In vitro Ploidy Manipulation for Crop Improvement

Frontiers in Plant Science

Volumn 11, Issue , 2020, Pages

  Touchell, Darren H ^a   Palmer, Irene E ^a   Ranney, Thomas G ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

chromosome doubling; in vitro regeneration; mitotic inhibitor; plant breeding; polyploidy; whole genome duplication

Indexed keywords

EID: 85086571870     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2020.00722     Document Type: Review

References (116)

1. Allum J. F., Bringloe D. H., Roberts A. V., (2007). Chromosome doubling in a Rosa rugosa Thunb. hybrid by exposure of in vitro nodes to oryzalin: the effects of node length, oryzalin concentration and exposure time. Plant Cell Rep. 26 1977–1984. 10.1007/s00299-007-0411-y 17641861
2. Anthony R. G., Hussey P. J., (1999). Double mutation in Eleusine indicaα-tubulin increases the resistance of transgenic maize calli to dinitroaniline and phophorothiomidate herbicides. Plant J. 18 669–674. 10.1046/j.1365-313x.1999.00484.x 10417718
3. Artichart P., (2013). Polyploid induction by colchicine treatments and plant regeneration of Dendrobium chrysotoxum. Thai J. Agric. Sci. 46 59–63.
4. Ascough G. D., van Staden J., Erwin J. E., (2008). Effectiveness of colchicine and oryzalin at inducing polyploidy in Watsonia lepida N.E. Brown. Hortscience 43 2248–2251. 10.21273/hortsci.43.7.2248
5. Bairu M. W., Stirk W. A., Dolezal K., Staden J. V., (2007). Optimizing the micropropagation protocol for the endangered Aloe polyphylla: Can meta-topolin and its derivatives serve as replacement for benzyladenine and zeatin? Plant Cell Tissue Organ. Cult. 90 15–23. 10.1007/s11240-007-9233-4
6. Banyai W., Sangthong R., Karaket N., Inthima P., Mii M., Supaibulwatana K., (2009). Overproduction of artemisinin in tetraploid Artemisia annua L. Plant Biotechnol. 27 427–433. 10.5511/plantbiotechnology.10.0726a
7. Bartels P., Hilton J., (1973). Comparison of trifluralin, oryzalin, pronamide, propham, and colchicine treatments on microtubules. Pest. Biochem. Physiol. 3 462–472. 10.1016/0048-3575(73)90072-2
8. Blakeslee A., Avery A., (1937). Methods of inducing doubling of chromosomes in plants by treatment with colchicine. J. Hered. 28 393–411. 10.1093/oxfordjournals.jhered.a104294
9. Blume Y. B., Krasylenko Y. A., Demchuk O. M., Yemets A. I., (2013). Tubulin tyrosine nitration regulates microtubule organization in plant cells. Front. Plant Sci. 4:530. 10.3389/fpls.2013.00530 24421781
10. Cai D.-Y., Lin J.-H., Deng J.-P., (2016). Studies of propyzamide on polyploidy mutation of Vitas davidii. J. Cent. S. Univ. For. Technol. 7 103–108.
11. Chandanie M. A., Singh S. K., Sindhu S. S., Singh A., Tomar S. M. S., Prasad K. V., (2011). Efficacy of oryzalin as a potent chemical for in vitro induction of polyploids in Asiatic lily (Lilium hybrid L.) var. Polyanna. Indian J. Genet. 71 262–268.
