Advertisement

Citrus Genomes: From Sequence Variations to Epigenetic Modifications

  • Qiang XuEmail author
  • Mikeal L. RooseEmail author
Chapter
  • 37 Downloads
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

Genome platform is critical to the basic molecular biological research and to the molecular marker assisted breeding. Genomics data of citrus species have accumulated rapidly after the first publication of sweet orange in 2013. With the cost of sequencing decreased dramatically, each individual research group can afford to sequence many genomes. This chapter summarizes methods for genome assembly and annotation, how we identify genes by comparative genomics, linkage mapping and association analysis, how we apply SNP markers in cultivar identification and breeding, and the current knowledge on epigenetic regulations in Citrus. This chapter also anticipates future genomic researches in Citrus.

Notes

Acknowledgements

The authors are grateful to Dr. Xia Wang, Dr. Yue Huang, and Chunli Chen for contribution and beneficial discussions on the population genomics, genome assembly and cytogenomics. We thank the funding by the National Key Research and Development Program of China (2018YFD1000100), and USDA-NIFA grant 2013-67013-21110

References

  1. Aritua V, Achor D, Gmitter FG, Albrigo G, Wang N (2013) Transcriptional and microscopic analyses of citrus stem and root responses to Candidatus Liberibacter asiaticus infection. PLoS ONE 8(9):e73742PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bairoch A, Apweiler R (2000) The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res 28:45–48PubMedPubMedCentralCrossRefGoogle Scholar
  3. Birney E, Clamp M, Durbin R (2004) GeneWise and genomewise. Genome Res 14:988–995PubMedPubMedCentralCrossRefGoogle Scholar
  4. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W (2011) Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27:578–579PubMedCrossRefPubMedCentralGoogle Scholar
  5. Butelli E et al (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24:1242–1255PubMedPubMedCentralCrossRefGoogle Scholar
  6. Chin CS et al (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563–569PubMedCrossRefPubMedCentralGoogle Scholar
  7. Chuck G, O’Connor D (2010) Small RNAs going the distance during plant development. Curr Opin Plant Biol 13:40–45PubMedCrossRefPubMedCentralGoogle Scholar
  8. Chumsakul O, Nakamua K, Kurata T et al (2013) High-resolution mapping of in vivo genomic transcription factor binding sites using in situ DNase I footprinting and ChIP-seq/ DNA Res. 20:325–338PubMedPubMedCentralGoogle Scholar
  9. Consortium TTG (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641CrossRefGoogle Scholar
  10. Curk F et al (2015) Nuclear species-diagnostic SNP markers mined from 454 amplicon sequencing reveal admixture genomic structure of modern citrus varieties. PLoS ONE 10:e0125628PubMedPubMedCentralCrossRefGoogle Scholar
  11. Curk F, Ollitrault F, Garcia-Lore A, Luro F, Navarro L, Ollitrault P (2016) Phylogenetic origin of limes and lemons revealed by cytoplasmic and nuclear markers. Ann Bot 117:565–583PubMedPubMedCentralCrossRefGoogle Scholar
  12. Daccord N, Celton J-M, Linsmith G et al (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet 49:1099–1106PubMedPubMedCentralCrossRefGoogle Scholar
  13. Danecek P et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158PubMedPubMedCentralCrossRefGoogle Scholar
  14. Dardick C, Callahan A, Horn R, Ruiz KB, Zhebentyayeva T, Hollender C, Whitaker M, Abbott A, Scorza R (2013) PpeTAC1 promotes the horizontal growth of branches in peach trees and is a member of a functionally conserved gene family found in diverse plants species. Plant J. 75:618–630PubMedCrossRefPubMedCentralGoogle Scholar
  15. Delaneau O, Marchini J, Zagury JF (2011) A linear complexity phasing method for thousands of genomes. Nat Methods 9:179–181PubMedCrossRefPubMedCentralGoogle Scholar
