An evolutionary view of plant tissue culture: Somaclonal variation and selection

Plant Cell Reports

Volumn 31, Issue 9, 2012, Pages 1535-1547

  Wang, Qin Mei ^a   Wang, Li ^a  

^a NORTHEAST NORMAL UNIVERSITY   (China)

Author keywords

Dedifferentiation bottleneck; Differentiation bottleneck; Evolution; Plant tissue culture; Selection; Somaclonal variation

Indexed keywords

BIOLOGICAL MODEL; EVOLUTION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; METHODOLOGY; PLANT; REVIEW; TISSUE CULTURE TECHNIQUE;

BIOLOGICAL EVOLUTION; GENETIC VARIATION; MODELS, BIOLOGICAL; PLANTS; SELECTION, GENETIC; TISSUE CULTURE TECHNIQUES;

EID: 84865616665     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-012-1281-5     Document Type: Review

References (131)

1. Alatzas A, Foundouli A (2006) Distribution of ubiquitinated histone H2A during plant cell differentiation in maize root and dedifferentiation in callus culture. Plant Sci 171: 481-487.
2. Al-Zahim MA, Ford-Lloyd BV, Newbury HJ (1999) Detection of somaclonal variation in garlic (Allium sativum L.) using RAPD and cytological analysis. Plant Cell Rep 18(6): 473-477.
3. Atwood KC, Schneider LK, Ryan FJ (1951) Periodic selection in Escherichia coli. Proc Natl Acad Sci USA 37: 146-155.
4. Bender J (2004) Chromatin-based silencing mechanisms. Curr Opin Plant Biol 7: 521-526.
5. Bennett AF, Lenski RE (1993) Evolutionary adaptation to temperature. II. Thermal niches of experimental lines of Escherichia coli. Evolution 47: 1-12.
6. 1. Genome 30: 318-325.
7. Berdasco M, Alcázar R, García-Ortiz MV et al (2008) Promoter DNA hypermethylation and gene repression in undifferentiated Arabidopsis cells. PLoS ONE 3: e3306.
8. Borsani O, Zhu J, Verslueshttp PE, Sunkar R, Zhu J-K (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123: 1279-1291.
9. Bottley A, Chapman NH, Koebner RMD (2008) Homoeologous gene silencing in tissue cultured wheat callus. BMC Genet 9: 65.
10. Bouman H, De Klerk GJ (2001) Measurement of the extent of somaclonal variation in begonia plants regenerated under various conditions. Comparison of three assays. Theor Appl Genet 102: 111-117.
11. Cao X, Jacobsen SE (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12: 1136-1144.
12. Chakrabarty D, Yu KW, Paek KY (2003) Detection of DNA methylation changes during somatic embryogenesis of Siberian ginseng (Eleuterococcus senticosus). Plant Sci 165: 61-68.
13. Chen F-Q, Fu Y, Wang D-L, Gao X, Wang L (2007) The effect of plant growth regulators and sucrose on the micropropagation and microtuberization of Dioscorea nipponica. Makino. J Plant Growth Regul 26: 38-45.
14. Chen S, Chai M, Jia Y, Gao Z, Zhang L, Gu M (2011) In vitro selection of salt tolerant variants following 60Co gamma irradiation of long-term callus cultures of Zoysia matrella [L.] Merr. Plant Cell Tissue Org Cult. doi: 10. 1007/s11240-011-9999-2.
15. Cooper LA, Scott TW (2001) Differential evolution of eastern equine encephalitis virus populations in response to host cell type. Genetics 157: 1403-1412.
16. Cooper VS, Lenski RE (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736-739.
17. Cooper VS (2002) Long-term experimental evolution in Escherichia coli. X. Quantifying the fundamental and realized niche. BMC Evol Biol 2: 12.
18. Costa S, Shaw P (2006) 'Open minded' cells: how cells can change fate. Trends Cell Biol 3: 101-106.
19. Côte FX, Teisson C, Perrier X (2001) Somaclonal variation rate evolution in plant tissue culture: contribution to understanding through a statistical approach. In Vitro Cell Dev Plant 37: 539-542.
20. Crill WD, Wichman HA, Bull JJ (2000) Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154: 27-37.