12. Chauvin J. E., Label A., Kermarrec M. P., (2005). In vitro chromosome-doubling in tulip (Tulipa gesneriana L.). J. Hortic. Sci. Biotechnol. 80 693–698. 10.1080/14620316.2005.11512000
13. Chen L.-P., Wang Y.-J., Zhao M., (2006). In vitro induction and characterization of tetraploid Lychnis senno Siebold et Zucc. Hortscience 41 759–761. 10.21273/hortsci.41.3.759
14. Chu Z., Chen J., Nyporko A., Han H., Yu Q., Powles S., (2018). Novel α-tubulin mutations conferring resistance to dinitroaniline herbicides in Lolium rgidum. Front. Sci. 9:97. 10.3389/fpls.2018.00097 29472938
15. Cohen D., Yao J.-L., (1996). In vitro chromosome doubling of nine Zantedeschia cultivars. Plant Cell Tissue Organ. Cult. 47 43–49. 10.1007/BF00224065 24162397
16. Comai L., (2005). The advantages and disadvantages of being polyploid. Nature 6 836–846. 10.1038/nrg1711 16304599
17. Contreras R. N., Meneghelli L., (2016). In vitro chromosome doubling of Prunus laurocerasus ‘Otto Luyken’ and ‘Schipkaensis’. Hortscience 51 1463–1466. 10.21273/hortsci11329-16
18. Contreras R. N., Ranney T. G., Tallury S. P., (2007). Reproductive behavior of diploid and allotetraploid Rhododendron L. ‘Fragrant Affinity’. Hortscience 42 31–34. 10.21273/hortsci.42.1.31
19. Darzynkiewicz Z., Halicka H. D., Zhao H., Podhorecka M., (2011). Cell synchronization by inhibitors of DNA replication induces replication stress and DNA damage response: analysis by flow cytometry. Methods Mol. Biol. 761 85–96. 10.1007/978-1-61779-182-6_6 21755443
20. de Carvalho J. F. R. P., de Carvahlo C. R. P., Otoni W. C., (2005). In vitro induction of polyploidy in annatto (Bixa orellana) Plant Cell Tissue Organ. Cult. 80 69–75. 10.1007/s11240-004-8833-5
21. Dermen H., (1953). Periclinal cytochimeras and origin of tissues in stem and leaf of peach. Am. J. Bot. 40 154–158.
22. Dhooghe E., Denis S., Eeckhaut T., Reheul D., Van Labeke M.-C., (2009a). In vitro induction of tetraploids in ornamental Ranunculus. Euphytica 168 33–40. 10.1007/s10681-008-9876-1
23. Dhooghe E., Grunewald W., Leus L., Van Labeke M.-C., (2009b). In vitro polyploidisation of Helleborus species. Euphytica 165 89–95. 10.1007/s10681-008-9763-9
24. Dhooghe E., Laere K. V., Eeckhaut T., Leus L., Huylenbroeck J. V., (2010). Mitotic chromosome doubling of plant tissues in vitro. Plant Cell Tissue Organ. Cult. 104 359–373. 10.1007/s11240-010-9786-5
25. Dunham H. H., Banta A. M., (1940). Some effects of colchicine on heredity in Daphnia longispina. Genetics 25 310–325.
26. Dunn B. L., Lindstrom J. T., (2007). Oryzalin-induced chromosome doubling in Buddleja to facilitate interspecific hybridization. Hortscience 42 1326–1328. 10.21273/hortsci.42.6.1326
27. Ebrahimzadeh H., Soltanloo H., Shariatpanahi M. E., Eskandari A., Ramezanpour S. S., (2018). Improved chromosome doubling of parthenogenetic gaploid plants of cucumber (Cucumis sativus L.) using colchicine, trifluralin, and oryzalin. Plant Cell Tissue Organ. Cult. 135 407–417. 10.1007/s11240-018-1473-y
28. Eeckhaut T., Samijn G., Van Bockstaele E., (2002). In vitro polyploidy induction in Rhododendron simsii hybrids. Acta Hortic. 572 43–49. 10.17660/actahortic.2002.572.4 15954635
29. Eeckhaut T., Werbrouck S., Leus L., Van Bockstaele E., Debergh P., (2004). Chemically induced polyploidization in Spathiphyllum wallisii Regel through somatic embryogenesis. Plant Cell Tissue Organ. Cult. 78 241–246. 10.1023/b:ticu.0000025659.19232.04
30. Emsweller S. L., Ruttle M. L., (1941). Induced polyploidy in floriculture. Am. Nat. 75 310–328. 10.1086/280967
31. Gallone A., Hunter A., Douglas G. C., (2014). Polyploid induction in vitro using colchicine and oryzalin on Hebe ‘Oratia Beauty’: production and characterization of vegetative traits. Sci. Hortic. 179 59–66. 10.1016/j.scienta.2014.09.014
32. Gantait S., Mandal N., Bhattacharyya S., Das P. K., (2011). Induction and identification of tetraploids using in vitro colchicine treatment of Gerbera jamesonii Bolus cv. Sciella. Plant Cell Tissue Organ. Cult. 106 485–493. 10.1007/s11240-011-9947-1
33. Geoffriau E., Kahane R., Bellamy C., Rancillac M., (1997). Ploidy Stability and in vitro chromosome doubling in gynogenic clones of onion (Allium cepa L.). Plant Sci. 28 201–208. 10.1016/s0168-9452(96)04556-6
34. Ghanbari M. A., Jowkar A., Salehi H., Zarei M., (2019). Effects of polyploidization on petal characteristics and optical properties of Impatients walleriana (Hook.). Plant Cell Tissue Organ. Cult. 138 299–310. 10.1007/s11240-019-01625-3
35. Giles N. L., Armson A., Reid S. A., (2009). Characterization of trifluralin binding with recombinant tubulin from Trypanosoma brucei. Parasitol. Res. 104 893–903. 10.1007/s00436-008-1271-2 19050925
36. Gillooly D. A., Touchell D. H., Ranney T. G., (2015). In vitro polyploid induction of Ophiopogon planiscapus. SNA Res. Conf. 60 181–185.
