Abstract
In an attempt to elucidate the biological effects and underlying mutations involving flower color in ornamental plants following carbon ion beam radiation, shoots of geranium were exposed at dosages of 0, 10, 15, 30, and 40 Gy, and one flower color mutant was obtained. The morphological characteristics, physiological aspects, and DNA polymorphisms between wild-type and flower color mutants were analyzed. The colors of petal, peduncle, pistil, and stamen of the mutant displayed significant differences compared to those of the wild-type. Compared to the original plants, the total anthocyanin content in the petals of the mutant significantly decreased, resulting in a light pink petal phenotype. DNA polymorphisms detected by random amplified polymorphic DNA analysis showed that the ratio of different bands between the wild-type and mutant reached up to 13.2 %. The present study demonstrates that carbon ion beam irradiation is effective in inducing genomic variations, resulting in flower color geranium mutants within a relatively short period of time. Meanwhile, the developed flower-color mutants may be potentially used in future mutational research studies involving ornamental plants.
Similar content being viewed by others
References
J. Van der Walt, L. Van Zyl, A taxonomic revision of Pelargonium section Campylia (Geraniaceae). S. Afr. J. Bot. 54, 145–171 (1988)
T. Abe, C.H. Bae, T. Ozaki et al., Stress-tolerant mutants induced by heavy-ion beams, stress tolerance and mutation in plants. In Proceedings of 39th Gamma Field Symposium, Naka-gun, Ibaraki-ken, Japan, 12–13 July 2000
Y. Kazama, H. Saito, M. Miyagai et al., Effect of heavy ion-beam irradiation on plant growth and mutation induction in Nicotiana tabacum. Plant Biotechnol. 25, 105–111 (2008). doi:10.5511/plantbiotechnology.25.105
A. Tanaka, S. Tano, T. Chantes et al., A new Arabidopsis mutant induced by ion beams affects flavonoid synthesis with spotted pigmentation in testa. Genes Genet. Syst. 72, 141–148 (1997). doi:10.1266/ggs.72.141
Y. Hase, A. Tanaka, T. Baba et al., FRL1 is required for petal and sepal development in Arabidopsis. Plant J. 24, 21–32 (2000). doi:10.1046/j.1365-313x.2000.00851.x
A. Tanaka, A. Sakamoto, Y. Ishigaki et al., An ultraviolet-B-resistant mutant with enhanced DNA repair in Arabidopsis. Plant Physiol. 129, 64–71 (2002). doi:10.1104/pp.010894
Y. Du, W.J. Li, L.X. Yu et al., Mutagenic effects of carbon-ion irradiation on dry Arabidopsis thaliana seeds. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 759, 28–36 (2014). doi:10.1016/j.mrgentox.2013.07.018
Z.X. Tang, Z.F. Liu, J.G. Shi et al., Studies on mutagenic effects of winter wheat by heavy ions irradiation. Nucl. Sci. Tech. 28, 30–33 (2005)
Q.F. Chen, H.Y. Ya, G.Y. Qin et al., Study on screening of TaGA2ox1 mutants in wheat by ion beam irradiation. Plasma Sci. Technol. 12, 757–760 (2010). doi:10.1088/1009-0630/12/6/22
X.C. Dong, W.J. Li, Evaluation of KFJT-1, an early-maturity mutant of sweet sorghum acquired by carbon ions irradiation. Nucl. Sci. Tech. 25, 1–4 (2014). doi:10.13538/j.1001-8042/nst.25.020305
M. Okamura, N. Yasuno, M. Ohtsuka et al., Wide variety of flower-color and -shape mutants regenerated from leaf cultures irradiated with ion beams. Nucl. Instrum. Methods B 206, 574–578 (2003). doi:10.1016/s0168-583x(03)00835-8