21. de Visser JA, Elena SF (2007) The evolution of sex: empirical insights into the roles of epistasis and drift. Nat Rev Genet 8: 139-149.
22. Dennis ES, Brettell RIS, Peacock WJ (1987) A tissue culture induced Adh1 mutant of maize results from a single base change. Mol Genet Genomics 210: 181-183.
23. Devarumath R, Nandy S, Rani V, Marimuthu S, Muraleedharan N, Raina S (2002) RAPD, ISSR and RFLP fingerprints as useful markers to evaluate genetic integrity of micropropagated plants of three diploid and triploid elite tea clones representing Camellia sinensis (China type) and C. assamica ssp. assamica (Assam-India type). Plant Cell Rep 21(2): 166-173.
24. Dubrovnaya OV, Ljal'ko II, Gubanova Nla (2004) Somaclonal variability of sugarbeet plants on the basis of pollen sterility. Cytol Genet 38: 24-29.
25. Dykhuizen DE (1990) Experimental studies of natural selection in bacteria. Annu Rev Ecol Evol Syst 21: 373-398.
26. Ebert D (1998) Experimental evolution of parasites. Science 282: 1432-1435.
27. Elena SF, Lenski RE (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4: 457-469.
28. Fang JY, Wetten A, Adu-Gyamfi R, Wilkinson M, Rodriguez-Lopez C (2009) Use of secondary somatic embryos promotes genetic fidelity in cryopreservation of cocoa (Theobroma cacao L.). Agric Food Sci 18: 152-159.
29. Flores P, Otoni W, Dhingra O, de Souza Diniz S, Santos T, Bruckner C (2011) In vitro selection of yellow passion fruit genotypes for resistance to Fusarium vascular wilt. Plant Cell Tissue Org Cult. doi: 10. 1007/s11240-011-0009-5.
30. Fojtova M, Houdt HV, Depicker A, Kovarik A (2003) Epigenetic switch from posttranscriptional to transcriptional silencing is correlated with promoter hypermethylation. Plant Physiol 133: 1240-1250.
31. Franklin CI, Mott RL, Vuke TM (1989) Stable ploidy levels in long-term callus cultures of loblolly pine. Plant Cell Rep 8: 101-104.
32. Funchain P, Yeung A, Stewart JL, Lin R, Slupsa MM, Miller JH (2000) The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics 154: 59-970.
33. Gao X, Yang D, Cao D, Ao M, Sui X, Wang Q, Kimatu JN, Wang L (2010) In vitro micropropagation of Freesia hybrida and the assessment of genetic and epigenetic stability in regenerated plantlets. J Plant Growth Regul 29: 257-267.
34. Gaponenko AK, Petrova TF, Iskakov AR, Sozinov AA (1988) Cytogenetics of in vitro cultured somatic cells and regenerated plants of barley (Hordeum vulgare L.). Theor Appl Genet 75: 905-911.
35. Gavidia I, del Castillo AgudoL, Perez-Bermudez P (1996) Selection and longterm cultures of high-yielding Digitalis obscura plants: RAPD markers for analysis of genetic stability. Plant Sci 121: 197-205.
36. Gendrel A-V, Colot V (2005) Arabidopsis epigenetics: when RNA meets chromatin. Curr Opin Plant Biol 8: 142-147.
37. Gillis K, Gielis J, Peeters H, Dhooghe E, Oprins J (2007) Somatic embryogenesis from mature Bambusa balcooa Roxburgh as basis for mass production of elite forestry bamboos. Plant Cell Tissue Org Cult 91: 115-123.
38. Giraud A, Matic I, Tenaillon O, Clara A, Radman M, Fons M, Taddei F (2001) Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 291: 2606-2608.
39. Grafi G, Ben-Meir H, Avivi Y, Moshe M, Dahan Y, Zemach A (2007) Histone methylation controls telomerase-independent telomere lengthening in cells undergoing dedifferentiation. Dev Biol 306: 838-846.
40. Guo WL, Wu R, Zhang YF, Liu XM, Wang HY, Gong L, Zhang ZH, Liu B (2007) Tissue culture-induced locus-specific alteration in DNA methylation and its correlation with genetic variation in Codonopsis lanceolata Benth. et Hook. f. Plant Cell Rep 26: 1297-1307.