37. Griesbach R. J., (1990). A fertile tetraploid Anigozanthis hybrid produced by in vitro colchicine treatment. Hortscience 25 802–803. 10.21273/hortsci.25.7.802
38. Gu X. F., Yang A. F., Meng H., Zhang J. R., (2005). In vitro induction of tetraploid plants from diploid Zizyphus jujube Mill. Cv.Zhanhua. Plant Cell Rep. 24 671–676. 10.1007/s00299-005-0017-1 16094528
39. Hannweg K., Sippel A., Bertling I., (2013). A simple and effective method for the micropropagation and in vitro induction of polyploidy and the effect on floral characteristics of the South African iris, Crocosmia aurea. S. Afr. J. Bot. 88 357–372.
40. Hannweg K., Steyn W., Bertling I., (2016a). In-vitro induced tetraploids of Plectranthus esculentus are nematode-tolerant and have enhanced nutritional value. Euphytica 207 343–351. 10.1007/s10681-015-1547-4
41. Hannweg K., Visser G., de Jager K., Bertling I., (2016b). In vitro-induced polyploidy and its effect on horticultural characteristics, essential oil composition and bioactivity of Tetradenia riparia. S. Afr. J. Bot. 106 186–191. 10.1016/j.sajb.2016.07.013
42. Hansen N. G. P., Andersen S. B., (1998). In vitro chromosome doubling with colchicine during microspore culture in wheat (Triticum aestivum L.). Euphytica 102 101–108.
43. Hebert C. J., Touchell D. H., Ranney T. G., LeBude A. V., (2010). In vitro shoot regeneration and polyploidy induction of Rhododendron ‘Frangrantissimum Improved’. Hortscience 45 801–804. 10.21273/hortsci.45.5.801
44. Heinz D. J., Mee G. W. P., (1970). Colchicine-induced polyploids from cell suspension cultures of sugarcane. Crop Sci. 696–699. 10.2135/cropsci1970.0011183x001000060030x
45. Hias N., Leus L., Davey M. W., Vanderzande S., Van Huylenbroeck J., Keulemans J., (2017). Effect of polyploidization in two apple (Malus x doemestica) genotypes. Hortic. Sci. 44 55–63. 10.17221/7/2016-hortsci 23045665
46. Hugdahl J. D., Morejohn L. C., (1993). Rapid and reversible high-affinity binding of the dinitroaniline herbicide oryzalin to tubulin from Zea mays L. Plant Physiol. 102 725–740. 10.1104/pp.102.3.725 12231861
47. Hussey G., Hypher A., (1978). Clonal propagation of sugar beet plants and the formation of polyploids by tissue culture. Ann. Bot. 42 477–479. 10.1093/oxfordjournals.aob.a085483
48. Javadian N., Karimzadeh G., Sharifi M., Moieni A., Behmanesh M., (2017). In vitro polyploid induction: changes in morphology, podophyllotoxin biosynthesis, and the expression of the related genes in Linum album (Linaceae). Planta 245 1165–1178. 10.1007/s00425-017-2671-2 28293732
49. Jiang Y., Liu S., Hu J., He G., Liu Y., Chen X., et al. (2020). Polyploidization of Plumbago auriculate Lam. In vitro and its characterization including cold tolerance. Plant Cell Tissue Organ. Cult. 140 315–325. 10.1007/s11240-019-01729-w
50. Jovanović A. M., Durst S., Nick P., (2010). Plant cell division is specifically affected by nitrotyrosine. J. Exp. Bot. 61 901–909. 10.1093/jxb/erp369 20018903
51. Kadota M., Niimi Y., (2002). In vitro induction of tetraploid plantsfrom a diploid Japanese pear cultivar (Pyrus pyrifolia N. cv. Hosui). Plant Cell Rep. 21 282–286. 10.1007/s00299-002-0509-1
52. Kaensaksiri T., Soontornchainaksaeng P., Soonthorncharennon N., Prathanturarug S., (2011). In vitro induction of polyploidy in Centella asiatica (L.) Urban. Plant Cell Tissue Organ. Cult. 107 187–194. 10.1007/s11418-013-0761-4 23529542
