Flow cytometry in plant research: A success story

Plant Cell Monographs

Volumn 22, Issue , 2014, Pages 395-430

  Vrána, Jan ^a   Cápal, Petr ^a   Bednářová, Martina ^a   Doležel, Jaroslav ^a  

^a INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84904873092     PISSN: 18611370     EISSN: 18611362     Source Type: Book Series    
DOI: 10.1007/978-3-642-41787-0_13     Document Type: Article

References (240)

1. Aleza P, Juárez J, Hernández M, Ollitrault P, Navarro L (2012) Implementation of extensive citrus triploid breeding programs based on 4x ´ 2x sexual hybridisations. Tree Genet Genome 8:1293–1306
2. Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218
3. Awoleye F, van Duren M, Doležel J, Novák FJ (1994) Nuclear DNA content and in vitro induced somatic polyploidization cassava (Manihot esculenta Crantz) breeding. Euphytica 76:195–202
4. Bagniewska-Zadworna A (2008) The root microtubule cytoskeleton and cell cycle analysis through desiccation of Brassica napus seedlings. Protoplasma 233:177–185
5. Bainard JD, Newmaster SG (2010) Endopolyploidy in bryophytes: widespread in mosses and absent in liverworts. J Bot 2010, Article ID 316356
6. Bainard JD, Fazekas AJ, Newmaster SG (2010) Methodology significantly affects genome size estimates: quantitative evidence using bryophytes. Cytometry 77A:725–732
7. Bainard JD, Husband BC, Aldwin SJ, Fazekas AJ, Gregory TR, Newmaster SG, Kron P (2011a) The effects of rapid desiccation on estimates of plant genome size. Chromosome Res 19:825–842
8. Bainard LD, Bainard JD, Newmaster SG, Klironomos JN (2011b) Mycorrhizal symbiosis stimulates endoreduplication in angiosperms. Plant Cell Environ 34:1577–1585
9. Baranyi M, Greilhuber J, Swiecicki WK (1996) Genome size in wild Pisum species. Theor Appl Genet 93:717–721
10. Barow M (2006) Endopolyploidy in seed plants. Bioassays 28:271–281
11. Barow M, Jovtchev G (2007) Endopolyploidy in plants and its analysis by flow cytometry. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Wiley-VCH, Weinheim, pp 349–372
12. Barow M, Meister A (2002) Lack of correlation between AT frequency and genome size in higher plants and the effect of nonrandomness of base sequences on dye binding. Cytometry 47A:1–7
13. Barow M, Meister A (2003) Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant Cell Environ 26:571–584
14. Barre P, Layssac M, D’Hont A, Louarn J, Charrier A, Hamon S, Noirot M (1998) Relationship between parental chromosomic contribution and nuclear DNA content in the coffee interspecific hybrid C. pseudozanguebariae ´ C. liberica var ‘dewevrei’. Theor Appl Genet 96:301–305
15. Bashir A, Auger JA, Rayburn AL (1993) Flow cytometric DNA analysis of wheat-rye addition lines. Cytometry 14A:843–847
16. Basiji DA, Ortyn WE, Liang L, Venkatachalam V, Morrissey P (2007) Cellular image analysis and imaging by flow cytometry. Clin Lab Med 27:653–670
17. Beatson RA, Ferguson AR, Weir IE, Graham LT, Ansell KA, Ding H (2003) Flow cytometric identification of sexually derived polyploids in hop (Humulus lupulus L.) and their use in hop breeding. Euphytica 134:189–194
18. Beaulieu JM, Moles AT, Leitch IJ, Bennett MD, Dickie JB, Knight CA (2007) Correlated evolution of genome size and seed mass. New Phytol 173:422–437
19. Becker RL, Mikel UV (1990) Interrelation of formalin fixation, chromatin compactness and DNA values as measured by flow cytometry and image cytometry. Anal Quant Cytol 12:333–341
20. Bennet MD, Leitch IJ (2011) Nuclear DNA amounts in angiosperms: targets, trends and tomorrow. Ann Bot 107:467–590
21. Bennett MD, Leitch IJ (1995) Nuclear DNA amounts in angiosperms. Ann Bot 76:113–176
22. Bennett MD, Leitch IJ (1997) Nuclear DNA amounts in angiosperms–583 new estimates. Ann Bot 80:169–196
23. Bennett MD, Leitch IJ (2005) Nuclear DNA amounts in angiosperms–progress, problems and prospects. Ann Bot 95:45–90
24. Bennett MD, Smith JB (1976) Nuclear DNA amounts in angiosperms. Philos Trans R Soc Lond Ser B Biol Sci 274:227–274
25. Bennett MD, Smith JB, Smith RIL (1982) DNA amounts of angiosperms from the Antarctic and South Georgia. Environ Exp Bot 22:307–318
26. Bennett MD, Leitch IJ, Hanson L (1998) DNA amounts in two samples of angiosperm weeds. Ann Bot 82:121–134
27. Bennett MD, Bhandol P, Leitch IJ (2000) Nuclear DNA amounts in angiosperms and their modern uses–807 new estimates. Ann Bot 86:859–909
28. Bennett MD, Leitch IJ, Price HJ, Johnston JP (2003) Comparisons with Caenorhabditis (100 Mb) and Drosophila (175 Mb) using flow cytometry show genome size in Arabidopsis to be 157 Mb and thus 25 % larger than the Arabidopsis genome initiative estimate of 125 Mb. Ann Bot 91:547–557
29. Bergounioux C, Perennes C, Brown SC, Gadal P (1988) Nuclear RNA quantification in protoplast cell cycle phases. Cytometry 9:84–87
30. Binarová P, Doležel J (1993) Effect of anti-microtubular drug amiprophos-methyl on somatic embryogenesis and DNA ploidy levels in alfalfa and carrot cell suspension cultures. Biol Plant 35:329–339
31. Binarová P, Číhalíková J, Doležel J (1993) Localization of MPM–2 recognized phosphoproteins and tubulin during cell cycle progression in synchronized Vicia faba root meristem cells. Cell Biol Int 17:847–856