41. Hang A, Bregitzer P (1993) Chromosomal variations in immature embryo-derived calli from six barley cultivars. J Hered 84: 105-108.
42. Hao YJ, Deng XX (2002) Occurrence of chromosomal variations and plant regeneration from long-term-cultured citrus callus. In Vitro Cell Dev Plant 38: 472-476.
43. Hao YJ, You CX, Deng XX (2002) Analysis of ploidy and the patterns of amplified fragment length polymorphism and methylation-sensitive amplified polymorphism in strawberry plants recovered from cryopreservation. Cryoletters 23: 37-46.
44. Hao Y-J, Wen X-P, Deng X-X (2004) Genetic and epigenetic evaluations of citrus calluses recovered from slow-growth culture. Plant Physiol 161: 479-484.
45. Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447: 418-424.
46. Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci USA 93: 7783-7788.
47. Huettel B, Kanno T, Daxinger L, Bucher E, van der Winden J, Matzke AJM, Matzke M (2007) RNA-directed DNA methylation mediated by DRD1 and Pol IVb: a versatile pathway for transcriptional gene silencing in plants. BBA 1769: 358-374.
48. Jaligot E, Beulé T, Rival A (2002) Methylation-sensitive RFLPs: characterisation of two oil palm markers showing somaclonal variation-associated polymorphism. Theor Appl Genet 104: 1263-1269.
49. Jaligot E, Beulé T, Baurens F-C, Billotte N, Rival A (2004) Search for methylation-sensitive amplification polymorphisms associated with the 'mantled' variant phenotype in oil palm (Elaeis guineensis Jacq.). Genome 47: 224-228.
50. Johnson SS, Phillips RL, Rines HW (1987) Possible role of heterochromatin in chromosome breakage induced by tissue culture in oats (Avena sativa L.). Genome 29: 439-446.
51. Joyce SM, Cassells AC (2002) Variation in potato microplant morphology in vitro and DNA methylation. Plant Cell Tissue Org Cult 70: 125-137.
52. Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43: 179-188.
53. Kidwell MG, Lisch D (1997) Transposable elements as sources of variation in animals and plants. Proc Natl Acad Sci USA 94: 7704-7711.
54. 1[w]. Plant Physiol 139: 275-286.
55. 1[W]. Plant Physiol 149: 1493-1504.
56. Lambé P, Schié H, Mutambel N, Fouché J-G, Deltour R, Foidart J-M, Gaspar T (1997) DNA methylation as a key process in regulation of organogenic totipotency and plant neoplastic progression? In Vitro Cell Dev Plant 33: 155-162.
57. Larkin PJ, Scowcroft WR (1981) Somaclonal variation-a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60: 197-214.
58. Law RD, Suttle JC (2002) Transient decreases in methylation at 5'-CCGG-3′ sequences in potato (Solanum tuberosum L.) meristem DNA during progression of tubers through dormancy precede the resumption of sprout growth. Plant Mol Biol 51: 437-447.
59. Law RD, Suttle JC (2005) Chromatin remodeling in plant cell culture: patterns of DNA methylation and histone H3 and H4 acetylation vary during growth of asynchronous potato cell suspensions. Plant Physiol Biochem 43: 527-534.
60. Lenski RE (1988) Experimental studies of pleiotropy and epistasis in Escherichia coli. I. Variation in competitive fitness among mutants resistant to virus T4. Evolution 42: 425-432.
61. Lenski RE, Levin BR (1985) Constraints on the coevolution of bacteria and virulent phage: a model, some experiments, and predictions for natural communities. Am Nat 125: 585-602.
62. Lenski RE, Rose MR, Simpson SC, Tadler SC (1991) Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2, 000 generations. Am Nat 138: 1315-1341.
63. Lenski RE, Travisano M (1994) Dynamics of adaptation and diversification: a 10, 000-generation experiment with bacterial populations. Proc Natl Acad Sci USA 91: 6808-6814.