53. Kehr A., (1996). Woody plant polyploidy. Am. Nurseryman 183 38–47.
54. Kermani M. J., Sarasan V., Roberts A. V., Yokoya K., Wentworth J., Sieber V. K., (2003). Oryzalin-induced chromosome doubling in Rosa and its effect on plant morphology and pollen viability. Theor. Appl. Genet. 107 1195–1200. 10.1007/s00122-003-1374-1 12955205
55. Khosravi P., Kermani M. J., Nematzadeh G. A., Bihamta M. R., Yokoya K., (2008). Role of mitotic inhibitors and genotype on chromosome doubling of Rosa. Euphytica 160 267–275. 10.1007/s10681-007-9571-7
56. Kitamura S., Akutsu M., Okazaki K., (2009). Mechanism of action of nitrous oxide gas applied as a polyploidizing agent during meiosis in lilies. Sex. Plant Reprod. 22 9–14. 10.1007/s00497-008-0084-x 20033451
57. Klekowski E. J., (2003). Plant clonality, mutation, diplontic selection and mutational meltdown. Biol. J. Linn. Soc. 79 61–67. 10.1046/j.1095-8312.2003.00183.x
58. Lambertini C., (2019). Why are tall-statured energy grasses of polyploid species complexes potentially invasive? A review of their genetic variation patterns and evolutionary plasticity. Biol. Invasions 21 3019–3041. 10.1007/s10530-019-02053-2
59. Lattier J. D., Touchell D. H., Ranney T. G., Smith J. C., (2013). Micropropagation and Polyploid Induction of Acer platanoides ‘Crimson Sentry’. J. Environ. Hortic. 31 246–252.
60. Leung Y. Y., Hui L. L. Y., Kroaus V. B., (2015). Colchicine – update on mechanisms of action and therapeutic uses. Semin. Arthritis Rheum. 45 341–350. 10.1016/j.semarthrit.2015.06.013 26228647
61. Lipka E., Müller S., (2014). Nitrosative stress triggers microtubule reorganization in Arabidopsis thaliana. J. Exp. Bot. 65 4177–4189. 10.1093/jxb/eru194 24803503
62. Liu G., Li Z., Bao M., (2007). Colchicine-induced chromosome doubling in Platanus acerifolia and its effect on plant morphology. Euphytica 157 145–154. 10.1007/s10681-007-9406-6
63. Ma C., Tran J., Gu F., Ochoa R., Li C., Sept D., et al. (2010). Dinitroaniline activity in Toxoplasma gondii expressing wild-type or mutant α-tubulin. Antimicrob. Agents Chemother. 54 1453–1460. 10.1128/AAC.01150-09 20145086
64. Meyer E. M., Touchell D. H., Ranney T. G., (2009). In vitro shoot regeneration and polyploid induction from leaves of Hypericum species. Hortscience 44 1957–1961. 10.21273/hortsci.44.7.1957
65. Mitrofanova I. V., Zilbervarg I. R., Yemets A. I., Mitrofanova O. V., Blume Y. B., (2003). The effect of dinitroaniline and phosphorothioamidate herbicides on polyploidisation in vitro of Nepeta plants. Cell Biol. Int. 27, 229–231. 10.1016/S1065-6995(02)00317-7
66. Morejohn L. C., Bureau T. E., Molebajer J., Bajer A. S., Fosket D. E., (1987). Oryzalin, a dinitroaniline herbicide, binds to plant tubulin and inhibits microtubule polymerization in vitro. Planta 172 252–264. 10.1007/BF00394595 24225878
