The “polyploid effect” in the breeding of aromatic and medicinal species

Scientia Horticulturae

Volumn 260, Issue , 2020, Pages

  Iannicelli, J ^a,c   Guariniello, J ^a   Tossi, V E ^b   Regalado, J J ^b   Di Ciaccio, L ^a,d   van Baren, C M ^b   Pitta Alvarez S I ^b   Escandon A S ^a  

^a INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^d Agencia Nacional de Promoción Científica y Tecnológica ANPCyT   (Argentina)

Author keywords

Autopolyploids; Genetic variability; Secondary metabolites; Whole genome duplication

Indexed keywords

BIOACTIVITY; BREEDING; CHROMOSOME; COMPLEXITY; GENETIC ANALYSIS; GENETIC VARIATION; GENOME; HERB; MEDICINAL PLANT; METABOLISM; MOLECULAR ANALYSIS; PHYSIOLOGY; PLANT BREEDING; SECONDARY METABOLITE;

EUKARYOTA;

EID: 85072652083     PISSN: 03044238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.scienta.2019.108854     Document Type: Review

References (105)

1. Adams, K.L., Wendel, J.F., 2005. Polyploidy and genome evolution in plants. Curr. Opin. Plant Biol. 8, 135-141. https://doi.org/10.1016/j.pbi.2005.01.001
2. Adaniya, S., Shirai, D., 2001. In vitro induction of tetraploid ginger (Zingiber officinale Roscoe) and its pollen fertility and germinability. Sci. Hort. 88, 277-287. https://doi.org/10.1016/S0304-4238(00)00212-0
3. Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-814. https://doi.org/10.1038/35048692
4. Arrigo, N., Barker, M.S., 2012. Rarely successful polyploids and their legacy in plant genomes. Curr, Opin, Plant Biol, 15, 140-146. https://doi.org/10.1016/j.pbi.2012.03.010
5. Barata, A.M., Rocha, F., Lopes, V., Carvalho, A.M., 2016. Conservation and sustainable uses of medicinal and aromatic plants genetic resources on the worldwide for human welfare. Ind. Crops Prod. 88, 8-11. https://doi.org/10.1016/j.indcrop.2016.02.035
6. Bardil, A., Tayal, A., Parisod, C., 2015. Evolutionary dynamics of retrotransposons following autopolyploidy in the Buckler Mustard species complex. Plant J. 82, 621-631. https://doi.org/10.1111/tpj.12837
7. Barker, M.S., Kane, N.C., Matvienko, M., Kozik, A., Michelmore, R.W., Knapp, S.J., Rieseberg, L.H., 2008. Multiple paleopolyploidizations during the evolution of the Compositae reveal parallel patterns of duplicate gene retention after millions of years. Mol. Biol. Evol. 25, 2445-2455. https://doi.org/10.1093/molbev/msn187
8. Baubec, T., Dinh, H.Q., Pecinka, A., Rakic, B., Rozhon, W., Wohlrab, B., von Haeseler, A., Scheid, O.M., 2010. Cooperation of multiple chromatin modifications can generate unanticipated stability of epigenetic states in Arabidopsis. Plant Cell. 22, 34-47.
9. Beest, M., Le Roux, J.J., Richardson, D.M., Brysting, A.K., Suda, J., Kubesôvá, M., Pysêk, P., 2012. The more the better? The role of polyploidy in facilitating plant invasions. Ann. Bot. 109, 19-45. https://doi.org/10.1093/aob/mcr277
10. Berkov, S., Philipov, S., 2002. Alkaloid production in diploid and autotetraploid plants of Datura stramonium. Pharm. Biol. 40, 617-621. https://doi.org/10.1076/phbi.40.8.617.14650
11. Bernard, F., Moghbel, N., Hassannejad, S., 2012. Treatment of licorice seeds with colchicine: changes in seedlings DNA level and in anthocyanin and glycyrrhizic acid content of derived callus cultures. Nat. Prod. Commun. 7, 1457-1460.
