Abstract
Modern powerful techniques in plant biotechnology have been developed in lilies (Lilium spp., Liliaceae) to propagate, improve and make new phenotypes. Reliable in vitro culture methods are available to multiply lilies rapidly and shorten breeding programs. Lilium is also an ideal model plant to study in vitro pollination and embryo rescue methods. Although lilies are recalcitrant to genetic manipulation, superior genotypes are developed with improved flower colour and form, disease resistance and year round forcing ability. Different DNA molecular markers have been developed for rapid indirect selection, genetic diversity evaluation, mutation detection and construction of Lilium linkage map. Some disease resistance-QTLs are already mapped on the Lilium linkage map. This review presents latest information on in vitro propagation, genetic engineering and molecular advances made in lily.
Similar content being viewed by others
Abbreviations
- 2,4-D:
-
2,4-dichlorophenoxyacetic acid
- 2ip:
-
2-isopentenyladenine
- ABA:
-
Abscisic acid
- AC:
-
Activated charcoal
- ACC:
-
1-aminocyclopropane-1-carboxylic acid
- AFLP:
-
Amplified fragment length polymorphism
- AsA:
-
l-ascorbic acid
- AVG:
-
Aminoethoxyvinyl glycine
- B5 :
-
Gamborg
- BA:
-
6-benzylaminopurine
- CMV:
-
Cucumber mosaic virus
- CPPU:
-
N-(2-chloro- 4-pyridyl)-N’-phenylurea
- DArT:
-
Diversity arrays technology
- DW:
-
Dry weight
- ELS:
-
Embryo like structure
- EST-SSRs:
-
Expressed sequence tag derived-SSRs
- FISH:
-
Fluorescence in situ hybridization
- FW:
-
Fresh weight
- GA3 :
-
Gibberellic acid
- GISH:
-
Genomic in situ hybridization
- GLDH:
-
l-galactono-1, 4-lactone dehydrogenase
- IAA:
-
Indole-3-acetic acid
- IBA:
-
Indole-3-butyric acid
- ISSR:
-
Inter simple sequence repeat
- Kn:
-
Kinetin
- Llccs:
-
Capsanthin-capsorubin synthase
- LMoV :
-
Lily mottle virus
- LS:
-
Linsmaier and Skoog
- MeJA:
-
Methyl jasmonic acid
- MS:
-
Murashige and Skoog
- N6 :
-
Chu
- NAA:
-
1-naphthaleneacetic acid
- NBS:
-
Nucleotide binding site
- NN:
-
Nitsch and Nitsch
- NOD:
-
Meristematic nodular calli
- PGR:
-
Plant growth regulator
- RAPD:
-
Randomly amplified polymorphic DNA
- ROS:
-
Reactive oxygen species
- SE:
-
Somatic embryogenesis
- TDZ:
-
Thidiazuron
- TIBA:
-
2,3,5-triiodobenzoic acid
- tTCL:
-
Transverse thin cell layer
References
Agius F, Gonzalez-Lamothe R, Caballero JL, Munoz-Blanco J, Botella MA, Valpuesta V (2003) Engineering increased vitamin C levels in plants by overexpression of a d-galacturonic acid reductase. Nat Biotechnol 21:177–181
Aguettaz P, Paffen A, Delvallee I, Van der Linde P, De Klerk GJ (1990) The development of dormancy in bulblets of Lilium speciosum generated in vitro: 1. The effects of culture conditions. Plant Cell Tissue Organ Cult 22:167–172
Anderson NO (1986) The distribution of the genus Lilium with reference to its evaluation. Lily Yearbook North Am Lily Soc 42:1–18
Arzate-Fernandez AM, Nakazaki T, Okumoto Y, Tanasika T (1997a) Efficient callus induction and plant regeneration from filaments with anther in lily (Lilium longiflorum Thunb.). Plant Cell Rep 16:836–840
Arzate-Fernandez AM, Nakazaki T, Yamagata H, Tanisaka T (1997b) Production of doubled-haploid plants from Lilium longiflorum Thunb. anther culture. Plant Sci 123:179–187
Ault JR, Siqueira SS (2008) Morphogenetic response of Lilium michiganense to four auxin-type plant growth regulators in vitro. HortScience 43:1922–1924
Azadi P, Khosh-Khui M (2007) Micropropagation of Lilium ledebourii (Baker) Boiss. as affected by plant growth regulator, sucrose concentration, harvesting season and cold treatments. Electron J Biotechnol 10:582–591
Azadi P, Chin DP, Kuroda K, Khan RS, Mii M (2010a) Macro elements in inoculation and co-cultivation medium strongly affect the efficiency of Agrobacterium-mediated transformation in Lilium. Plant Cell Tissue Organ Cult 101:201–209
Azadi P, Otang NV, Chin DP, Nakamura I, Fujisawa M, Harada H, Misawa N, Mii M (2010b) Metabolic engineering of Lilium × formolongi using multiple genes of the carotenoid biosynthesis pathway. Plant Biotechnol Rep 4:269–280
Azadi P, Otang NV, Supaporn H, Khan RS, Chin DP, Nakamura I, Mii M (2011) Increased resistance to cucumber mosaic virus (CMV) in Lilium transformed with a defective CMV replicase gene. Biotechnol Lett 33:1249–1255
Azadi P, Ntui VO, Chin DP, Mii M (2013) Genetic transformation and metabolic engineering of Lilium., Bulbous Plants: Biotechnology CRC Press, Boca Raton, pp 197–213
Bacchetta L, Remotti PC, Bernardini C, Saccardo F (2003) Adventitious shoot regeneration from leaf explants and stem nodes of Lilium. Plant Cell Tissue Organ Cult 74:37–44
Bakhshaie M, Babalar M, Mirmasoumi M, Khalighi A (2010a) Effects of light, sucrose, and cytokinins on somatic embryogenesis in Lilium ledebourii (Baker) Bioss. via transverse thin cell-layer cultures of bulblet microscales. J Hortic Sci Biotechnol 85:491–496
