Abstract
Although the application of exogenous hormones and the status of endogenous hormones play a crucial factor in somatic embryogenesis (SE), our understanding of the status of endogenous hormones and the molecular framework for hormone biosynthesis during SE are still elusive. With a data mining approach, we analyzed public RNA-seq data of SE from two model plants, Arabidopsis thaliana and Oryza sativa var. Japonica, which showed that several plant hormone biosynthesis genes had distinct patterns during SE. The expressions of auxin, cytokinin, gibberellin, and ethylene biosynthesis genes were induced during SE in A. thaliana, while only jasmonic acid showed an expression increase during somatic embryogenesis in both plants. Furthermore, by analyzing public RNA sequencing and DNA affinity purification sequencing (DAP-seq), we revealed some possibilities of the role of ethylene during SE through the activity of EIN3, by increasing the expression level of major transcription factors of somatic embryo development such as AGL15, BBM, and FUS3.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Afgan E, Baker D, van den Beek M, Blankenberg D, Bouvier D, Čech M, Chilton J, Clements D, Coraor N, Eberhard C, Grüning B, Guerler A, Hillman-Jackson J, Von Kuster G, Rasche E, Soranzo N, Turaga N, Taylor J, Nekrutenko A, Goecks J (2016) The galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Res 44(W1):W3–W10. https://doi.org/10.1093/nar/gkw343
Arteca RN, Arteca JM (2008) Effects of brassinosteroid, auxin, and cytokinin on ethylene production in Arabidopsis thaliana plants. J Exp Bot 59(11):3019–3026. https://doi.org/10.1093/jxb/ern159
Bai B, Su YH, Yuan J, Zhang XS (2013) Induction of somatic embryos in Arabidopsis requires local YUCCA expression mediated by the down-regulation of ethylene biosynthesis. Mol Plant 6(4):1247–1260. https://doi.org/10.1093/mp/sss154
Bassaganya-Riera J, Nolan KE, Song Y, Liao S, Saeed NA, Zhang X, Rose RJ (2014) An unusual abscisic acid and gibberellic acid synergism increases somatic embryogenesis, facilitates its genetic analysis and improves transformation in Medicago truncatula. PLoS One 9(6):e99908. https://doi.org/10.1371/journal.pone.0099908
Chang KN, Zhong S, Weirauch MT, Hon G, Pelizzola M, Li H, Huang SS, Schmitz RJ, Urich MA, Kuo D, Nery JR, Qiao H, Yang A, Jamali A, Chen H, Ideker T, Ren B, Bar-Joseph Z, Hughes TR, Ecker JR (2013) Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. Elife 2:e00675. https://doi.org/10.7554/eLife.00675
Etienne H, Bertrand B, Dechamp E, Maurel P, Georget F, Guyot R, Breitler J (2016a) Are genetic and epigenetic instabilities of plant embryogenic cells a fatality? The experience of coffee somatic embryogenesis. Hum Genet Embryol 6(136). https://doi.org/10.4172/2161-0436.1000136
Etienne H, Guyot R, Beulé T, Breitler J-C, Jaligot E (2016b) Plant fidelity in somatic embryogenesis-regenerated plants. In: L-V V, O-A N (eds) Somatic embryogenesis: fundamental aspects and applications. Springer, Cham, pp 121–150
Freese NH, Norris DC, Loraine AE (2016) Integrated genome browser: visual analytics platform for genomics. Bioinformatics 32(14):2089–2095. https://doi.org/10.1093/bioinformatics/btw069
Gaj MD, Trojanowska A, Ujczak A, Mędrek M, Kozioł A, Garbaciak B (2006) Hormone-response mutants of Arabidopsis thaliana (L.) Heynh. impaired in somatic embryogenesis. Plant Growth Regul 49(2–3):183–197. https://doi.org/10.1007/s10725-006-9104-8
Georget F, Courtel P, Garcia EM, Hidalgo M, Alpizar E, Breitler J-C, Bertrand B, Etienne H (2017) Somatic embryogenesis-derived coffee plantlets can be efficiently propagated by horticultural rooted mini-cuttings: a boost for somatic embryogenesis. Sci Hortic 216:177–185. https://doi.org/10.1016/j.scienta.2016.12.017
