Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual reproduction

Nature Genetics

Volumn 49, Issue 5, 2017, Pages 765-772

  Wang, Xia ^a   Xu, Yuantao ^a   Zhang, Siqi ^a   Cao, Li ^b   Huang, Yue ^a   Cheng, Junfeng ^a   Wu, Guizhi ^a   Tian, Shilin ^c   Chen, Chunli ^a   Liu, Yan ^a   Yu, Huiwen ^a   Yang, Xiaoming ^a   Lan, Hong ^a   Wang, Nan ^a   Wang, Lun ^a   Xu, Jidi ^a   Jiang, Xiaolin ^a   Xie, Zongzhou ^a   Tan, Meilian ^a   Larkin, Robert M ^a   Chen, Ling Ling ^a   Ma, Bin Guang ^a   Ruan, Yijun ^a,d   Deng, Xiuxin ^a   Xu, Qiang ^a   more..

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b SOUTHWEST UNIVERSITY   (China)

^c SICHUAN AGRICULTURAL UNIVERSITY   (China)

^d JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOMIXIS; ARTICLE; CITRUS; CONTROLLED STUDY; CULTIVATED SPECIES; GENE INSERTION; GENE LOCUS; GENE SEQUENCE; GENOME ANALYSIS; NONHUMAN; OVULE; PLANT GENETICS; PLANT GENOME; PRIORITY JOURNAL; PROMOTER REGION; TRANSPOSON; WILD PLANT; ASEXUAL REPRODUCTION; CHROMOSOMAL MAPPING; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETIC VARIATION; GENETICS; GENOMICS; PHYLOGENY; PLANT CHROMOSOME; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENCE;

APOMIXIS; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; CITRUS; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE ONTOLOGY; GENETIC VARIATION; GENOME, PLANT; GENOMICS; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCTION, ASEXUAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

EID: 85017198613     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3839     Document Type: Article

References (61)

