Citrus somatic hybrid: an alternative system to study rapid structural and epigenetic reorganization in allotetraploid genomes

Plant Cell, Tissue and Organ Culture

Volumn 119, Issue 3, 2014, Pages 511-522

  Xu, Shi Xiao ^a,c   Cai, Dong Fang ^a   Tan, Feng Quan ^a   Fang, Yan Ni ^a   Xie, Kai Dong ^a   Grosser, Jude W ^b   Guo, Wen Wu ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF FLORIDA   (United States)

^c HENAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Allotetraploid; Citrus; DNA methylation; Epigenetics; Somatic hybrid

Indexed keywords

GENES; METHYLATION; PLANTS (BOTANY); POLYMORPHISM;

ALLOTETRAPLOID; CITRUS; DNA METHYLATION; EPIGENETICS; SOMATIC HYBRIDS;

ALKYLATION;

CITRUS;

EID: 84911811901     PISSN: 01676857     EISSN: 15735044     Source Type: Journal    
DOI: 10.1007/s11240-014-0551-z     Document Type: Article

References (69)

1. Ainouche ML, Baumel A, Salmon A (2004) Spartina anglica C. E. Hubbard: a natural model system for analysing early evolutionary changes that affect allopolyploid genomes. Biol J Linn Soc 82:475–484
2. Ainouche ML, Fortune PM, Salmon A, Parisod C, Grandbastien MA, Fukunaga K, Ricou M, Misset MT (2009) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biol Invasions 11:1159–1173
3. Akhunova AR, Matniyazov RT, Liang HQ, Akhunov ED (2010) Homoeolog-specific transcriptional bias in allopolyploid wheat. BMC Genom 11:505
4. Albertin W, Balliau T, Brabant P, Chevre A, Eber F, Malosse C, Thiellement H (2006) Numerous and rapid nonstochastic modifications of gene products in newly synthesized Brassica napus allotetraploids. Genetics 173:1101–1113
5. Bassene JB, Berti L, Costantino G, Carcouet E, Kamiri M, Tomi F, Dambier D, Ollitrault P, Froelicher Y (2009) Inheritance of characters involved in fruit quality in a citrus interspecific allotetraploid somatic hybrid. J Agric Food Chem 57:5065–5070
6. Bassene JB, Froelicher Y, Dubois C, Ferrer RM, Navarro L, Ollitrault P, Ancillo G (2010) Non-additive gene regulation in a citrus allotetraploid somatic hybrid between C. reticulata Blanco and C. limon (L.) Burm. Heredity 105:299–308
7. Bassene JB, Froelicher Y, Navarro L, Ollitrault P, Ancillo G (2011) Influence of mitochondria on gene expression in a citrus cybrid. Plant Cell Rep 30:1077–1085
8. Beaulieu J, Jean M, Belzile F (2009) The allotetraploid Arabidopsis thaliana-Arabidopsis lyrata subsp petraea as an alternative model system for the study of polyploidy in plants. Mol Genet Genomics 281:421–435
9. Cai XD, Fu J, Deng XX, Guo WW (2007a) Production and molecular characterization of potential seedless cybrid plants between pollen sterile Satsuma mandarin and two seedy Citrus cultivars. Plant Cell Tiss Org Cult 90:275–283
10. Cai YF, Xiang FN, Zhi DY, Liu H, Xia GM (2007b) Genotyping of somatic hybrids between Festuca arundinacea Schreb. and Triticum aestivum L. Plant Cell Rep 26:1809–1819
11. Chague V, Just J, Mestiri I, Balzergue S, Tanguy AM, Huneau C, Huteau V, Belcram H, Coriton O, Jahier J, Chalhoub B (2010) Genome-wide gene expression changes in genetically stable synthetic and natural wheat allohexaploids. New Phytol 187:1181–1194
12. Chaudhary B, Flagel L, Stupar RM, Udall JA, Verma N, Springer NM, Wendel JF (2009) Reciprocal silencing, transcriptional bias and functional divergence of homeologs in polyploid cotton (Gossypium). Genetics 182:503–517