12. Buggs, R.J., Chamala, S., Wu, W., Tate, J.A., Schnable, P.S., Soltis, D.E., Barbazuk, W.B., 2012. Rapid, repeated, and clustered loss of duplicate genes in allopolyploid plant populations of independent origin. Curr. Biol. 22, 248-252. https://doi.org/10.1016/j.cub.2011.12.027
13. Caruso, I., Lepore, L., De Tommasi, N., Dal Piaz, F., Frusciante, L., Aversano, R., Garramone, R., Carputo, D., 2011. Secondary metabolite profile in induced tetraploids of wild Solanum commersonii Dun. Chem. Biodivers. 8, 2226-2237. https://doi.org/10.1002/cbdv.201100038
14. Corneillie, S., De Storme, N., Van Acker, R., Fangel, J.U., De Bruyne, M., De Rycke, R.M., Geelen, D.N.V., Willats, W.G.T., Vanholme, B., Boerjan, W.A., 2019. Polyploidy affects plant growth and alters cell wall composition. Plant Physiol. 179, 74-87. https://doi.org/10.1104/pp.18.00967
15. Corrêa, J.P.O., Vital, C.E., Pinheiro, M.V.M, Batista, D.S., Saldanha, C.W., da Cruz, A.C.F., Notini, M.M., Freitas, D.M.S., Da Matta, F.M., Otoni, W.C., 2016. Induced polyploidization increases 20-hydroxyecdysone content, in vitro photoautotrophic growth, and ex vitro biomass accumulation in Pfaffia glomerata (Spreng.) Pedersen. In vitro Cell Dev. Biol. Plant 52, 45-55. https://doi.org/10.1007/s11627-016-9746-9
16. Dehghan, E., Hakkinen, S.T., Oksman-Caldentey, K.M., Ahmadi, F.S., 2012. Production of tropane alkaloids in diploid and tetraploid plants and in vitro hairy root cultures of Egyptian henbane (Hyoscyamus muticus L.). Plant Cell Tissue Organ Cult. 110, 35-44. https://doi.org/10.1007/s11240-012-0127-8
17. De Storme, N., Mason, A., 2014. Plant speciation through chromosome instability and ploidy change: Cellular mechanisms, molecular factors and evolutionary relevance. Current Plant Biology, 1: 10–33.
18. Dhawan, O.E., Lavania, U.C., 1996. Enhancing the productivity of secondary metabolites via induced polyploidy: a review. Euphytica 87, 81-89. https://doi.org/10.1007/BF00021879
19. Dhooghe, E., Van Laere, K., Eeckhaut, T., Leus, L., Van Huylenbroeck, J., 2011. Mitotic chromosome doubling of plant tissues in vitro. Plant Cell Tissue Organ Cult. 104, 359-373. https://doi.org/10.1007/s11240-010-9786-5
20. Dijkstra, H., Speckmann, G.J., 1980. Autotetraploidy in caraway (Carum carvi L.) for the increase of the aetheric oil content of the seed. Euphytica 29, 89-96. https://doi.org/10.1007/BF00037252
21. Eng, W.H., Ho, W.S., 2019. Polyploidization using colchicine in horticultural plants: A review. Scientia Horticulturae. 246, 604-617. https://doi.org/10.1016/j.scienta.2018.11.010
22. Escandón, A.S., Hopp, H.E., Hahne, G., 1989. Differential amplification of five selected genes in callus cultures of two shrubby Oxalis species. Plant Science 63, 177-185. https://doi.org/10.1016/0168-9452(89)90243-4
23. Fanciullino, A.L., Gancel, A.L., Froelicher, Y., Luro, F., Ollitrault, P., Brillouet, J.M., 2005. Effects of nucleo-cytoplasmic interactions on leaf volatile compounds from citrus somatic diploid hybrids. J. Agric. Food. Chem. 53, 4517-4523. https://doi.org/10.1021/jf0502855
24. Fasano, C., Diretto, G., Aversano, R., D'Agostino, N., Di Matteo, A., Frusciante, L., Giuliano, G., Carput, D., 2016. Transcriptome and metabolome of synthetic Solanum autotetraploids reveal key genomic stress events following polyploidization. New Phytologist 210, 1382-1394. https://doi.org/10.1111/nph.13878
25. Finn, T.E., Wang, L., Smolilo, D., Smith, N.A., White, R., Chaudhury, A., Dennis, E.S., Wang, M.-B., 2011. Transgene expression and transgeneinduced silencing in diploid and autotetraploid Arabidopsis. Genetics. 187, 409–423.