32. Binarová P, Doležel J, Dráber P, Heberle-Bors E, Strnad M, Bogre L (1998a) Treatment of Vicia faba root tip cells with specific inhibitors to cyclin–dependent kinases leads to abnormal spindle formation. Plant J 16:697–707
33. Binarová P, Hause B, Doležel J, Dráber P (1998b) Association of γ–tubulin with kinetochore/ centromeric region of plant chromosomes. Plant J 14:751–757
34. Binarová P, Cenklová V, Hause B, Kubátová E, Lysák M, Doležel J, Bögre L, Dráber P (2000) Nuclear γ-tubulin during acentriolar plant mitosis. Plant Cell 12:433–442
35. Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN (2003) A gene expression map of the Arabidopsis root. Science 302:1956–1960
36. Boivin A, Vendrely R, Vendrely C (1948) L’acide désoxyribonucléique du noyau cellulaire dépositaire des caractéres héréditaires; arguments d’ordre analytique. C R Acad Sci 226:1061–1063
37. Bourdon M, Coriton O, Pirrello J, Cheniclet C, Brown SC, Poujol C, Chevalier C, Renaudin JP, Frangne N (2011) In planta quantification of endoreduplication using fluorescent in situ hybridization (FISH). Plant J 66:1089–1099
38. Bourdon M, Pirrello J, Cheniclet C, Coriton O, Bourge M, Brown S, Moïse A, Peypelut M, Rouyère V, Renaudin JP, Chevalier C, Frangne N (2012) Evidence for karyoplasmic homeostasis during endoreduplication and a ploidy-dependent increase in gene transcription during tomato fruit growth. Development 139:3817–3826
39. Buck SB, Bradford J, Gee KR, Agnew BJ, Clarke ST, Salic A (2008) Detection of S–phase cell cycle progression using 5–ethynyl–20–deoxyuridine incorporation with click chemistry, an alternative to using 5–bromo–20–deoxyuridine antibodies. Biotechniques 44:927–929
40. Cardoso DC, Carvalho CR, Cristiano MP, Soares FAF, Tavares MG (2012) Estimation of nuclear genome size of the genus Mycetophylax emery, 1913: evidence of no whole–genome duplication in Neoattini. C R Biol 335:619–624
41. Ceccarelli M, Sanantonio E, Marmottini F, Amzallag GN, Cionini PG (2006) Chromosome endoreduplication as a factor of salt adaptation in Sorghum bicolour. Protoplasma 227:113–118
42. Cerbah M, Mortreau E, Brown S, Siljak-Yakovlev S, Bertrand H, Lambert C (2001) Genome size variation and species relationships in the genus Hydrangea. Theor Appl Genet 103:45–51
43. Chattopadhyay PK, Hogerkorp CM, Roederer M (2008) A chromatic explosion: the development and future of multiparameter flow cytometry. Immunology 125:441–449
44. Cheniclet C, Rong WY, Causse M, Frangne N, Bolling L, Carde J-P, Renaudin J-P (2005) Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth. Plant Physiol 139:1984–1994
45. Chevalier C, Nafati M, Mathieu-Rivet E, Bourdon M, Frangne N, Cheniclet C, Renaudin JP, Gévaudant F, Hernould M (2011) Elucidating the functional role of endoreduplication in tomato fruit development. Ann Bot 107:1159–1169
46. Chiatante D, Brusa P, Levi M, Sgorbati S, Sparvoli E (1990) A simple protocol to purify fresh nuclei from milligram amounts of meristematic pea root tissue for biochemical and flow cytometry applications. Physiol Plant 78:501–506
47. Cires E, Cuesta C, Peredo EL, Revilla MA, Prieto JAF (2009) Genome size variation and morphological differentiation within Ranunculus parnassifolius group (Ranunculaceae) from calcareous screes in the Northwest of Spain. Plant Syst Evol 281:193–208
48. Clarindo WR, Carvalho CR (2011) Flow cytometric analysis using SYBR Green I for genome size estimation in coffee. Acta Histochem 113:221–225
49. Cookson SJ, Radziejwoski A, Granier C (2006) Cell and leaf size plasticity in Arabidopsis: what is the role of endoreduplication? Plant Cell Environ 29:1273–1283
50. Cousin A, Heel K, Cowling WA, Nelson MN (2009) An efficient high-throughput flow cytometric method for estimating DNA ploidy level in plants. Cytometry 75A:1015–1019
51. D’Hondt L, Höfte M, Van Bockstaele E, Leus L (2011) Applications of flow cytometry in plant pathology for genome size determination, detection and physiological status. Mol Plant Pathol 12:815–828
52. Dart S, Kron P, Mable BK (2004) Characterizing polyploidy in Arabidopsis lyrata using chromosome counts and flow cytometry. Can J Bot 82:185–197
53. Darzynkiewicz Z (1994) Simultaneous analysis of cellular RNA and DNA content. Methods Cell Biol 41:401–420
54. de Laat AMM, Göhde W, Vogelzakg MJDC (1987) Determination of ploidy of single plants and plant populations by flow cytometry. Plant Breed 99:303–307
55. Diermeier-Daucher S, Clarke ST, Hill D, Vollmann-Zweren A, Bradford JA, Brockhoff G (2009) Cell type specific applicability of 5–ethynyl–20–deoxyuridine (EdU) for dynamic proliferation assessment in flow cytometry. Cytometry 75A:536–546
56. Dobesˇ C, Luckl A, Hulber K, Paule J (2013) Prospects and limits of the flow cytometric seed screen–insights from Potentilla sensu lato (Potentilleae, Rosaceae). New Phytol 198:605–616
57. Doležel J (1991) Flow cytometric analysis of nuclear DNA content in higher plants. Phytochem Anal 2:143–154
58. Doležel J (1997) Application of flow cytometry for the study of plant genomes. J Appl Genet 38:285–302