13. Cheng YJ, Guo WW, Yi HL, Pang XM, Deng XX (2003) An efficient protocol for genomic DNA extraction from Citrus species. Plant Mol Biol Rep 21:177a–177g
14. Du XY, Zhang QL, Luo ZR (2009) Comparison of four molecular markers for genetic analysis in Diospyros L. (Ebenaceae). Plant Syst Evol 281:171–181
15. Eeckhaut T, Lakshmanan PS, Deryckere D, Van Bockstaele E, Van Huylenbroeck J (2013) Progress in plant protoplast research. Planta 238:991–1003
16. Fang RQ, Li LY, Li JX (2013) Spatial and temporal expression modes of MicroRNAs in an elite rice hybrid and its parental lines. Planta 238:259–269
17. Fu LL, Yang XY, Zhang XL, Wang ZW, Feng CH, Liu CX, Jiang PY, Zhang JL (2009) Regeneration and identification of interspecific asymmetric somatic hybrids obtained by donor–recipient fusion in cotton. Chin Sci Bull 54:3035–3044
18. Fu J, Peng ZJ, Cai XD, Guo WW (2011) Regeneration and molecular characterization of interspecific somatic hybrids between Satsuma mandarin and two seedy sweet oranges for scion improvement. Plant Breed 130:287–290
19. Gaeta RT, Yoo SY, Pires JC, Doerge RW, Chen ZJ, Osborn TC (2009) Analysis of gene expression in resynthesized Brassica napus allopolyploids using Arabidopsis 70mer oligo microarrays. PLoS ONE 4(3):e4760
20. Grosser JW, Gmitter FG Jr (2011) Protoplast fusion for production of tetraploids and triploids: applications for scion and rootstock breeding in citrus. Plant Cell Tiss Org Cult 104:343–357
21. Guo WW, Deng XX (2000) Two interspecific somatic hybrid plants regenerated via protoplast electro-fusion. Chin J Biotechn 16:179–182 (in Chinese with English abstract)
22. Guo WW, Cai XD, Grosser JW (2004a) Somatic cell cybrids and hybrids in plant improvement. In: Daniell H, Chase CD (eds) Molecular biology and biotechnology of plant organelles. Springer, New York, pp 635–659
23. Guo WW, Prasad D, Cheng YJ, Serrano P, Deng XX, Grosser JW (2004b) Targeted cybridization in Citrus: transfer of Satsuma cytoplasm to seedy cultivars for potential seedlessness. Plant Cell Rep 22:752–758
24. Guo WW, Wu RC, Cheng YJ, Deng XX (2008a) Regeneration and molecular characterization of two interspecific somatic hybrids of Citrus for potential rootstock improvement. J Hortic Sci Biotechnol 83:407–410
25. Guo WW, Wu RC, Fan GE, Cheng YJ (2008b) Analysis of mitochondrial genomes in Citrus interspecific somatic hybrids produced by protoplast fusion. Bot Stud 49:295–300
26. Guo WW, Xiao SX, Deng XX (2013) Somatic cybrid production via protoplast fusion for citrus improvement. Sci Hortic 163:20–26
27. He GM, Zhu XP, Elling AA, Chen LB, Wang XF, Guo L, Liang MZ, He H, Zhang HY, Chen FF, Qi YJ, Chen RS, Deng XW (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33
28. Jackson S, Chen ZJ (2010) Genomic and expression plasticity of polyploidy. Curr Opin Plant Biol 13:153–159
29. Jiang JJ, Zhao XX, Tian W, Li TB, Wang YP (2009) Intertribal somatic hybrids between Brassica napus and Camelina sativa with high linolenic acid content. Plant Cell Tiss Org Cult 99:91–95
30. Kanchanaketu T, Sangduen N, Toojinda T, Hongtrakul V (2012) Genetic diversity analysis of Jatropha curcas L. (Euphorbiaceae) based on methylation-sensitive amplification polymorphism. Genet Mol Res 11:944–955
31. Laird PW (2010) Principles and challenges of genome-wide DNA methylation analysis. Nat Rev Genet 11:191–203