67. Morejohn L. C., Bureau T. E., Tocchi L. P., Fosket D. E., (1984). Tubulins from different higher plant species are immunologically nonidentical and bind colchicine differentially. Proc. Natl. Acad. Sci. U.S.A. 81 1440–1444. 10.1073/pnas.81.5.1440 16593430
68. Murashige T., Nakano R., (1966). Tissue culture as a potential tool in obtaining polyploid plants. J. Hered. 57 114–118. 25016827
69. Murthy J. V., Kim H.-H., Hanesworth V. R., Hugdahl J. D., Morejohn L. C., (1994). Competitive inhibition of high-affinity oryzalin binding to plant tubulin by the phosphoric amide herbicide amiprophos-methyl. Plant Physiol. 105 309–320. 10.1104/pp.105.1.309 12232204
70. Nadler J. D., Pooler M., Olsen R. T., Coleman G. D., (2012). In vitro induction of polyploidy in Cercis glabra Pamp. Sci. Hortic. 148 126–130. 10.1016/j.scienta.2012.09.024
71. Nasr M. L., Habib H. M., Ibrahim I. A., Kapiel T. Y., (2004). “In vitro induction of autotetraploid watermelons using colchicine and four dinitroaniline compounds,” in Proceedings of the International Conference On Engineering & Application, Sharm Elsheik. 10.13140/2.1.3144.3840
72. Neill S. J., Desikan R., Hancock J. T., (2003). Nitric oxide signaling in plants. New Phytol. 159 11–35.
73. Niimi H., Wantanabe M., Serizawa H., Koba T., Nkamura I., Mii M., (2015). Amiprophosmethyl-inducedeffecient in vitro production of polyploids in rhapanobrassica with the aid of aminoethoxyvinylglycin (AVG) in the culture medium. Breeed. Sci. 65 396–402. 10.1270/jsbbs.65.396 26719742
74. Nilanthi D., Chen X.-L., Zhao F.-C., Yang Y.-S., Wu H., (2009). Induction of tetraploids from petiole explants through colchicine treatments in Echinaceae purpurea L. J. Biomed. Biotechnol. 2009:343485. 10.1155/2009/343485 19696915
75. Nimura M., Kato J., Horaguchi H., Mii M., Sakai K., Katoh T., (2006). Induction of fertile amphidiploids by artificial chromosome-doubling in interspecific hybrid between Dianthus caryophyllus L. and D. japonicas Thunb. Breeed. Sci. 56 303–310. 10.1270/jsbbs.56.303 26081539
76. Noori S. A. S., Norouzi M., Karimzadeh G., Shirkool K., Niazian M., (2017). Effect of colchicine-induced polyploidy on morphological characteristics and essential oil composition of ajowan (Trachyspermum ammi L.). Plant Cell Tissue Organ Cult. 130 543–551. 10.1007/s11240-017-1245-0
77. Notsuka K., Tsurs T., Shiraishi M., (2000). Induced polyploid graps via in vitro chromosome doubling. J. Jpn. Soc. Hortic. Sci. 69 543–551. 10.2503/jjshs.69.543
78. Oates K. M., Ranney T. G., Touchell D. H., (2012). Influence of Induced Polyploidy on Fertility and Morphology of Rudbeckia Species and Hybrids. Hortscience 47 1217–1221. 10.21273/hortsci.47.9.1217
79. Olsen R. T., Ranney T. G., Viloria Z., (2006). Reproductive behavior of induced allotetraploid x Chitalpa and in vitro embryo culture of polyploidy progeny. J. Am. Soc. Horict. Sci. 131 716–724. 10.21273/jashs.131.6.716
80. Palmer I. E., Touchell D. H., Ranney T. G., (2008). In vitro polyploid induction of Rudbeckia sp. SNA Res. Conf. 53 186–189.
