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http://dx.doi.org/10.5010/JPB.2015.42.4.326

Current status and prospects of citrus genomics  

Kim, Ho Bang (Life Sciences Research Institute, Biomedic Co., Ltd.)
Lim, Sanghyun (Life Sciences Research Institute, Biomedic Co., Ltd.)
Kim, Jae Joon (Life Sciences Research Institute, Biomedic Co., Ltd.)
Park, Young Cheol (Agricultural Research and Extension Services, Jeju Special Self-Governing Province)
Yun, Su-Hyun (Citrus Research Institute, National Institute of Horticultural & Herbal Science)
Song, Kwan Jeong (Faculty of Bioscience and Industry, SARI, Jeju National University)
Publication Information
Journal of Plant Biotechnology / v.42, no.4, 2015 , pp. 326-335 More about this Journal
Abstract
Citrus is an economically important fruit tree with the largest amount of fruit production in the world. It provides important nutrition such as vitamin C and other health-promoting compounds including its unique flavonoids for human health. However, it is classified into the most difficult crops to develop new cultivars through conventional breeding approaches due to its long juvenility and some unique reproductive biological features such as gamete sterility, nucellar embryony, and high level of heterozygosity. Due to global warming and changes in consumer trends, establishing a systematic and efficient breeding programs is highly required for sustainable production of high quality fruits and diversification of cultivars. Recently, reference genome sequences of sweet orange and clementine mandarin have been released. Based on the reference whole-genome sequences, comparative genomics, reference-guided resequencing, and genotyping-by-sequencing for various citrus cultivars and crosses could be performed for the advance of functional genomics and development of traits-related molecular markers. In addition, a full understanding of gene function and gene co-expression networks can be provided through combined analysis of various transcriptome data. Analytic information on whole-genome and transcriptome will provide massive data on polymorphic molecular markers such as SNP, INDEL, and SSR, suggesting that it is possible to construct integrated maps and high-density genetic maps as well as physical maps. In the near future, integrated maps will be useful for map-based precise cloning of genes that are specific to citrus with major agronomic traits to facilitate rapid and efficient marker-assisted selection.
Keywords
Citrus; Genome; Transcriptome; Molecular Markers; Genetic Map; Molecular Breeding;
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1 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 (2012) A reference genetic map of Citrus clementina hort. ex Tan.; citrus evolution inferences from comparative mapping. BMC Genomics 13:593   DOI
2 Orhan IE, Nabavi SF, Daglia M, Tenore GC, Mansouri K, Nabavi SM (2015) Naringenin and atherosclerosis: a review of literature. Curr Pharm Biotechnol 16:245-251   DOI
3 Park JW, Lee HY, Riu KZ, Yun SH, Kim JH, Boo KH, Jin SB, Bachchu MAA, Kim YW, Lee DS (2010) Expression profiling of cultivar-related genes in satsuma mandarins, Miyagawa Wase and Ueno Wase. J. Kor Soc Appl Biol Chem 53:691-701   DOI
