Abstract
Recalcitrant plants are difficult to handle in tissue culture, and this limits their accessibility for various studies. Novel strategies are being developed to compensate the restricted nature of these plants to make them more adapted to tissue culture applications. Sorghum is one of the most recalcitrant plants with decreased efficiency and non-standardized tissue culture protocols. The advances in embryogenic genes ease the somatic embryo formation and regeneration ability in sorghum. BABY BOOM (BBM) is the most prominent transcription factor involved in somatic embryogenesis, even without exogenous auxin application, the spontaneous somatic embryo formation could occur in plants, which makes this gene(s) an optimal target for recalcitrant plants. This study is designed to characterize SbBBM-like genes in sorghum. Two similar length of protein pairs, SbBBM-like 1 (XP_021313568.1) and SbBBM-like 2 (XP_002452443.1), were identified in cv. Aldarı and cis-regulatory elements of these proteins were observed to be involved in particularly light response and hormonal regulation. The protein –protein interaction data indicated possible role in auxin mechanism. The expression data showed SbBBM-like was highly expressed in seedling root and embryogenic callus, however the expression was highest in embryogenic callus for SbBBM-like 2 with almost 200-fold increase, compared to other tissues.
Similar content being viewed by others
Change history
07 November 2022
A Correction to this paper has been published: https://doi.org/10.1007/s42976-022-00325-7
References
Awasthi P, Sharma V, Kaur N, Kaur N, Pandey P, Tiwari S (2017) Genome-wide analysis of transcription factors during somatic embryogenesis in banana (Musa spp.) cv. Grand Naine. PLoS One 12(8):e0182242. https://doi.org/10.1371/journal.pone.0182242
Bilichak A, Luu J, Jiang F, Eudes F (2018) Identification of BABY BOOM homolog in bread wheat. Agri Gene 7:43–51. https://doi.org/10.1016/j.aggene.2017.11.002
Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AAM, Miki BLA, Custers JBM, van Lookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14(8):1737–1749. https://doi.org/10.1105/tpc.001941
Braybrook SA, Stone SL, Park S, Bui AQ, Le BH, Fischer RL, Goldberg RB, Harada JJ (2006) Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci 103(9):3468–3473. https://doi.org/10.1073/pnas.0511331103
Bui LT, Pandzic D, Youngstrom CE, Wallace S, Irish EE, Szovenyi P, Cheng CL (2017) A fern AINTEGUMENTA gene mirrors BABY BOOM in promoting apogamy in Ceratopteris richardii. Plant J 90:122–132. https://doi.org/10.1111/tpj.13479
Chege P, Palagyi A, Lantos C, Kiss E, Pauk J (2020) Improved culture media for embryogenic callus generation in sorghum [Sorghum bicolor (L.) Moench]. Phyton 89(1):111–119. https://doi.org/10.32604/phyton.2020.07554
Chen Y, Xu X, Liu Z, Zhang Z, XuHan X, Lin Y, Lai Z (2020) Global scale transcriptome analysis reveals differentially expressed genes involve in early somatic embryogenesis in Dimocarpus longan Lour. BMC Genomics 21:4. https://doi.org/10.1186/s12864-019-6393-7
Conner JA, Mookkan M, Huo H, Chae K, Ozias-Akins P (2015) A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant. Proc Natl Acad Sci 112(36):11205–11210. https://doi.org/10.1073/pnas.1505856112
Conner JA, Podio M, Ozias-Akins P (2017) Haploid embryo production in rice and maize induced by PsASGR-BBML transgenes. Plant Reprod 30(1): 41–52. https://doi.org/10.1007/s00497-017-0298-x