Bakhshaie M, Babalar M, Mirmasoumi M, Khalighi A (2010b) Somatic embryogenesis and plant regeneration of Lilium ledebourii (Baker) Boiss., an endangered species. Plant Cell Tissue Organ Cult 102:229–235
Barba-Gonzalez R, Lokker AC, Lim KB, Ramanna MS, Van Tuyl JM (2004) Use of 2n gametes for the production of sexual polyploids from sterile Oriental × Asiatic hybrids of lilies (Lilium). Theor Appl Genet 109:1125–1132
Barba-Gonzalez R, Miller CT, Ramanna MS, Van Tuyl JM (2006) Nitrous oxide (N2O) induces 2n gametes in sterile F1 hybrids between Oriental × Asiatic lily (Lilium) hybrids and leads to intergenomic recombination. Euphytica 148:303–309
Benedito VA, Kronenburg-van der Ven BCE, Van Tuyl JM, Angenent GC, Krens FA (2005) Transformation of Lilium longiflorum via particle bombardment and generation of herbicide-resistant plants. Crop Breed Appl Biotechnol 5:259–264
Bi WL, Yin ZF, Guo L, Chen L, Pan C, Wang QC (2015) Plant regeneration from shoot regrowth and de novo embryo-like structures from cryopreserved shoot tips of Lilium spp. In vitro Cell Dev Biol Plant 51:390–398
Bonnier FJM, Van Tuyl JM (1997) Long term in vitro storage of lily: effects of temperature and concentration of nutrients and sucrose. Plant Cell Tissue Organ Cult 49:81–87
Bouman H, De Klerk GJ (1990) Cryopreservation of lily meristems. Acta Hortic 266:331–338
Bouman H, Tiekstra A, Petutschnig E, Homan M, Schreurs R (2003) Cryopreservation of Lilium species and cultivars. Acta Hortic 612:147–154
Bui VL, Nhut DT, Van Tran Thanh K (1999) Plant production via shoot regeneration from thin cell layer pseudo-bulblet explants of Lilium longiflorum in vitro. C R Acad Sci Paris 322:303–310
Cardoso JC, Teixeira da Silva JA (2013) Gerbera micropropagation. Biotechnol Adv 31:1344–1357
Chen H, Chen XL, Chen LQ, Lu XX (2007) Cryopreservation of shoot tips from in vitro plants of cut flower of lily (Lilium L.) by vitrification method. J Plant Genet Resour 8:170–173
Chen XL, Li JH, Xin X, Zhang ZE, Xin PP, Lu XX (2011) Cryopreservation of in vitro-grown apical meristems of Lilium by droplet-vitrification. South Afr J Bot 77:397–403
Chi HS (2000) Interspecific crosses of lily by in vitro pollinated ovules. Bot Bull Acad Sin 41:143–149
Chinestra SC, Curvetto NR, Marinangeli PA (2015) Production of virus-free plants of Lilium spp. from bulbs obtained in vitro and ex vitro. Sci Hortic 194:304–312
Chu CC, Wang CC, Sun CS, Hsu C, Yin KC, Chu CY, Bi FY (1975) Establishment of an efficient medium for anther culture of rice through comparative experiments on the nitrogen sources. Sci Sin 18:659–668
Chung MY, Chung JD, Ramanna M, Van Tuyl JM, Lim KB (2013) Production of polyploids and unreduced gametes in Lilium auratum × L. henryi hybrid. Int J Biol Sci 9:693–701
De Jeu MJ (2000) In vitro techniques for ornamental breeding. Acta Hortic 508:55–60
De Jong PC (1974) Some notes on the evolution of lilies. Lily Yearbook North Am Lily Soc 27:23–28
De Verna JW, Myers JR, Collins GB (1987) Bypassing prefertilization barriers to hybridization in Nicotiana using in vitro pollination and fertilization. Theor Appl Genet 73:665–671
Dhyani A, Sharma G, Nautiyal BP, Nautiyal MC (2014) Propagation and conservation of Lilium polyphyllum D. Don ex Royle. J Appl Res Med Aromat Plants 1:144–147
Dong W, Mao YF, Li W (2007) Factors influencing T-DNA transferring into pollen of lily in vitro. Russ J Plant Physiol 54:420–425
Du F, Jiang J, Jia H, Zhao XY, Wang WH, Gao QK, Mao WH, Wu Y, Zhang L, Grierson D, Xia YP, Gao ZS (2015a) Selection of generally applicable SSR markers for evaluation of genetic diversity and identity in Lilium. Biochem Syst Ecol 61:278–285
Du F, Wu Y, Zhang L, Li XW, Zhao XY, Wang WH, Gao ZS, Xia YP (2015b) De novo assembled transcriptome analysis and SSR marker development of a mixture of six tissues from Lilium Oriental hybrid ‘Sorbonne’. Plant Mol Biol Rep 33:281–293
FloraHolland, Facts and figures (2014) https://www.floraholland.com/media/3949227/Kengetallen-2014-Engels.pdf. Accessed 29 Feb 2016
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soyabean root cells. Exp Cell Res 50:151–158
Godo T, Matsui K, Kida T, Mii M (1996) Effect of sugar type on the efficiency of plant regeneration form protoplasts isolated from shoot tip-derived meristematic nodular cell clumps of Lilium × formolongi hort. Plant Cell Rep 15:401–404
Godo T, Kobayashi K, Tagami T, Matsui K, Kida T (1998) In vitro propagation utilizing suspension cultures of meristematic nodular cell clumps and chromosome stability of Lilium × formolongi hort. Sci Hortic 72:193–202
GRIN (2016) (Germplasm Resources Information Network). Available at http://www.ars-grin.gov. Accessed 29 Feb 2016
Guo W, Jeong J, Kim Z, Wang R, Kim E, Kim S (2011) Genetic diversity of Lilium tsingtauense in China and Korea revealed by ISSR markers and morphological characters. Biochem Syst Ecol 39:352–360
Hamid B, Kim JH (2011) Cross compatibility between Lilium × fomolongi group and Lilium brownii. Afr J Agric Res 6:968–977
