24]Stebbins G: Variation and evolution in plants: Columbia University Press ed. Columbia University Press, New York; 1950.
• [25]Grant V: Plant Speciation: 2nd Edit. ed. Colombia University Press, New York; 1981.
• [26]Arnold ML: Natural hybridization and evolution. Oxford University Press, New York; 1997.
• [27]Doolittle WF: Phylogenetic Classification and the Universal Tree. Science 1999, 284(5423):2124-2129.
• [28]Otto SP, Whitton J: Polyploid incidence and evolution. Annu Rev Genet 2000, 34:401-437.
• [29]Linder CR, Rieseberg LH: Reconstructing patterns of reticulate evolution in plants. Am J Bot 2004, 91:1700-1708.
• [30]Pamilo P, Nei M: Relationships between gene trees and species trees. Mol Biol Evol 1988, 5:568-583.
• [31]Rieseberg LH, Soltis DE: Phylogenetic consequences of cytoplasmic gene flow in plants. Trends in Plants 1991, 5:65-84.
• [32]Beiko RG, Hamilton N: Phylogenetic identification of lateral genetic transfer events. BMC Evol Biol 2006, 6:15. BioMed Central Full Text
• [33]Rieseberg LH, Sinervo B, Linder CR, Ungerer MC, Arias DM: Role of gene interactions in hybrid speciation: evidence from ancient and experimental hybrids. SCIENCE-NEW YORK THEN WASHINGTON- 1996, 272:741–744.
• [34]Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, Durphy JL, Schwarzbach AE, Donovan LA, Lexer C: Major ecological transitions in annual sunflowers facilitated by hybridization. Science 2003, 301:1211-1216.
• [35]Rousseau-Gueutin M, Gaston A, Aïnouche A, Aïnouche ML, Olbricht K, Staudt G, Richard L, Denoyes-Rothan B: Tracking the evolutionary history of polyploidy in Fragaria L. (strawberry): new insights from phylogenetic analyses of low-copy nuclear genes. Mol Phylogenet Evol 2009, 51(3):515-530.
• [36]Fortune P, Pourtau N, Viron N, Ainouche M: Molecular phylogeny and reticulate origins of the polyploid Bromus species from section Genea (Poaceae). Am J Bot 2008, 95(4):454-464.
• [37]Ramadugu C, Pfeil BE, Keremane ML, Lee RF, Maureira-Butler IJ, Roose ML: A six nuclear gene phylogeny of Citrus (Rutaceae) taking into account hybridization and lineage sorting. PLoS One 2013, 8(7):e68410.
• [38]Maddison WP, Knowles LL: Inferring phylogeny despite incomplete lineage sorting. Syst Biol 2006, 55(1):21-30.
• [39]Jumpponen A, Jones KL: Massively parallel 454-sequencing of Quercus macrocarpa phyllosphere fungal communities indicates reduced richness and diversity in urban environments. New Phytol 2009, 184:438-448.
• [40]Sønstebø JH, Gielly L, Brysting AK, Elven R, Edwards M, Haile J, Willersleve E, Coissac E, Rioux D, Sannier J, Taberlet P, Brochmann C: Using next-generation sequencing for molecular reconstruction of past Arctic vegetation and climate. Mol Ecol Resour 2010, 10(6):1009-1018.
• [41]Taudien S, Groth M, Huse K, Petzold A, Szafranski K, Hampe J, Rosenstiel P, Schreiber S, Platzer M: Haplotyping and copy number estimation of the highly polymorphic human beta-defensin locus on 8p23 by 454 amplicon sequencing. BMC Genomics 2010, 11(1):252. BioMed Central Full Text
• [42]Xu Q, Chen L, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao W, Hao B, Lyon PM, Chen J, Gao S, Xing F, Lan H, Chang J, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas KM, Zeng W, Guo F, Cao H, Yang X, Xu X, Cheng Y, Xu J, Liu J, et al.: The draft genome of sweet orange (Citrus sinensis). Nat Genet 2013, 45:59-66.