  16. D’Hont A, Denoeud F, Aury JM, Baurens FC, Carreel F, Garsmeur O, Noel B, Bocs S, Droc G, Rouard M, Da Silva C, Jabbari K, Cardi C, Poulain J, Souquet M, Labadie K, Jourda C, Lengelle J, Rodier-Goud M, Alberti A, Bernard M, Correa M, Ayyampalayam S, McKain MR, Leebens-Mack J, Burgess D, Freeling M, Mbeguie AMD, Chabannes M, Wicker T, Panaud O, Barbosa J, Hribova E, Heslop-Harrison P, Habas R, Rivallan R, Francois P, Poiron C, Kilian A, Burthia D, Jenny C, Bakry F, Brown S, Guignon V, Kema G, Dita M, Waalwijk C, Joseph S, Dievart A, Jaillon O, Leclercq J, Argout X, Lyons E, Almeida A, Jeridi M, Dolezel J, Roux N, Risterucci AM, Weissenbach J, Ruiz M, Glaszmann JC, Quetier F, Yahiaoui N, Wincker P (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217PubMedPubMedCentralCrossRefGoogle Scholar
  17. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:64–70CrossRefGoogle Scholar
  18. Ellinghaus D, Kurtz S, Willhoeft U (2008) LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinform 9:18CrossRefGoogle Scholar
  19. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP Related Tools. Nat Protoc 2:953–971PubMedCrossRefPubMedCentralGoogle Scholar
  20. Fang J-G, Song C-N, Qian J-L, Zhang X-Y, Shangguan L-F, Yu H-P, Wang X-C (2010) Variation of cytosine methylation in 57 sweet orange cultivars. Acta Physiol Plant 32:1023–1030CrossRefGoogle Scholar
  21. Fernandez L, Torregrosa L, Segura V, Bouquet A, Martinez-Zapater JM (2010) Transposon-induced gene activation as a mechanism generating cluster shape somatic variation in grapevine. Plant J 61:545–557PubMedCrossRefGoogle Scholar
  22. Fujii H, Shimada T, Nonaka K, Kita M, Kuniga T, Endo T, Ikoma Y, Omura M (2013) High-throughput genotyping in citrus accessions using an SNP genotyping array. Tree Genet Genomes 9:145–153CrossRefGoogle Scholar
  23. Gao L, McCarthy EM, Ganko EW, McDonald JF (2004) Evolutionary history of Oryza sativa LTR retrotransposons: a preliminary survey of the rice genome sequences. BMC Genom 5:18CrossRefGoogle Scholar
  24. Garcia D (2008) A miRacle in plant development: role of microRNAs in cell differentiation and patterning. Sem Cell Dev Biol 19:586–595CrossRefGoogle Scholar
  25. Garcia-Lor A et al (2013) 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 111:1–19PubMedCrossRefGoogle Scholar
  26. Garciamas J, Benjak A, Sanseverino W et al (2012) The genome of melon (Cucumis melo L.). Proc Natl Acad Sci USA 109:11872–11877Google Scholar
  27. Ge XX, Chai LJ, Liu Z, Wu XM, Deng XX, Guo WW (2012) Transcriptional profiling of genes involved in embryogenic, non-embryogenic calluses and somatic embryogenesis of Valencia sweet orange by SSH-based microarray. Planta 236:1107–1124PubMedCrossRefGoogle Scholar
  28. Guerra M (1993) Cytogenetics of Rutaceae. V. High chromosomal variability in citrus species revealed by CMA/DAPI staining. Heredity 71:234–241CrossRefGoogle Scholar
  29. Guo S, Zhang J, Sun H et al (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 45:51–58CrossRefGoogle Scholar
  30. Haas BJ et al (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res 31:5654–5666PubMedPubMedCentralCrossRefGoogle Scholar
  31. Han YH, Zhang ZH, Liu JH, Huang SW, Jin WW (2008) Distribution of the tandem repeat sequences and karyotyping in cucumber (Cucumis Sativus L.) by fluorescence in situ hybridization. Cytogenet Genome Res 122:80–88Google Scholar
  32. Hao Y, Deng X (2002) Stress treatments and DNA methylation affected the somatic embryogenesis of citrus callus. Acta Bot Sin 44:673–677Google Scholar
  33. Hao Y, Wen X, Deng X (2004) Genetic and epigenetic evaluations of citrus calluses recovered from slow-growth culture. J Plant Physiol 161:479–484Google Scholar
  34. He G, Elling AA, Deng XW (2011) The epigenome and plant development. Ann Rev Plant Biol 62:411–435CrossRefGoogle Scholar
  35. Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447:418–424PubMedCrossRefPubMedCentralGoogle Scholar
  36. Hong L, Deng X (2005) Analysis of DNA methylation in navel oranges based on MSAP marker. Zhongguo Nongye Kexue 38:2301–2307Google Scholar