Han DS, Niimi Y, Nakano M (1997) Regeneration of haploid plants from anther cultures of the Asiatic hybrid lily ‘Connecticut King’. Plant Cell Tissue Organ Cult 47:153–158
Han BH, Yu HJ, Yae BW, Paek KY (2004) In vitro micropropagation of Lilium longiflorum ‘Georgia’ by shoot formation as influenced by addition of liquid medium. Sci Hortic 103:39–49
Han BH, Yae BW, Yu HJ, Peak KY (2005) Improvement of in vitro micropropagation of Lilium Oriental hybrid ‘Casablanca’ by the formation of shoots with abnormally swollen basal plates. Sci Hortic 103:351–359
Han DS, Niimi Y, Kimura S (2006) Localization of lily symptomless virus and cucumber mosaic virus in anther- and filament-derived calli and effect of callus culture duration on virus-free bulblet production in Lilium × ‘Enchantment’. Plant Cell Tissue Organ Cult 87:211–217
Harlan JR, De Wet JMJ (1975) On Ö. Winge and a prayer: the origins of polyploidy. Bot Rev 41:361–390
Haruki K, Hosoki T, Nako Y (1998) Tracing the parentages of some Oriental hybrid lily cultivars by PCR–RFLP analysis. J Jpn Soc Hortic Sci 67:352–359
Higgins WS, Stimart DP (1990) Influence of in vitro generation temperature and post-in vitro cold storage duration on growth response of Lilium longiflorum bulblets. J Am Soc Hort Sci 115:930–933
Ho CW, Jian WT, Lai HC (2006) Plant regeneration via somatic embryogenesis from suspension cell cultures of Lilium × formolongi Hort. using a bioreactor system. In vitro Cell Dev Biol Plant 42:240–246
Horita M, Morohashi H, Komai F (2002) Regeneration of flowering plants from difficile lily protoplasts by means of a nurse culture. Planta 215:880–884
Horita M, Morohashi H, Komai F (2003) Production of fertile somatic hybrid plants between Oriental hybrid lily and Lilium × formolongi. Planta 217:597–601
Horning ME, Maloney SC, Webster MS (2003) Isolation and characterization of variable microsatellite loci in Lilium philadelphicum (Liliaceae). Mol Ecol Notes 3:412–413
Hoshi Y, Kondo M, Mori S, Adachi Y, Nakano M, Kobayashi H (2004) Production of transgenic lily plants by Agrobacterium-mediated transformation. Plant Cell Rep 22:359–364
Ikeda N, Niimi Y, Han DS (2003) Production of seedlings from ovules excised at the zygote stage in Lilium spp. Plant Cell Tissue Organ Cult 73:159–166
Ishimori T, Niimi Y, Han DS (2007) Benzyladenine and low temperature promote phase transition from juvenile to vegetative adult in bulblets of Lilium × formolongi ‘White Aga’ cultured in vitro. Plant Cell Tissue Organ Cult 88:313–318
Ishimori T, Niimi Y, Han DS (2009) In vitro flowering of Lilium rubellum Baker. Sci Hortic 120:246–249
Ivanova A, Gerets M, De Klerk GJ, Van Onckelen H, Atanassov A, Djilianov D (1994) Endogenous abscisic acid and dormancy of in vitro regenerated lily bulblets. Biotechnol Biotechnol Equip 8:30–35
Jasik J, De Klerk GJ (2006) Effect of methyl jasmonate on morphology and dormancy development in lily bulblets regenerated in vitro. J Plant Growth Regul 25:45–51
Jeknic Z, Morre JT, Jeknic S, Jevremovic S, Subotic A, Chen THH (2012) Cloning and functional characterization of a gene for capsanthin-capsorubin synthase from tiger lily (Lilium lancifolium Thunb. ‘Splendens’). Plant Cell Physiol 53:1899–1912
Jin S, Wang J, Wang X, Sun D, Li G, Genovesi AD, Liu S (2014) Direct and indirect shoot and bulblet regeneration from cultured leaf explants of Lilium pumilum, an endangered species. In vitro Cell Dev Biol Plant 50:69–75
Joshi SK, Dhar U (2009) In vitro propagation from axenic explants of Lilium oxypetalum (D. Don) Baker, an endemic bulbous plant of high altitude Himalaya. Acta Physiol Plant 31:833–838
Kamo K (2014) Long term, transgene expression in Lilium longiflorum ‘Nellie White’ grown outdoors and in the greenhouse. Sci Hortic 167:158–163
Kamo K, Han BH (2008) Biolistic-mediated transformation of Lilium longifiorum cv. Nellie White. HortScience 43:1864–1869
Kapoor R, Kumar S, Kanwar JK (2008) Bulblet regeneration from ex vitro root explant in lily hybrids. Hort Sci 35:107–112
Kapoor R, Kumar S, Kanwar JK (2009) Bulblet production from node explant grown in vitro in hybrid lilies. Int J Plant Prod 3:1–6
Karalija E, Parić A, Muratović E (2013) Biochemical status of in vitro regenerated Lilium bosniacum and Lilium cattaniae plantlets. Cent Eur J Biol 8:912–920
Khan N, Barba-Gonzalez R, Ramanna MS, Arens P, Visser RGF, Van Tuyl JM (2010) Relevance of unilateral and bilateral sexual polyploidization in relation to intergenomic recombination and introgression in Lilium species hybrids. Euphytica 171:157–173
Kim KS, Davelaar E, De Klerk GJ (1994) Abscisic acid controls dormancy development and bulb formation in lily plantlets regenerated in vitro. Physiol Plant 90:59–64
Kim HH, Yoon JW, Park YE, Cho EG, Sohn JK, Kim TS, Engelmann F (2006) Cryopreservation of potato cultivated varieties and wild species: critical factors in droplet vitrification. Cryo Letters 27:223–234
