Genetic stability evaluation of caladium somaclonal variants by morphological, cytological, and SSR analysis in three successive generations

Authors

  • Liu HU Hubei Key Laboratory of Spices and Horticultural Plant Germplasm Innovation and Utilization, College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025 (CN)
  • Yida Wang Hubei Key Laboratory of Spices and Horticultural Plant Germplasm Innovation and Utilization, College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025 (CN)
  • Shuangying YU Hubei Key Laboratory of Spices and Horticultural Plant Germplasm Innovation and Utilization, College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025 (CN)
  • Songli LI Hubei Key Laboratory of Spices and Horticultural Plant Germplasm Innovation and Utilization, College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025 (CN)
  • Xiaodong CAI Hubei Key Laboratory of Spices and Horticultural Plant Germplasm Innovation and Utilization, College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025 (CN)

DOI:

https://doi.org/10.15835/nbha52313746

Keywords:

caladium breeding, chromosome number, nuclear DNA content, somaclonal variation, tuber generations

Abstract

Somaclonal variants with valuable agronomic traits play a crucial role in crop breeding, provided that they are stably passed down in subsequent generations. Although numerous somaclonal variants have been identified and studied among in vitro regenerated plants in the foliage plant caladium (Caladium × hortulanum Birdsey), no research has been carried out to evaluate their genetic stability in subsequent generations. This study aimed to evaluate the genetic stability of three types of diploid caladium somaclonal variants, previously derived from in vitro callus cultures, over three successive tuber-propagated generations. The analysis of quantitative morphological characteristics revealed a greater degree of variation among the established plants in the first generation (G1) compared to the second (G2) and third generations (G3). Seven plants exhibiting distinct leaf coloration changes were identified in the G1 generation and were found to be stably passed down to the subsequent G2 and G3 generations. These findings indicate a wide range of morphological variation in the G1 generation, followed by relative stability in subsequent generations. A comprehensive cytological and molecular analysis revealed that five of the seven newly observed variants displayed notable differences in relative nuclear DNA content, chromosome number, or SSR (simple sequence repeat) banding patterns compared to their corresponding normal counterparts. The findings of this study will be instrumental in developing new cultivars with distinctive plant morphology through the exploitation of somaclonal variation in caladium.

References

Abd Elaziem TM, Ahmed MEAE, Abou El-Dis GR (2022). In vitro propagation for conservation of the rare date palm (Phoenix dactylifera L.) ‘Amri’ using immature inflorescence. In Vitro Cellular & Developmental Biology–Plant 58:1048-1056. https://doi.org/10.1007/s11627-022-10296-3

Akhter S, Rauf S, Akhter B, Ghias M, Parveen N, Ibrar I, Gill SA, Ali Q (2021). Variability assessed in red rot resistant somaclones of sugarcane genotype S97us297 in R1 and R2 generations. Plant Cell Biotechnology and Molecular Biology 22:17-29.

Bairu MW, Aremu AO, Van Staden J (2011). Somaclonal variation in plants: causes and detection methods. Pant Growth Regulation 63:147-173. https://doi.org/10.1007/s10725-010-9554-x

Barpete S, Gupta P, Singh M, Kumar S (2020). Culture selected somaclonal variants showing low-ODAP and high protein content in nineteen grass pea (Lathyrus sativus L.) genotypes. Plant Cell, Tissue and Organ Culture 142:625-634. https://doi.org/10.1007/s11240-020-01889-0

Biswas MK, Dutt M, Roy UK, Islam R, Hossain M (2009). Development and evaluation of in vitro somaclonal variation in strawberry for improved horticultural traits. Scientia Horticulturae 122:409-416. https://doi.org/10.1016/j.scienta.2009.06.002

Cao Z, Deng Z (2020). Morphological, cytological and molecular marker analyses of ‘Tapestry’ caladium variants reveal diverse genetic changes and enable association of leaf coloration pattern loci with molecular markers. Plant Cell, Tissue and Organ Culture 143:363-375. https://doi.org/10.1007/s11240-020-01922-2

Cao Z, Sui S, Cai X, Yang Q, Deng Z (2016). Somaclonal variation in ‘Red Flash’ caladium: morphological, cytological and molecular characterization. Plant Cell, Tissue and Organ Culture 126:269-279. https://doi.org/10.1007/s11240-016-0996-3

Cai X, Cao Z, Xu S, Deng Z (2015). Induction, regeneration and characterization of tetraploids and variants in ‘Tapestry’ caladium. Plant Cell, Tissue and Organ Culture 120:689-700. https://doi.org/10.1007/s11240-014-0636-8