J.Y. He, D. Lu, L.X. Yu et al., Pigment analysis of a color-leaf mutant in Wandering Jew (Tradescantia fluminensis) irradiated by carbon ions. Nucl. Sci. Tech. 22, 77–83 (2011). doi:10.13538/j.1001-8042/nst.22.77-83
K. Sasaki, R. Aida, T. Niki et al., High-efficiency improvement of transgenic torenia flowers by ion beam irradiation. Plant Biotechnol. 25, 81–89 (2008). doi:10.5511/plantbiotechnology.25.81
L.X. Yu, W.J. Li, X.C. Dong et al., RAPD analysis on dwarf mutant of Dahlia pinnata Cav induced by 80 MeV/μ 12C6+ ions. Nucl. Sci. Tech. 31, 830–833 (2008)
H. Ishizaka, E. Kondo, N. Kameari, Production of novel flower color mutants from the fragrant cyclamen (Cyclamen persicum × C. purpurascens) by ion-beam irradiation. Plant Biotechnol. 29, 201–208 (2012). doi:10.5511/plantbiotechnology.12.0116a
T. Kanaya, H. Saito, Y. Hayashi et al., Heavy-ion beam-induced sterile mutants of verbena (Verbena × hybrida) with an improved flowering habit. Plant Biotechnol. 25, 91–96 (2008). doi:10.5511/plantbiotechnology.25.91
L.B. Zhou, W.J. Li, L.X. Yu et al., Linear energy transfer dependence of the effects of carbon ion beams on adventitious shoot regeneration from in vitro leaf explants of Saintpaulia ionahta. Int. J. Radiat. Biol. 82, 473–481 (2006). doi:10.1080/09553000600863080
L.B. Zhou, W.J. Li, S. Ma et al., Effects of ion beam irradiation on adventitious shoot regeneration from in vitro leaf explants of Saintpaulia ionahta. Nucl. Instrum. Methods B 244, 349–353 (2006). doi:10.1016/j.nimb.2005.10.034
Y. Tanaka, Y. Katsumoto, F. Brugliera et al., Genetic engineering in floriculture. Plant Cell Tissue Organ Cult. 80, 1–24 (2005). doi:10.1007/s11240-004-0739-8
M. Nieuwhof, L.W.D. Van Raamsdonk, J.P. Van Eijk, Pigment composition of flowers of Tulipa species as a parameter for biosystematic research. Biochem. Syst. Ecol. 18, 399–404 (1990). doi:10.1016/0305-1978(90)90083-R
T.A. Holton, E.C. Cornish, Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7, 1071–1083 (1995). doi:10.1105/tpc.7.7.1071
Y. Yuan, X. Ma, D. Tang et al., Comparison of anthocyanin components, expression of anthocyanin biosynthetic structural genes, and TfF3′H1 sequences between Tulipa fosteriana ‘Albert heijn’ and its reddish sport. Sci. Hortic. 175, 16–26 (2014). doi:10.1016/j.scienta.2014.05.032
Q. Li, J. Wang, H.Y. Sun et al., Flower color patterning in pansy (Viola × wittrockiana Gams.) is caused by the differential expression of three genes from the anthocyanin pathway in acyanic and cyanic flower areas. Plant Physiol. Biochem. 84, 134–141 (2014). doi:10.1016/j.plaphy.2014.09.012
G. Tornielli, R. Koes, F. Quattrocchio, The genetics of flower color, in Petunia, ed. by T. Gerats, J. Strommer (Springer, New York, 2009), pp. 269 –299
G. Forkmann, Flavonoids as flower pigments: the formation of the natural spectrum and its extension by genetic engineering. Plant Breed. 106, 1–26 (1991). doi:10.1111/j.1439-0523.1991.tb00474.x
C. Zhang, W. Wang, Y. Wang et al., Anthocyanin biosynthesis and accumulation in developing flowers of tree peony (Paeonia suffruticosa) ‘Luoyang Hong’. Postharvest Biol. Technol. 97, 11–22 (2014). doi:10.1016/j.postharvbio.2014.05.019
J.F. Ziegler, M.D. Ziegler, J.P. Biersack, SRIM - The stopping and range of ions in matter. Nucl. Instrum. Methods B 268, 1818–1823 (2010). doi:10.1016/j.nimb.2010.02.091