Kim SS, Shin DI, Park HS (2007) Transient β-glucuronidase expression in lily (Lilium longiflorum L.) pollen via wounding-assisted Agrobacterium-mediated transformation. Biotechnol Lett 29:965–969
Kim K, Hwang YJ, Lee SC, Yang TJ, Lim KB (2015) The complete chloroplast genome sequence of Lilium hansonii Leichtlin ex D.D.T. Moore. Mitochondrial DNA A DNA MappSeq Anal 27(5):3678–3690. doi:10.3109/19401736.2015.1079852
Komai F, Morohashi H, Horita M (2006) Application of nurse culture for plant regeneration from protoplasts of Lilium japonicum Thunb. In vitro Cell Dev Biol Plant 42:252–255
Kumar S, Kashyap M, Sharma DR (2005) In vitro regeneration and bulblet growth from lily bulbscale explants as affected by retardants, sucrose and irradiance. Biol Plant 49:629–632
Kumar S, Awasthi V, Kanwar JK (2007) Influence of growth regulators and nitrogenous compounds on in vitro bulblet formation and growth in Oriental lily. Hort Sci 34:77–83
Langens-Gerrits MM, Albers M, De Klerk GJ (1998) Hot-water treatment before tissue culture reduces initial contamination in Lilium and Acer. Plant Cell Tissue Organ Cult 52:75–77
Langens-Gerrits MM, Nashimoto S, Croes AF, De Klerk GJ (2001) Development of dormancy in different lily genotypes regenerated in vitro. Plant Growth Regul 34:215–222
Langens-Gerrits MM, Miller WBM, Croes AF, De Klerk GJ (2003) Effect of low temperature on dormancy breaking and growth after planting in lily bulblets regenerated in vitro. Plant Growth Regul 40:267–275
Lee SI, Park KC, Song YS, Son JH, Kwon SJ, Na JK, Kim JH, Kim NS (2011) Development of expressed sequence tag derived-simple sequence repeats in the genus Lilium. Genes Genom 33:727–733
Leshem B, Lilien-Kipnis H, Steinitz B (1982) The effect of light and of explant orientation on the regeneration and subsequent growth of bulblets on Lilium longiflorum Thunb. bulb-scale sections cultured in vitro. Sci Hortic 17:129–136
Li H, Liu D, He H, Zhang N, Ge F, Chen C (2014) Molecular cloning of a 14-3-3 protein gene from Lilium regale Wilson and overexpression of this gene in tobacco increased resistance to pathogenic fungi. Sci Hortic 168:9–16
Lian ML, Murthy HN, Paek KY (2002) Effects of light emitting diodes (LEDs) on the in vitro induction and growth of bulblets of Lilium Oriental hybrid ‘Pesaro’. Sci Hortic 94:365–370
Lian ML, Chakrabarty D, Paek KY (2003a) Bulblet formation from bulbscale segments of Lilium using bioreactor system. Biol Plant 46:199–202
Lian ML, Chakrabarty D, Paek KY (2003b) Growth of Lilium Oriental hybrid ‘Casablanca’ bulblet using bioreactor culture. Sci Hortic 97:41–48
Lian ML, Murthy HN, Paek KY (2003c) Photoautotrophic culture conditions and photosynthetic photon flux influence growth of Lilium bulblets in vitro. In vitro Cell Dev Biol Plant 39:532–535
Lim KB, Van Tuyl JM (2006) Lily, Lilium hybrids. In: Anderson NO (ed) Flower breeding and genetics-issues, challenges and opportunities for the 21st century. Springer, Dordrecht, pp 517–537
Lim KB, Chung JD, Van Kronenburg BCE, Ramanna MS, De Jong JH, Van Tuyl JM (2000) Introgression of Lilium rubellum Baker chromosomes into L. longiflorum Thunb.: a genome painting study of the F1 hybrid, BC1 and BC2 progenies. Chromosome Res 8:119–125
Lim KB, Ramanna MS, Jacobsen E, Van Tuyl JM (2003) Evaluation of BC2 progenies derived from 3x–2x to 3x–4x crosses of Lilium hybrids: a GISH analysis. Theor Appl Genet 106:568–574
Lim KB, Shen TM, Barba-Gonzalez R, Ramana MS, Van Tuyl JM (2004) Occurrence of SDR 2n-gametes in Lilium hybrids. Breed Sci 54:13–18
Lim KB, Barba-Gonzalez R, Zhou S, Ramanna MS, Van Tuyl JM (2005) Meiotic polyploidization with homoeologous recombination induced by caffeine treatment in interspecific lily hybrids. Korean J Genet 27:219–226
LingFei X, FengWang M, Dong L (2009) Plant regeneration from in vitro cultured leaves of Lanzhou lily (Lilium davidii var. unicolor). Sci Hortic 119:458–461
Linsmaier EM, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18:100–127
Liu X, Yang G (2012) Adventitious shoot regeneration of Oriental lily (Lilium orientalis) and genetic stability evaluation based on ISSR marker variation. In vitro Cell Dev Biol Plant 48:172–179
Liu J, Zhang J, Xu B, Jia C, Zhang J, Tan G, Jin Z (2011) Regeneration and production of transgenic Lilium longiflorum via Agrobacterium tumefaciens. In vitro Cell Dev Biol Plant 47:348–356
Lokker AC, Barba-Gonzalez R, Lim KB, Ramanna MS, Van Tuyl JM (2005) Genotypic and environmental variation in production of 2n-gametes of Oriental × Asiatic lily hybrids. Acta Hortic 673:453–456
Matsumoto T, Sakai A, Yamada K (1995) Cryopreservation of in vitro-grown apical meristems of lily by vitrification. Plant Cell Tissue Organ Cult 41:237–241
Mii M, Yuzawa Y, Suetomi H, Motegi T, Godo T (1994) Fertile plant regeneration from protoplasts of a seed-propagated cultivar of Lilium × formolongi by utilizing meristematic nodular cell clumps. Plant Sci 100:221–226