4 Park JW, Jin SB, Boo KH, Chung SJ, Yun SH, Bachchu MAA, Yun JH, Han SI, Riu KZ, Kim JH (2012) Comparative analysis among four citrus species by DNA microarray. Kor J Breed Sci 44:229-237
5 Redwan RM, Saidin A, Kumar SV (2015) Complete chloroplast genome sequence of MD-2 pineapple and its comparative analysis among nine other plants from the subclass Commelinidae. BMC Plant Biol 15:196   DOI
6 Sahin-Cevik M, Moore GA (2012) Quantitative trait loci analysis of morphological traits in Citrus. Plant Biotechol Rep 6:47-57   DOI
7 Shalom L, Samuels S, Zur N, Shlizerman L, Doron-Faigenboim A, Blumwald E, Sadka A (2014) Fruit load induces changes in global gene expression and in abscisic acid (ABA) and indole acetic acid (IAA) homeostasis in citrus buds. J Exp Bot 65:3029-3044   DOI
8 Shi Q, Febres VJ, Jones JB, Moore GA (2014) Responsiveness of different citrus genotypes to the Xanthomonas citri ssp. citri-derived pathogen-associated molecular pattern (PAMP) flg22 correlates with resistance to citrus canker. Mol Plant Pathol 16:507-520
9 Stringari D, Glienke C, de Christo D, Maccheroni W, de Azevedo JL (2009) High molecular diversity of the fungus Guignardia citricarpa and Guignardia mangiferae and new primers for the diagnosis of the citrus black spot. Brazilian Archiv Biol Technol 52:1063-1073   DOI
10 Sugiyama A, Ikoma Y, Fujii H, Shimada T, Endo T, Shimizu T, Omura M (2010) Structure and expression levels of alleles of Citrus zeaxanthin epoxidase genes. J Japan Soc Hort Sci 79:263-274   DOI
11 Su HJ, Hogenhout SA, Al-Sadi AM, Kuo CH (2014) Complete chloroplast genome sequence of Omani lime (Citrus aurantiifolia) and comapartive analysis within the Rosids. PloS One 9:e113049   DOI
12 Suh SJ, Lee SH, Lee DH, Kim IJ (2013) Transcriptome analysis of a spontaneous reddish mutant in Miyagawa Wase satsuma mandarin. J Korean Soc Appl Biol Chem 56:391-399   DOI
13 Talon M, Gmitter Jr FG (2008) Citrus genomics. Inter J Plant Genomics Article ID 528361
14 Terol J, Tadeo F, Ventimilla D, Talon M (2015) An RNA-Seq-based reference transcriptome for citrus. Plant Biotechnol J doi: 10.1111/pbi.12447.[Epub ahead of print]   DOI
15 The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815   DOI
16 Torres AM, Mau-Lastovicka T, Williams TE, Soost RK (1985) Segregation distortion and linkage of Citrus and Poncirus isozyme genes. J Hered (1985) 76:289-294   DOI
17 Weber CA, Moore GA, Deng Z, Gmitter FG (2003) Mapping freeze tolerance quantitative trait loci in a Citrus grandis x Poncirus trifoliata F-1 pseudo-testcross using molecular markers. J Amer Soc Hort Sci 128:508-514
18 Tozlu I, Guy CL, Moore GA (1999) QTL analysis of $Na^+$ and $Cl^-$ accumulation related traits in an intergeneric BC1 progeny of Citrus and Poncirus under saline and nonsaline environments. Genome 42:692-705   DOI
19 Wang J, Chen D, Lei Y, Chang JW, Hao BH, Xing F, Li S, Xu Q, Deng XX, Chen LL (2014) Citrus sinensis annotation project (CAP): a comprehensive database for sweet orange genome. PLoS One 9:e87723   DOI
20 Wang Y, Zhou L, Li D, Dai L, Lawton-Rauh A, Srimani PK, Duan Y, Luo F (2015) Genome-wide comparative analysis reveals similar types of NBS genes in hybrid Citrus sinensis genome and original Citrus clementine genome and provides new insights into non-TIR NBS genes. PLoS One 10:e0121893   DOI
21 Wong DCJ, Sweetman C, Ford CM (2014) Annotation of gene function in citrus using gene expression information and co-expression networks. BMC Plant Biol 14:186   DOI