32. Lavania UC, Srivastava S, Lavania S, Basu S, Misra NK, Mukai Y (2012) Autopolyploidy differentially influences body size in plants, but facilitates enhanced accumulation of secondary metabolites, causing increased cytosine methylation. Plant J 71:539–549
33. Li XL, Guo WW, Wang B, Li XS, Chen HG, Wei LH, Wang YJ, Wu JS, Long H (2010) Instability of chromosome number and DNA methylation variation induced by hybridization and amphidiploid formation between Raphanus sativus L. and Brassica alboglabra Bailey. BMC Plant Biol 10:207
34. Li A, Hu BQ, Xue ZY, Chen L, Wang WX, Song WQ, Chen CB, Wang CG (2011) DNA Methylation in genomes of several annual herbaceous and woody perennial plants of varying ploidy as detected by MSAP. Plant Mol Biol Rep 29:784–793
35. Li CL, Cheng AX, Wang MQ, Xia GM (2014) Fertile introgression products generated via somatic hybridization between wheat and Thinopyrum intermedium. Plant Cell Rep 33:633–641
36. Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66
37. Liu SW, Xia GM (2014) The place of asymmetric somatic hybridization in wheat breeding. Plant Cell Rep 33:595–603
38. Liu B, Xu CM, Zhao N, Qi B, Kimatu JN, Pang JS, Han FP (2009) Rapid genomic changes in polyploid wheat and related species: implications for genome evolution and genetic improvement. J Genet Genomics 36:519–528
39. Lukens LN, Pires JC, Leon E, Vogelzang R, Oslach L, Osborn T (2006) Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids. Plant Physiol 140:336–348
40. Madlung A (2013) Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110:99–104
41. Nei M, Li W (1979) Mathematical model for study the genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci 74:5267–5273
42. Ochogavia AC, Cervigni G, Selva JP, Echenique VC, Pessino SC (2009) Variation in cytosine methylation patterns during ploidy level conversions in Eragrostis curvula. Plant Mol Biol 70:17–29
43. Osabe K, Kawanabe T, Sasaki T, Ishikawa R, Okazaki K, Dennis ES, Kazama T, Fujimoto R (2012) Multiple mechanisms and challenges for the application of allopolyploidy in plants. Int J Mol Sci 13:8696–8721
44. Rebollo R, Horard B, Hubert B, Vieira C (2010) Jumping genes and epigenetics: towards new species. Gene 454:1–7
45. Rohlf FJ (1997) NTSYS-PC 2.1. Numerical taxonomy and multivariate analysis system. Exeter Software, Setauket
46. Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, Stacey G, Doerge RW, Jackson SA (2013) The fate of duplicated genes in a polyploid plant genome. Plant J 73:143–153
47. Sahu PP, Pandey G, Sharma N, Puranik S, Muthamilarasan M, Prasad M (2013) Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 32:1151–1159
48. Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14:1163–1175
49. Sarilar V, Palacios PM, Rousselet A, Ridel C, Falque M, Eber F, Chevre AM, Joets J, Brabant P, Alix K (2013) Allopolyploidy has a moderate impact on restructuring at three contrasting transposable element insertion sites in resynthesized Brassica napus allotetraploids. New Phytol 198:593–604
50. Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13:1749–1759
51. Shen HS, He H, Li J, Chen W, Wang XC, Guo L, Peng ZY, He GM, Zhong SW, Qi YJ, Terzaghi W, Deng XW (2012) Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24:875–892
52. Sheng XG, Zhao ZQ, Yu HF, Wang JS, Gu HH (2013) Rapid alterations of DNA sequence and cytosine methylation induced by somatic hybridization between Brassica oleracea L. var. italica and Brassica nigra (L.) Koch. Plant Cell Tiss Organ Cult 115:395–405