26. Gancel, A.L., Ollitrault, P., Froelicher, Y., Tomi, F., Jacquemond, C., Luro, F., Brillouet, J.M., 2003. Leaf volatile compounds of seven citrus somatic tetraploid hybrids sharing Willowleaf mandarin (Citrus deliciosa Ten) as their common parent. J. Agric. Food Chem. 51, 6006-6013. https://doi.org/10.1021/jf0345090
27. Gao, S.L., Zhu, D.N., Cai, Z.H., Xu, D.R., 1996. Autotetraploid plants from colchicine-treated bud culture of Salvia miltiorrhiza Bge. Plant Cell Tissue Organ Cult. 47, 73-77. https://doi.org/10.1007/BF02318968
28. Gao, S.L., Chen, B.J., Zhu, D.N., 2002. In vitro production and identification of autotetraploids of Scutellaria baicalensis. Plant Cell Tissue Organ Cult. 70, 289-293. https://doi.org/10.1023/A:1016577002039
29. Gao, R., Wang, H., Dong, B., Yang, X., Chen, S., Jiang, J., Zhang, Z., Liu, C., Zhao, N., Chen, F., 2016. Morphological, genome and gene expression changes in newly induced autopolyploid Chrysanthemum lavandulifolium (Fisch. ex Trautv.) Makino. Int. J. Mol. Sci. 17, E1690. https://doi.org/10.3390/ijms17101690
30. Ghotbi Ravandi, E., Rezanejad, F., Zolala, J., Dehghan, E. 2013. The effects of chromosome-doubling on selected morphological and phytochemical characteristics of Cichorium intybus L. J. Hortic. Sci. Biotech. 88, 701-709. https://doi.org/10.1080/14620316.2013.11513027
31. Gomes, S.S.L., Saldanha, C.W., Neves, C.S., Trevizani, M., Raposo, N.R.B., Notini, M.M., de Oliveira Santos, M., Campos, J.M.S., Otoni, W.C., Viccini, L.F., 2014. Karyotype, genome size, and in vitro chromosome doubling of Pfaffia glomerata (Spreng.) Pedersen. Plant Cell Tissue Organ Cult. 118, 45-56. https://doi.org/10.1007/s11240-014-0460-1
32. Griesbach, R.J., Kamo, K.K., 1996. The effect of induced polyploidy on the flavonoids of Petunia Mitchell. Phytochem 42:361-363. https://doi.org/10.1016/0031-9422(95)00893-4
33. Guo, M., Davis, D., Birchler, J.A., 1996. Dosage effect on gene expression in a maize ploidy series. Genet. 142, 1349-1355.
34. Halfmann, R., Lindquist, S., 2010. Epigenetics in the extreme: prions and the inheritance of environmentally acquired traits. Science 330, 629-632. https://doi.org/10.1126/science.1191081
35. Hannweg, K., Visser, G., de Jager, K., Bertling, I., 2016. 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. https://doi.org/10.1016/j.sajb.2016.07.013
36. Heping, H., Shanlin, G., Lanlan, C., Xiaoke, J., 2008. In vitro induction and identification of autotetraploids of Dioscorea zingiberensis. In Vitro Cell Dev. Biol. Plant 44, 448-455. https://doi.org/10.1007/s11627-008-9177-3
37. IAEA/MVD. 2019. IAEA Mutant Variety Database. Accessed 2019-07-23. https://mvd.iaea.org/
38. Iannicelli, J., Elechosa, M.A., Juárez, M.A., Martínez, A., Bugallo, V., Bandoni, A.L., Escandón, A.S., van Baren, C.M., 2016a. Effect of polyploidization in the production of essential oils in Lippia integrifolia. Ind. Crops. Prod. 81, 20-29. https://doi.org/10.1016/j.indcrop.2015.11.053
39. Iannicelli, J., Pérez de la Torre, M., Coviella, A., Del Valle Aguirre, E., Elechosa, M.A., van Baren, C.M., Pacheco, M.G., Escandón, A., 2016b. In vitro propagation of Lippia integrifolia (Griseb.) Hier. and detection of genetic instability through ISSR markers of in vitrocultured plants. Rev Fac Cienc Agric Forest. 115: 67-76.
40. Iannicelli, J., Guariniello, J., Pitta-Álvarez, S.I., Escandón, A.S., 2018. Traditional uses, conservation status and biotechnological advances for a group of aromatic/medicinal native plants from the American continent. BLACPMA 17, 453-491.