22 Woo JW, Kim J, Kwon SI, Corvalan C, Cho SW, Kim H, Kim SG, Kim ST, Choe S, Kim JS (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol 33:1162-1164   DOI
23 Wu GA et al (2013) Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotech 32:656-662
24 Wu J, Xu Z, Zhang Y, Chai L, Yi H, Deng X (2014) An integrative analysis of the transcriptome and proteome of the pulp of a spontaneous late-ripening sweet orange mutant and its wild type improves our understanding of fruit ripening in citrus. J Exp Bot 65:1651-1671   DOI
25 Yang CQ, Liu YZ, An JC, Li S, Jin LF, Zhou GF, Wei QJ, Yan HQ, Wang NN, Fu LN, Liu X, Hu XM, Yan TS, Peng SA (2013) Digital gene expression analysis of corky split vein caused by boron deficiency in 'Newhall' navel orange (Citrus sinensis Osbeck) for selecting differentially expressed genes related to vascular hypertrophy. PLoS One 8(6):e65737   DOI
26 Xiao JP, Chen LG, Xie M, Liu HL, Ye WQ (2009) Identification of AFLP fragments linked to seedlessness in Ponkan mandarin (Citrus reticulata Blanco) and conversion to SCAR markers. Sci Hortic 121:505-510   DOI
27 Xie R, Pang S, Ma Y, Deng L, He S, Yi S, Lv Q, Zheng Y (2015) The ARF, AUX/IAA and GH3 gene families in citrus: genome-wide identification and expression analysis during fruitlet drop from abscission zone A. Mol Genet Genomics 290:2089-2105   DOI
28 Xu Q et al. (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59-66   DOI
29 Yang ZN, Ye XR, Choi S, Molina J, Moonan F, Wing RA, Roose ML, Mirkov TE (2001) Construction of a 1.2-Mb contig including the citrus tristeza virus resistance gene locus using a bacterial artificial chromosome library of Poncirus trifoliata (L.) Raf. Genome 44:382-93   DOI
30 Yildiz E, Kaplankiran M, Demirkeser TH, Uzun A, Toplu C (2013) Identification of zygotic and nucellar individuals produced from several citrus crosses using SSRs markers. Not Bot Horti Agrobo 41:478-484   DOI
31 Yu K, Xu Q, Da X, Guo F, Ding Y, Deng X (2012) Transcriptome changes during fruit development and ripening of sweet orange (Citrus sinensis). BMC Genomics 13:10   DOI
32 Zhang JZ, Zhao K, Ai XY, Hu CG (2014) Involvements of PCD and changes in gene expression profile during self-pruning of spring shoots in sweet orange (Citrus sinensis). BMC Genomics 15:892   DOI
33 Fang DQ, Roose ML (1999) A novel gene conferring citrus tristeza virus resistance in Citrus maxima (Burm.) Merrill. Hortsci 34:334-335
34 Zhong Y, Cheng CZ, Jiang NH, Jiang B, Zhang YY, Wu B, Hu MI, Zeng JW, Yan HX, Yi GJ, Zhong GY (2015) Comparative transcriptome and iTRAQ proteome analyses of citrus root responses to Candidatus Liberibacter asiaticus infection. PLoS One 10:e0126973   DOI
35 Deng Z, Tao Q, Chang YL, Huang S, Ling P, Yu C, Chen C, Gmitter Jr FG, Zhang HB (2001) Construction of a bacterial artificial chromosome (BAC) library for citrus and identification of BAC contigs containing resistance gene candidates. Theor Appl Genet 102:1177-1184   DOI
36 Donmez D, Sismek O, Izgu T, Kacar YA, Mendi YY (2013) Genetic transformation in Citrus. Scientific World J 2013:491207
37 Du D, Rawat N, Deng Z, Gmitter Jr FG (2015) Construction of citrus gene coexpression networks from microarray data using random matrix theory. Hortic Res 2:15026   DOI