• [43]Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U, Murat F, Perrier X, Ruiz M, Scalabrin S, Terol J, Takita MA, Labadie K, Poulain J, Couloux A, Jabbari K, Cattonaro F, Del Fabbro C, Pinosio S, Zuccolo A, Chapman J, Grimwood J, Tadeo FR, Estornell LH, Munoz-Sanz JV, Ibanez V, Herrero-Ortega A, Aleza P, Perez-Perez J, Ramon D, Brunel D, et al.: Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol 2014, 32(7):656-662.
• [44]Okou DT, Steinberg KM, Middle C, Cutler DJ, Albert TJ, Zwick ME: Microarray-based genomic selection for high-throughput resequencing. Nat Methods 2007, 4(11):907-909.
• [45]Bybee SM, Bracken-Grissom H, Haynes BD, Hermansen RA, Byers RL, Clement MJ, Udall JA, Wilcox ER, Crandall KA: Targeted amplicon sequencing (TAS): a scalable next-gen approach to multilocus, multitaxa phylogenetics. Genome Biol Evol 2011, 3:1312-1323.
• [46]Department of Energy’s Joint Genome Institute, Center for Integrative Genomics: Phytozome;http://www.phytozome.net/. 2014.
• [47]Fluidigm Corp.: Access Array TM System;http://www.fluidigm.com/access-array-system.html; 2014.
• [48]Curk, F.;Ancillo, G.;Garcia-Lor, A.;Luro, F.;Navarro, L.;Ollitrault, P.; Multilocus SNPs analysis allows phylogenetic assignation of DNA fragments to decipher the interspecific mosaic genome structure of cultivated citrus; Plant Genome Evolution 2011 , 4–6 Sep 2011, P2.1572 [http://f1000.com/posters/browse/summary/1089299]
• [49]Life Sciences Corp.: Using Multiplex Identifier (MID) Adaptors for the GS FLX Titanium Chemistry - Extended Mid Set Technical Bulletin Genome Sequencer FLX System 2009, 005:1-7.
• [50]Life Sciences Corp.: Amplicon Fusion Primer Design Guidelines for GS FLX Titanium Series Lib-A Chemistry Technical Bulletin Genome Sequencer FLX System 2009, 013:1-3.
• [51]PRINSEQ: PReprocessing and INformation of SEQuence data: Easy and rapid quality control and data preprocessing;http://prinseq.sourceforge.net/index.html. 2012.
• [52]Life Sciences Corp.: 454 Sequencing System Software Manual, v 2.5.3; Part C – GS De Novo Assembler, GS Reference Mapper, SFF Tools. 454 Sequencing System Software Manual 2010:2–213.
• [53]DNASTAR Inc.: DNASTAR Sofware for life Scientists;http://www.dnastar.com/t-nextgen-seqman-ngen.aspx. 2014.
• [54]Wright S: Variability Within and Among Natural Populations. In Evolution and the Genetics of Populations. Volume 4. The University of Chicago Press, Anonymous Chicago, IL; 1978.
• [55]Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F: GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations.Laboratoire Génome, Populations, Interactions, CNRS UMR 5000 1996–2004, (Université de Montpellier II, Montpellier (France).).
• [56]Dereeper A, Nicolas S, Lecunff L, Bacilieri R, Doligez A, Peros JP, Ruiz M, This P: SNiPlay: a web-based tool for detection, management and analysis of SNPs. Application to grapevine diversity projects. BMC Bioinformatics 2011, 12(1):134. BioMed Central Full Text
• [57]Dereeper A, Nicolas S, Lecunff L, Bacilieri R, Doligez A, Peros JP, Ruiz M, This P: http://sniplay.cirad.fr/cgi-bin/home.cgi. 2013, 2014.
• [58]Perrier X, Jacquemoud-Collet JP: DARwin software. 2006, (http://darwin.cirad.fr/).