59. Doležel J, Bartoš J (2005) Plant DNA flow cytometry and estimation of nuclear genome size. Ann Bot 95:99–110
60. Doležel J, Göhde W (1995) Sex determination in dioecious plants Melandrium album and M. rubrum using high–resolution flow cytometry. Cytometry 19:103–106
61. Doležel J, Greilhuber J (2010) Nuclear genome size: are we getting closer? Cytometry 77A:635–642
62. Doležel J, Binarová P, Lucretti S (1989) Analysis of nuclear DNA content in plant cells by flow cytometry. Biol Plant 31:113–120
63. Doležel J, Sgorbati S, Lucretti S (1992a) Comparison of three DNA fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiol Plantarum 85:625–631
64. Doležel J, Číhalíková J, Lucretti S (1992b) A high–yield procedure for isolation of metaphase chromosomes from root tips of Vicia faba L. Planta 188:93–98
65. Doležel J, Greilhuber J, Lucretti S, Meister A, Lysák MA, Nardi L, Obermayer R (1998) Plant genome size estimation by flow cytometry: inter–laboratory comparison. Ann Bot 82:17–26
66. Doležel J, Bartosˇ J, Voglmayr H, Greilhuber J (2003) Nuclear DNA content and genome size of trout and human. Cytometry 51A:127–128
67. Doležel J, Greilhuber J, Suda J (2007) Estimation of nuclear DNA content in plants using flow cytometry. Nat Protoc 2:2233–2244
68. Doležel J, Vrána J, Šafář J, Bartosˇ J, Kubaláková M, Šimková H (2012) Chromosomes in the flow to simplify genome analysis. Funct Integr Genomics 12:397–416
69. Doleželová M, Doležel J, Van den Houwe I, Roux N, Swennen R (2005) Focus on the Musa collection: ploidy levels revealed. InfoMusa 14:34–36
70. Doskočilová A, Kohoutová L, Volc J, Kourová H, Benada O, Chumová J, Plíhal O, Petrovská B, Halada P, Bögre L, Binarová P (2013) Nitrilase1 regulates the exit from proliferation, genome stability and plant development. New Phytol 198:685–698
71. Dubelaar GBJ, Gerritzen PL, Beeker AER, Jonker RR, Tangen K (1999) Design and first results of CytoBuoy: a wireless flow cytometer for in situ analysis of marine and fresh waters. Cytometry 37:247–254
72. Dubelaar GBJ, Casotti R, Tarran GA, Biegala IC (2007) Phytoplankton and their analysis by flow cytometry. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Wiley-VCH, Weinheim, pp 287–322
73. Eeckhaut T, Leus L, van Huylenbroeck J (2005) Exploitation of flow cytometry for plant breeding. Acta Phys Plant 27:743–750
74. Egesi CN, Pillay M, Asiedu R, Egunjobi JK (2002) Ploidy analysis in water yam, Dioscorea alata L., germplasm. Euphytica 128:225–230
75. Favoreto FC, Carvalho CR, Lima ABP, Ferreira A, Clarindo WR (2012) Genome size and base composition of Bromeliaceae species assessed by flow cytometry. Plant Syst Evol 298:1185–1193
76. Fox MH, Galbraith DW (1990) The application of flow cytometry and sorting to higher plant systems. In: Melamed MR, Lindmo T, Mendelsohn ML (eds) Flow cytometry and sorting, 2nd edn. Wiley-Liss, New York, pp 633–650
77. Fujikura Y, Doležel J, Číhalíková J, Bögre L, Heberle-Bors E, Hirt H, Binarová P (1999) Vicia faba germination: synchronized cell growth and localization of nucleolin and α–tubulin. Seed Sci Res 9:297–304
78. Galbraith DW (1990) Flow cytometric analysis of plant genomes. Methods Cell Biol 33:549–562
79. Galbraith DW (1994) Flow cytometry and sorting of plant protoplasts and cells. Methods Cell Biol 42B:539–561
80. Galbraith DW (2007) Protoplast analysis using flow cytometry. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Wiley- VCH, Weinheim, pp 231–250
81. Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051
82. Gaurav V, Kolewe ME, Roberts SC (2010) Flow cytometric methods to investigate culture heterogeneities for plant metabolic engineering. In: Germano A (ed) Plant secondary metabolism engineering. Methods in molecular biology. Humana Press, New York, pp 243–262, Springer protocols
83. Gendreau E, Hofte H, Grandjean O, Brown S, Traas J (1998) Phytochrome controls the number of endoreduplication cycles in the Arabidopsis thaliana hypocotyls. Plant J 13:221–230
84. Giglioli-Guivarc’h N, Pierre JN, Vidal J, Brown S (1996) Flow cytometric analysis of cytosolic pH of mesophyll cell protoplasts from the crabgrass Digitaria sanguinalis. Cytometry 23:241–249
85. Glab N, Labidi B, Qin LX, Trehin C, Bergounioux C, Meijer L (1994) Olomoucine, an inhibitor of the cdc2/cdk2 kinases activity, blocks plant cells at the G1 to S and G2 to M cell cycle transitions. FEBS Lett 353:207–211
86. Godelle B, Cartier D, Marie D, Brown SC, Siljak-Yakovlev S (1993) Heterochromatin study demonstrating the non–linearity of fluorometry useful for calculating genomic base composition. Cytometry 14A:618–626
87. Greilhuber J (1986) Severely distorted Feulgen–DNA amounts in Pinus (Coniferophytina) after nonadditive fixations as a result of meristematic self–tanning with vacuole contents. Can J Genet Cytol 28:409–415
88. Greilhuber J (1988) Self–tanning: a new and important source of stoichiometric error in cytophotometric determination of nuclear DNA content in plants. Plant Syst Evol 158:87–96
89. Greilhuber J (2008) Cytochemistry and C-values: the less-well-known world of nuclear DNA amounts. Ann Bot 101:791–804