da Silva GM, da Cruz AC, Otoni WC, Pereira TN, Rocha DI, da Silva ML (2015) Histochemical evaluation of induction of somatic embryogenesis in Passiflora edulis Sims (Passifloraceae). In Vitro Cell Dev Biol Plant 51(5): 539–545.https://doi.org/10.1007/s11627-015-9699-4
Davidson RM, Gowda M, Moghe G, Lin H, Vaillancourt B, Shiu SH, Jiang N, Robin Buell C (2012) Comparative transcriptomics of three Poaceae species reveals patterns of gene expression evolution. Plant J 71(3): 492–502. https://doi.org/10.1111/j.1365-313X.2012.05005.x
Dugas DV, Monaco MK, Olson A, Klein RR, Kumari S, Ware D, Klein PE (2011) Functional annotation of the transcriptome of Sorghum bicolor in response to osmotic stress and abscisic acid. BMC Genomics 12(1):1–21. https://doi.org/10.1186/1471-2164-12-514
El Ouakfaoui S, Schnell J, Abdeen A, Colville A, Labbé H, Han S, Baum B, Laberge S, Miki B (2010) Control of somatic embryogenesis and embryo development by AP2 transcription factors. Plant Mol Biol 74(4–5): 313–326. https://doi.org/10.1007/s11103-010-9674-8
Florez SL, Erwin RL, Maximova SN, Guiltinan MJ, Curtis WR (2015) Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor. BMC Plant Biol 15(1): 1–13. https://doi.org/10.1186/s12870-015-0479-4
Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222(6):977–988. https://doi.org/10.1007/s00425-005-0041-y
Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449(7165): 1053–1057. https://doi.org/10.1038/nature06206
Garcês H, Sinha N (2009) The ‘mother of thousands’ (Kalanchoe daigremontiana): a plant model for asexual reproduction and CAM studies. Cold Spring Harb Protoc. https://doi.org/10.1101/pdb.emo133
Gelli M, Duo Y, Konda AR, Zhang C, Holding D, Dweikat I (2014) Identification of differentially expressed genes between sorghum genotypes with contrasting nitrogen stress tolerance by genome-wide transcriptional profiling. BMC Genomics 15(1):1–16. https://doi.org/10.1186/1471-2164-15-179
Gulzar B, Malik MQ, Sayeed R, Mamgain J, Ejaz B (2020) Genes, proteins and other networks regulating somatic embryogenesis in plants. J Genet Eng Biotechnol 18: 31. https://doi.org/10.1186/s43141-020-00047-5
Harding EW, Tang W, Nichols KW, Fernandez DE, Perry SE (2003) Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-Like 15. Plant Pysiol 133(2):653–663. https://doi.org/10.1104/pp.103.023499
Heidmann I, De Lange B, Lambalk J, Angenent GC, Boutilier K (2011) Efficient sweet pepper transformation mediated by the BABY BOOM transcription factor. Plant Cell Rep 30(6):1107–1115. https://doi.org/10.1007/s00299-011-1018-x
Horstman A, Bemer M, Boutilier K (2017) A transcriptional view on somatic embryogenesis. Regeneration 4(4):201–216. https://doi.org/10.1002/reg2.91
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Irikova T, Grozeva S, Denev I (2012) Identification of BABY BOOM and LEAFY COTYLEDON genes in sweet pepper (Capsicum annuum L.) genome by their partial gene sequences. Plant Growth Regul 67:191–198. https://doi.org/10.1007/s10725-012-9676-4
Jiménez VM (2001) Regulation of in vitro somatic embryogenesis with emphasis on to the role of endogenous hormones. Rev Bras Fisiol Veg 13(2):196–223. https://doi.org/10.1590/S0103-31312001000200008
Kagaya Y, Toyoshima R, Okuda R, Usui H, Yamamoto A, Hattori T (2005) LEAFY COTYLEDON 1 controls seed storage proteins through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE 3. Plant Cell Physiol 46(3):399–406. https://doi.org/10.1093/pcp/pci048