41. Kaensaksiri, T., Soontornchainaksaeng, P., Soonthornchareonnon, N., Prathanturarug, S., 2011. In vitro induction of polyploidy in Centella asiatica (L.) Urban. Plant Cell Tissue Organ Cult. 107, 187-194. https://doi.org/10.1007/s11240-011-9969-8
42. Kim, Y.S., Hahn, E.J., Murthy, H.N., Paek, K.Y., 2004. Effect of polyploidy induction on biomass and ginsenoside accumulations in adventitious roots of ginseng. J. Plant Biol. 47, 356-360. https://doi.org/10.1007/BF03030551
43. Koul, S., Sambyal, M., Kitchlu, S., Bakshi, S., Kaul, M., 2010. Development, micropropagation and characterization of colchiploid of Echinacea purpurea (L.) Moench. Indian J. Biotech. 9, 221-224.
44. Lavania, U.C. 1986. Genetic improvement of Egyptian henbane, Hyoscyamus muticus L. through induced tetraploidy. Theoretical and Applied Genetics 73, 292-298.
45. Lavania, U.C., 1988. Enhanced productivity of the essential oil in the artificial autopolyploid of vetiver (Vetiveria zizanioides L. Nash). Euphytica 38, 271-276. https://doi.org/10.1007/BF00023530
46. Lavania, U.C., Srivastava, S., 1990. Evolutionary genomic change paralleled by differential responses in 2x and 4x calli cultures. Experientia 46, 322-324. https://doi.org/10.1007/BF01951778
47. Lavania, U.C, Srivastava, S., 1991. Enhanced productivity of tropane alkaloids and fertility in artificial autotetraploids of Hyoscyamus niger L. Euphytica 52 :73-77.
48. Lavania, U.C., 1995. Genesis of high bivalent pairing in autotetraploids and autotriploids, and resuction in bound arm associations over generations. In: Brandham PE, Bennet MD, editors. Kew Chromosome Conf. IV. Royal Botanic Gardens, Kew; 397–406.
49. Lavania, U.C., 2005. Genomic and ploidy manipulation for enhanced production of phyto-pharmaceuticals. Plant Genet. Resour. 3, 170-177. https://doi.org/10.1079/PGR200576
50. Lavania, U.C., Srivastava, S. Lavania, S., 2010. Ploidy-Mediated Reduced Segregation Facilitates Fixation of Heterozygosity in the Aromatic Grass, Cymbopogon martinii (Roxb.) Journal of Heredity, 101: 11923,https://doi.org/10.1093/jhered/esp071
51. Lavania, U.C., Srivastava, S., Lavania, S., Basu, S., Kumar Misra, N., Mukai, Y., 2012. Autopolyploidy differentially influences body size in plants, but facilitates enhanced accumulation of secondary metabolites, causing increased cytosine methylation. The Plant Journal. 71, 539–549. https://doi.org/10.1111/j.1365-313X.2012.05006.x
52. Lavania, U.C., 2013. Polyploidy, body size, and opportunities for genetic enhancement and fixation of heterozygosity in plants. Nucleus 56: 1-6. https://doi.org/10.1007/s13237-013-0075-7