Ming S, Xiao-fan L, Ying K, Jin-fang S, Qi-xiang Z (2012) Polyploidy induction of three Lilium species endemic to china (Lilium pumilum, L. Sargentiae, L. Tsingtauense). Acta Hortic 935:83–90
Mirmasoumi M, Bakhshaie M (2015) Effects of liquid, temporary immersion bioreactor and solid culture systems on micropropagation of Lilium ledebourii via bulblet microscales—an endangered valuable plant with ornamental potential. Prog Biol Sci 5:169–180
Mirmasoumi M, Azadi P, Sharafi A, Ntui VO, Mii M (2013) Simple protocol for plant regeneration of Lilium ledebourii using transverse thin cell layer. Prog Biol Sci 3:117–122
Misra P, Kochhar S (2008) Acclimatization of in vitro-raised Asiatic hybrid lily plants in subtropical climate and associated changes in stress proteins and antioxidant enzymes. J Plant Biochem Biotechnol 17:45–50
Misra P, Pandey V, Kochhar S (2010) Study of antioxidant enzymes activity during organogenesis and in vitro propagation of Asiatic hybrid lily. J Plant Biochem Biotechnol 19:119–122
Mojtahedi N, Koobaz P, Fathi M, Dabirashrafi O, Azadi P, Khosravi S (2014) Maturating, enlarging and breaking dormancy of in vitro Lilium bulblets. Int J Hortic Sci Technol 1:101–109
Mori S, Adachi Y, Horimoto S, Suzuki S, Nakano M (2005) Callus formation and plant regeneration in various Lilium species and cultivars. In vitro Cell Dev Biol Plant 41:783–788
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Naing AH, Yun H, Lucidos J, Hwang YJ, Kim CK, Ahn BJ, Lim KB (2014) Plant regeneration through various explants of Lilium longiflorum hybrid ‘Bright Tower’ and determination of ploidy level of regenerated plants. Plant Biosyst 148:191–199
Nakano M, Sakakibara T, Suzuki S, Saito H (2000) Decrease in the regeneration potential of long-term cell suspension cultures of Lilium formosanum Wallace and its restoration by the auxin transport inhibitor, 2,3,5-triiodobenzoic acid. Plant Sci 158:129–137
Nakano M, Nakatsuka A, Nakayama M, Koshioka M, Yamagishi M (2005) Mapping of quantitative trait loci for carotenoid pigmentation in flower tepals of Asiatic hybrid lily. Sci Hortic 104:57–64
Nhut DT (1998) Micropropagation of lily (Lilium longiflorum) via in vitro stem node and pseudo-bulblet culture. Plant Cell Rep 17:913–916
Nhut DT (2003) The control of in vitro direct main stem formation of Lilium longiflorum derived from receptacle culture, and rapid propagation by using in vitro stem nodes. Plant Growth Regul 40:179–184
Nhut DT, Bui VL, Tanaka M, Van Tran Thanh K (2001a) Shoot induction and plant regeneration from receptacle tissues of Lilium longiflorum. Sci Hortic 87:131–138
Nhut DT, Le BV, Fukai S, Tanaka M, Van Tran Thanh K (2001b) Effects of activated charcoal, explant size, explant position and sucrose concentration on plant and shoot regeneration of Lilium longiflorum via young stem culture. Plant Growth Regul 33:59–65
Nhut DT, Le BV, Teixeira da Silva JA, Aswath CR (2001c) Thin cell layer culture system in Lilium: regeneration and transformation perspectives. In vitro Cell Dev Biol Plant 37:516–523
Nhut DT, Le BV, Van Tran Thanh K (2001d) Manipulation of the morphogenetic pathways of Lilium longiflorum transverse thin cell layer explants by auxin and cytokinin. In vitro Cell Dev Biol Plant 37:44–49
Nhut DT, Le BV, Minh NT, Teixeira da Silva JA, Fukai S, Tanaka M, Van Tran Thanh K (2002) Somatic embryogenesis through pseudo-bulblet transverse thin cell layer of Lilium longiflorum. Plant Growth Regul 37:193–198
Nhut DT, Hanh NTM, Tuan PQ, Nguyet LTM, Tram NTH, Chinh NC, Nguyen NH, Vinh DN (2006) Liquid culture as a positive condition to induce and enhance quality and quantity of somatic embryogenesis of Lilium longiflorum. Sci Hortic 110:93–97
Niimi Y, Onozawa T (1979) In vitro bulblet formation from leaf segments of lilies, especially Lilium rubellum Baker. Sci Hortic 11:379–389
Niimi Y, Nakano M, Goto M (1995) Comparison of seedling production among several embryo rescue techniques in Lilium formosanum Wallace. Plant Tissue Cult Lett 12:317–319
Niimi Y, Han DS, Fujisaki M (2001) Production of virus-free plantlets by anther culture of Lilium × ‘Enchantment’. Sci Hortic 90:325–334
Nishimura H, Atsumi S (2001) Breaking dormancy in micropropagated bulblets of Lilium japonicum using gibberlic acid4. J Japan Soc Hortic Sci 70:522–524
Nitsch JP, Nitsch C (1969) Haploid plants from pollen grains. Science 163:85–87
Novak FJ, Petru E (1981) Tissue culture propagation of Lilium hybrids. Sci Hortic 14:191–199
Nukui S, Kitamura S, Hioki T, Ootsuka H, Miyoshi K, Satou T, Takatori Y, Oomiya T, Okazaki K (2011) N2O induces mitotic polyploidization in anther somatic cells and restores fertility in sterile interspecific hybrid lilies. Breed Sci 61:327–337
Nunez de Caceres Gonzalez FF, Davey MR, Cancho Sanchez E, Wilson ZA (2015) Conferred resistance to Botrytis cinerea in Lilium by overexpression of the RCH10 chitinase gene. Plant Cell Rep 34:1201–1209
Obata Y, Niimi Y, Nakano M, Okazaki K, Miyajima I (2000) Interspecific hybrids between Lilium nobilissimum and L. regale produced via ovules-with-placental-tissue culture. Sci Hortic 84:191–204