81. Pan-pan H., Wei-xu L., Hui-hui L., Zeng-xu X., (2018). In vitro induction and identification of autotetraploid of Bletilla striata (Thunb.) Reichb.f. by colchicine treatment. Plant Cell Tissue Organ. Cult. 132 425–432. 10.1007/s11240-017-1339-8
82. Parsons J. L., Martin S. L., James T., Golenia G., Boudko E. A., Hepworth S. R., (2019). Polyploidization for the genetic improvement of Cannabis sativa. Front. Plant Sci. 10:476. 10.3389/fpls.2019.00476 31114593
83. Petersen K. K., Hagberg P., Kristiansen K., (2002). In vitro chromosome doubling of Miscanthus sinensis. Plant Breed. 121 445–450. 10.1046/j.1439-0523.2002.738314.x
84. Petersen K. K., Hagberg P., Kristiansen K., (2003). Colchicine and oryzalin mediated chromosome doubling in different genotypes of Miscanthus sinensis. Plant Cell Tissue Organ. Cult. 73 137–146.
85. Planchais S., Glab N., Inzé D., Bergounioux C., (2000). Chemical inhibitors: a tool for plant cell cycle studies. FEBS Lett. 476 78–83. 10.1016/s0014-5793(00)01675-6 10878255
86. Ranney T. G., (2006). Polyploidy: From evolution to new plant development. Combined Proc. Intl. Plant Propagators Soc. 56 137–142.
87. Raza H., Jaskani M. J., Khan M. M., Malik T. A., (2003). In vitro induction of polyploids in watermelon and estimation based on DNA content. Intern. J. Agric. Biol. 5 298–302.
88. Regalado J. J., Carmona-Martin E., Querol V., Veléz C. G., Encina C. L., Pitta-Alvarez S. I., (2017). Production of compact petunias through polyplidization. Plant Cell Tissue Organ. Cult. 129, 61–71.
89. Rêgo M. M., Rêgo E. R., Bruckner C. H., Finger F. L., Otoni W. C., (2011). In vitro induction of autotetraploids from diploid yellow passion fruit mediated by colchicine and oryzalin. Plant Cell Tissue Organ. Cult. 107 451–459. 10.1007/s11240-011-9995-6
90. Ren J., Wu X., Song C., Liang Y., Gao W., Wang Y., (2018). Induction of polyploid tillered onion using colchicine and pendamethalin. Sains Malaysiana 47 2617–2624. 10.17576/jsm-2018-4711-04
91. Rose J. B., Kubba J., Tobutt K. R., (2000). Chromosome doubling in sterile Syringa vulgaris x S. pinnatifolia hybrids by in vitro culture of nodal explants. Plant Cell Tissue Organ. Cult. 63 127–132.
92. Rounsaville T. J., Touchell D. H., Ranney T. G., (2011). Fertility and reproductive pathways in diploid and triploid Miscanthus sinensis. Hortscience 46 1353–1357. 10.21273/hortsci.46.10.1353
93. Sakhanokho H. F., Rajasekaran K., Kelley R. Y., Islam-Faridi N., (2009). Induced polyploidy in diploid ornamental ginger (Hedychium muluense R. M. Smith) using colchicine and oryzalin. Hortscience 44 1809–1814. 10.21273/hortsci.44.7.1809
94. Sattler M. C., Carvalho C. R., Clarindo W. R., (2015). The polyploidy and its key role in plant breeding. Planta 281–296. 10.1007/s00425-015-2450-x 26715561
95. Soltis D. E., Burleigh J. D., (2009). Surviving the K-T mass extinction: new perspectives of polyploidization in angiosperms. PNAS 106, 5455–5456. 10.1007/s00425-015-2450-x 26715561
96. Soltis D. E., Albert V. A., Leebans-Mack J., Bell C. D., Paterson A. H., Zheng C., et al. (2009). Polyploidy and angiosperm diversification. Am. J. Bot. 96 336–348. 10.3732/ajb.0800079 21628192
97. Stanys V., Weckman A., Staniene G., Duchovkis P., (2006). In vitro induction of polyploidy in Japanese quince (Chaenomeles japonica) Plant Cell Tissue Organ. Cult. 84 263–268. 10.1007/s11240-005-9029-3
98. Sun Q., Sun H., Li L., Bell R. L., (2009). In vitro colchicine-induced polyploid plantlet production and regeneration from leaf explants of the diploid pear (Pyrus communis L.) cultivar, ‘Fertility’. J. Hortic. Sci. Biotechnol. 84 548–552. 10.1080/14620316.2009.11512564