90. Greilhuber J, Doležel J (2009) 2C or not 2C: a closer look at cell nuclei and their DNA content. Chromosoma 118:391–400
91. Greilhuber J, Leitch IJ (2013) Genome size and the phenotype. In: Leitch IJ, Greilhuber J, Doležel J, Wendel JF (eds) Plant genome diversity. Vol. 2: Physical structure, behaviour and evolution of plant genomes. Springer, Wien, pp 323–344
92. Greilhuber J, Doležel J, Lysák MA, Bennett MD (2005) The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C–value’ to describe nuclear DNA contents. Ann Bot 95:255–260
93. Greilhuber J, Bosch T, Muller K, Worberg A, Porembski S, Barthlott W (2006) Smallest angiosperm genomes found in lentibulariaceae, with chromosomes of bacterial size. Plant Biol 8:770–777
94. Greilhuber J, Temsch EM, Loureiro JCM (2007) Nuclear DNA content measurement. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Wiley-VCH, Weinheim, pp 423–438
95. Grewal RK, Lulsdorf M, Croser J, Ochatt S, Vandenberg A, Warkentin TD (2009) Doubledhaploid production in chickpea (Cicer arietinum L.): role of stress treatments. Plant Cell Rep 28:1289–1299
96. Halverson K, Heard SB, Nason JD, Stireman JO (2008) Differential attack on diploid, tetraploid, and hexaploid Solidago altissima L. by five insect gallmakers. Oecologia 154:755–761
97. Hardie DC, Gegory TR, Hebert PDN (2002) From pixels to picograms–A beginners’ guide to genome quantification by Feulgen image analysis densitometry. J Histochem Cytochem 50:735–749
98. Harmon AF, Zarlenga DS, Hildreth MB (2006) Improved methods for isolating DNA from Ostertagia ostertagi eggs in cattle feces. Vet Parasitol 135:297–302
99. Haymes KM, Ibrahim IA, Mischke S, Scott DL, Saunders JA (2004) Rapid isolation of DNA from chocolate and date palm tree crops. J Agric Food Chem 52:5456–5462
100. Heller FO (1973) DNS–Bestimmung an Keimwurzeln von Vicia faba L. mit Hilfe der Impulscytophotometrie. Bericht der Deutschen Botanischen Gesellschaft 86:437–441
101. Herben T, Suda J, Klimesˇová J, Mihulka S, Říha P, Šímová I (2012) Ecological effects of cell–level processes: genome size, functional traits and regional abundance of herbaceous plant species. Ann Bot 110:1357–1367
102. Hiddemann W, Schumann J, Andreef M, Barlogie B, Herman CJ, Leif RC, Mayall BH, Murphy RF, Sandberg AA (1984) Convention on nomenclature for DNA cytometry. Cancer Genet Cytogenet 13:181–183
103. Hopping ME (1993) Preparation and preservation of nuclei from plant–tissues for quantitative DNA analysis by flow cytometry. N Z J Bot 31:391–401
104. Jarret RL, Oziasakins P, Phatak S, Nadimpalli R, Duncan R, Hiliard S (1995) DNA contents in Paspalum spp. determined by flow cytometry. Genet Resour Crop Evol 42:237–242
105. Jedrzejczyk I, Sliwinska E (2010) Leaves and seeds as materials for flow cytometric estimation of the genome size of 11 Rosaceae woody species containing DNA-staining inhibitors. J Bot 2010, Article ID 930895
106. Jersáková J, Trávníček P, Kubátová B, Krejčíková J, Urfus T, Liu ZJ, Lamb A, Ponert J, Schulte K, Čurn V, Vrána J, Leitch IJ, Suda J (2013) Genome size variation in Orchidaceae subfamily Apostasioideae: filling the phylogenetic gap. Bot J Linn Soc 172:95–105
107. Jeschke MR, Tranel PJ, Rayburn AL (2003) DNA content analysis of smooth pigweed (Amaranthus hybridus) and tall waterhemp (A–tuberculatus): implications for hybrid detection. Weed Sci 51:1–3
108. Johnston JS, Bennett MD, Rayburn AL, Galbraith DW, Price HJ (1999) Reference standards for determination of DNA content of plant nuclei. Am J Bot 86:609–613
109. Jovtchev G, Schubert V, Meister A, Schubert I (2006) Nuclear DNA content and nuclear and cell volume are positively correlated in angiosperms. Cytogenet Genome Res 114:77–82
110. Kausch AP, Bruce BD (1994) Isolation and immobilization of various plastid subtypes by magnetic immunoabsorption. Plant J 6:767–779
111. Keller ERJ, Schubert I, Fuchs J, Meister A (1996) Interspecific crosses of onion with distant Allium species and characterization of the presumed hybrids by means of flow cytometry, karyotype analysis and genomic in situ hybridization. Theor Appl Genet 92:417–424
112. Knight CA, Beaulieu JM (2008) Genome size scaling through phenotype space. Ann Bot 101:759–766
113. Knight CA, Molinari NA, Petrov DA (2005) The large genome constraint hypothesis: evolution, ecology and phenotype. Ann Bot 95:177–190
114. Kolář F, Lučanová M, Těsˇitel J, Loureiro J, Suda J (2012) Glycerol–treated nuclear suspensions–an efficient preservation method for flow cytometric analysis of plant samples. Chromosome Res 20:303–315
115. Kotogány E, Dudits D, Horváth GV, Ayaydin F (2010) A rapid and robust assay for detection of S-phase cell cycle progression in plant cells and tissues by using ethynyl deoxyuridine. Plant Methods 6:5–19
116. Koutecký P, Štěpánek J, Baďurová T (2012a) Differentiation between diploid and tetraploid Centaurea phrygia: mating barriers, morphology and geographic distribution. Preslia 84:1–32
117. Koutecký P, Tuleu G, Baďurová T, Kosnar J, Stech M, Tesitel J (2012b) Distribution of cytotypes and seasonal variation in the Odontites vernus group in central Europe. Preslia 84:887–904
