Journal of Plant Biotechnology

The Korean Society of Plant Biotechnology (한국식물생명공학회)
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Current status and prospects of citrus genomics

감귤 유전체 연구 동향 및 전망

  • 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)
  • 김호방 ((주)바이오메딕 생명과학연구소) ;
  • 임상현 ((주)바이오메딕 생명과학연구소) ;
  • 김재준 ((주)바이오메딕 생명과학연구소) ;
  • 박영철 (제주특별자치도 농업기술원 감귤육종센터) ;
  • 윤수현 (국립원예특작과학원 감귤연구소) ;
  • 송관정 (제주대학교 생물산업학부 원예환경전공)
  • Received : 2015.12.16
  • Accepted : 2015.12.25
  • Published : 2015.12.31
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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.

감귤은 전 세계적으로 가장 많이 생산되는 주요 과수작물이고 비타민 C와 구연산 및 감귤 고유의 플라보노이드를 비롯한 다양한 기능성 성분으로 인해 건강 기능성 식품 소재로도 각광받고 있다. 그러나 긴 유년기와 배우체 불임, 주심배 발생 및 고도의 유전적 잡종성 등 감귤 특유의 생식생물학적 특성으로 인해 교배를 통한 전통 육종의 품종개발에 있어서는 가장 어려운 작물에 속한다. 지구 온난화, 소비자 욕구 변화 등으로 인해 고품질 감귤의 안정적 생산과 품종 다양화를 위한 체계적 육종 프로그램의 도입이 시급한 실정이다. 감귤에서도 분자 육종 프로그램을 통한 품종 육성을 위해 세계적으로 가장 많이 재배되는 스위트 오렌지와 클레멘타인 만다린에 대한 고품질 표준 유전체 정보가 최근에 확보되었다. 표준유전체 서열을 기반으로 다양한 품종 및 교배집단들에 대한 유전체 해독, 비교유전체 분석, GBS 등을 통해 형질연관 마커 발굴, 유전자 기능 연구 등이 이루어질 것으로 전망된다. 아울러 다양한 전사체 분석이 이루어지고 있으며, 유전자 기능 및 유전자 co-expression 네트워크의 이해를 증진할 수 있을 것이다. 유전체 및 전사체 분석을 통해 확보한 대규모 SNP, InDel 및 SSR의 다형성 분자마커 big data를 이용한 고밀도 연관 및 물리 지도 작성이 이루어지고 있고, 궁극적으로 통합지도 작성이 이루어지게 될 것이다. 이를 통해 가까운 장래에 감귤 특이 주요 농업형질 연관 유전자의 정확도 높은 map-based 클로닝 및 빠르고 효율적인 분자표지 선발육종이 이루어질 것이다.