  37. Jaillon O et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467PubMedCrossRefPubMedCentralGoogle Scholar
  38. Jiang J, Gill BS, Wang GL, Ronald PC, Ward DC (1995) Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci USA 92:4487–4491PubMedCrossRefGoogle Scholar
  39. Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. In: Matzke MA, Matzke AJM (eds) Plant gene silencing. Springer, Dordrecht, pp 59–68CrossRefGoogle Scholar
  40. Kaity A, Ashmore SE, Drew RA, Dulloo ME (2008) Assessment of genetic and epigenetic changes following cryopreservation in papaya. Plant Cell Rep 27:1529–1539PubMedCrossRefGoogle Scholar
  41. Kalisz S, Purugganan MD (2004) Epialleles via DNA methylation: consequences for plant evolution. Trends Ecol Evol 19:309–314PubMedCrossRefPubMedCentralGoogle Scholar
  42. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30PubMedPubMedCentralCrossRefGoogle Scholar
  43. Kelley DR, Schatz MC, Salzberg Quake SL (2009) Quality-aware detection and correction of sequencing errors. Genome Biol 11:1–13Google Scholar
  44. Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982PubMedCrossRefPubMedCentralGoogle Scholar
  45. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580PubMedCrossRefPubMedCentralGoogle Scholar
  46. Lang P, Zhang C, Ebel RC, Dane F, Dozier WA (2005) Identification of cold acclimated genes in leaves of Citrus unshiu by mRNA differential display. Gene 359:111–118PubMedCrossRefPubMedCentralGoogle Scholar
  47. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359PubMedPubMedCentralCrossRefGoogle Scholar
  48. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760PubMedPubMedCentralCrossRefGoogle Scholar
  49. Li X, Xu M, Korban SS (2002) DNA methylation profiles differ between field- and in vitro-grown leaves of apple. J Plant Physiol 159:1229–1234CrossRefGoogle Scholar
  50. Lim KY (2004) Karyotype and ribosomal gene mapping in Fragaria vesca L. Acta Hort 649:103–106CrossRefGoogle Scholar
  51. Liu B, Davis TM (2011) Conservation and loss of ribosomal RNA gene sites in diploid and polyploid Fragaria (Rosaceae). BMC Plant Biol 11:157PubMedPubMedCentralCrossRefGoogle Scholar
  52. Liu Q, Zhu A, Chai L, Zhou W, Yu K, Ding J, Xu J, Deng X (2009) Transcriptome analysis of a spontaneous mutant in sweet orange [Citrus sinensis (L.) Osbeck] during fruit development. J Exp Bot 60:801–813PubMedPubMedCentralCrossRefGoogle Scholar
  53. Liu Y, Wang G, Wang Z, Yang F, Wu G, Hong N (2012) Identification of differentially expressed genes in response to infection of a mild Citrus tristeza virus isolate in Citrus aurantifolia by suppression subtractive hybridization. Sci Hortic 134:144–149CrossRefGoogle Scholar
  54. Liu Y, Ke L, Wu G, Xu Y, Wu X, Xia R, Deng X, Xu Q (2017) miR3954 is a trigger of phasiRNAs that affects flowering time in citrus. Plant J 92:263–275PubMedCrossRefGoogle Scholar
  55. Lu C, Tej SS, Luo S, Haudenschild CD, Meyers BC, Green PJ (2005) Elucidation of the small RNA component of the transcriptome. Science 309:1567–1569PubMedCrossRefGoogle Scholar
  56. Luo R et al (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:1–6CrossRefGoogle Scholar
  57. Majoros WH, Pertea M, Salzberg SL (2004) TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20:2878–2879CrossRefGoogle Scholar
  58. Marcais G, Kingsford C (2011) A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27:764–770PubMedPubMedCentralCrossRefGoogle Scholar
  59. Martinelli F, Uratsu SL, Albrecht U, Reagan RL, Phu ML et al (2012) Transcriptome profiling of Citrus Fruit Response to Huanglongbing Disease. PLoS ONE 7(5):e38039PubMedPubMedCentralCrossRefGoogle Scholar
  60. Ming R et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996PubMedPubMedCentralCrossRefGoogle Scholar
  61. Moraes AP, Mirkov TE, Guerra M (2008) Mapping the chromosomes of Poncirus trifoliata Raf. by BAC-FISH. Cytogenet Genome Res 121:277–281Google Scholar
  62. Novelli VM, Takita MA, Machado MA (2004) Identification and analysis of single nucleotide polymorphisms (SNPs) in citrus. Euphytica 138:227–237CrossRefGoogle Scholar