S.A. Becher, K. Steinmetz, K. Weising et al., Microsatellites for cultivar identification in Pelargonium. Theor. Appl. Genet. 101, 643–651 (2000). doi:10.1007/s001220051526
M. Nei, W.H. Li, Mathematical-model for studying genetic-variation in terms of restriction endonucleases. Proc. Natl. Acad Sci. USA 76, 5269–5273 (1979). doi:10.1073/pnas.76.10.5269
M.F. Zhang, L.M. Jiang, D.M. Zhang et al., De novo transcriptome characterization of Lilium ‘Sorbonne’ and key enzymes related to the flavonoid biosynthesis. Mol. Genet. Genomics 290, 399–412 (2015). doi:10.1007/s00438-014-0919-0
D.Y. Xie, S.B. Sharma, E. Wright et al., Metabolic engineering of proanthocyanidins through co-expression of anthocyanidin reductase and the PAP1 MYB transcription factor. Plant J. 45, 895–907 (2006). doi:10.1111/j.1365-313X.2006.026553.x
R. Aida, K. Yoshida, T. Kondo et al., Copigmentation gives bluer flowers on transgenic torenia plants with the antisense dihydroflavonol-4-reductase gene. Plant Sci. 160, 49–56 (2000). doi:10.1016/S0168-9452(00)00364-2
Noda K-i, B.J. Glover, P. Linstead et al., Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature 369, 661–664 (1994). doi:10.1038/369661a0
C. Leloup, G. Garty, G. Assaf et al., Evaluation of lesion clustering in irradiated plasmid DNA. Int. J. Radiat. Biol. 81, 41–54 (2005). doi:10.1080/09553000400017895
L. Sui, J.Y. Guo, F.Q. Kong et al., Investigation of direct and indirect interaction of DNA damage induced by high LET 7Li ions. Nucl. Sci. Tech. 30, 250–254 (2007)
N. Shikazono, C. Suzuki, S. Kitamura et al., Analysis of mutations induced by carbon ions in Arabidopsis thaliana. J. Exp. Bot. 56, 587–596 (2005). doi:10.1093/jxb/eri047
C. Moretti, M. Quaglia, M. Cerri et al., A real-time PCR assay for detection and quantification of Botrytis cinerea in Pelargonium × hortorum plants and its use for evaluation of plant resistance. Eur. J. Plant Pathol. 143, 159–171 (2015). doi:10.1007/s10658-015-0673-0
H. Hadrys, M. Balick, B. Schierwater, Applications of random amplified polymorphic DNA (RAPD) in molecular ecology. Mol. Ecol. 1, 55–63 (1992). doi:10.1111/j.1365-294X.1992.tb00155.x
D.T. Goodhead, The initial physical damage produced by ionizing radiations. Int. J. Radiat. Biol. 56, 623–634 (1989). doi:10.1080/09553008914551841
X.C. Dong, W.J. Li, Biological features of an early-maturity mutant of sweet sorghum induced by carbon ions irradiation and its genetic polymorphism. Adv. Space Res. 50, 496–501 (2012). doi:10.1016/j.asr.2012.04.028
L.Q. Luan, H.P.U. Nguyen, T.T.H. Vo, In vitro mutation breeding of Paphiopedilum by ionization radiation. Sci. Hortic. 144, 1–9 (2012). doi:10.1016/j.scienta.2012.06.028
M. Nakayama, N. Tanikawa, Y. Morita et al., Comprehensive analyses of anthocyanin and related compounds to understand flower color change in ion-beam mutants of cyclamen (Cyclamen spp.) and carnation (Dianthus caryophyllus). Plant Biotechnol. 29, 215–221 (2012). doi:10.5511/plantbiotechnology.12.0102a
T. Nakatsuka, M. Nishihara, K. Mishiba et al., Two different mutations are involved in the formation of white-flowered gentian plants. Plant Sci. 169, 949–958 (2005). doi:10.1016/j.plantsci.2005.06.013
R. Saito, N. Fukuta, A. Ohmiya et al., Regulation of anthocyanin biosynthesis involved in the formation of marginal picotee petals in Petunia. Plant Sci. 170, 828–834 (2006). doi:10.1016/j.plantsci.2005.12.003