99. Tavan M., Mirjalili M. H., Karimzadeh G., (2015). In vitro polyploidy induction: changes in morphological, anatomical and phytochemical characteristics of Thymus persicus (Lamiaceae). Plant Cell Tissue Organ. Cult. 122 573–583. 10.1007/s11240-015-0789-0
100. Taylor N. L., Anderson M. K., Queenberry K. H., Watson L., (1976). Doubling the chromosome number of Trifolium species using nitrous oxide. Crop Sci. 16 516–518. 10.2135/cropsci1976.0011183x001600040019x
101. The American Naturalist (1941). Symposium on theoretical and practical aspects of polyploidy in crop plants. Am. Nat. 75, 289–365. 10.2135/cropsci1976.0011183x001600040019x
102. Thomas J., Chen Q., Howes N., (1997). Chromosome doubling of haploids of common wheat with caffeine. Genome 40 552–558. 10.1139/g97-072 18464846
103. Touchell D. H., Ranney T. G., (2012). Chromosome doubling and fertility restoration in Miscanthus × giganteus. HortScience 47 S334. 10.1139/g97-072 18464846
104. Tresch S., Plath P., Grossman K., (2005). Herbicidal cyanoacrylates with antimicrotubule mechanism of action. Pest. Manag. Sci. 61 1052–1059. 10.1002/ps.1093 16035035
105. Trojal-Golush A., Skomra U., (2013). Artificially induced polyploidization in Humulus lupulus L. and its effect on morphological and chemical traits. Breed. Sci. 63 393–399. 10.1270/jsbbs.63.393 24399911
106. Väinölä A., (2000). Polyploidization and early screening of Rhododendron hybrids. Euphytica 112 239–244.
107. Vaughn K. C., Lehnen L. P., Jr. (1991). Mitotic disrupter herbicides. Weed Sci. 39 450–457. 10.1017/s0043174500073215
108. Viehmannová I., Fernández Cusimamani E., Bechyne M., Vyvadilová M., Greplova M., (2009). In vitro induction of polyploidy in yacon (Smallanthus sonchifolius) Plant Cell Tissue Organ Cult. 97 21–25. 10.1007/s11240-008-9494-6
109. Wang C., Lei J., (2012). In vitro induction of tetraploids from immature embryos through colchicine treatments in Clivia miniata Regal. J. Agric. Res. 7 3712–3718.
110. Wu J., Sang Y., Zhou Q., Zhang P., (2020). Colchicine in vitro tetraploid induction of Populus hopeiensis from leaf blades. Plant Cell Tissue Organ. Cult. 141 339–349. 10.1007/s11240-020-01790-w
111. Wu J.-H., Ferguson A. R., Murray B. G., (2011). Manipulation of ploidy for kiwifruit breeding: in vitro chromosome doubling in diploid Actinidia chinensis Planch. Plant Cell Tissue Organ. Cult. 106 503–511. 10.1007/s11240-011-9949-z
112. Xu C., Huang Z., Liao T., Li Y., Kang X., (2016). In vitro tetraploid plants regeneration from leaf explants of multiple genotypes in Populus. Plant Cell Tissue Organ. Cult. 125 1–9. 10.1007/s11240-015-0922-0
113. Yang Z., Shen Z., Tetreault H., Johnson L., Friebe B., Frazier T., et al. (2014). Production of autopolyploid lowland switchgrass lines through in vitro chromosome doubling. Bioenergy Res. 7 232–242. 10.1007/s12155-013-9364-x
114. Yuan S., Su Y., Liu Y., Li Z., Fang Z., Yang L., et al. (2015). Chromsome doubling of microspore-derived plants from cabbage (Brassica oleraceae var, capitate L.) and broccoli (Brassica oleraceae var. italica L.). Front. Plant Sci. 6:1118. 10.3389/fpls.2015.01118 26734028
115. Zhang Q. Y., Luo F. X., Liu L., Guo F. C., (2010). In vitro induction of tetraploids in crape myrtle (Lagerstoemia indica L.). Plant Cell Tissue Organ. Cult. 101 41–47. 10.1007/s11240-009-9660-5
116. Zhang Z., Dai H., Xiao M., Liu X., (2008). In vitro induction of tetraploids in Phlox subulata L. Euphytica 159 59–65. 10.1007/s10681-007-9457-8