53. Soriano L, Mourao Filho FDAA, Camargo LEA, Cristofani-Yaly M, Latado RR, de Andrade Pacheco C, de Azevedo FA, Mendes BMJ (2012) Regeneration and characterization of somatic hybrids combining sweet orange and mandarin/mandarin hybrid cultivars for citrus scion improvement. Plant Cell Tiss Org Cult 111:385–392
54. Szadkowski E, Eber F, Huteau V, Lode M, Coriton O, Jenczewski E, Chevre AM (2011) Polyploid formation pathways have an impact on genetic rearrangements in resynthesized Brassica napus. New Phytol 191:884–894
55. Tarwacka J, Polkowska-Kowalczyk L, Kolano B, Sliwka J, Wielgat B (2013) Interspecific somatic hybrids Solanum villosum (+) S. tuberosum, resistant to Phytophthora infestans. J Plant Physiol 170:1541–1548
56. Teixeira FK, Colot V (2010) Repeat elements and the Arabidopsis DNA methylation landscape. Heredity 105:14–23
57. Verhoeven KJF, Van Dijk PJ, Biere A (2010) Changes in genomic methylation patterns during the formation of triploid asexual dandelion lineages. Mol Ecol 19:315–324
58. Wang J, Tian L, Lee H, Wei N, Jiang H, Watson B, Madlung A, Osborn T, Doerge R, Comai L (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507–517
59. Wang J, Jiang JJ, Wang YP (2013) Protoplast fusion for crop improvement and breeding in China. Plant Cell Tiss Org Cult 112:131–142
60. Xiao SX, Biswas MK, Li MY, Deng XX, Xu Q, Guo WW (2014) Production and molecular characterization of diploid and tetraploid somatic cybrid plants between male sterile Satsuma mandarin and seedy sweet orange cultivars. Plant Cell Tiss Org Cult 116:81–88
61. Xu YH, Zhong L, Wu XM, Fang XP, Wang JB (2009) Rapid alterations of gene expression and cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta 229:471–483
62. Xu SX, Cai XD, Tan B, Li DL, Guo WW (2011) Effect of ploidy increase on transgene expression: example from Citrus diploid cybrid and allotetraploid somatic hybrid expressing the EGFP gene. Protoplasma 248:531–540
63. Xu YH, Xu H, Wu XM, Fang XP, Wang JB (2012) Genetic changes following hybridization and genome doubling in synthetic Brassica napus. Biochem Genet 50:616–624
64. Yang XH, Ye CY, Cheng ZM, Tschaplinski TJ, Wullschleger SD, Yin WL, Xia XL, Tuskan GA (2011) Genomic aspects of research involving polyploid plants. Plant Cell Tiss Org Cult 104:387–397
65. Yu XS, Chu BJ, Liu RE, Sun J, Brian JJ, Wang HZ, Zhu S, Sun YQ (2012) Characteristics of fertile somatic hybrids of G-hirsutum L. and G-trilobum generated via protoplast fusion. Theor Appl Genet 125:1503–1516
66. Zhang XL, Ge XH, Shao YJ, Sun GL, Li ZY (2013) Genomic change, retrotransposon mobilization and extensive cytosine methylation alteration in Brassica napus introgressions from two intertribal hybridizations. PLoS ONE 8(2):e56346
67. Zhao JW, Buchwaldt L, Rimmer SR, Brkic M, Bekkaoui D, Hegedus D (2009) Differential expression of duplicated peroxidase genes in the allotetraploid Brassica napus. Plant Physiol Biochem 47:653–656
68. Zheng BB, Wu XM, Ge XX, Deng XX, Grosser JW, Guo WW (2012) Comparative transcript profiling of a male sterile cybrid pummelo and its fertile type revealed altered gene expression related to flower development. PLoS ONE 7(8):e43758
69. Zheng BB, Xie ZZ, Guo WW (2013) Parental dominant inheritance of fruit carotenoids, sugars and organic acids in a citrus interspecific allotetraploid somatic hybrid between Bonnaza navel orange and rough lemon. Acta Hort Sin 40:1262–1268 (in Chinese with English abstract)