Abstract
Background
The potential of paddy breeding has reached its pinnacle, and hybrids have been the principal research outcome. Hence, our hypothesis was based on improvising the callus induction efficiency of recalcitrant Oryza sativa sub. indica hybrids by intervening into their cellular functions like cell division and histone regulation for the production of doubled haploids, a better output compared to hybrids.
Methodology and results
Insight into the mechanism of cell division is the foremost concern in altering the same and hence studies on evolution, expression and action of histone deacetylase and its 12 genes (9 HDA and 3 HD-tunin genes) were chosen in the hypothesis. Expression of HDA genes at three stages (anther dehiscence, 1st callusing and second callusing stages) with inhibitor (trichostatin-A) interventions indicated 1st callusing stage as the most important in influencing callus induction and also the genes HDA19, 6, 15 and 5 were the most important. TSA alone had a significant impact on the regulation of the genes HDT 702, HDA19, HDA9, and HDA6. Higher expression of HDA19 and HDA6 was involved in maximizing callus induction; HDA15 had an antagonistic expression compared to HDA19/6 and might be involved in chlorophyll regulation during regeneration. Results of evolutionary analysis on histone deacetylases indicated a long and single lineage of origin denoting its importance in the basic cellular functions. The tubulin deacetylation gene HDA5, which was exclusively found in dicotyledons, had a recent evolutionary history only from terrestrial plants, and also had significant conservation in its motifs and NLS region.
Conclusion
By combating the recalcitrant nature of Indica cultivars, molecular editing on a combination of HDA genes will enhance the callus induction and regeneration efficiency of the next generation of doubled haploids, therby improving the total yield.
Similar content being viewed by others
Data availability
Not applicable.
Code availability
Not applicable.
References
FAO (2020) Despite a cut in world cereal production, this year’s forecast output remains an all-time high. FAO, Rome
Naik N, Rout P, Umakanta N, Verma RL, Katara JL, Sahoo KK et al (2017) Development of doubled haploids from an elite indica rice hybrid (BS6444G) using anther culture. Plant Cell Tissue Organ Cult 128(3):679–689
Grewal D, Manito C, Bartolome V (2011) Doubled haploids generated through anther culture from crosses of elite indica and japonica cultivars and/or lines of rice: large-scale production, agronomic performance, and molecular characterization. Crop Sci 51(6):2544–2553
Hale B, Phipps C, Rao N, Wijeratne A, Phillips GC (2020) Differential expression profiling reveals stress-induced cell fate divergence in soybean microspores. Plants 9(11):1510
Koprinarova M, Schnekenburger M, Diederich M (2016) Role of histone acetylation in cell cycle regulation. Curr Top Med Chem 16(7):732–744
Ito K, Adcock IM (2002) Histone acetylation and histone deacetylation. Mol Biotechnol 20(1):99–106
Dhavarasa P (2017) Mechanistic understanding of PCNA-based interactions: the interplay between CAF-I and Rrm3p for the DNA sliding clamp PCNA (Doctoral dissertation)
Ma X, Zhang C, Zhang B, Yang C, Li S (2016) Identification of genes regulated by histone acetylation during root development in Populus trichocarpa. BMC Genomics 17(1):1–17
Lochmanová G, Ihnatová I, Kuchaříková H, Brabencová S, Zachová D, Fajkus J, Zdráhal Z, Fojtová M (2019) Different modes of action of genetic and chemical downregulation of histone deacetylases with respect to plant development and histone modifications. Int J Mol Sci 20(20):5093
Zhang Q, Wang P, Hou H, Zhang H, Tan J, Huang Y, Li Y, Wu J, Qiu Z, Li L (2017) Histone acetylation and reactive oxygen species are involved in the preprostage arrest induced by sodium butyrate in maize roots. Protoplasma 254(1):167–179
Ageeva-Kieferle A, Georgii E, Winkler B, Ghirardo A, Albert A, Hüther P et al (2021) Nitric oxide coordinates growth, development, and stress response via histone modification and gene expression. Plant Physiol 187:336
Hollender C, Liu Z (2008) Histone deacetylase genes in Arabidopsis development. J Integr Plant Biol 50(7):875–885
Alinsug MV, Chen FF, Luo M, Tai R, Jiang L, Wu K (2012) Subcellular localization of class II HDAs in Arabidopsis thaliana: nucleocytoplasmic shuttling of HDA15 is driven by light. PLoS ONE 7(2):e30846
Jiao Y, Paterson AH (2014) Polyploidy-associated genome modifications during land plant evolution. Philos Trans R Soc B Biol Sci 369(1648):20130355
Smaczniak C, Immink RG, Angenent GC, Kaufmann K (2012) Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139(17):3081–3098
Jin X, Ren J, Nevo E, Yin X, Sun D, Peng J (2017) Divergent evolutionary patterns of NAC transcription factors are associated with diversification and gene duplications in angiosperm. Front Plant Sci 8:1156
Han JD, Li X, Jiang CK, Wong GKS, Rothfels CJ, Rao GY (2017) Evolutionary analysis of the LAFL genes involved in the land plant seed maturation program. Front Plant Sci 8:439
Morea EGO et al (2016) Functional and evolutionary analyses of the miR156 and miR529 families in land plants. BMC Plant Biol 16(1):40
Xia R, Xu J, Meyers BC (2017) The emergence, evolution, and diversification of the miR390-TAS3-ARF pathway in land plants. Plant Cell 29(6):1232–1247