1. Meyer, R.S., DuVal, A.E. & Jensen, H.R. Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. New Phytol. 196, 29-48 (2012).
2. Conner, J.A., Mookkan, M., Huo, H., Chae, K. & Ozias-Akins, P. A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant. Proc. Natl. Acad. Sci. USA 112, 11205-11210 (2015).
3. Koltunow, A.M. Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5, 1425-1437 (1993).
4. Batygina, T.B. & Vinogradova, G.Y. Phenomenon of polyembryony. Genetic heterogeneity of seeds. Russ. J. Dev. Biol. 38, 126-151 (2007).
5. Spillane, C., Curtis, M.D. & Grossniklaus, U. Apomixis technology development-virgin births in farmers' fields? Nat. Biotechnol. 22, 687-691 (2004).
6. Bicknell, R.A. & Koltunow, A.M. Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16 (Suppl. 1), S228-S245 (2004).
7. Kepiro, J.L. & Roose, M.L. AFLP markers closely linked to a major gene essential for nucellar embryony (apomixis) in Citrus maxima × Poncirus trifoliata. Tree Genet. Genomes 6, 1-11 (2010).
8. Ueno, I., Iwamasa, M. & Nishiura, M. Embryo number of various varieties of Citrus and its relatives. Bull. Hort. Res. Sta. Japan 7, 11-22 (1967).
9. Iwamasa, M., Ueno, I. & Nishiura, M. Inheritance of nucellar embryony in citrus. Bull. Hort. Res. Sta. Japan 7, 1-8 (1967).
10. 1 hybrids and advanced crosses of Citrus with Poncirus. J. Am. Soc. Hortic. Sci. 104, 408-410 (1979).
11. Raga, V., Bernet, G.P., Carbonell, E.A. & Asins, M.J. Segregation and linkage analyses in two complex populations derived from the citrus rootstock Cleopatra mandarin. Inheritance of seed reproductive traits. Tree Genet. Genomes 8, 1061-1071 (2012).
12. Nakano, M. et al. Characterization of genomic sequence showing strong association with polyembryony among diverse Citrus species and cultivars, and its synteny with Vitis and Populus. Plant Sci. 183, 131-142 (2012).
13. Nakano, M. et al. Characterization of genes associated with polyembryony and in vitro somatic embryogenesis in Citrus. Tree Genet. Genomes 9, 795-803 (2013).
14. Kumar, V., Malik, S.K., Pal, D., Srinivasan, R. & Bhat, S.R. Comparative transcriptome analysis of ovules reveals stress related genes associated with nucellar polyembryony in citrus. Tree Genet. Genomes 10, 449-464 (2014).
15. Long, J.M. et al. Genome-scale mRNA and small RNA transcriptomic insights into initiation of citrus apomixis. J. Exp. Bot. 67, 5743-5756 (2016).
16. Swingle, W.T. & Reece, P.C. The botany of Citrus and its wild relatives. in The Citrus Industry (University of California Press, 1967).
17. Medina-Filho, H.P., Bordignon, R. & Ballvé, R.M.L. Sunkifolias and Buxisunkis: sexually obtained reciprocal hybrids of Citrus sunki × Severinia buxifolia. Genet. Mol. Biol. 21, 129-133 (1998).
18. Xu, Q. et al. The draft genome of sweet orange (Citrus sinensis). Nat. Genet. 45, 59-66 (2013).
19. Wu, G.A. et al. Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat. Biotechnol. 32, 656-662 (2014).
20. Luo, R. et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18 (2012).
21. Ashikari, M. et al. Cytokinin oxidase regulates rice grain production. Science 309, 741-745 (2005).
22. Schmutz, J. et al. A reference genome for common bean and genome-wide analysis of dual domestications. Nat. Genet. 46, 707-713 (2014).
23. Qi, J. et al. A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat. Genet. 45, 1510-1515 (2013).
24. Kieffer, M., Master, V., Waites, R. & Davies, B. TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J. 68, 147-158 (2011).
25. Greb, T. et al. Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev. 17, 1175-1187 (2003).
26. Zhao, Y. et al. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291, 306-309 (2001).
27. van der Graaff, E., Laux, T. & Rensing, S.A. The WUS homeobox-containing (WOX) protein family. Genome Biol. 10, 248 (2009).
28. Lin, T. et al. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 46, 1220-1226 (2014).
29. Wolf, J.B.W. & Ellegren, H. Making sense of genomic islands of differentiation in light of speciation. Nat. Rev. Genet. 18, 87-100 (2017).
30. Schomburg, F.M., Patton, D.A., Meinke, D.W. & Amasino, R.M. FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13, 1427-1436 (2001).
31. Köszegi, D. et al. Members of the RKD transcription factor family induce an egg cell-like gene expression program. Plant J. 67, 280-291 (2011).
32. Pagnussat, G.C. et al. Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132, 603-614 (2005).
33. Dreni, L. & Zhang, D. Flower development: the evolutionary history and functions of the AGL6 subfamily MADS-box genes. J. Exp. Bot. 67, 1625-1638 (2016).
34. Gifford, M.L., Dean, S. & Ingram, G.C. The Arabidopsis ACR4 gene plays a role in cell layer organisation during ovule integument and sepal margin development. Development 130, 4249-4258 (2003).
35. Miller, A.J. & Gross, B.L. From forest to field: perennial fruit crop domestication. Am. J. Bot. 98, 1389-1414 (2011).
36. Jeong, S., Palmer, T.M. & Lukowitz, W. The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signaling. Curr. Biol. 21, 1268-1276 (2011).
37. Waki, T., Hiki, T., Watanabe, R., Hashimoto, T. & Nakajima, K. The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr. Biol. 21, 1277-1281 (2011).
38. Schmidt, A. et al. Apomictic and sexual germline development differ with respect to cell cycle, transcriptional, hormonal and epigenetic regulation. PLoS Genet. 10, e1004476 (2014).
39. Pasternak, T.P. et al. The role of auxin, pH, and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa. Plant Physiol. 129, 1807-1819 (2002).
40. Okada, T. et al. Enlarging cells initiating apomixis in Hieracium praealtum transition to an embryo sac program prior to entering mitosis. Plant Physiol. 163, 216-231 (2013).
41. Shi, M., Guo, X., Chen, Y., Zhou, L. & Zhang, D. Isolation and characterization of 19 polymorphic microsatellite loci for Atalantia buxifolia (Rutaceae), a traditional medicinal plant. Conserv. Genet. Resour. 6, 857-859 (2014).
42. Chin, C.S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563-569 (2013).
43. Kelley, D.R., Schatz, M.C. & Salzberg, S.L. Quake: quality-aware detection and correction of sequencing errors. Genome Biol. 11, R116 (2010).
44. Boetzer, M., Henkel, C.V., Jansen, H.J., Butler, D. & Pirovano, W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27, 578-579 (2011).
45. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313 (2014).
46. Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).
47. Du, Z., Zhou, X., Ling, Y., Zhang, Z. & Su, Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64-W70 (2010).
48. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).
49. Li, L., Stoeckert, C.J. Jr. & Roos, D.S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189 (2003).
50. Simillion, C., Janssens, K., Sterck, L. & Van de Peer, Y. i-ADHoRe 2.0: an improved tool to detect degenerated genomic homology using genomic profiles. Bioinformatics 24, 127-128 (2008).
51. Finn, R.D., Clements, J. & Eddy, S.R. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39, W29-W37 (2011).
52. Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007).
53. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
54. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
55. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011).
56. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156-2158 (2011).
57. Otto, T.D., Sanders, M., Berriman, M. & Newbold, C. Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 26, 1704-1707 (2010).
58. Larkin, M.A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).
59. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
60. Trapnell, C. et al. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010).
61. -ΔΔCT method. Methods 25, 402-408 (2001).