Ogaki M, Furuichi Y, Kuroda K, Chin DP, Ogawa Y, Mii M (2008) Importance of co-cultivation medium pH for successful Agrobacterium-mediated transformation of Lilium × formolongi. Plant Cell Rep 27:699–705
Okazaki K, Nukui S, Ootuka H (2012) Application of nitrous oxide gas as a polyploidizing agent in tulip and lily breeding. Floric Ornam Biotechnol 6:39–43
Paek KY, Hahn EJ, Son SH (2001) Application of bioreactors for large-scale micropropagation systems of plants. In vitro Cell Dev Biol Plant 37:149–157
Pelkonen VP, Kauppi A (1999) The effect of light and auxins on the regeneration of lily (Lilium regale Wil.) cells by somatic embryogenesis and organogenesis. Int J Plant Sci 160:483–490
Priyadarshi S, Sen S (1992) A revised scheme for mass propagation of Easter lily. Plant Cell Tissue Organ Cult 30:193–197
Prosevicius J, Strikulyte L (2004) Interspecific hybridization and embryo rescue in breeding of lilies. Acta Univ Latv Biol 676:213–217
Qi Y, Lou Q, Quan Y, Liu Y, Wang Y (2013) Flower-specific expression of the Phalaenopsis flavonoid 3′,5′-hydoxylase modifies flower color pigmentation in Petunia and Lilium. Plant Cell Tissue Organ Cult 115:263–273
Qi Y, Du L, Quan Y, Tian F, Liu Y, Wang Y (2014) Agrobacterium-mediated transformation of embryogenic cell suspension cultures and plant regeneration in Lilium tenuifolium Oriental × trumpet ‘Robina’. Acta Physiol Plant 36:2047–2057
Qiu-Hua L, Bo H, Zheng T, Chao M, Ai-Nong G, Jing-Juan Y, Jun-Ping G (2008) Establishment of regeneration system and transformation of Zm401 gene in Lilium longiflorum × L. formosanum. Chin J Agric Biotechnol 5:113–119
Qu Y, Mok MC, Mok DWS, Stang JR (1988) Phenotypic and cytological variation among plants derived from anther cultures of Lilium longiflorum. In vitro Cell Dev Biol Plant 24:471–476
Robb SM (1957) The culture of excised tissue from bulb scales of Lilium speciosum Thun. J Exp Bot 8:348–352
Rout GR, Mohapatra A, Mohan Jain S (2006) Tissue culture of ornamental pot plant: a critical review on present scenario and future prospects. Biotechnol Adv 24:531–560
Saadon S, Zaccai M (2013) Lilium candidum bulblet and meristem development. In vitro Cell Dev Biol Plant 49:313–319
Sakazono S, Hiramatsu M, Watanabe M, Okubo H (2013) Development and characterization of microsatellite markers for Lilium longiflorum (Liliaceae). Appl Plant Sci 1:1300014
Scholten HJ, Pierik RLM (1998) Agar as a gelling agent: differential biological effects in vitro. Sci Hortic 77:109–116
Shahin A, Arens P, Van Heusden AW, Van Der Linden G, Van Kaauwen M, Khan N, Schouten HJ, Van De Weg WE, Visser RGF, Van Tuyl JM (2011) Genetic mapping in Lilium: mapping of major genes and quantitative trait loci for several ornamental traits and disease resistances. Plant Breed 130:372–382
Shahin A, Van Kaauwen M, Esselink D, Bargsten JW, Van Tuyl JM, Visser RGF, Arens P (2012) Generation and analysis of expressed sequence tags in the extreme large genomes Lilium and Tulipa. BMC Genom 13:640
Shahin A, Smulders MJM, Van Tuyl JM, Arens P, Bakker FT (2014) Using multi-locus allelic sequence data to estimate genetic divergence among four Lilium (Liliaceae) cultivars. Front Plant Sci 5:567
Shi S, Ma F, Li Y, Feng F, Shang Z (2012) Overexpression of l-galactono-1, 4-lactone dehydrogenase (GLDH) in Lanzhou lily (Lilium davidii var. unicolor) via particle bombardment-mediated transformation. In vitro Cell Dev Biol Plant 48:1–6
Simmonds JA, Cumming BG (1976) Propagation of Lilium hybrids. II. Production of plantlets from bulb-scale callus cultures for increased propagation rates. Sci Hortic 5:161–170
Stanilova MI, Ilcheva VP, Zagorska NA (1994) Morphogenetic potential and in vitro micropropagation of endangered plant species Leucojum aestivum L. and Lilium rhodopaeum Delip. Plant Cell Rep 13:451–453
Stebbins GL (1958) The inviability, weakness, and sterility of interspecific hybrids. Adv Genet 9:147–215
Straathof TP, Van Tuyl JM, Dekker B, Van Winden MJM, Sandbrink JM (1996) Genetic analysis of inheritance of partial resistance to Fusarium oxysporum in Asiatic hybrids of lily using RAPD markers. Acta Hortic 414:209–218
Supaibulwatana K, Mii M (1998) Induction of meristematic nodular calli from various explants of Lilium spp. and long term stability in plant regeneration ability and ploidy level of the calli. Plant Biotechnol 15:95–102
Takamura T, Miyajima I (1996) Colchicine induced tetraploids in yellow-flowered cyclamens and their characteristics. Sci Hortic 65:305–312
Takamura T, Lim KB, Van Tuyl JM (2002) Effect of a new compound on the mitotic polyploidization of Lilium longiflorum and Oriental hybrid lilies. Acta Hortic 572:37–42
Takayama S, Misawa M (1979) Differentiation in Lilium bulbscales grown in vitro. Effect of various cultural conditions. Physiol Plant 46:184–190