Goff L, Trapnell C, Kelley D (2013) cummeRbund: Analysis, exploration, manipulation, and visualization of Cufflinks high-throughput sequencing data. R package version 2.22.0
Grzyb M, Kalandyk A, Waligórski P, Mikuła A (2017) The content of endogenous hormones and sugars in the process of early somatic embryogenesis in the tree fern Cyathea delgadii Sternb. Plant Cell Tissue Organ Cult 129(3):387–397. https://doi.org/10.1007/s11240-017-1185-8
Grzyb M, Kalandyk A, Mikuła A (2018) Effect of TIBA, fluridone and salicylic acid on somatic embryogenesis and endogenous hormone and sugar contents in the tree fern Cyathea delgadii Sternb. Acta Physiol Plant 40(1). https://doi.org/10.1007/s11738-017-2577-4
Horstman A, Li M, Heidmann I, Weemen M, Chen B, Muiño JM, Angenent GC, Boutilier K (2017) The BABY BOOM transcription factor activates the LEC1-ABI3-FUS3-LEC2 network to induce somatic embryogenesis. Plant Physiol 175:848–857. https://doi.org/10.1104/pp.17.00232
Igielski R, Kępczyńska E (2017) Gene expression and metabolite profiling of gibberellin biosynthesis during induction of somatic embryogenesis in Medicago truncatula Gaertn. PLoS One 12(7):e0182055. https://doi.org/10.1371/journal.pone.0182055
Indoliya Y, Tiwari P, Chauhan AS, Goel R, Shri M, Bag SK, Chakrabarty D (2016) Decoding regulatory landscape of somatic embryogenesis reveals differential regulatory networks between japonica and indica rice subspecies. Sci Rep 6:23050. https://doi.org/10.1038/srep23050
Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan MIR (2017) Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front Plant Sci 8:475. https://doi.org/10.3389/fpls.2017.00475
Jayanthi M, Susanthi B, Murali Mohan N, Mandal PK (2015) In vitro somatic embryogenesis and plantlet regeneration from immature male inflorescence of adult dura and tenera palms of Elaeis guineensis (Jacq.). SpringerPlus 4:256. https://doi.org/10.1186/s40064-015-1025-4
Jones B, Gunnerås SA, Petersson SV, Tarkowski P, Graham N, May S, Dolezal K, Sandberg G, Ljung K (2010) Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell 22(9):2956–2969. https://doi.org/10.1105/tpc.110.074856
Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H (2009) Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21(10):3152–3169. https://doi.org/10.1105/tpc.109.068676
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359. https://doi.org/10.1038/nmeth.1923
Lardet L, Dessailly F, Carron MP, Montoro P, Monteuuis O (2008) Influences of aging and cloning methods on the capacity for somatic embryogenesis of a mature Hevea brasiliensis genotype. Tree Physiol 29(2):291–298. https://doi.org/10.1093/treephys/tpn027
Lema-Rumińska J, Goncerzewicz K, Gabriel M (2013) Influence of abscisic acid and sucrose on somatic embryogenesis in cactus Copiapoa tenuissima Ritt. forma mostruosa. Sci World J 2013:1–7. https://doi.org/10.1155/2013/513985
Liu X, Hou X (2018) Antagonistic regulation of ABA and GA in metabolism and signaling pathways. Front Plant Sci 9:251. https://doi.org/10.3389/fpls.2018.00251
Luo J-P, Jiang S-T, Pan L-J (2001) Enhanced somatic embryogenesis by salicylic acid of Astragalus adsurgens Pall.: relationship with H2O2 production and H2O2-metabolizing enzyme activities. Plant Sci 161(1):125–132. https://doi.org/10.1016/s0168-9452(01)00401-0
Malabadi RB, Teixeira da Silva JA, Nataraja K (2008) Salicylic acid induces somatic embryogenesis from mature trees of Pinus roxburghii (Chir pine) using TCL technology. Tree For Sci Biotech 2(1):34–39