Khanday I, Skinner D, Yang B, Mercier R, Sundaresan V (2019) A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds. Nature 565(7737):91–95. https://doi.org/10.1038/s41586-018-0785-8
Kulinska-Lukaszek K, Tobojka M, Adamiok A, Kurczynska EU (2012) Expression of the BBM gene during somatic embryogenesis of Arabidopsis thaliana. Biol Plant 56(2):389–394. https://doi.org/10.1007/s10535-012-0105-3
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23(21):2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho MJ, Scelonge C, Lenderts B, Chamberlin M, Cushatt J, Wang L, Ryan L, Khan T, Chow-Yiu J, Hua W, Yu M, Banh J, Bao Z, Brink K, Igo E, Rudrappa B, Shamseer PM, Bruce W, Newman L, Shen B, Zheng P, Bidney D, Falco C, Register J, Zhao ZY, Xu D, Jones T, Gordon-Kamm W (2016) Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell 28(9):1998–2015. https://doi.org/10.1105/tpc.16.00124
Lowe K, Rota ML, Hoerster G, Hastings C, Wang N, Chamberlin M, Wu E, Jones T, Gordon-Kamm W (2018) Rapid genotype “independent” Zea mays L. (maize) transformation via direct somatic embryogenesis. In Vitro Cell Dev Biol 54(3): 240–252. https://doi.org/10.1007/s11627-018-9905-2
Lutz KA, Martin C, Khairzada S, Maliga P (2015) Steroid-inducible BABY BOOM system for development of fertile Arabidopsis thaliana plants after prolonged tissue culture. Plant Cell Rep 34(10):1849–1856. https://doi.org/10.1007/s00299-015-1832-7
Maeo K, Tokuda T, Ayame A, Mitsui N, Kawai T, Tsukagoshi H, Ishiguro S, Nakamura K (2009) An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis. Plant J 60(3):476–487. https://doi.org/10.1111/j.1365-313X.2009.03967.x
Maher MF, Nasti RA, Vollbrecht M, Starker CG, Clark MD, Voytas DF (2020) Plant gene editing through de novo induction of meristems. Nat Biotechnol 38(1):84–89. https://doi.org/10.1038/s41587-019-0337-2
Makita Y, Shimada S, Kawashima M, Kondou-Kuriyama T, Toyoda T, Matsui M (2015) MOROKOSHI: transcriptome database in Sorghum bicolor. Plant Cell Physiol 56(1):e6–e6. https://doi.org/10.1093/pcp/pcu187
Maulidiya AUK, Sugiharto B, Deanti P, Handoyo T (2020) Expression of somatic embryogenesis-related genes in sugarcane (Saccharum ofcinarum L.). J Crop Sci Biotechnol. https://doi.org/10.1007/s12892-020-00024-x
Meinke DW (1992) A homoeotic mutant of Arabidopsis thaliana with leafy cotyledons. Science 258(5088):1647–1650. https://doi.org/10.1126/science.258.5088.1647
Mookkan M, Nelson-Vasilchik K, Hague J, Zhang ZJ, Kausch AP (2017) Selectable marker independent transformation of recalcitrant maize inbred B73 and sorghum P898012 mediated by morphogenic regulators BABY BOOM and WUSCHEL2. Plant Cell Rep 36:1477–1491. https://doi.org/10.1007/s00299-017-2169-1
Passarinho P, Ketelaar T, Xing M, van Arkel J, Maliepaard C, Hendriks MW, Joosen R, Lammers M, Herdies L, Boer B, van der Geest L, Boutilier K (2008) BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways. Plant Mol Biol 68(3):225–237. https://doi.org/10.1007/s11103-008-9364-y
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29(9):e45–e45. https://doi.org/10.1093/nar/29.9.e45
Pola SR, Mani NS (2006) Somatic embryogenesis and plantlet regeneration in Sorghum bicolor (L.) Moench, from leaf segments. J Cell Mol Biol 5:99–107
Ramulifho E, Goche T, Van As J, Tsilo TJ, Chivasa S, Ngara R (2019) Establishment and characterization of callus and cell suspension cultures of selected Sorghum bicolor (L.) Moench varieties: a resource for gene discovery in plant stress biology. Agronomy 9(5):218. https://doi.org/10.3390/agronomy9050218