38 Fang DQ, Federici CT, Roose ML (1997) Development of molecular markers linked to a gene controlling fruit acidity in citrus. Genome 40:841-849   DOI
39 Food and Agricultural Organization (FAO) (2014) FAOSTAT. http://www.fao.org/
40 Gaj T, Gersbach CA, Barbas CF (2013) ZFN, TALEN, and CRISPR/Casbased methods for genome engineering. Trends Biotechnol 31:397-405   DOI
41 Garcia R, Asins MJ, Forner J, Carbonell EA (1999) Genetic analysis of apomixis in Citrus and Poncirus by molecular markers. Theor Appl Genet 99:511-518   DOI
42 Garcia MR, Asins MJ, Carbonell EA (2000) QTL analysis of yield and seed number in Citrus. Theor Appl Genet 101:487-493   DOI
43 Gmitter FG, Xiao SY, Huang S, Hu XL, Garnsey SM, Deng Z (1996) A localized linkage map of the citrus tristeza virus resistance gene region. Theor Appl Genet 92:688-695   DOI
44 Gulsen O, Uzun A, Seday U, Kafa G (2011) QTL analysis and regression model for estimating fruit setting in young citrus trees based on molecular markers. Sci Hortic 130:418-424   DOI
45 Gmitter Jr FG, Chen C, Machado MA, de Souza AA, Ollitrault P, Froehlicher Y, Shimizu T (2012) Citrus genomics. Tree Genet Genomes 8:611-626   DOI
46 Goff et al., (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92-100   DOI
47 Gulsen O, Uzun A, Canan I, Seday U, Canihos E (2010) A new citrus linkage map based on SRAP, SSR, ISSR, POGP, RGA and RAPD markers. Euphytica 173:265-277   DOI
48 Guo F, Yu H, Xu Q, Deng X (2015) Transcriptomic analysis of differentially expressed genes in an orange-pericarp mutant and wild type in pummelo (Citrus grandis) BMC Plant Biol 15:44   DOI
49 Han SH, Ahn HJ, Kang SG, Kim HY (2005) Expression of green fluorescent protein gene in the callus of satsuma mandarin (Citrus unshiu cv. Miyagawa Wase) by Agrobacterium-mediated transformation. Hort Environ Biotechnol 46:39-42
50 Hershkovotz V, Sela N, Taha-Salaime L, Liu J, Rafael G, Kessler C, Aly R, Levy M, Wisniewski M, Droby S (2013) De-novo assembly and characterization of the transcriptome of Metschnikowia fructicola reveals differences in gene expression following interaction with Penicillium digitatum and grapefruit peel. BMC Genomics 14:168   DOI
51 Hou XJ, Li SB, Liu SR, Hu CG, Zhang JZ (2014) Genome-wide classification and evolutionary and expression analyses of citrus MYB transcription factor families in sweet orange. PLoS One 9:e112375   DOI
52 Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One 9:e93806   DOI
53 Hu XM, Shi CY, Liu X, Jin LF, Liu YZ, Peng SA (2015) Genome-wide identification of citrus ATP-citrate lyase genes and their transcript analysis in fruits reveals their possible role in citrate utilization. Mol Genet Genomics 290:29-38   DOI
54 Iranshahi M, Rezaee R, Parhiz H, Roohbakhsh A, Soltani F (2015) Protective effects of flavonoids against microbes and toxins: The cases of hesperidin and hesperetin. Life Sci 137:125-32   DOI
55 Islam MZ, Hu XM, Jin LF, Liu YZ, Peng SA (2014) Genome-wide identification and expression profile analysis of citrus sucrose synthase genes: investigation of possible roles in the regulation of sugar accumulation. PLoS One 9:e113623   DOI
56 Jiao WB, Huang D, Xing F, Hu Y, Deng XX, Xu Q, Chen LL (2013) Genome-wide characterization and expression analysis of genetic variants in sweet orange. Plant J 75:954-964   DOI