64. Li XQ, Xu ML, Korban SS (2002) DNA methylation profiles differ between field- and in vitro-grown leaves of apple. J Plant Physiol 159: 1229-1234.
65. López CMR, Wetten AC, Wilkinson MJ (2010) Progressive erosion of genetic and epigenetic variation in callus-derived cocoa (Theobroma cacao) plants. New Phytol 186: 856-868.
66. Martienssen R (1998) Transposons, DNA methylation and gene control. Trends Genet 14: 263-264.
67. Matthes M, Singh R, Cheah SC, Karp A (2001) Variation in oil palm (Elaeis guineensis Jacq.) tissue culture-derived regenerants revealed by AFLPs with methylation-sensitive enzymes. Theor Appl Genet 102: 971-979.
68. Meins F Jr (1989) Habituation: heritable variation in the requirement of cultured plant cells for hormones. Annu Rev Genet 23: 395-408.
69. Meins F Jr, Seldran M (1994) Pseudodirected variation in the requirement of cultured plant cells for cell-division factors. Development 120: 1163-1168.
70. Meins F Jr, Thomas M (2003) Meiotic transmission of epigenetic changes in the cell-division factor requirement of plant cells. Development 130: 6201-6208.
71. Meredith CP (1978) Selection and characterization of aluminum-resistant variants from tomato cell cultures. Plant Sci Lett 12: 25-34.
72. Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot 62: 3713-3725.
73. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe D (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328: 872-875.
74. Mongold JA, Bennett AF, Lenski RE (1996) Evolutionary adaptation to temperature. IV. Adaptation of Escherichia coli at a niche boundary. Evolution 50: 35-43.
75. Morcillo F, Gagneur C, Adam H, Richaud F, Singh R, Cheah S-C, Rival A, Duval Y, Tregear JW (2006) Somaclonal variation in micropropagated oil palm. Characterization of two novel genes with enhanced expression in epigenetically abnormal cell lines and in response to auxin. Tree Physiol 26: 585-594.
76. Ngezahayo F, Xu C, Wang H, Jiang L, Pang J, Liu B (2009) Tissue culture-induced transpositional activity of mPing is correlated with cytosine methylation in rice. BMC Plant Biol 9: 91.
77. Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Gene Dev 24: 2678-2692.
78. Novella IS, Clarke DK, Quer J et al (1995) Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandly cells. J Virol 69: 6805-6809.
79. Novella IS, Hershey CL, Escarmís C, Domingo E, Holland JJ (1999) Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J Mol Biol 287: 459-465.
80. Oakeley EJ (1999) DNA methylation analysis: a review of current methodologies. Pharmacol Ther 84: 389-400.
81. Oono K (1985) Putative homozygous mutants in regenerated plants of rice. Mol Gen Genet 198: 377-384.
82. Pavlopoulou A, Kossida S (2007) Plant cytosine-5 DNA methyltransferases: structure, function, and molecular evolution. Genomics 4: 530-541.
83. Peschke VM, Phillips RL (1991) Activation of the maize transposable element Suppressor-mutator (Spm) in tissue culture. Theor Appl Genet 81: 90-97.
84. Peschke VM, Phillips RL, Gengenbach BG (1987) Discovery of transposable element activity among progeny of tissue culture-derived maize plants. Science 238: 804-807.
85. Peschke VM, Phillips RL, Gengenbach BG (1991) Genetic and molecular analysis of tissue culture-derived Ac elements. Theor Appl Genet 82: 121-129.
86. Peraza-Echeverria S, Herrera-Valencia V, Andrew James K (2001) Detection of DNA methylation changes in micropropagated banana plants using methylation-sensitive amplification polymorphism (MSAP). Plant Sci 161: 359-367.
87. Peredo EL, Ángeles Revilla M, Arroyo-García R (2006) Assessment of genetic and epigenetic variation in hop plants regenerated from sequential subcultures of organogenic calli. J Plant Physiol 163: 1071-1079.