53. Leitch, A.R., Leitch, I.J., 2008. Genomic plasticity and the diversity of polyploid plants. Science 320, 481-483.
54. Levin, D.A., 1983. Polyploidy and Novelty in Flowering Plants. The Amer Nat. 122:1-25. https://doi.org/10.1126/science.1153585
55. Levin, D.A., 2002. The role of chromosomal change in plant evolution. Oxford University Press, New York, New York, USA. https://doi.org/10.1600/036364404774195656
56. Levin, D.A. and Soltis, D.E., 2018. Factors promoting polyploid persistence and diversification and limiting diploid speciation during the K-Pg interlude. Current in Plant Biology, 42: 1-7. https://dx.doi.org/10.1016/j.pbi.2017.09.010
57. Lin, X., Zhou, Y., Zhang, J., Lu, X., Zhang, F., Shen, Q., Wu, S., Chen, Y., Wang, T., Tang, K., 2011. Enhancement of artemisinin content in tetraploid Artemisia annua plants by modulating the expression of genes in artemisinin biosynthetic pathway. Biotechnol. Appl. Biochem. 58, 50-57. https://doi.org/10.1002/bab.13
58. Madani, H., Hosseini, B., Dehghan, E., Rezaei-chiyaneh, E. 2015. Enhanced production of scopolamine in induced autotetraploid plants of Hyoscyamus reticulatus L. Acta Physiol. Plant 37, 55. https://doi.org/10.1007/s11738-015-1795-x
59. Madlung, A. 2013. Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity (Edinb) 110, 99-104. https://doi.org/10.1038/hdy.2012.79
60. Maere, S., De Bodt, S., Raes, J., Casneuf, T., Van Montagu, M., Kuiper, M., Van de Peer, Y., 2005. Modeling gene and genome duplications in eukaryotes. Proc. Natl. Acad. Sci. 102, 5454-5459. https://doi.org/10.1073/pnas.0501102102
61. Martelotto, L.G., Ortiz, J.P.A., Stein, J., Espinoza, F., Quarin, C.L., Pessino, S.L., 2005. A comprehensive analysis of gene expression alterations in a newly synthesized Paspalum notatum autotetraploid. Plant Science 169, 211-220. https://doi.org/10.1016/j.plantsci.2005.03.015
62. Martelotto, L.G., Ortiz, J.P.A., Stein, J., Espinoza, F., Quarin, C.L., Pessino, S.L., 2007. Genome rearrangements derived from autopolyploidization in Paspalum sp. Plant Science 172, 970-977. https://doi.org/10.1016/j.plantsci.2007.02.001
63. McClintock, B., 1984. The significance of responses of the genome to challenge. Science 226, 792–801.
64. Mecchia, M., Ochogaví, A., Selva, J., Laspina, N., Felitti, S., 2007. Genome polymorphisms and gene differential expression in a ‘back-and-forth’ ploidy-altered series of weeping lovegrass. J. Plant Physiol. 164, 1051–1061. https://doi.org/10.1016/j.jplph.2006.07.002
65. Mishra, B.K., Pathak, S., Sharma, A., Trivedi, P.K., Shukla, S. 2010. Modulated gene expression in newly synthesized auto-tetraploid of Papaver somniferum L. S. Afr. J. Bot. 76, 447-452. https://doi.org/10.1016/j.sajb.2010.02.090
66. Øvrebø J.I., Edgar, B.A., 2018. Polyploidy in tissue homeostasis and regeneration. Development 145, dev156034. doi:10.1242/dev.156034
67. Osborn, T.C., Pires, J.C., Birchler, J.A., Auger, D.L., Chen, Z.J., Lee, H.S., Comai, L., Madlung, A., Doerge, R.W., Colot, V., Martienssen, R.A., 2003. Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19, 141-147. https://doi.org/10.1016/S0168-9525(03)00015-5
68. Parida, B.P., Misra, B.B., 2015. Is a plant's ploidy status reflected in its metabolome? PostDoc Journal 3, 4.
69. Parisod, C., Holderegger, R., Brochmann, C., 2010. Evolutionary consequences of autopolyploidy. New Phytol. 186, 5-17. https://doi.org/10.1111/j.1469-8137.2009.03142.x
70. Pathak, M.R., Abido, M.S., 2014. The role of biotechnology in the conservation of biodiversity. J. Exp. Biol. Agri. Sci. 2, 352-363.
71. Ramsey, J., Schemske, D.W., 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 29, 467-501. https://doi.org/10.1146/annurev.ecolsys.29.1.467
72. Ramsey, J., Schemske, D.W., 2002. Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33, 589-639. https://doi.org/10.1146/annurev.ecolsys.33.010802.150437
73. Ranney, T.G., 2006. Polyploidy: from evolution to new plant development. Combined Proceedings International Plant Propagators’ Society 56, 137-146.
74. Rauf, S., Khan, I.A., Khan, F.A., 2006. Colchicine-induced tetraploidy and changes in allele frequencies in colchicine-treated populations of diploids assessed with RAPD markers in Gossypium arboretum L. Turk. J. Biol. 30, 93-100.