Mantiri FR, Kurdyukov S, Lohar DP, Sharopova N, Saeed NA, Wang XD, VandenBosch KA, Rose RJ (2008) The transcription factor MtSERF1 of the ERF subfamily identified by transcriptional profiling is required for somatic embryogenesis induced by auxin plus cytokinin in Medicago truncatula. Plant Physiol 146(4):1622–1636. https://doi.org/10.1104/pp.107.110379
Merchant N, Lyons E, Goff S, Vaughn M, Ware D, Micklos D, Antin P (2016) The iPlant Collaborative: cyberinfrastructure for enabling data to discovery for the life sciences. PLoS Biol 14(1):e1002342. https://doi.org/10.1371/journal.pbio.1002342
Mira MM, Wally OSD, Elhiti M, El-Shanshory A, Reddy DS, Hill RD, Stasolla C (2016) Jasmonic acid is a downstream component in the modulation of somatic embryogenesis by Arabidopsis class 2 phytoglobin. J Exp Bot 67(8):2231–2246. https://doi.org/10.1093/jxb/erw022
Nhut DT, Le BV, Thanh Van KT (2000) Somatic embryogenesis and direct shoot regeneration of rice (Oryza sativa L.) using thin cell layer culture of apical meristematic tissue. J Plant Physiol 157(5):559–565. https://doi.org/10.1016/s0176-1617(00)80112-1
Nordstrom A, Tarkowski P, Tarkowska D, Norbaek R, Astot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proc Natl Acad Sci U S A 101(21):8039–8044. https://doi.org/10.1073/pnas.0402504101
Nowak K, Gaj MD (2016) Transcription factors in the regulation of somatic embryogenesis. In: L-V V, O-A N (eds) Somatic embryogenesis: fundamental aspects and applications. Springer, Cham, pp 53–79
Nowak K, Wójcikowska B, Gaj MD (2014) ERF022 impacts the induction of somatic embryogenesis in Arabidopsis through the ethylene-related pathway. Planta 241(4):967–985. https://doi.org/10.1007/s00425-014-2225-9
O’Malley RC, Huang S-shan C, Song L, Lewsey Mathew G, Bartlett A, Nery Joseph R, Galli M, Gallavotti A, Ecker Joseph R (2016) Cistrome and epicistrome features shape the regulatory DNA landscape. Cell 165(5):1280–1292. https://doi.org/10.1016/j.cell.2016.08.063
Omelyanchuk NA, Wiebe DS, Novikova DD, Levitsky VG, Klimova N, Gorelova V, Weinholdt C, Vasiliev GV, Zemlyanskaya EV, Kolchanov NA, Kochetov AV, Grosse I, Mironova VV (2017) Auxin regulates functional gene groups in a fold-change-specific manner in Arabidopsis thaliana roots. Sci Rep 7(1):2489. https://doi.org/10.1038/s41598-017-02476-8
Piyatrakul P, Putranto R-A, Martin F, Rio M, Dessailly F, Leclercq J, Dufayard J-F, Lardet L, Montoro P (2012) Some ethylene biosynthesis and AP2/ERF genes reveal a specific pattern of expression during somatic embryogenesis in Hevea brasiliensis. BMC Plant Biol 12(1):244. https://doi.org/10.1186/1471-2229-12-244
Quiroz-Figueroa F, Mendez Z,M, Larque-Saavedra A, Loyola-Vargas V (2001) Picomolar concentrations of salicylates induce cellular growth and enhance somatic embryogenesis in Coffea arabica tissue culture. Plant Cell Rep 20(8):679–684. https://doi.org/10.1007/s002990100386
Raghavan V (2004) Role of 2,4-dichlorophenoxyacetic acid (2,4-D) in somatic embryogenesis on cultured zygotic embryos of Arabidopsis: cell expansion, cell cycling, and morphogenesis during continuous exposure of embryos to 2,4-D. Am J Bot 91(11):1743–1756. https://doi.org/10.3732/ajb.91.11.1743
Shi X, Dai X, Liu G, Bao M (2009) Enhancement of somatic embryogenesis in camphor tree (Cinnamomum camphora L.): osmotic stress and other factors affecting somatic embryo formation on hormone-free medium. Trees 23(5):1033–1042. https://doi.org/10.1007/s00468-009-0345-9
Su YH, Zhao XY, Liu YB, Zhang CL, O’Neill SD, Zhang XS (2009) Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J 59(3):448–460. https://doi.org/10.1111/j.1365-313X.2009.03880.x
Su YH, Liu YB, Bai B, Zhang XS (2015) Establishment of embryonic shoot-root axis is involved in auxin and cytokinin response during Arabidopsis somatic embryogenesis. Front Plant Sci 5:792. https://doi.org/10.3389/fpls.2014.00792