Chakraborty N, Banerjee M, Acharya K (2020). In vitro selection of elite clone of Withania somnifera against leaf blight disease caused by Alternaria alternata. Physiological and Molecular Plant Pathology 112:101560. https://doi.org/10.1016/j.pmpp.2020.101560

Chen JJ, Zhang YS, Duan JX, Cao YM, Cai XD (2021). Morphological, cytological, and pigment analysis of leaf color variants regenerated from long–term subcultured caladium callus. In Vitro Cellular & Developmental Biology–Plant 57:60-71. https://doi.org/10.1007/s11627-020-10106-8

Dang J, Wu T, Liang G, Wu D, He Q, Guo Q (2019). Identification and characterization of a loquat aneuploid with novel leaf phenotypes. Hortscience 54:804-808. https://doi.org/10.21273/hortsci13844-18

Deng Z, Peres NA, Desaeger J (2021). Two new lance–leaved caladium cultivars: Pink Panther and Crimson Skye. Hortscience 56 (7):853-859. https://doi.org/10.21273/hortsci15854-21

Deng Z, Peres NA, Desaeger J (2023). ‘Lava Glow’: A novel red, fancy–leaved caladium for containers and landscapes. HortScience 58 (1):122-126. https://doi.org/10.21273/hortsci16937-22

Deng Z, Harbaugh BK (2006). Independent inheritance of leaf shape and main vein color in caladium. Journal of the American Society for Horticultural Science 131(1):53-58. https://doi.org/10.32473/edis-ep257-2005

Eeckhaut T, Van Houtven W, Bruznican S, Leus L, Van Huylenbroeck J (2020). Somaclonal variation in Chrysanthemum × morifolium protoplast regenerants. Frontiers in Plant Science 11:607171. https://doi.org/10.3389/fpls.2020.607171

Fazili MA, Bashir I, Ahmad M, Yaqoob U, Geelani SN (2022). In vitro strategies for the enhancement of secondary metabolite production in plants: a review. Bulletin of the National Research Centre 46:35. https://doi.org/10.1186/s42269-022-00717-z

Ferreira MDS, Rocha ADJ, Nascimento FDS, Oliveira WDDS, Soares JMDS, Rebouças TA, … Amorim EP (2023). The role of somaclonal variation in plant genetic improvement: a systematic review. Agronomy 13:730. https://www.mdpi.com/2073-4395/13/3/730

Fulton TM, Chunzoongse J, Tanksley SD (1995). Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Molecular Biology Reporter 13:207-209. https://doi.org/10.1007/bf02670897

Gong L, Deng Z (2011). Development and characterization of microsatellite markers for caladiums (Caladium Vent.). Plant Breeding 130(5):591-595. https://doi.org/10.1111/j.1439-0523.2011.01863.x

Halim NAA, Tan BC, Midin MR, Madon M, Khalid N, Yaacob JS (2018). Abscisic acid and salinity stress induced somaclonal variation and increased histone deacetylase (HDAC) activity in Ananas comosus var. MD2. Plant Cell, Tissue and Organ Culture 133:123-135. https://doi.org/10.1007/s11240-017-1367-4

Hannachi S, Werbrouck S, Bahrini I, Abdelgadir A, Siddiqui HA, Van Labeke MC (2021). Obtaining salt stress-tolerant eggplant somaclonal variants from in vitro selection. Plants 10:2539. https://doi.org/10.3390/plants10112539

Henry IM, Dilkes BP, Miller ES, Burkart-Waco D, Comai L (2010). Phenotypic consequences of aneuploidy in Arabidopsis thaliana. Genetics 186:1231-1245. https://doi.org/10.1534/genetics.110.121079

Kaeppler SM, Kaeppler HF, Rhee Y (2000). Epigenetic aspects of somaclonal variation in plants. Plant Molecular Biology 43:179-188. https://doi.org/10.1023/A:1006423110134

Krishna H, Alizadeh M, Singh D, Singh U, Chauhan N, Eftekhari M, Sadh RK (2016). Somaclonal variations and their applications in horticultural crops improvement. 3 Biotech 6:54. https://doi.org/10.1007/s13205-016-0389-7

Li J, Suzuki Y, Hoshino Y (2023). Phenotypic analysis of polyploid and aneuploid haskap (Lonicera caerulea L. subsp. edulis (Turcz. ex Herder) Hultén) plants and their progeny production. Euphytica 219:52. https://doi.org/10.1007/s10681-023-03181-6

Loureiro J, Rodriguez E, Doležel J, Santos C (2007). Two new nuclear isolation buffers for plant DNA flow cytometry: a test with 37 species. Annals of Botany 100:875-888. https://doi.org/10.1093/aob/mcm152