88. Phillips RL, Kaepplert SM, Olhoft P (1994) Genetic instability of plant tissue cultures: breakdown of normal controls. Proc Natl Acad Sci USA 91: 5222-5226.
89. 1[W]. Plant Physiol 140: 1255-1278.
90. Polanco C, Ruiz ML (2002) AFLP analysis of somaclonal variation in Arabidopsis thaliana regenerated plants. Plant Sci 162: 817-824.
91. Puente R, González AI, Ruiz ML, Polanco C (2008) Somaclonal variation in rye (Secale cereale L.) analyzed using polymorphic and sequenced AFLP markers. In Vitro Cell Dev Biol Plant 44: 419-426.
92. Rapp RA, Wendel JF (2005) Epigenetics and plant evolution. New Phytol 168: 81-91.
93. Reboud X, Bell G (1997) Experimental evolution in Chlamydomonas. III. Evolution of specialist and generalist types in environments that vary in space and time. Heredity 8: 507-514.
94. Renau-Morata B, Nebauer SG, Arrillaga I, Segura J (2005) Assessments of somaclonal variation in micropropagated shoots of Cedrus: consequences of axillary bud breaking. Tree Genet Genomes 1: 3-10.
95. Riddle NC, Richards EJ (2002) The control of natural variation in cytosine methylation in Arabidopsis. Genetics 162: 355-363.
96. Roth JR, Kofoid E, Roth FP, Berg OG, Seger J, Andersson DI (2003) Regulating general mutation rates: examination of the hypermutable state model for Cairnsian adaptive mutation. Genetics 163: 1483-1496.
97. Ryan FJ (1953) Evolution observed. Sci Am 189: 78-82.
98. Schmitt F, Oakeley EJ, Jost JP (1997) Antibiotics induce genome-wide hypermethylation in cultured Nicotiana tabacum plants. J Biol Chem 272: 1534-1540.
99. Singh RJ (1986) Chromosomal variation in immature embryo derived calluses of barley (Hordeum vulgate L.). Theor Appl Genet 72: 710-716.
100. Smulders MJM, Rus-Kortekaas W, Vosman B (1995) Tissue culture-induced DNA methylation polymorphisms in repetitive DNA of tomato calli and regenerated plants. Theor Appl Genet 91: 1257-1264.
101. Sniegowski PD, Lenski RE (1995) Mutation and adaptation: the directed mutation controversy in evolutionary perspective. Annu Rev Ecol Evol Syst 26: 553-578.
102. Sui X, Gao X, Ao M, Wang Q-M, Yang D, Wang M, Fu Y, Wang L (2011) cDNA cloning and characterization of UDP-glucose: anthocyanidin 3-O-glucosyltransferase in Freesia hybrida. Plant Cell Rep 30: 1209-1218.
103. Swedlund B, Vasil IK (1985) Cytogenetic characterization of embryogenic callus and regenerated plants of Pennisetum americanum (L.) K. Schum. Theor Appl Genet 69: 575-581.
104. Tanurdzic M, Vaughn MW, Jiang H, Lee T-J, Slotkin RK, Sosinski B, Thompson WF, Doerge RW, Martienssen RA (2008) Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6: e302.
105. Tariq M, Saze H, Probst AV, Lichota J, Habu Y, Paszkowski J (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci USA 100: 8823-8827.
106. Teixeira da Silva JA (2003) Chrysanthemum: advances in tissue culture, cryopreservation, postharvest technology, genetics and transgenic biotechnology. Biotechnol Adv 21: 715-766.
107. Thakur JK, Malika MR, Bhattb V, Reddyc MK, Soporyc SK, Tyagia AK, Khuranaa JP (2003) A POLYCOMB group gene of rice (Oryza sativa L. subspecies indica), OsiEZ1, codes for a nuclear-localized protein expressed preferentially in young seedlings and during reproductive development. Gene 314: 1-13.
108. Travisano M (1997) Long-term experimental evolution in Escherichia coli. VI. Environmental constraints on adaptation and divergence. Genetics 146: 471-479.
109. Travisano M, Lenski RE (1996) Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. Genetics 143: 15-26.
110. Travisano M, Vasi F, Lenski RE (1995) Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments. Evolution 49: 189-200.