118. Kron P, Husband BC (2012) Using flow cytometry to estimate pollen DNA content: improved methodology and applications. Ann Bot 110:1067–1078
119. Kron P, Suda J, Husband BC (2007) Applications of flow cytometry to evolutionary and population biology. Annu Rev Ecol Evol Syst 38:847–876
120. Larkins BA, Dilkes BP, Dante RA, Coelho CM, Woo Y, Liu Y (2001) Investigating the hows and whys of DNA endoreduplication. J Exp Bot 52:183–192
121. Lee TJ, Shultz RW, Hanley-Bowdoin L, Thompson WF (2004) Establishment of rapidly proliferating rice cell suspension culture and its characterization by fluorescence-activated cell sorting analysis. Plant Mol Biol Rep 22:259–267
122. Leitch IJ, Bennett MD (2007) Genome size and its uses: the impact of flow cytometry. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Wiley-VCH, Weinheim, pp 153–176
123. Leitch AR, Leitch IJ (2012) Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytol 194:629–646
124. Leitch AR, Leitch IJ (2013) Genome size diversity and evolution in land plants. In: Leitch IJ, Greilhuber J, Doležel J, Wendel JF (eds) Plant genome diversity. Vol. 2: Physical structure, behaviour and evolution of plant genomes. Springer, Wien, pp 307–322
125. Leitch IJ, Chase MW, Bennett MD (1998) Phylogenetic analysis of DNA C–values provides evidence for a small ancestral genome size in flowering plants. Ann Bot 82:85–94
126. Leitch IJ, Soltis DE, Soltis PS, Bennett MD (2005) Evolution of DNA amounts across land plants (Embryophyta). Ann Bot 95:207–217
127. Liu JH, Dixelius C, Eriksson I, Glimelius K (1995) Brassica napus (+) B. tournefortii, a somatic hybrid containing traits of agronomic importance for rapeseed breeding. Plant Sci 109:75–86
128. Loureiro J, Pinto G, Lopes T, Doležel J, Santos C (2005) Assessment of ploidy stability of the somatic embryogenesis process in Quercus suber L. using flow cytometry. Planta 221:815–822
129. Loureiro J, Rodriguez E, Doležel J, Santos C (2006a) Comparison of four nuclear isolation buffers for plant DNA flow cytometry. Ann Bot 98:679–689
130. Loureiro J, Rodriguez E, Doležel J, Santos C (2006b) Flow cytometric and microscopic analysis of the effect of tannic acid on plant nuclei and estimation of DNA content. Ann Bot 98:515–527
131. Loureiro J, Rodriguez E, Doležel J, Santos C (2007a) Two new nuclear isolation buffers for plant DNA flow cytometry: a test with 37 species. Ann Bot 100:875–888
132. Loureiro J, Kopecký D, Castro S, Santos C, Silveira P (2007b) Flow cytometric and cytogenetic analyses of Iberian Peninsula Festuca spp. Plant Syst Evol 269:89–105
133. Loureiro J, Trávníček P, Rauchová J, Urfus T, Vít P, Sˇtech M, Castro S, Suda J (2010) The use of flow cytometry in the biosystematics, ecology and population biology of homoploid plants. Preslia 82:3–21
134. Lucretti S, Nardi L, Nisini PT, Moretti F, Gualberti G, Doležel J (1999) Bivariate flow cytometry DNA/BrdUrd analysis of plant cell cycle. Methods Cell Sci 21:155–166
135. Lysák MA, Doleželová M, Horry JP, Swennen R, Doležel J (1999) Flow cytometric analysis of nuclear DNA content in Musa. Theor Appl Genet 98:1344–1350
136. Macas J, Lambert GM, Doležel D, Galbraith DW (1998) Nuclear expressed sequence tag (NEST) analysis: a novel means to study transcription through amplification of nuclear RNA. Cytometry 33:460–468
137. Marhold K, Kudoh H, Pak JH, Watanabe K, Španiel S, Lihová J (2010) Cytotype diversity and genome size variation in eastern Asian polyploid Cardamine (Brassicaceae) species. Ann Bot 105:249–264
138. Marie D, Brown SC (1993) A cytometric exercise in plant DNA histograms, with 2C values for 70 species. Biol Cell 78:41–51
139. Marum L, Rocheta M, Maroco J, Oliveira MM, Muguel C (2009) Analysis of genetic stability at SSR loci during somatic embryogenesis in maritime pine (Pinus pinaster). Plant Cell Rep 28:673–682
140. Matzk F (2007) Reproduction mode screening. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Wiley-VCH, Weinheim, pp 131–152
141. Matzk F, Meister A, Schubert I (2000) An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Plant J 21:97–108
142. Meister A, Barow M (2007) DNA base composition of plant genomes. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells. analysis of genes, chromosomes, and genomes. Viley-VCH, Weinheim, pp 177–215
143. Melaragno JE, Mehrotra B, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5:1661–1668
144. Mishra MK (1997) Stomatal characteristics at different ploidy levels in Coffea L. Ann Bot 80:689–692
145. Morgan-Richards M, Trewick SA, Chapman HM, Krahulcova A (2004) Interspecific hybridization among Hieracium species in New Zealand: evidence from flow cytometry. Heredity 93:34–42
146. Naill MC, Roberts SC (2005) Flow cytometric analysis of protein content in Taxus protoplasts and single cells as compared to aggregated suspension cultures. Plant Cell Rep 23:528–533
147. Neelakandan AK, Wang K (2012) Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications. Plant Cell Rep 31:597–620