Steward FC, Mapes MO, Mears K (1958) Growth and organized development of cultured cells. Organisation in cultures grown from freely suspended cells. Am J Bot 45:705–708. https://doi.org/10.1002/j.1537-2197.1958.tb10599.x
Sudhakar Reddy P, Srinivas Reddy D, Sivasakthi K, Bhatnagar-Mathur P, Vadez V, Sharma KK (2016) Evaluation of sorghum [Sorghum bicolor (L.)] reference genes in various tissues and under abiotic stress conditions for quantitative real-time PCR data normalization. Front Plant Sci 7:529. https://doi.org/10.3389/fpls.2016.00529
Thakare D, Tang W, Hill K, Perry SE (2008) The MADS-domain transcriptional regulator AGAMOUS-LIKE 15 promotes somatic embryo development in Arabidopsis and soybean. Plant Physiol 146:1663–1672. https://doi.org/10.1104/pp.108.115832
Valencia-Lozano E, Ibarra JE, Herrera-Ubaldo H, De Folter S, Cabrera-Ponce JL (2021) Osmotic stress-induced somatic embryo maturation of coffee Coffea arabica L., shoot and root apical meristems development and robustness. Sci Rep 11:9661. https://doi.org/10.1038/s41598-021-88834-z
Wen L, Li W, Parris S, West M, Lawson J, Smathers M, Li Z, Jones D, Jin S, Saski CA (2020) Transcriptomic profiles of non-embryogenic and embryogenic callus cells in a highly regenerative upland cotton line (Gossypium hirsutum L.). BMC Dev Biol 20:25. https://doi.org/10.1186/s12861-020-00230-4
Yang HF, Kou YP, Gao B, Soliman TMA, Xu KD, Ma N, Cao X, Zhao LJ (2014) Identification and functional analysis of BABY BOOM genes from Rosa canina. Biol Plant 58(3):427–435. https://doi.org/10.1007/s10535-014-0420-y
Yavuz C, Tillaboeva S, Bakhsh A (2020) Apprehending the potential of BABY BOOM transcription factors to mitigate cotton regeneration and transformation. J Cotton Res 3(1):1–14. https://doi.org/10.1186/s42397-020-00071-3
Yazawa T, Kawahigashi H, Matsumoto T, Mizuno H (2013) Simultaneous transcriptome analysis of Sorghum and Bipolaris sorghicola by using RNA-seq in combination with de novo transcriptome assembly. PLoS ONE 8(4):e62460. https://doi.org/10.1371/journal.pone.0062460
Zhao M, Li Q, Chen Z, Lv Q, Bao F, Wang X, He Y (2018) Regulatory Mechanism of ABA and ABI3 on Vegetative Development in the Moss Physcomitrella patens. Int J Mol Sci 19(9):2728. https://doi.org/10.3390/ijms19092728
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
Zhou J, Tang X, Martin GB (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J 16(11):3207–3218. https://doi.org/10.1093/emboj/16.11.3207
Zuo J, Niu Q-W, Frugis G, Chua N-H (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359. https://doi.org/10.1046/j.1365-313x.2002.01289.x
Acknowledgements
We greatly appreciate Shakhnozakhan Tillaboeva for improving the use of English in the manuscript. This research is a part of PhD work.
Funding
This research was awarded funding from Nigde Omer Halisdemir University Research Project Units, project no TGT 2021/7-HIDEP.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Consent for publication
Authors do have consent for publication.
Additional information
The original version of this article has been revised: A sentence has been added to the Acknowledgements section.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yavuz, C., Çalışkan, M.E. Identification of BABY BOOM-like genes (SbBBM) in Sorghum [(Sorghum bicolor) L. Moench]. CEREAL RESEARCH COMMUNICATIONS 50, 667–676 (2022). https://doi.org/10.1007/s42976-021-00210-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42976-021-00210-9