111. Turner PE, Elena SF (2000) Cost of host radiation in an RNA virus. Genetics 156: 1465-1670.
112. Varga A, Thoma LH, Bruinsma J (1988) Effects of auxins and cytokinins on epigenetic instability of callus-propagated Kalanchoe blossfeldiana Poelln. Plant Cell Tissue Org Cult 15: 223-231.
113. Vasi F, Travisano M, Lenski RE (1994) Long-term experimental evolution in Escherichia coli. II. Changes in lifehistory traits during adaptation to a seasonal environment. Am Nat 144: 432-456.
114. Velicer GJ, Lenski RE (1999) Evolutionary tradeoffs under conditions of resource abundance and scarcity: experiments with bacteria. Ecology 80: 1168-1179.
115. Voinnet O, Vain P, Angell S, Baulcombe DC (1998) Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95: 177-187.
116. Wang L, Huang B, He M, Hao S (1990) Somatic embryogenesis and its hormonal regulation in tissue cultures of Fressia refracta. Ann Bot 65: 271-276.
117. Wang L, Bao X, Liu Y, Hao S (1994) Origin of direct somatic embryos from cultured inflorescence axis segments of Freesia refrata. Int J Plant Sci 155: 672-676.
118. Wang L, Wang X, Huang B (1996) Direct somatic embryogenesis and plant regeneration from single cell suspension cultures of Elymus giganteus Vahl. Plant Cell Rep 15: 865-868.
119. Wang L, Bao X, Huang B, Hao S (1998) Somatic embryogenic potential determined by the morphological polarity of the explant in tissue cultures of Freesia refracta. Acta Bot Sin 40: 138-143.
120. Wang Q-M, Gao F-Z, Gao X, Zou F-Y, Sui X, Wang M, Hui Y-J, Wang L (2011) Regeneration of Clivia miniata and assessment of clonal fidelity of plantlets. Plant Cell Tissue Org Cult. doi: 10. 1007/s11240-011-0085-6.
121. Wang Q-M, Wang Y-Z, Sun L-L, Gao F-Z, Sun W, He J, Gao X, Wang L (2012) Direct and indirect organogenesis of Clivia miniata and assessment of DNA methylation changes in various regenerated plantlets. Plant Cell Rep. doi: 10. 1007/s00299-012-1248-6.
122. Wang X-H, Lazzeri PA, Lörz H (1992) Chromosomal variation in dividing protoplasts derived from cell suspensions of barley (Hordeum vulgate L.). Theor Appl Genet 85: 181-185.
123. Weaver WC, Brault AC, Kang W, Holland JJ (1999) Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol 73: 4316-4326.
124. Williams L, Zhao J, Morozova N, Li Y, Avivi Y, Grafi G (2003) Chromatin reorganization accompanying cellular dedifferentiation is associated with modifications of histone H3, redistribution of HP1, and activation of E2F-target genes. Dev Dyn 228: 113-120.
125. Wu D, Wright DA, Wetzel C, Voytas DF, Rodermel S (1999) The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11: 43-55.
126. Yang H, Tabei Y, Kamada H, Kayano T, Takaiwa F (1999) Detection of somaclonal variation in tissue cultured rice cells using digoxygenin based random amplified polymorphic DNA. Plant Cell Rep 18: 520-526.
127. Yu F, Park S, Rodermel SR (2004) The Arabidopsis FtsH metalloprotease gene family: Interchangeability of subunits in chloroplast oligomeric complexes. Plant J 34: 864-876.
128. Yu F, Fu A, Aluru M et al (2007) Variegation mutants and mechanisms of chloroplast biogenesis. Plant Cell Environ 30: 350-365.
129. Zambrano MM, Siegele DA, Almiron M, Tormo A, Kolter R (1993) Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259: 1757-1760.
130. Zeliang PK, Pattanayak A, Iangrai B, Khongwir EA, Sarma BK (2010) Fertile plant regeneration from cryopreserved calli of Oryza rufipogon Griff. and assessment of variation in the progeny of regenerated plants. Plant Cell Rep 29: 1423-1433.
131. Zhang E, Ferenci T (1999) OmpF changes and the complexity of Escherichia coli adaptation to prolonged lactose limitation. FEMS Microbiol Lett 176: 395-401.