Takayama S, Misawa M (1980) Differentiation in Lilium bulbscales grown in vitro. Effects of activated charcoal, physiological age of bulbs and sucrose concentration on differentiation and scale leaf formation in vitro. Physiol Plant 48:121–125
Takayama S, Misawa M (1983) A scheme for mass propagation of Lilium in vitro. Sci Hortic 18:353–362
Tan XL, Cui GF, Zheng SX, Wang JH, Liu FH (2011) Effects of different in vitro pollination methods on capsule formation in Lilium hybridization. Southwest China J Agric Sci 24:270–274
Tang YP, Liu XQ, Wahiti Gituru R, Chen LQ (2010) Callus induction and plant regeneration from in vitro cultured leaves, petioles and scales of Lilium leucanthum (Baker) Baker. Biotechnol Biotechnol Equip 24:2071–2076
Tang N, Mo G, Van Tuyl JM, Arens P, Liu J, Tang D (2014) Genetic diversity and structure of Lilium pumilum DC. in southeast of Qinghai-Tibet plateau. Plant Syst Evol 300:1453–1464
Tanimoto S, Matsubara Y (1995) Stimulating effect of spermine on bulblet formation in bulb-scale segments of Lilium longiflorum. Plant Cell Rep 15:297–300
Teixeira da Silva JA, Dobránszki J (2013) Plant thin cell layers: a 40-year celebration. J Plant Growth Regul 113:149–161
Thakur R, Sood A, Nagar PK, Pandey S, Sobti RC, Ahuja PS (2006) Regulation of growth of Lilium plantlets in liquid medium by application of paclobutrazol or ancymidol, for its amenability in a bioreactor system: growth parameters. Plant Cell Rep 25:382–391
Thomas TD (2008) The role of activated charcoal in plant tissue culture. Biotechnol Adv 26:618–631
Tribulato A, Remotti PC, Löffler HJM, Van Tuyl JM (1997) Somatic embryogenesis and plant regeneration in Lilium longiflorum Thunb. Plant Cell Rep 17:113–118
Urbaniec-Kiepura M, Bach A (2014) Effect of pre-storage on Lilium martagon L. seed longevity following cryopreservation. Cryo Letters 35:462–472
USDA Statistics Floriculture Crops (2015) Floriculture Crops 2014 Summary, June 2015. www.usda.gov/nass/PUBS/TODAYRPT/floran15.pdf. Accessed 29 Feb 2016
Van Aartrijk J, Blom-Barnhoorn GJ (1981) Growth regulator requirements for adventitious regeneration from Lilium bulb-scale tissue in vitro, in relation to duration of bulb storage and cultivar. Sci Hortic 14:261–268
Van Aartrijk J, Blom-Barnhoorn GJ, Bruinsma J (1985) Adventitious bud formation from bulb-scale explants of Lilium speciosum Thunb. in vitro effects of aminoethoxyvinyl-glycine, t-aminocyclopropane-tcarboxylic acid, and ethylene. J Plant Physiol 117:401–410
Van Heusden AW, Jongerius MC, Van Tuyl JM, Straathof TP, Mes JJ (2002) Molecular assisted breeding for disease resistance in lily. Acta Hortic 572:131–138
Van Rossum MWPC, De Klerk GJ, Van der Plas LHW (1998) Adventitious regeneration from tulip, lily and apple explants at different oxygen levels. J Plant Physiol 153:141–145
Van Tuyl JM, Straathof TP, Bino RJ, Kwakkenbos AAM (1988) Effect of three pollination methods on embryo development and seed set in intra- and interspecific crosses between seven Lilium species. Sex Plant Reprod 1:119–123
Van Tuyl JM, Van Dien MP, Van Creij MGM, Van Kleinwee TCM, Franken J, Bino RJ (1991) Application of in vitro pollination, ovary culture, ovule culture, and embryo rescue for overcoming incongruity barriers in interspecific Lilium crosses. Plant Sci 74:115–126
Van Tuyl JM, Meijer B, Van Dien MP (1992a) The use of oryzalin as an alternative for colchicine in in-vitrochromosome doubling of Lilium. Lily Yearbook North Am Lily Soc 43:19–22
Van Tuyl JM, Van Creij MGM, Van Dien MP (1992b) In vitro pollination and ovary culture as a breeding tool in wide hybridization of Lilium and Nerine. Acta Hortic 325:461–466
Van Tuyl JM, Maas IWGM, Lim KB (2002) Introgression in interspecific hybrids of lily. Acta Hortic 570:213–218
Van Tuyl JM, Barba-Gonzalez R, Van Silfhout AA, Lim KB, Ramanna MS (2005) Meiotic polyploidization in five different interspecific Lilium hybrids. Acta Hortic 673:99–105
Varshney A, Dhawan V, Srivastava PS (2000) A protocol for in vitro mass propagation of Asiatic hybrids of lily through liquid stationary culture. In vitro Cell Dev Biol Plant 36:383–391
Varshney A, Lakshmikumaran M, Srivastava PS, Dhawan V (2001) Establishment of genetic fidelity of in vitro-raised Lilium bulblets through RAPD markers. In vitro Cell Dev Biol Plant 37:227–231
Varshney A, Sharma MP, Adholeya A, Dhawan V, Srivastava PS (2002) Enhanced growth of micropropagated bulblets of Lilium sp. inoculated with arbuscular mycorrhizal fungi at different P fertility levels in an alfisol. J Hortic Sci Biotechnol 77:258–263
Vieira P, Wantoch S, Lilley CJ, Chitwood DJ, Atkinson HJ, Kamo K (2015) Expression of a cystatin transgene can confer resistance to root lesion nematodes in Lilium longiflorum cv. ‘Nellie White’. Transgenic Res 24:421–432
Wang J, Huang L, Bao MZ, Liu GF (2009) Production of interspecific hybrids between Lilium longiflorum and L. lophophorum var. linearifolium via ovule culture at early stage. Euphytica 167:45–55