75. Regalado, J.J., Carmona-Martín, E., Castro, P., Moreno, R., Gil, J., Encina, C.L., 2015. Study of the somaclonal variation produced by different methods of polyploidization in Asparagus officinalis L. Plant Cell Tiss Organ Cult. 122, 31-44. https://doi.org/10.1007/s11240-015-0747-x
76. Richardson, D.M., Petr, P., Rejmánek, M., Barbour, M.G., Panetta, D., West, C.J., 2000. Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib. 6, 93-107. https://doi.org/10.1046/j.1472-4642.2000.00083.x
77. Rodriguez, M., Cervigni, G., Quarin, C., Ortiz, J., 2012. Frequencies and variation in cytosine methylation patterns in diploid and tetraploid cytotypes of Paspalum notatum. Biol Plant 56, 276-282. https://doi.org/10.1007/s10535-012-0087-1
78. Salma, U., Kundu, S., Mandal, N., 2017. Artificial polyploidy in medicinal plants: advancement in the last two decades and impending prospects. J. Crop. Sci. Biotech. 20, 9-19. https://doi.org/10.1007/s12892-016-0080-1
79. Schippmann, U., Leaman, D., Cunningham, A.B., 2006. A comparison of cultivation and wild collection of medicinal and aromatic plants under sustainability aspects. In: Bogers, R.J., Crakerand, L.E., Lange, D., (Eds.), Medicinal and aromatic plants: agricultural, commercial, ecological, legal, pharmacological and social aspects. Springer, Dordrecht, The Netherlands. pp 75-95
80. Shahriari-Ahmadi, F., Dehghan, E., Farsi, M., Azizi, M., 2008. Tetraploid induction of Hyoscyamus muticus L. using colchicine treatment. Pak. J. Biol. Sci. 11, 2653-2659. https://doi.org/10.3923/pjbs.2008.2653.2659
81. Silvarolla, M.B., Mazzafera, P., Lima, M.M.A, de Medina Filho, H.P., Fazuoli, L.C., 1999. Ploidy level and caffeine content in leaves of Coffea. Scientia Agricola 56: 661–663.
82. Smith, M.K., Hamill, S.D., Gogel, B.J., Severn-Ellis, A., 2004. Ginger (Zingiber officinale) autotetraploids with improved processing quality produced by an in vitro colchicine treatment. Aust. J. Exp. Agric. 44, 1065-1072. https://doi.org/10.1071/EA03204
83. Soltis, D.E, Soltis, P.S., Schemske, D.W., Hancock, J.F., Thompson, J.N. Husband, B.C., Judd, W.S., 2007. Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon. 56:13–30.
84. Srivastava, S., Lavania, U.C., 1990. Meiotic Regularization, Restoration of Seed Fertility and Alkaloid Content in the Induced Autotetraploids of Hyoscyamus albus L. Plant Breeding 104: 160-166 https://doi.org/10.1111/j.14390523.1990.tb00418.x
85. Srivastava, S., Lavania U.C., Sybenga, J., 1992. Genetic variation in meiotic behavior and fertilily in tetraploid Hyoscyamus muticus: correlation with diploid meiotic. Heredity 68: 231-239.
86. Stebbins, G.L., 1971. Chromosomal evolution in higher plants. Arnold, London, UK.
87. Tal, M., 1980. Physiology of polyploids. In: Lewis, W.H., (ed.) Polyploidy: Biological Relevance. New York: Plenum Press. 61-75.
88. Tan, F.Q., Tu, H., Liang, W.J., Long, J.M., Wu, X.M., Zhang, H.Y., Guo, W.W., 2015. Comparative metabolic and transcriptional analysis of a doubled diploid and its diploid citrus rootstock (C. junos cv. Ziyang xiangcheng) suggests its potential value for stress resistance improvement. BMC Plant Biology. 15:89. https://doi.org/10.1186/s12870-015-0450-4
89. Tan, F.Q., Tu, H., Wang, R., Wu, X.M., Xie, K.D., Chen, J.J., Zhang, H.Y., Xu, J., Guo, W.W., 2017. Metabolic adaptation following genome doubling in citrus doubled diploids revealed by non-targeted metabolomics. Metabolomics. 13:143. DOI 10.1007/s11306-017-1276-x
90. Thong-on, W., Arimatsu, P., Pitiporn, S., Soonthornchareonnon, N., Prathanturarug, S., 2014. Field evaluation of in vitro-induced tetraploid and diploid Centella asiatica (L.). Urban J. Nat. Med. 68, 267-273. https://doi.org/10.1007/s11418-013-0761-4