57 Jin SB, Yun SH, Park JH, Park SM, Koh SW, Lee DH (2015) Early identification of citrus zygotic seedlings using pollen-specific molecular markers. Korean J Hort Sci Biotechnol 33:598-604
58 Kang SK, Yun SH, Lee DH (2008) Development a SCAR marker linked to polyembryonic trait in citrus. Korean J Hort Sci Tech 26:51-55
59 Kato M, Matsumoto H, Ikoma Y, Kuniga T, Nakajima N, Yoshida T, Yano M (2007) Accumulation of carotenoids and expression of carotenoid biosynthetic genes and carotenoid cleavage dioxygenase genes during fruit maturation in the juice sacs of 'Tamami', 'Kiyomi' tangor, and 'Wilking' mandarin. J Japan Soc Hort Sci 76:103-111   DOI
60 Kim JH, Handayani E, Wakana A, Sakai K, Sato M, Han JH (2013) Segregation of self-incompatible hybrid seedlings in crosses with grapefruit and possible RAPD markers for the S gene alleles. J Faculty Agric Kyushu Univ 58:269-275
61 Lee M, Park J, Lee H, Sohn SH, Lee J (2015) Complete chloroplast genomic sequence of Citrus platymamma determined by combined analysis of Sanger and NGS data. Hort Environ Biotechnol 56:704-711   DOI
62 Liang M, Yang X, Li H, Su S, Yi H, Chai L, Deng X (2015) De novo transcriptome assembly of pummelo and molecular marker development. PLoS One 10(3):e0120615   DOI
63 Ling P, Duncan LW, Deng Z, Dunn D, Hu X, Huang S, Gmitter FG (2000) Inheritance of citrus nematode resistance and its linkage with molecular markers. Theor Appl Genet 100:1010-1017   DOI
64 Liu SR, Li WY, Long D, Hu CG, Zhang JZ (2013) Development and characterization of genomic and expressed SSRs in citrus by genome-wide analysis. PLoS One 8:e75149   DOI
65 Longley AE (1925) Polycary, polyspory and polyploidy in Citrus and Citrus relatives. J Wash Acad Sci 15:347-351
66 Martinelli F, Uratsu SL, Albrecht U, Reagan RL, Phu ML, Britton M, Buffalo V, Fass J, Leicht E, Zhao W, Lin D, D'Souza R, Dacis CE, Bowman KD, Dandekar AM (2012) Transcriptome profiling of citrus fruit response to huanglongbing disease. PLos One 7(5):e38039   DOI
67 Meiyanto E, Hermawan A, Anindyajati (2012) Natural products for cancer-targeted therapy: citrus flavonoids as potent chemopreventive agents. Asian Pac J Cancer Prev 13:427-436   DOI
68 Nakano M, Shimizu T, Kuniga T, Nesumi H, Omura M (2008) Mapping and haplotyping of the flanking region of the polyembryony locus in Citrus unshiu Marcow. J Japanese Soc Hort Sci 77:109-114   DOI
69 Mestre PF, Asins MJ, Pina JA, Carbonell EA, Navarro L (1997) Molecular markers flanking citrus tristeza virus resistance gene from Poncirus trifoliata (L) Raf. Theor Appl Genet 94:458-464   DOI
70 Moore GA (2001) Oranges and lemons: clues to the taxonomy of Citrus from molecular markers. Trends Genet 17:536-540   DOI
71 Nakano M, Kigoshi K, Shimizu T, Endo T, Shimada T, Fujii H, Omura M (2013) Characterization of genes associated with polyembryony and in vitro somatic embryogenesis in Citrus. Tree Genet Genomes 9:795-803   DOI
72 Nicolosi E (2007) Origin and taxonomy. In: I Khan, (ed), Citrus genetics, breeding and biotechnology. CAB International, OX, UK, pp 19-43
73 Nicolosi E, Deng ZN, Gentile A, La Malfa S, Continella G, Tribulato E (2000) Citrus phylogeny and genetic origin of important species as investigated by molecular markers. Theor Appl Genet 100:1155-1166   DOI