Wang B, Zhang Z, Yin Z, Feng C, Wang Q (2012a) Novel and potential application of cryopreservation to plant genetic transformation. Biotechnol Adv 30:604–612
Wang Y, Van Kronenburg B, Menzel T, Maliepaard C, Shen X, Krens F (2012b) Regeneration and Agrobacterium-mediated transformation of multiple lily cultivars. Plant Cell Tissue Organ Cult 111:113–122
Wang Q, Wang J, Zhang Y, Zhang Y, Xu S, Lu Y (2015) The application of fluorescence in situ hybridization in different ploidy levels cross-breeding of lily. PLoS One 10:e0126899
Watad AA, Yun DJ, Matsumoto T, Niu X, Wu Y, Kononowicz AK, Bressan RA, Hasegawa PM (1998) Microprojectile bombardment-mediated transformation of Lilium longiflorum. Plant Cell Rep 17:262–267
Wawrosch C, Malla PR, Kopp B (2001) Clonal propagation of Lilium nepalense D. Don, a threatened medicinal plant of Nepal. Plant Cell Rep 20:285–288
Wen CS, Hsiao JY (2001) Altitudinal genetic differentiation and diversity of Taiwan lily (Lilium longiflorum var. formosanum; Liliaceae) using rapd markers and morphological characters. Int J Plant Sci 162:287–295
White PR (1963) The cultivation of animal and plant cells, 2nd edn. The Ronald Press, New York
Wickremesinhe ERM, Holcomb EJ, Arteca RN (1994) A practical method for the production of flowering Easter lilies from callus cultures. Sci Hortic 60:143–152
Wozniewski T, Blaschek W, Franz G (1991) In vitro propagation of Lilium testaceum and structural investigation of the storage β-1,4-glucomannan. Plant Cell Rep 10:457–460
Wu H, Zheng S, He Y, Yan G, Bi Y, Zhu Y (2007) Diploid female gametes induced by colchicine in Oriental lilies. Sci Hortic 114:50–53
Wu QQ, Zheng SX, Wang JH, Xu C (2010) Polyploid induction of lily derived from intersectional hybrid. J West China For Sci 39:82–84
Xi M, Sun L, Qiu S, Liu J, Xu J, Shi J (2012) In vitro mutagenesis and identification of mutants via ISSR in lily (Lilium longiflorum). Plant Cell Rep 31:1043–1051
Xie S, Khan N, Ramanna MS, Niu L, Marasek-Ciolakowska A, Arens P, Van Tuyl JM (2010) An assessment of chromosomal rearrangements in neopolyploids of Lilium hybrids. Genome 53:439–446
Xiong Z, Gaeta RT, Pires JC (2011) Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc Natl Acad Sci USA 108:7908–7913
Xu J, Liu Q, Jia M, Liu Y, Li B, Shi Y (2014) Generation of reactive oxygen species during cryopreservation may improve Lilium × siberia pollen viability. In vitro Cell Dev Biol Plant 50:369–375
Yabuta Y, Mieda T, Rapolu M, Nakamura A, Motoki T, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S (2007) Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis. J Exp Bot 58:2661–2671
Ya-juan L, Ming-yang L, Ting Z, Han L, Yun-hui Q (2009) Polyploidy induction and identification in Lilium formosanum × Lilium longiflorum var. scabrum. J Yunnan Agric Univ 24:859–864
Yamagishi M (1998) Effects of culture temperature on the enlargement, sugar uptake, starch accumulation, and respiration of in vitro bulblets of Lilium japonicum Thunb. Sci Hortic 73:239–247
Yamagishi M (2013) How genes paint lily flowers: regulation of colouration and pigmentation patterning. Sci Hortic 163:27–36
Yamagishi M, Abe H, Nakano M, Nakatsuka A (2002) PCR-based molecular markers in Asiatic hybrid lily. Sci Hortic 96:225–234
Yamagishi M, Kishimoto S, Nakayama M (2010) Carotenoid composition and changes in expression of carotenoid biosynthetic genes in tepals of Asiatic hybrid lily. Plant Breed 129:100–107
Yamagishi M, Yoshida Y, Nakayama M (2012) The transcription factor LhMYB12 determines anthocyanin pigmentation in the tepals of Asiatic hybrid lilies (Lilium spp.) and regulates pigment quantity. Mol Breed 30:913–925
Yi JY, Lee GA, Chung JW, Lee SY, Lim KB (2013) Efficient cryopreservation of Lilium spp. shoot tips using droplet-vitrification. Plant Breed Biotechnol 1:131–136
Yin ZF, Zhao B, Bi WL, Chen L, Wang QC (2013) Direct shoot regeneration from basal leaf segments of Lilium and assessment of genetic stability in regenerants by ISSR and AFLP markers. In vitro Cell Dev Biol Plant 49:333–342
Yin ZF, Bi WL, Chen L, Zhao B, Volk GM, Wang QC (2014) An efficient, widely applicable cryopreservation of Lilium shoot tips by droplet vitrification. Acta Physiol Plant 36:1683–1692
Yoon JW, Kim HH, Ko HC, Hwang HS, Hong ES, Cho EG, Engelmann F (2006) Cryopreservation of cultivated and wild potato varieties by droplet vitrification: effect of subculture of mother-plants and of preculture of shoot tips. Cryo Letters 27:211–222
Zaccaro MC, Kato A, Zulpa G, Storni MM, Steyerthal N, Lobasso K, Stella AM (2006) Bioactivity of Scytonema hofmanni (Cyanobacteria) in Lilium alexandrae in vitro propagation. Electron J Biotechnol 9:210–214
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by N. Stewart.
Rights and permissions
About this article
Cite this article
Bakhshaie, M., Khosravi, S., Azadi, P. et al. Biotechnological advances in Lilium . Plant Cell Rep 35, 1799–1826 (2016). https://doi.org/10.1007/s00299-016-2017-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-016-2017-8