  63. Ollitrault P et al (2012a) A reference genetic map of C. clementina hort. ex Tan.; citrus evolution inferences from comparative mapping. BMC Genomics 13:593PubMedPubMedCentralCrossRefGoogle Scholar
  64. Ollitrault P (2012b) SNP mining in C. clementina BAC end sequences; transferability in the Citrus genus (Rutaceae), phylogenetic inferences and perspectives for genetic mapping. BMC Genomics 13:170–170PubMedPubMedCentralCrossRefGoogle Scholar
  65. Otto TD, Sanders M, Berriman M, Newbold C (2010) Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 26:1704–1707PubMedPubMedCentralCrossRefGoogle Scholar
  66. Pasentsis K, Falara V, Pateraki I, Gerasopoulos D, Kanellis AK (2007) Identification and expression profiling of low oxygen regulated genes from Citrus flavedo tissues using RT-PCR differential display. J Exp Bot 58:2203–2216PubMedCrossRefGoogle Scholar
  67. Peng T, Zhu XF, Fan QJ, Sun PP, Liu JH (2012) Identification and characterization of low temperature stress responsive genes in Poncirus trifoliata by suppression subtractive hybridization. Gene 492:220–228PubMedCrossRefGoogle Scholar
  68. Peraza-Echeverria S, Herrera-Valencia VA, Kay A (2001) Detection of DNA methylation changes in micropropagated banana plants using methylation-sensitive amplification polymorphism (MSAP). Plant Sci 161:359–367PubMedCrossRefGoogle Scholar
  69. Price AL, Jones NC, Pevzner PA (2005) De novo identification of repeat families in large genomes. Bioinformatics 21:i351–i358CrossRefGoogle Scholar
  70. Purcell S et al (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575PubMedCrossRefGoogle Scholar
  71. Rho M, Choi JH, Kim S, Lynch M, Tang H De (2007) novo identification of LTR retrotransposons in eukaryotic genomes. BMC Genom 8:90CrossRefGoogle Scholar
  72. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277CrossRefPubMedGoogle Scholar
  73. Schuster M, Fuchs J, Schubert I (1997) Cytogenetics in fruit breeding—localization of ribosomal RNA genes on chromosomes of apple (Malus x domestica Borkh.). Theor Appl Genet 94:322–324CrossRefGoogle Scholar
  74. Selmer KK et al (2009) Genome-wide linkage analysis with clustered SNP markers. J Biomol Screen 14:92–96PubMedCrossRefPubMedCentralGoogle Scholar
  75. Shulaev V et al (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116PubMedPubMedCentralCrossRefGoogle Scholar
  76. Song C, Wang C, Zhang C, Korir NK, Yu H, Ma Z, Fang J (2010) Deep sequencing discovery of novel and conserved microRNAs in trifoliate orange (Citrus trifoliata). BMC Genomics 111:431CrossRefGoogle Scholar
  77. Sun L-M, Ai X-Y, Li W-Y, Guo W-W, Deng X, Hu C-G, Zhang J-Z (2012) Identification and comparative profiling of miRNAs in an early flowering mutant of trifoliate orange and its wild type by genome-wide deep sequencing. PLoS ONE 7(8):e43760PubMedPubMedCentralCrossRefGoogle Scholar
  78. Szinay D et al (2008) High-resolution chromosome mapping of BACs using multi-colour FISH and pooled-BAC FISH as a backbone for sequencing tomato chromosome. Plant J 56:6CrossRefGoogle Scholar
  79. Telias A, Lin-Wang K, Stevenson DE et al (2011) Apple skin patterning is associated with differential expression of MYB10. BMC Plant Biol 11:93PubMedPubMedCentralCrossRefGoogle Scholar
  80. Trapnell C et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515PubMedPubMedCentralCrossRefGoogle Scholar
  81. Valledor L, Hasbun R, Meijon M et al (2007) Involvement of DNA methylation in tree development and micropropagation. Plant Cell, Tissue, Organ Cult 91:75–86Google Scholar
  82. Velasco R et al (2010) The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 42:833–839Google Scholar
  83. Verde I, Abbott AG, Scalabrin S et al (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494PubMedCrossRefPubMedCentralGoogle Scholar
  84. Walling JG, Jiang J (2011) DNA and chromatin fiber-based plant cytogenetics. Plant cytogenetics, pp 121–130. In: Bass H, Birchler J (eds) Plant cytogenetics. Plant genetics and genomics: crops and models, vol 4. Springer, New York, NYGoogle Scholar