74 Ngoc LBT, Verniere C, Vital K, Guerin F, Gagnevin L, Brisse S, Ah-You N, Pruvost O (2009) Development of 14 minisatellite markers for the citrus canker bacterium, Xanthomonas citri pv. Citri. Mol Ecol Resources 9:125-127   DOI
75 Ollitrault P, Dambier D, Luro F, Duperray C (1994) Nuclear genome variation in Citrus. Fruits 49:390-393
76 Benavente-Garcia O, Castillo J (2008) Update on uses and properties of citrus flavonoids: new findings in anticancer, cardiovascular, and anti-inflammatory activity. J Agric Food Chem 56:6185-6205   DOI
77 Asins MJ, Fernandez-Ribacoba J, Bernet GP, Gadea J, Cambra M, Gorris MT, Carbonell EA (2012) The position of the major QTL for citrus tristeza virus resistance is conserved among Citrus grandis, C. aurantium and Poncirus trifoliata. Mol Breed 29:575-587   DOI
78 Bachchu MAA, Jin SB, Park JW, Boo KH, Sun HJ, Kim YW, Lee HY, Riu KZ, Kim JH (2011) Functional expression of miraculin, a taste-modifying protein, in transgenic Miyagawa Wase satsuma mandarin (Citrus unshiu Marc.) J Korean Soc Appl Biol Chem 54:24-29
79 Bastianel M, Cristofani-Yaly M, de Oliveira AC, Freitas-Astua J, Garcia AAF, de Resende MDV, Rodrigues V, Machado MA (2009) Quantitative trait loci analysis of citrus leprosis resistance in an interspecific backcross family of (Citrus reticulata Blanco x C. sinensis L. Osbeck) x C. sinensis L. Osb. Euphytica 169:101-111   DOI
80 Biswas MK, Xu Q, Mayer C, Deng X (2014) Genome wide characterization of short tandem repeat markers in sweet orange (Citrus sinensis). PLoS One 9:e104182   DOI
81 Boo KH, Kim DW, Kim S, Jin SB, Kim JH, Lee HY, Riu KZ (2007) Construction and profiling of a cDNA library from young fruit of satsuma mandarin. J Plant Biol 50:403-409   DOI
82 Chen C, Bowman KD, Choi YA, Dang PM, Rao MN, Huang S, Soneji JR, Greg McCollum T, Gmitter Jr FG (2008) EST-SSR genetic maps for Citrus sinensis and Poncirus trifoliata. 4:1-10
83 Carbonell-Caballero J, Alonso R, Ibanez V, Terol J, Talon M, Dopazo J (2015) A phylogenetic analysis of 34 chloroplast genomes elucidates the relationships between wild and domestic species within the genus Citrus. Mol Biol Evol 32:2015-2035   DOI
84 Chavez DJ, Chaparro JX (2011) Identification of markers linked to seedlessness in Citrus kinokuni hort. ex Tanaka and its progeny using bulked segregant analysis. HortSci 46:693-697
85 Chen C, Zhou P, Choi YA, Huang S, Gmitter Jr FG (2006) Mining and characterization microsatellites from citrus ESTs. Theor Appl Genet 112:1248-1257   DOI
86 Chen C, Gmitter Jr FG (2013) Mining of haplotype-based expressed sequence tag single nucleotide polymorphisms in citrus. BMC Genomics 14:746   DOI
87 Cuenca J, Aleza P, Vicent A, Brunel D, Ollitrault P, Navarro L (2013) Genetically based location from triploid populations and gene ontology of a 3.3-mb genome region linked to Alternaria brown spot resistance in citrus reveal clusters of resistance genes. PLoS One 8:e76755   DOI
88 de Paula Santos Martins C, Pedrosa AM, Du D, Goncalves LP, Yu Q, Gmitter Jr FG, Costa MG (2015) Genome-wide characterization and expression analysis of major intrinsic proteins during abiotic and biotic stresses in sweet orange (Citrus sinensis L. Osb.). PLoS One 10:e0138786   DOI
89 Deng ZN, Huang S, Xiao SY, Gmitter FG (1997) Development and characterization of SCAB markers linked to the citrus tristeza virus resistance gene from Poncirus trifoliata. Genome 40:697-704   DOI