Wang X, Shi X, Chen S, Ma C, Xu S (2018) Evolutionary origin, gradual accumulation and functional divergence of heat shock factor gene family with plant evolution. Front Plant Sci 9:71
Rout P, Naik N, Ngangkham U, Verma RL, Katara JL, Singh ON, Samantaray S (2016) Doubled haploids generated through anther culture from an elite long duration rice hybrid, CRHR32: method optimization and molecular characterization. Plant Biotechnol 33(3):177–186
Zhang L, Zhang Y, Gao Y, Jiang X, Zhang M, Wu H et al (2016) Effects of histone deacetylase inhibitors on microspore embryogenesis and plant regeneration in Pakchoi (Brassica rapa ssp. chinensis L.). Sci Hortic 209:61–66
Gregoretti I, Lee YM, Goodson HV (2004) Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J Mol Biol 338(1):17–31
Alinsug MV, Yu CW, Wu K (2009) Phylogenetic analysis, subcellular localization, and expression patterns of RPD3/HDA1 family histone deacetylases in plants. BMC Plant Biol 9(1):1–15
Cheng J, Khan MA, Qiu WM, Li J, Zhou H, Zhang Q et al (2012) Diversification of genes encoding granule-bound starch synthase in monocots and dicots is marked by multiple genome-wide duplication events. PLoS ONE 7(1):e30088
Li C, Li QG, Dunwell JM, Zhang YM (2012) Divergent evolutionary pattern of starch biosynthetic pathway genes in grasses and dicots. Mol Biol Evol 29(10):3227–3236
Jasencakova Z et al (2000) Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription. Plant Cell 12:2087–2100
Lusser A, Kölle D, Loidl P (2001) Histone acetylation: lessons from the plant kingdom. Trends Plant Sci 6(2):59–65
Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506
Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25(9):3159–3173
Kim H, Shim D, Moon S, Lee J, Bae W, Choi H et al (2019) Transcriptional network regulation of the brassinosteroid signaling pathway by the BES1–TPL–HDA19 co-repressor complex. Planta 250(4):1371–1377
Lee K, Park OS, Jung SJ, Seo PJ (2016) Histone deacetylation-mediated cellular dedifferentiation in Arabidopsis. J Plant Physiol 191:95–100
Zhao J, Zhang J, Zhang W, Wu K, Zheng F, Tian L et al (2015) Expression and functional analysis of the plant-specific histone deacetylase HDT701 in rice. Front Plant Sci 5:764
Liu X, Chen CY, Wang KC, Luo M, Tai R, Yuan L et al (2013) PHYTOCHROME INTERACTING FACTOR3 associates with the histone deacetylase HDA15 in repression of chlorophyll biosynthesis and photosynthesis in etiolated Arabidopsis seedlings. Plant Cell 25(4):1258–1273
Alinsug MV, Radziejwoski A, Deocaris CC (2020) AtHDA15 binds directly to COP1 positively regulating photomorphogenesis. Biochem Biophys Res Commun 533:806
Grafi G, Florentin A, Ransbotyn V, Morgenstern Y (2011) The stem cell state in plant development and in response to stress. Front Plant Sci 2:53
Jang IC, Pahk YM, Song SI, Kwon HJ, Nahm BH, Kim JK (2003) Structure and expression of the rice class-I type histone deacetylase genes OsHDAC1–3: OsHDAC1 overexpression in transgenic plants leads to increased growth rate and altered architecture. Plant J 33(3):531–541
Zhang H, Yue M, Zheng X, Gautam M, He S, Li L (2018) The role of promoter-associated histone acetylation of haem oxygenase-1 (HO-1) and giberellic acid-stimulated like-1 (GSL-1) genes in heat-induced lateral root primordium inhibition in maize. Front Plant Sci 9:1520
Ding B, del Rosario Bellizzi M, Ning Y, Meyers BC, Wang GL (2012) HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell 24(9):3783–3794
Hu Y, Qin F, Huang L, Sun Q, Li C, Zhao Y, Zhou DX (2009) Rice histone deacetylase genes display specific expression patterns and developmental functions. Biochem Biophys Res Commun 388(2):266–271
Zhang H, Guo F, Qi P, Huang Y, Xie Y, Xu L et al (2020) OsHDA710-mediated histone deacetylation regulates callus formation of rice mature embryo. Plant Cell Physiol 61(9):1646–1660
Acknowledgements
We acknowledge DST-SERB for their financial support to our project “Sanction order no: PDF12017/001241, dated 31, May 2018”. We also acknowledge Director, National Rice Research institute, ICAR, Cuttack for providing lab facilities and permission for the experimental work and we also cordially thank Ms. Manjusha Chandravani and Ms. Suryasmita mallick for their help in maintaining the regenerants, and we also thank Kishor Pundlik Jeughale and Bandita Sahoo for their timely help in wet-lab work. Further we thank all other JRFs and SRFs of lab 225 for their co-operation and assistance.
Funding
DST-SERB (financial support) project “Sanction order no: PDF12017/001241, dated 31, May 2018”.
Author information
Authors and Affiliations
Contributions
CBS: Research work, data analysis and manuscript writing, PC manuscript editing, SS mentor of the project.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Research involving human and animal rights
This research work does not involve any human or animals.
Informed consent
This manuscript has been submitted after the consent of all the three authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sai, C.B., Chidambaranathan, P. & Samantaray, S. Role of histone deacetylase inhibitors in androgenic callus induction of Oryza sativa sub indica, in sight into evolution and mode of action of histone deacetylase genes. Mol Biol Rep 49, 2169–2183 (2022). https://doi.org/10.1007/s11033-021-07036-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-021-07036-y