  85. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nature Rev Genet 10:56–63CrossRefGoogle Scholar
  86. Wang Z, Meng D, Wang A, Li T, Jiang S, Cong P, Li T (2013) The methylation of the PcMYB10 promoter is associated with green-skinned sport in Max Red Bartlett pear. Plant Physiol 162:885–896PubMedPubMedCentralCrossRefGoogle Scholar
  87. Wang X, Xu Y, Zhang S et al (2017) Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual reproduction. Nat Genet 49:765–772PubMedPubMedCentralCrossRefGoogle Scholar
  88. Wu GA et al (2014) Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol 32:656–662PubMedPubMedCentralCrossRefGoogle Scholar
  89. Wu X-M, Kou S-J, Liu Y-L, Fang Y-N, Xu Q, Guo W-W (2015) Genomewide analysis of small RNAs in non-embryogenic and embryogenic tissues of citrus: microRNA-and siRNA-mediated transcript cleavage involved in somatic embryogenesis. Plant Biotech J 13:383–394CrossRefGoogle Scholar
  90. Xu Q, Yu KQ, Deng XX et al (2009) Comparative transcripts profiling reveals new insight into molecular processes regulating lycopene accumulation in a sweet orange (Citrus sinensis) red-flesh mutant. BMC Genom 10:1–15CrossRefGoogle Scholar
  91. Xu Q, Liu Y, Zhu A, Wu X, Ye J, Yu K, Guo W, Deng X (2010) Discovery and comparative profiling of microRNAs in a sweet orange red-flesh mutant and its wild type. BMC Genom 11:246CrossRefGoogle Scholar
  92. Xu Q et al (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66PubMedPubMedCentralCrossRefGoogle Scholar
  93. Xu J, Xu H, Xu Q, Deng X (2015) Characterization of DNA methylation variations during fruit development and ripening of sweet orange. Plant Mol Biol Rep 33:1–11CrossRefGoogle Scholar
  94. Yao J-L, Dong Y-H, Morris BAM (2001) Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc Nat Acad Sci USA 98:1306–1311PubMedCrossRefGoogle Scholar
  95. Zdobnov EM, Apweiler R (2001) InterProScan–an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848PubMedCrossRefGoogle Scholar
  96. Zenoni S, Ferrarini A, Giacomelli E, Xumerle L, Fasoli M, Malerba G, Bellin D, Pezzotti M, Delledonne M (2010) Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-Seq. Plant Physiol 152:1787–1795PubMedPubMedCentralCrossRefGoogle Scholar
  97. Zhang J-Z, Li Z-M, Liu L, Mei L, Yao J-L, Hu C-G (2008) Identification of early-flower-related ESTs in an early-flowering mutant of trifoliate orange (Poncirus trifoliata) by suppression subtractive hybridization and macroarray analysis. Tree Physiol 28:1449–1457PubMedCrossRefGoogle Scholar
  98. Zhang W, Wai CM, Ming R, Yu Q, Jiang J (2010) Integration of genetic and cytological maps and development of a pachytene chromosome-based karyotype in papaya. Tropical Plant Biol 3:166–170CrossRefGoogle Scholar
  99. Zhang X-N, Li X, Liu J-H (2014) Identification of conserved and novel cold-responsive microRNAs in trifoliate orange (Poncirus trifoliata (L.) Raf.) using high-throughput sequencing. Plant Mol Biol Report 32:328–341CrossRefGoogle Scholar
  100. Zheng and Zhao (2013) Transcriptome comparison and gene coexpression network analysis provide a systems view of citrus response to ‘Candidatus Liberibacter asiaticus’ infection. BMC Genomic 14:27CrossRefGoogle Scholar
  101. Zhong S, Fei Z, Chen Y-R, Zheng Y et al (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotech 31:154–159PubMedCrossRefGoogle Scholar
  102. Zhou RN, Hu ZM (2007) The development of chromosome microdissection and microcloning technique and its applications in genomic research. Curr Genomics 8:67–72PubMedPubMedCentralCrossRefGoogle Scholar
  103. Zhu AD (2012) Citrus genome evolution and transcriptomic studies on postharvest fruits. PhD dissertation, Huazhong Agricultural University, Wuhan (in Chinese)Google Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Key Laboratory of Horticultural Plant Biology (Ministry of Education)Huazhong Agricultural UniversityWuhanChina
  2. 2.Department of Botany and Plant SciencesUniversity of CaliforniaRiversideUSA

Personalised recommendations