148. Noirot M, Barre P, Louarn J, Duperray C, Hamon S (2000) Nucleus-cytosol interactions–A source of stoichiometric error in flow cytometric estimation of nuclear DNA content in plants. Ann Bot 86:309–316
149. Noirot M, Barre P, Louarn J, Duperray C, Hamon S (2002) Consequences of stoichiometric error on nuclear DNA content evaluation in Coffea liberica var. dewevrei using DAPI and propidium iodide. Ann Bot 89:385–389
150. Noirot M, Barre P, Duperray C, Louarn J, Hamon S (2003) Effects of caffeine and chlorogenic acid on propidium iodide accessibility to DNA: consequences on genome size evaluation in coffee tree. Ann Bot 92:259–264
151. Noirot M, Barre P, Duperray C, Hamon S, De Kochko A (2005) Investigation on the causes of stoichiometric error in genome size estimation using heat experiments: consequences on data interpretation. Ann Bot 95:111–118
152. Nsabimana A, van Staden J (2006) Ploidy investigation of bananas (Musa spp.) from the National Banana Germplasm Collection at Rubona–Rwanda by flow cytometry. S Afr J Bot 72:302–305
153. Obermayer R, Leitch IJ, Hanson L, Bennett MD (2002) Nuclear DNA C–values in 30 species double the familial representation in Pteridophytes. Ann Bot 90:209–217
154. Ochatt SJ (2008) Flow cytometry in plant breeding. Cytometry 73A:581–598
155. Ochatt SJ, Durieu P, Jacas L, Pontécaille C (2001) Protoplast, cell and tissue cultures for the biotechnological breeding of grass pea (Lathyrus sativus L.). Lathyrus Lathyrism Newsl 2:35–38
156. Ochatt SJ, Patat-Ochatt EM, Moessner A (2011) Ploidy level determination within the context of in vitro breeding. Plant Cell Tissue Organ Cult 104:329–341
157. Overton WR, McCoy JP (1994) Reversing the effect of formalin on the binding of propidium iodide to DNA. Cytometry 16:351–356
158. Ozaki Y, Kumiko N, Michikazu H, Kenji U, Hiroshi O (1998) Application of flow cytometry for rapid determination of ploidy levels in Asparagus (Asparagus officinalis L.). J Fac Agric Kyushu Univ 43:83–88
159. Palomino G, Doležel J, Mendez I, Rubluo A (2003) Nuclear genome size analysis of Agave tequilana. Caryologia 56:37–46
160. Pawlowski TA, Bergervoet JHW, Bino RJ, Groot SPC (2004) Cell cycle activity and β-Tubulin accumulation during dormancy breaking of Acer platanoides L. seeds. Biol Plant 48:211–218
161. Pellicer J, Fay MF, Leitch IJ (2010) The largest eukaryotic genome of them all? Bot J Linn Soc 164:10–15
162. Perfetto SP, Chattopadhyay PK, Roederer M (2004) Seventeen–colour flow cytometry: unravelling the immune system. Nat Rev Immunol 4:648–655
163. Petit PX (1992) Flow Cytometric Analysis of rhodamine 123 fluorescence during modulation of the membrane potential in plant mitochondria. Plant Physiol 98:279–286
164. Petit PX, Diolez P, Muller P, Brown SC (1986) Binding of concanavalin A to the outer membrane of potato tuber mitochondria detected by flow cytometry. Febs Lett 196:65–70
165. Petrovská B, Cenklová V, Pochylová Z, Kourová H, Doskočilová A, Plíhal O, Binarová L, Binarová P (2012) Plant Aurora kinases play a role in maintenance of primary meristems and control of endoreduplication. New Phytol 193:590–604
166. Pfosser M (1989) Improved method for critical comparison of cell cycle data of asynchronously dividing and synchronized cell cultures of Nicotiana tabacum. J Plant Physiol 134:741–745
167. Pfosser M, Heberle-Bors E, Amon A, Lelley T (1995) Evaluation of sensitivity of flow cytometry in detecting aneuploidy in wheat using disomic and ditelosomic wheat–rye addition lines. Cytometry 21A:387–393
168. Pfündel E, Meister A (1996) Flow cytometry of mesophyll and bundle sheath chloroplast thylakoids of maize (Zea mays L.). Cytometry 23A:97–105
169. Picot J, Guerin CL, Le Van KC, Boulanger CM (2012) Flow cytometry: retrospective, fundamentals and recent instrumentation. Cytotechnology 64:109–130
170. Pillay M, Ogundiwin E, Tenkouano A, Doležel J (2006) Ploidy and genome composition of Musa germplasm at the International Institute of Tropical Agriculture (IITA). Afr J Biotechnol 5:1224–1232
171. Praça-Fontes MM, Carvalho CR, Clarindo WR, Cruz CD (2011) Revisiting the DNA C-values of the genome size-standards used in plant flow cytometry to choose the “best primary standards”. Plant Cell Rep 30:1183–1191
172. Price HJ, Hodnett G, Johnston JS (2000) Sunflower (Helianthus annuus) leaves contain compounds that reduce nuclear propidium iodide fluorescence. Ann Bot 86:929–934
173. Rani V, Raina SN (2000) Genetic fidelity of organized meristem–derived micropropagated plants: a critical reappraisal. In Vitro Cell Dev Biol Plant 36:319–330
174. Reichheld JP, Vernoux T, Lardon F, van Montagu M, Inzé D (1999) Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant J 17:647–656
175. Rewers M, Sliwinska E (2012) Endoreduplication Intensity as a marker of seed developmental stage in the Fabaceae. Cytometry 81A:1067–1075
176. Ricroch A, Yockteng R, Brown SC, Nadot S (2005) Evolution of genome size across some cultivated Allium species. Genome 48:511–520
177. Roberts AV (2007) The use of bead beating to prepare suspensions of nuclei for flow cytometry from fresh leaves, herbarium leaves, petals and pollen. Cytometry 71A:1039–1044