Keywords

References

  1. 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 https://doi.org/10.1007/s11032-011-9574-x
  2. 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
  3. 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 https://doi.org/10.1007/s10681-009-9950-3
  4. 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 https://doi.org/10.1021/jf8006568
  5. 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 https://doi.org/10.1371/journal.pone.0104182
  6. 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 https://doi.org/10.1007/BF03030675
  7. 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 https://doi.org/10.1093/molbev/msv082
  8. 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
  9. 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 https://doi.org/10.1007/s00122-006-0226-1
  10. 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
  11. Chen C, Gmitter Jr FG (2013) Mining of haplotype-based expressed sequence tag single nucleotide polymorphisms in citrus. BMC Genomics 14:746 https://doi.org/10.1186/1471-2164-14-746
  12. 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 https://doi.org/10.1371/journal.pone.0076755
  13. 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 https://doi.org/10.1371/journal.pone.0138786
  14. 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 https://doi.org/10.1139/g97-792
  15. 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 https://doi.org/10.1007/s001220000527
  16. Donmez D, Sismek O, Izgu T, Kacar YA, Mendi YY (2013) Genetic transformation in Citrus. Scientific World J 2013:491207
  17. 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 https://doi.org/10.1038/hortres.2015.26
  18. Fang DQ, Federici CT, Roose ML (1997) Development of molecular markers linked to a gene controlling fruit acidity in citrus. Genome 40:841-849 https://doi.org/10.1139/g97-809
  19. Fang DQ, Roose ML (1999) A novel gene conferring citrus tristeza virus resistance in Citrus maxima (Burm.) Merrill. Hortsci 34:334-335
  20. Food and Agricultural Organization (FAO) (2014) FAOSTAT. http://www.fao.org/
  21. Gaj T, Gersbach CA, Barbas CF (2013) ZFN, TALEN, and CRISPR/Casbased methods for genome engineering. Trends Biotechnol 31:397-405 https://doi.org/10.1016/j.tibtech.2013.04.004
  22. 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 https://doi.org/10.1007/s001220051264
  23. Garcia MR, Asins MJ, Carbonell EA (2000) QTL analysis of yield and seed number in Citrus. Theor Appl Genet 101:487-493 https://doi.org/10.1007/s001220051507
  24. 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 https://doi.org/10.1007/BF00226090
  25. 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 https://doi.org/10.1007/s11295-012-0499-2
  26. Goff et al., (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92-100 https://doi.org/10.1126/science.1068275
  27. 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 https://doi.org/10.1007/s10681-010-0146-7
  28. 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 https://doi.org/10.1016/j.scienta.2011.07.010
  29. 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 https://doi.org/10.1186/s12870-015-0435-3
  30. 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
  31. 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 https://doi.org/10.1186/1471-2164-14-168
  32. 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 https://doi.org/10.1371/journal.pone.0112375
  33. 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 https://doi.org/10.1007/s00438-014-0897-2
  34. 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 https://doi.org/10.1016/j.lfs.2015.07.014
  35. 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 https://doi.org/10.1371/journal.pone.0113623
  36. Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One 9:e93806 https://doi.org/10.1371/journal.pone.0093806
  37. 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 https://doi.org/10.1111/tpj.12254
  38. 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
  39. 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
  40. 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 https://doi.org/10.2503/jjshs.76.103
  41. 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
  42. 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 https://doi.org/10.1007/s13580-015-0061-x
  43. 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 https://doi.org/10.1371/journal.pone.0120615
  44. 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 https://doi.org/10.1007/s001220051382
  45. 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 https://doi.org/10.1371/journal.pone.0075149
  46. Longley AE (1925) Polycary, polyspory and polyploidy in Citrus and Citrus relatives. J Wash Acad Sci 15:347-351
  47. 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 https://doi.org/10.1371/journal.pone.0038039
  48. 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 https://doi.org/10.7314/APJCP.2012.13.2.427
  49. 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 https://doi.org/10.1007/s001220050437
  50. Moore GA (2001) Oranges and lemons: clues to the taxonomy of Citrus from molecular markers. Trends Genet 17:536-540 https://doi.org/10.1016/S0168-9525(01)02442-8
  51. 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 https://doi.org/10.2503/jjshs1.77.109
  52. 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 https://doi.org/10.1007/s11295-013-0598-8
  53. Nicolosi E (2007) Origin and taxonomy. In: I Khan, (ed), Citrus genetics, breeding and biotechnology. CAB International, OX, UK, pp 19-43
  54. 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 https://doi.org/10.1007/s001220051419
  55. 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 https://doi.org/10.1111/j.1755-0998.2008.02242.x
  56. Ollitrault P, Dambier D, Luro F, Duperray C (1994) Nuclear genome variation in Citrus. Fruits 49:390-393
  57. 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 https://doi.org/10.1186/1471-2164-13-593
  58. 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 https://doi.org/10.2174/1389201015666141202110216
  59. 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 https://doi.org/10.3839/jksabc.2010.105
  60. 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
  61. 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 https://doi.org/10.1186/s12870-015-0587-1
  62. Sahin-Cevik M, Moore GA (2012) Quantitative trait loci analysis of morphological traits in Citrus. Plant Biotechol Rep 6:47-57 https://doi.org/10.1007/s11816-011-0194-z
  63. 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 https://doi.org/10.1093/jxb/eru148
  64. 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
  65. 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 https://doi.org/10.1590/S1516-89132009000500002
  66. 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 https://doi.org/10.2503/jjshs1.79.263
  67. 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 https://doi.org/10.1371/journal.pone.0113049
  68. 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 https://doi.org/10.1007/s13765-013-3085-x
  69. Talon M, Gmitter Jr FG (2008) Citrus genomics. Inter J Plant Genomics Article ID 528361
  70. 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]
  71. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815 https://doi.org/10.1038/35048692
  72. 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 https://doi.org/10.1093/oxfordjournals.jhered.a110094
  73. 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 https://doi.org/10.1139/gen-42-4-692
  74. 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 https://doi.org/10.1371/journal.pone.0087723
  75. 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 https://doi.org/10.1371/journal.pone.0121893
  76. 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
  77. 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 https://doi.org/10.1186/1471-2229-14-186
  78. 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 https://doi.org/10.1038/nbt.3389
  79. 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
  80. 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 https://doi.org/10.1093/jxb/eru044
  81. 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 https://doi.org/10.1016/j.scienta.2009.03.006
  82. 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 https://doi.org/10.1007/s00438-015-1063-1
  83. Xu Q et al. (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59-66 https://doi.org/10.1038/ng.2472
  84. 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 https://doi.org/10.1371/journal.pone.0065737
  85. 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 https://doi.org/10.1139/gen-44-3-382
  86. 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 https://doi.org/10.15835/nbha4129037
  87. 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 https://doi.org/10.1186/1471-2164-13-10
  88. 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 https://doi.org/10.1186/1471-2164-15-892
  89. 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 https://doi.org/10.1371/journal.pone.0126973

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