• [59]Tamura K, Stecher G, Peterson D, Filipski A, Kumar S: MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 2013, 30(12):2725-2729.
• [60]Van Berloo R: GGT 2.0: versatile software for visualization and analysis of genetic data. J Hered 2008, 99(2):232-236.
• [61]Pritchard Lab SU: Structure Software;http://pritchardlab.stanford.edu/structure.html 2014.
• [62]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155(2):945-959.
• [63]Falush D, Stephens M, Pritchard JK: Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 2003, 164(4):1567-1587.
• [64]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.
• [65]Herrero R, Asins MJ, Pina JA, Carbonell EA, Navarro L: Genetic diversity in the orange subfamily Aurantioideae. II. Genetic relationships among genera and species. Theor Appl Genet 1996, 93(8):1327-1334.
• [66]Froelicher Y, Mouhaya W, Bassene JB, Costantino G, Kamiri M, Luro F, Morillon R, Ollitrault P: New universal mitochondrial PCR markers reveal new information on maternal citrus phylogeny. Tree Genetics and Genomes 2011, 7(1):49-61.
• [67]Uzun A, Yesiloglu T, Polat I, Aka-Kacar Y, Gulsen O, Yildirim B, Tuzcu O, Tepe S, Canan I, Anil S: Evaluation of Genetic Diversity in Lemons and Some of Their Relatives Based on SRAP and SSR Markers. Plant Mol Biol Report 2011, 29(3):693-701.
• [68]Uzun A, Yesiloglu T, Aka-Kacar Y, Tuzcu O, Gulsen O: Genetic diversity and relationships within Citrus and related genera based on sequence related amplified polymorphism markers (SRAPs). Sci Hortic 2009, 121(3):306-312.
• [69]Bayer RJ, Mabberley DJ, Morton C, Miller CH, Sharma IK, Pfeil BE, Rich S, Hitchcock R, Sykes S: A molecular phylogeny of the orange subfamily(Rutaceae: Aurantioideae) using nine cpDNA sequences. Am J Bot 2009, 96(3):668-685.
• [70]Roose ML, Federici CT, Mu L, Kwok K, Vu C: Map-based ancestry of sweet orange and other citrus variety groups. Gentile A, Tribulato E eds Second International Citrus Biotechnology Symposium, 28 Tremestieri Etneo. Emme Erre Grafica, Italy; 2009.
• [71]Ollitrault F, Terol J, Pina JA, Navarro L, Talon M, Ollitrault P: Development of SSR markers from Citrus clementina (Rutaceae) BAC end sequences and interspecific transferability in Citrus. Am J Bot 2010, 97(11):e124-e129.
• [72]Webber HJ: Cultivated varieties of citrus. The Citrus Industry. History, World Distribution, Botany andVarieties 1943, 475-668.
• [73]de Moraes A, dos Santos Soares Filho W, Guerra M: Karyotype diversity and the origin of grapefruit. Chromosome Research 2007, 15(1):115–121.
• [74]Scora RW, Kumamoto J, Soost RK, Nauer EM: Contribution to the origin of the grapefruit Citrus paradisi (Rutaceae). Syst Bot 1982, 7:170-177.
• [75]Gallesio G: Traité du citrus: Louis Fantin ed. Chez Louis Fantin Libraire, Paris; 1811.
• [76]Chen LG, Omura M, Hidaka T: A study on the taxonomy of citrus with GOT isozymes. Acta Horticulturae Sinica 1991, 18(1):27-32.
• [77]Federici CT, Roose ML, Scora RW: RFLP analysis of the origin of Citrus bergamia, Citrus jambhiri, and Citrus limonia. Acta Horticult 2000, 535:55-62.
• [78]Li X, Xie R, Lu Z, Zhou Z: The origin of cultivated citrus as inferred from internal transcribed spacer and chloroplast DNA sequence and amplified fragment length polymorphism fingerprints. J Am Soc Hortic Sci 2010, 135(4):341-350.