178. Roux N, Doležel J, Swennen R, Zapata-Arias FJ (2001) Effectiveness of three micropropagation techniques to dissociate cytochimeras in Musa spp. Plant Cell Tissue Organ Cult 66:189–197
179. Roux N, Toloza A, Radecki Z, Zapata-Arias FJ, Doležel J (2003) Rapid detection of aneuploidy in Musa using flow cytometry. Plant Cell Rep 21:483–490
180. Rowan BA, Oldenburg DJ, Bendich AJ (2007) A high–throughput method for detection of DNA in chloroplasts using flow cytometry. Plant Methods 3:5
181. Šafářová L, Duchoslav M, Jandová M, Krahulec F (2011) Allium oleraceum in Slovakia: cytotype distribution and ecology. Preslia 83:513–527
182. Schmidt G, Thannhauser SJ (1945) A method for the determination of deoxyribonucleic acid, ribonucleic acid and phosphoproteins in animal tissues. J Biol Chem 161:83–89
183. Schönswetter P, Suda J, Popp M, Weis-Schneeweiss H, Brochmann C (2007) Circumpolar phylogeography of Juncus biglumis (Juncaceae) inferred from AFLP fingerprints, cpDNA sequences, nuclear DNA content and chromosome numbers. Mol Phylogen Evol 42:92–103
184. Schulze D, Pauls KP (1998) Flow cytometric characterization of embryogenic and gametophytic development in Brassica napus microspore cultures. Plant Cell Physiol 39:226–234
185. Šesek P, Šuštar-Vozlič J, Bohanec B (2000) Determination of aneuploids in hop (Humulus lupulus L.) using flow cytometry. Pflugers Arch 439:16–18
186. Sgorbati S, Levi M, Sparvoli E, Trezzi F, Lucchini G (1986) Cytometry and flow cytometry of 40,6-diamidino-2-phenylindole (DAPI)-stained suspensions of nuclei released from fresh and fixed tissues of plants. Physiol Plant 68:471–476
187. Sgorbati S, Sparvoli E, Levi M, Galli MG, Citterio S, Chiatante D (1991) Cell cycle kinetic analysis with flow cytometry in pea root meristem synchronized with aphidicolin. Physiol Plant 81:507–512
188. Shapiro HM (1985) Practical flow cytometry. Wiley, New York
189. Shapiro HM (1988) Practical flow cytometry, 2nd edn. Wiley-Liss, New York
190. Shapiro HM (1995) Practical flow cytometry, 3rd edn. Wiley-Liss, New York
191. Shapiro HM (2003) Practical flow cytometry, 4th edn. Wiley, Hoboken
192. Siljak-Yakovlev S, Benmale S, Cerbah M, Coba de la Pena T, Bounaga N, Brown SC, Sarr A (1996) Chromosomal sex determination and heterochromatin structure in date palm. Sex Plant Reprod 9:127–132
193. Silva TCR, Abreu IS, Carvalho CR (2010) Improved and reproducible flow cytometry methodology for nuclei isolation from single root meristem. J Bot 2010, Article ID 320609
194. Śliwinska E, Thiem B (2007) Genome size stability in six medicinal plant species propagated in vitro. Biol Plant 51:556–558
195. Śliwinska E, Zielinska E, Jedrzejcyk I (2005) Are seeds suitable for flow cytometric estimation of plant genome size? Cytometry 64A:72–79
196. Śliwinska E, Bassel GW, Bewley D (2009) Germination of Arabidopsis thaliana seeds is not completed as a result of elongation of the radicle but of the adjacent transition zone and lower hypocotyl. J Exp Bot 60:3578–3594
197. Šmarda P (2006) DNA ploidy levels and intraspecific DNA content variability in Romanian fescues (Festuca, Poaceae) measured in fresh and herbarium material. Folia Geobot 41:417–432
198. Šmarda P, Stančík D (2006) Ploidy level variability in South American fescues (Festuca L., Poaceae): use of flow cytometry in up to 5 1/2–year–old caryopses and herbarium specimens. Plant Biol 8:73–80
199. Šmarda P, Müller J, Vrána J, Kočí K (2005) Ploidy level variability of some Central European fescues (Festuca subg. Festuca, Poaceae). Biologia (Bratislava) 60:25–36
200. Šmarda P, Buresˇ P, Horová L, Foggi B, Rossi G (2008) Genome size and GC content evolution of Festuca: ancestral expansion and subsequent reduction. Ann Bot 101:421–433
201. Šmarda P, Buresˇ P, Šmerda J, Horová L (2011) Measurements of genomic GC content in plant genomes with flow cytometry: a test for reliability. New Phytol 193:513–521
202. Soltis DE, Soltis PS, Bennett MD, Leitch IJ (2003) Evolution of genome size in the angiosperms. Am J Bot 90:1596–1603
203. Stehlík I, Barrett SCH (2005) Mechanisms governing sex-ratio variation in dioecious Rumex nivalis. Evolution 59:814–825
204. Stehlík I, Kron P, Barrett SCH, Husband BC (2007) Sexing pollen reveals female bias in a dioecious plant. New Phytol 175:185–194
205. Suda J, Leitch IJ (2010) The quest for suitable reference standards in genome size research. Cytometry 77A:717–720
206. Suda J, Trávníček P (2006) Reliable DNA ploidy determination in dehydrated tissues of vascular plants by DAPI flow cytometry: new prospects for plant research. Cytometry 69A:273–280
207. Suda J, Kyncl T, Jarolímová V (2005) Genome size variation in Macaronesian angiosperms: forty percent of the Canarian endemic flora completed. Plant Syst Evol 252:215–238
208. Suda J, Krahulcová A, Trávníček P, Krahulec F (2006) Ploidy level versus DNA ploidy level: an appeal for consistent terminology. Taxon 55:447–450
209. Suda J, Kron P, Husband BC, Trávníček P (2007a) Flow cytometry and ploidy: applications in plant systematics, ecology and evolutionary biology. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Wiley-VCH, Weinheim, pp 103–130