91. Urwin, N.A.R., Horsnell, J., Moon, T., 2007. Generation and characterisation of colchicine-induced autotetraploid Lavandula angustifolia. Euphytica 156, 257–266. https://doi.org/10.1007/s10681-007-9373-y
92. Vieira, D.D.S.S., Emiliani, G., Michelozzid, M., Centritto, M., Luro, F., Morillonf, R., Loreto, F., Gesteira, A., Masertia, B., 2016. Polyploidization alters constitutive content of volatile organic compounds (VOC) and improves membrane stability under water deficit in Volkamer lemon (Citrus limonia Osb.) leaves. Environ. Exp. Bot. 126, 1–9. https://doi.org/10.1016/j.envexpbot.2016.02.010
93. Walbot, V., Cullis, C., 1985. Rapid genomic change in higher plants. Annu. Rev. Plant. Physiol. 36, 987-396. https://doi.org/10.1146/annurev.pp.36.060185.002055
94. Wallaart, T., Pras, N., Quax, W.J., 1999. Seasonal variations of artemisinin and its biosynthetic precursors in tetraploid Artemisia annua plants compared with the diploid wild-type. Planta Med. 65, 723-728. https://doi.org/10.1055/s-2000-11115
95. Wendel, J.F., Lisch, D., Hu, G., Mason, A.S., 2018. The long and short of doubling down: polyploidy, epigenetics, and the temporal dynamics of genome fractionation. Curr. Opin. Genet. Dev. 49, 1-7. https://doi.org/10.1016/j.gde.2018.01.004
96. Widoretno, W., 2016. In vitro induction and characterization of tetraploid Patchouli (Pogostemon cablin Benth.) plant. Plant Cell Tiss Organ Cult. 125, 261–267. https://doi.org/10.1007/s11240-016-0946-0
97. Wildermuth, M.C., 2010. Modulation of host nuclear ploidy: a common plant biotroph mechanism. Curr. Opin. Plant Biol. 13, 449-458. https://doi.org/10.1016/j.pbi.2010.05.005
98. Wohlmuth, H., Leach, D.N., Smith, M.K., Myers, S.P., 2005. Gingerol content of diploid and tetraploid clones of ginger (Zingiber officinale Roscoe). J. Agric. Food Chem. 53:5772-5778. https://doi.org/10.1021/jf050435b
99. Wood, T., Takebayashi, N., Barker, M.S., Mayrose, I., Greenspoon, P.B., Rieseberg, L.H., 2009. The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA 106:13875-13879. https://doi.org/10.1073/pnas.0811575106
100. Xing, S.H., Guo, X.B., Wang, Q., Pan, Q.F., Tian, Y.S., Liu, P., Zhao, J.Y., Wang, G.F., Sun, X.F., Tang, K.X., 2011. Induction and flow cytometry identification of tetraploids from seed-derived explants through colchicine treatments in Catharanthus roseus (L.) G. Don. J. Biomed. Biotechnol. 2011, 793198. https://doi.org/10.1155/2011/793198.
101. Xu, C., Tang, Y, Chen, R., Liang, C., Liu, X., Wu, C., Yang, Y., Yang, D., Wu, H., 2014. A comparative study of bioactive secondary metabolite production in diploid and tetraploid Echinacea purpurea (L.) Moench. Plant Cell Tiss Organ Cult. 116, 323-332. https://doi.org/10.1007/s11240-013-0406-z
102. Yadav, A.K., Singh, S., Yadav, S., Dhyani, D., Bhardwaj, G., Sharma, A., Singh, B., 2013. Induction and morpho-chemical characterization of Stevia rebaudiana colchiploids. Indian J. Agr. Sc. 83, 159-165.
103. Yan, H.J., Xiong, Y., Zhang, H.Y., He, M.L. 2016. In vitro induction and morphological characteristics of octoploid plants in Pogostemon cablin. Breed. Sci. 66, 169-174. https://dx.doi.org/10.1270%2Fjsbbs.66.169
104. Yang, X., Ye, C.Y., Cheng, Z.M., Tschaplinski, T.J., Wullschleger, S.D., Yin, W., Xia, X., Tuskan, G.A., 2011. Genomic aspects of research involving polyploid plants. Plant Cell Tiss Organ Cult. 104: 387-397. https://doi.org/10.1007/s11240-010-9826-1
105. Zhang, X.Y., Hu, C.G., Yao, J.L., 2010. Tetraploidization of diploid Dioscorea results in activation of the antioxidant defense system and increased heat tolerance. J. Plant Physiol. 167, 88-94. https://doi.org/10.1016/j.jplph.2009.07.006