R. Saito, K. Kuchitsu, Y. Ozeki et al., Spatiotemporal metabolic regulation of anthocyanin and related compounds during the development of marginal picotee petals in Petunia hybrida (Solanaceae). J. Plant. Res. 120, 563–568 (2007). doi:10.1007/s10265-007-0086-z
S. Shimada, K. Takahashi, Y. Sato et al., Dihydroflavonol 4-reductase cDNA from non-anthocyanin-producing species in the Caryophyllales. Plant Cell Physiol. 45, 1290–1298 (2004). doi:10.1093/Pcp/Pch156
S. Shimada, Y.T. Inoue, M. Sakuta, Anthocyanidin synthase in non-anthocyanin-producing caryophyllales species. Plant J. 44, 950–959 (2005). doi:10.1111/j.1365-313X.2005.02574.x
C. Yamamizo, N. Noda, A. Ohmiya, Anthocyanin and carotenoid pigmentation in flowers of section Mina, subgenus Quamoclit, genus Ipomoea. Euphytica 184, 429–440 (2012). doi:10.1007/s10681-011-0618-4
H.M. Schaefer, Why fruits go to the dark side. Acta Oecol. 37, 604–610 (2011). doi:10.1016/j.actao.2011.04.008
M.F. Willson, C.J. Whelan, The evolution of fruit color in fleshy-fruited plants. Am. Nat. 136, 790–809 (1990). doi:10.1086/285132
L.J. Cooney, H.M. Schaefer, B.A. Logan et al., Functional significance of anthocyanins in peduncles of Sambucus nigra. Environ. Exp. Bot. 119, 18–26 (2015). doi:10.1016/j.envexpbot.2015.03.001
V.L. Chandler, J.P. Radicella, T.P. Robbins et al., Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences. Plant Cell 1, 1175–1183 (1989). doi:10.1105/tpc.1.12.1175
K.-I. Park, N. Ishikawa, Y. Morita et al., A bHLH regulatory gene in the common morning glory, Ipomoea purpurea, controls anthocyanin biosynthesis in flowers, proanthocyanidin and phytomelanin pigmentation in seeds, and seed trichome formation. Plant J. 49, 641–654 (2007). doi:10.1111/j.1365-313X.2006.02988.x
S. Shimada, H. Otsuki, M. Sakuta, Transcriptional control of anthocyanin biosynthetic genes in the Caryophyllales. J. Exp. Bot. 58, 957–967 (2007). doi:10.1093/jxb/erl256
Y. Morita, M. Saitoh, A. Hoshino et al., Isolation of cDNAs for R2R3-MYB, bHLH and WDR transcriptional regulators and identification of c and ca mutations conferring white flowers in the Japanese morning glory. Plant Cell Physiol. 47, 457–470 (2006). doi:10.1093/pcp/pcj012
Acknowledgments
We express our gratitude to Mr. Huai-An Gu (Institute of Modern Physics, Chinese Academy of Sciences) and Dr. Jinyu He for their invaluable assistance. We also thank our colleagues at HIRFL for providing the carbon ion beams.
Author information
Authors and Affiliations
Corresponding author
Additional information
Li-Xia Yu, Wen-Jian Li, and Yan Du have contributed equally to this research.
This work is supported by the National Natural Science Foundation of China (Grant Nos. 11205218, 11275171, and 11405234), the Knowledge Innovation Project of the Chinese Academy of Sciences (CAS) (No. KJCX2-EW-N05), CAS “Light of West China” Program (No. 29Y506020), and the Youth Innovation Promotion Association of CAS (No. 29Y506030) supported this study.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yu, LX., Li, WJ., Du, Y. et al. Flower color mutants induced by carbon ion beam irradiation of geranium (Pelargonium × hortorum, Bailey). NUCL SCI TECH 27, 112 (2016). https://doi.org/10.1007/s41365-016-0117-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s41365-016-0117-3