Mirani AA, Jatoi MA, Bux L, Teo CH, Kabiita AI, Harikrishna JA, Markhand GS, Jatt T, Solangi N, Abro S, Channa GS (2022). Genetic stability analysis of tissue culture derived date palm cv. Dedhi plants using IRAP markers. Acta Ecologica Sinica 42:76-81. https://doi.org/10.1016/j.chnaes.2021.02.011

Parrish SB, Deng Z (2022). Discovery and characterization of novel fertile triploids and a new chromosome number in caladium (Caladium × hortulanum). HortScience 57(9):1078-1085. https://doi.org/10.21273/hortsci16701-22

Parrish SB, Kane ME, Deng Z (2023). Morphological, cytogenetic and molecular characterization of new somaclonal variants in four caladium (Caladium × hortulanum) cultivars. Ornamental Plant Research 3:1. https://doi.org/10.48130/opr-2023-0001

Ravindra NS, Ramesh SI, Gupta MK, Jhang T, Shukla AK, Darokar MP, Kulkarni RN (2012). Evaluation of somaclonal variation for genetic improvement of patchouli (Pogostemon patchouli), an exclusively vegetatively propagated aromatic plant. Journal of Crop Science and Biotechnology 15(1):33-39. https://doi.org/10.1007/s12892-011-0068-5

Stelpflug SC, Eichten SR, Hermanson PJ, Springer NM, Kaeppler SM (2014). Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198:209-218. https://doi.org/10.1534/genetics.114.165480

Stroud H, Ding B, Simon SA, Feng S, Bellizzi M, Pellegrini M, Wang GL, Meyers BC, Jacobsen SE (2013). Plants regenerated from tissue culture contain stable epigenome changes in rice. eLife 2:e00354. https://doi.org/10.7554/elife.00354

Yu S, Zhao X, Wang Y, Jiang D, Zhang Y, Hu L, Liu Y, Cai X (2022). Morphological, cytological, and molecular-based genetic stability analysis of in vitro-propagated plants from newly induced aneuploids in caladium. Agriculture 12:1708. https://doi.org/10.3390/agriculture12101708

Zeid IMA, Soliman HI, Metwali EM (2022). In vitro evaluation of some high yield potato (Solanum tuberosum L.) cultivars under imposition of salinity at the cellular and organ levels. Saudi Journal of Biological Sciences 29:2541-2551. https://doi.org/10.1016/j.sjbs.2021.12.040

Zhang W, Wang Y, Diao S, Zhong S, Wu S, Wang L, Su X, Zhang B (2021). Assessment of epigenetic and phenotypic variation in Populus nigra regenerated via sequential regeneration. Frontiers in Plant Science 12:632088. https://doi.org/10.3389/fpls.2021.632088

Zhang Y, Cao Y, Wang Y, Cai X (2023). Somatic embryogenesis induction and genetic stability assessment of plants regenerated from immature seeds of Akebia trifoliate (Thunb.) Koidz. Forests 4:473. https://doi.org/10.3390/f14030473

Zhang YS, Chen JJ, Cao YM, Duan JX, Cai XD (2020). Induction of tetraploids in ‘Red Flash’ caladium using colchicine and oryzalin: morphological, cytological, photosynthetic and chilling tolerance analysis. Scientia Horticulturae 272:109524. https://doi.org/10.1016/j.scienta.2020.109524

Zhao X, Yu S, Wang Y, Jiang D, Zhang Y, Hu L, Zhu Y, Jia Q, Yin J, Liu Y, Cai X (2023). Field performance of disease-free plants of ginger produced by tissue culture and agronomic, cytological, and molecular characterization of the morphological variants. Agronomy 13:74. https://doi.org/10.3390/agronomy13010074

Downloads

Published

2024-09-23

How to Cite

HU, L., Wang, Y., YU, S., LI, S., & CAI, X. (2024). Genetic stability evaluation of caladium somaclonal variants by morphological, cytological, and SSR analysis in three successive generations. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 52(3), 13746. https://doi.org/10.15835/nbha52313746

Issue

Vol. 52 No. 3 (2024)

Section

Research Articles
CITATION
DOI: 10.15835/nbha52313746

License

Copyright (c) 2024 Liu HU, Yida Wang, Shuangying Yu, Songli Li, Xiao Dong Cai

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

License:

© Articles by the authors; licensee UASVM and SHST, Cluj-Napoca, Romania. Papers published in the journal Notulae Botanicae Horti Agrobotanici Cluj-Napoca are open access distributed under the terms and conditions of the Creative Commons Attribution License (http://creativecommons.org/licenses).

Open Access Journal:

The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.