210. Suda J, Krahulcová A, Trávníček P, Rosenbaumová R, Peckert T, Krahulec F (2007b) Genome size variation and species relationships in Hieracium subgen. Pilosella (Asteraceae) as inferred by flow cytometry. Ann Bot 100:1323–1335
211. Suda J, Trávníček P, Mandák B, Berchová-Bímová K (2010) Genome size as a marker for identifying the invasive alien taxa in Fallopia section Reynoutria. Preslia 82:97–106
212. Sugimoto-Shirasu K, Roberts K (2003) “Big it up”: endoreduplication and cell-size control in plants. Curr Opin Plant Biol 6:544–553
213. Sun YL, Sun Y, Lin GG, Zhang R, Zhang K, Xie JH, Wang LN, Li JM (2012) Multicolor flow cytometry analysis of the proliferations of T-lymphocyte subsets in vitro by EdU incorporation. Cytometry 81A:901–909
214. Swift H (1950) The constancy of desoxyribose nucleic acid in plant nuclei. Proc Natl Acad Sci U S A 36:643–654
215. Taylor IW, Milthorpe BK (1980) An evaluation of DNA fluorochromes, staining techniques, and analysis for flow cytometry. I. Unperturbed cell populations. J Histochem Cytochem 28:1224–1232
216. Temsch EM, Greilhuber J (2000) Genome size variation in Arachis hypogaea and A. monticola re-evaluated. Genome 43:449–451
217. Temsch EM, Greilhuber J (2001) Genome size in Arachis duranensis: a critical study. Genome 44:826–830
218. Temsch EM, Temsch W, Ehrendorfer-Schratt L, Greilhuber J (2010) Heavy metal pollution, selection, and genome size: the species of the Žerjav study revisited with flow cytometry. J Bot 2010, Article ID 596542
219. Tiersch TR, Chandler RW, Wachtel SS, Elias S (1989) Reference standards for flow cytometry and application in comparative studies of nuclear DNA content. Cytometry 10A:706–710
220. Typas MA, Heale JB (1980) DNA content of germinating sores, individual hyphal cells and resting structure cells of Verticillium spp. measured by microdensitometry. Microbiology 121:231–242
221. Ulrich I, Ulrich W (1991) High-resolution flow cytometry of nuclear DNA in higher plants. Protoplasma 165:212–215
222. Ulrich I, Fritz B, Ulrich W (1988) Application of DNA fluorochromes for flow cytometric DNA analysis of plant protoplasts. Plant Sci 55:151–158
223. van Duren M, Morpurgo R, Doležel J, Afza R (1996) induction and verification of autotetraploids in diploid banana (Musa acuminata) by in vitro techniques. Euphytica 88:25–34
224. Vidic T, Greilhuber J, Vilhar B, Dermastia M (2009) Selective significance of genome size in a plant community with heavy metal pollution. Ecol Appl 19:1515–1521
225. Vilhar B, Greilhuber J, Koce JD, Temsch EM, Dermastia M (2001) Plant genome size measurement with DNA image cytometry. Ann Bot 87:719–728
226. Vilhar B, Kladnik A, Blejec A, Chourey PS, Dermastia M (2002) Cytometrical evidence that the loss of seed weight in the miniature seed mutant of maize is associated with reduced mitotic activity in the developing endosperm. Plant Physiol 129:23–30
227. Vinogradov AE (1994) Measurement by flow cytometry of genomic AT/GC ratio and genome size. Cytometry 16A:34–40
228. Voglmayr H (2000) Nuclear DNA amounts in mosses (Musci). Ann Bot 85:531–546
229. Voglmayr H, Greilhuber J (1998) Genome size determination in Peronosporales (Oomycota) by Feulgen image analysis. Fungal Genet Biol 25:181–195
230. Watanabe M, Setoguchi D, Uehara K, Ohtsuka W, Watanabe Y (2002) Apoptosis–like cell death of Brassica napus leaf protoplasts. New Phytol 156:417–426
231. Weber S, Unker F, Friedt W (2005) Improved doubled haploid production protocol for Brassica napus using microspore colchicine treatment in vitro and ploidy determination by flow cytometry. Plant Breed 124:511–513
232. Whittemore AT, Olsen RT (2011) Ulmus americana (Ulmaceae) is a polyploid complex. Am J Bot 98:754–760
233. Yanpaisan W, King NJC, Doran PM (1998) Analysis of cell cycle activity and population dynamics in heterogeneous plant cell suspensions using flow cytometry. Biotechnol Bioeng 58:515–528
234. Yao N, Eisfelder BJ, Marvin J, Greenberg JT (2004) The mitochondrion–an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J 40:596–610
235. Yokoya K, Roberts AV, Mottley J, Lewis R, Brandham PE (2000) Nuclear DNA amounts in roses. Ann Bot 85:557–561
236. Záveský L, Jarolímová V, Štěpánek J (2005) Nuclear DNA content variation within the genus Taraxacum (Asteraceae). Folia Geobotanica 40:91–104
237. Zhang CQ, Gong FC, Lambert GM, Galbraith DW (2005) Cell type-specific characterization of nuclear DNA contents within complex tissues and organs. Plant Methods 1:7
238. Zhang CQ, Barthelson RA, Lambert GM, Galbraith DW (2008) Characterization of cell-specific gene expression through fluorescence–activated sorting of nuclei. Plant Physiol 147:30–40
239. Zhao J, Cui J, Liu J, Liao F, Henny RJ, Chen J (2012) Direct somatic embryogenesis from leaf and petiole explants of Spathiphyllum ‘Supreme’ and analysis of regenerants using flow cytometry. Plant Cell Tissue Organ Cult 110:239–249
240. Zonneveld BJM, Leitch IJ, Bennett MD (2005) First nuclear DNA amounts in more than 300 angiosperms. Ann Bot 96:229–244