Sun T (2008) Gibberellin metabolism, perception and signaling pathways in Arabidopsis. Arabidopsis Book 6:e0103. https://doi.org/10.1199/tab.0103
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515. https://doi.org/10.1038/nbt.1621
Verma D, Joshi R, Shukla A, Kumar P (2011) Protocol for in vitro somatic embryogenesis and regeneration of rice (Oryza sativa L.). Indian J Exp Biol 49(12):958–963
Verma SK, Das AK, Cingoz GS, Uslu E, Gurel E (2016) Influence of nutrient media on callus induction, somatic embryogenesis and plant regeneration in selected Turkish crocus species. Biotechnol Rep (Amst) 10:66–74. https://doi.org/10.1016/j.btre.2016.03.006
Vondráková Z, Eliášová K, Fischerová L, Vágner M (2011) The role of auxins in somatic embryogenesis of Abies alba. Cent Eur J Biol 6(4):587–596. https://doi.org/10.2478/s11535-011-0035-7
Wickramasuriya AM, Dunwell JM (2015) Global scale transcriptome analysis of Arabidopsis embryogenesis in vitro. BMC Genomics 16:301. https://doi.org/10.1186/s12864-015-1504-6
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2(8):e718. https://doi.org/10.1371/journal.pone.0000718
Wójcik AM, Gaj MD (2016) miR393 contributes to the embryogenic transition induced in vitro in Arabidopsis via the modification of the tissue sensitivity to auxin treatment. Planta 244(1):231–243. https://doi.org/10.1007/s00425-016-2505-7
Wójcikowska B, Jaskóła K, Gąsiorek P, Meus M, Nowak K, Gaj MD (2013) LEAFY COTYLEDON2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis. Planta 238(3):425–440. https://doi.org/10.1007/s00425-013-1892-2
Wu Y, Dor E, Hershenhorn J (2016) Strigolactones affect tomato hormone profile and somatic embryogenesis. Planta 245(3):583–594. https://doi.org/10.1007/s00425-016-2625-0
Yu YB, Yang SF (1979) Auxin-induced ethylene production and its inhibition by aminoethyoxyvinylglycine and cobalt ion. Plant Physiol 64(6):1074–1077. https://doi.org/10.1104/pp.64.6.1074
Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009) Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21(9):2563–2577. https://doi.org/10.1105/tpc.109.068890
Zheng Q, Zheng Y, Perry SE (2013) AGAMOUS-Like15 promotes somatic embryogenesis in Arabidopsis and soybean in part by the control of ethylene biosynthesis and response. Plant Physiol 161(4):2113–2127. https://doi.org/10.1104/pp.113.216275
Zheng Q, Zheng Y, Ji H, Burnie W, Perry SE (2016) Gene regulation by the AGL15 transcription factor reveals hormone interactions in somatic embryogenesis. Plant Physiol 172(4):2374–2387. https://doi.org/10.1104/pp.16.00564
Zur I, Dubas E, Krzewska M, Janowiak F (2015) Current insights into hormonal regulation of microspore embryogenesis. Front Plant Sci 6:424. https://doi.org/10.3389/fpls.2015.00424
Acknowledgements
We are grateful to Z. Nasim (Korea University, South Korea) for his technical advices on bioinformatics analysis and to Dr. R. A. Putranto (Indonesian Research Institute for Biotechnology and Bioindustry, Indonesia) for the discussion during manuscript preparation.
Funding
This paper is also made possible through the support of Indonesian Endowment Fund for Education (LPDP) to R. T. Saptari.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Editor: Ewen Mullins
Electronic supplementary material
ESM 1
(DOCX 232 kb)
Rights and permissions
About this article
Cite this article
Saptari, R.T., Susila, H. Data mining study of hormone biosynthesis gene expression reveals new aspects of somatic embryogenesis regulation. In Vitro Cell.Dev.Biol.-Plant 55, 139–152 (2019). https://doi.org/10.1007/s11627-018-9947-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11627-018-9947-5