Abstract
Main conclusion
The possible molecular mechanisms regulating sorghum callus regeneration were revealed by RNA-sequencing.
Abstract
Plant callus regeneration has been widely applied in agricultural improvement. Recently, callus regeneration has been successfully applied in the genetic transformation of sorghum by using immature sorghum embryos as explants. However, the mechanism underlying callus regeneration in sorghum is still largely unknown. Here, we describe three types of callus (Callus I–III) with different redifferentiation abilities undergoing distinct induction from immature embryos of the Hiro-1 variety. Compared with nonembryonic Callus III, Callus I produced only some identifiable roots, and embryonic Callus II was sufficient to regenerate whole plants. Genome-wide transcriptome profiles were generated to reveal the underlying mechanisms. The numbers of differentially expressed genes for the three types of callus varied from 5906 to 8029. In accordance with the diverse regeneration abilities observed for different types of callus and leaf tissues, the principal component analysis revealed that the gene expression patterns of Callus I and Callus II were different from those of Callus III and leaves regenerated from Callus II. Notably, Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) analyses, pharmacological treatment, and substance content determinations revealed that plant ribosomes, lignin metabolic processes, and metabolism of starch and sucrose were significantly enriched, suggesting that these factors are associated with callus regeneration. These results helped elucidate the molecular regulation of three types of callus with different regeneration abilities in sorghum.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Armstrong CL, Green CE (1985) Establishment and maintenance of friable, embryogenic maize callus and the involvement of l-proline. Planta 164:207–214. https://doi.org/10.1007/BF00396083
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bout S, Vermerris W (2003) A candidate-gene approach to clone the sorghum Brown midrib gene encoding caffeic acid O-methyltransferase. Mol Genet Genomics 269:205–214. https://doi.org/10.1007/s00438-003-0824-4
Byrne ME (2009) A role for the ribosome in development. Trends Plant Sci 14:512–519. https://doi.org/10.1016/j.tplants.2009.06.009
Che P, Anand A, Wu E, Sander JD, Simon MK, Zhu W, Sigmund AL, Zastrow-Hayes G, Miller M, Liu D, Lawit SJ, Zhao ZY, Albertsen MC, Jones TJ (2018) Developing a flexible, high-efficiency Agrobacterium-mediated sorghum transformation system with broad application. Plant Biotechnol J 16:1388–1395. https://doi.org/10.1111/pbi.12879
Chen J, Zhang L, Zhu M, Han L, Lv Y, Liu Y, Li P, Jing H, Cai H (2018) Non-dormant axillary bud 1 regulates axillary bud outgrowth in sorghum. J Integr Plant Biol 60:938–955. https://doi.org/10.1111/jipb.12665
Chow PS, Landhäusser SM (2004) A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol 24:1129–1136. https://doi.org/10.1093/treephys/24.10.1129
Deng S, Dong Z, Zhan K, Hu Y, Yin D, Cui D (2009) Moderate desiccation dramatically improves shoot regeneration from maize (Zea mays L.) callus. Vitro Cell Dev Biol Plant 45:99–103. https://doi.org/10.1007/s11627-008-9154-x
Do PT, Lee H, Vasilchik KV, Kausch A, Zhang ZJ (2018) Rapid and efficient genetic transformation of sorghum via Agrobacterium-mediated method. Curr Protoc Plant Biol 3:e20077. https://doi.org/10.1002/cppb.20077
Haddon L, Northcote DH (1976) Correlation of the induction of various enzymes concerned with phenylpropanoid and lignin synthesis during differentiation of bean callus (Phaseolus vulgaris L.). Planta 28:255–262. https://doi.org/10.1007/BF00393237
Han L, Chen J, Mace ES, Liu Y, Zhu M, Yuyama N, Jordan DR, Cai H (2015) Fine mapping of qGW1, a major QTL for grain weight in sorghum. Theor Appl Genet 128:1813–1825. https://doi.org/10.1007/s00122-015-2549-2
Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U, de Vrieset SC (2001) The Arabidopsis somatic embryogenesis receptor kinase 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816. https://doi.org/10.1104/pp.127.3.803
Heidstra R, Sabatini S (2014) Plant and animal stem cells: similar yet different. Nat Rev Mol Cell Biol 15:301–312. https://doi.org/10.1038/nrm3790
Horiguchi G, Mollá-Morales A, Pérez-Pérez JM, Kojima K, Robles P, Ponce MR, Micol JL, Tsukaya H (2011) Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development. Plant J 65:724–736. https://doi.org/10.1111/j.1365-313X.2010.04457.x
Ibáñez S, Ruiz-Cano H, Fernández MA, Sánchez-García AB, Villanova J, Micol JL, Pérez-Pérezet JM (2019) A Network-guided genetic approach to identify novel regulators of adventitious root formation in Arabidopsis thaliana. Front Plant Sci 10:461. https://doi.org/10.3389/fpls.2019.00461
Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173. https://doi.org/10.1105/tpc.113.116053
Ikeuchi M, Ogawa Y, Iwase A, Sugimoto K (2016) Plant regeneration: cellular origins and molecular mechanisms. Development 143:1442–1451. https://doi.org/10.1242/dev.134668
Iwase A, Harashima H, Ikeuchi M, Ryman B, Ohnuma M, Komaki S, Morohashi K, Kurata T, Nakata M, Ohme-Takagi M, Grotewold E, Sugimoto K (2017) WIND1 promotes shoot regeneration through transcriptional activation of enhancer of shoot regeneration1 in Arabidopsis. Plant Cell 29:54–69. https://doi.org/10.1105/tpc.16.00623
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36. https://doi.org/10.1186/gb-2013-14-4-r36
Laurentin A, Edwards CA (2003) A microtiter modification of the anthrone-sulfuric acid colorimetric assay for glucose-based carbohydrates. Anal Biochem 315:143–145. https://doi.org/10.1016/s0003-2697(02)00704-2
Lee ST, Huang WL (2013) Cytokinin, auxin, and abscisic acid affects sucrose metabolism conduce to de novo shoot organogenesis in rice (Oryza sativa L.) callus. Bot Stud 54:5. https://doi.org/10.1186/1999-3110-54-5
Li Y, Wang W, Feng Y, Tu M, Wittich PE, Bate NJ, Messinget J (2019) Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes. Plant Biotechnol J 17:472–487. https://doi.org/10.1111/pbi.12991
Liu X, Lu T, Dou Y, Yu B, Zhang C (2014) Identification of RNA silencing components in soybean and sorghum. BMC Bioinformatics 15:4. https://doi.org/10.1186/1471-2105-15-4
Liu G, Gilding EK, Godwin ID (2015) A robust tissue culture system for sorghum [Sorghum bicolor (L) Moench]. S Afr J Bot 98:157–160. https://doi.org/10.1016/j.sajb.2015.03.179
Lotan T, Ohto M, Yee KM, West MA, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis Leafy Cotyledon1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205. https://doi.org/10.1016/s0092-8674(00)81463-4
Lowe K, Wu E, Wang N et al (2016) Morphogenic regulators Baby Boom and Wuschel improve monocot transformation. Plant Cell 28:1998–2015. https://doi.org/10.1105/tpc.16.00124
Ma L, Liu M, Yan Y, Qing C, Zhang X, Zhang Y, Long Y, Wang L, Pan L, Zou C, Li Z, Wang Y, Peng H, Pan G, Jiang Z, Shen Y (2018) Genetic dissection of maize embryonic callus regenerative capacity using multi-locus genome-wide association studies. Front Plant Sci 9:561. https://doi.org/10.3389/fpls.2018.00561
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
Mullet J, Morishige D, McCormick R, Truong S, Hilley J, McKinley B, Anderson R, Olson SN, Rooney W (2014) Energy sorghum-a genetic model for the design of C4 grass bioenergy crops. J Exp Bot 65:3479–3489. https://doi.org/10.1093/jxb/eru229
Naija S, Elloumi N, Jbir N, Ammar S, Kevers C (2008) Anatomical and biochemical changes during adventitious rooting of apple rootstocks MM 106 cultured in vitro. C R Biol 331:518–525. https://doi.org/10.1016/j.crvi.2008.04.002
Nelson-Vasilchik K, Hague J, Mookkan M, Zhang ZJ, Kausch A (2018) Transformation of recalcitrant sorghum varieties facilitated by Baby Boom and Wuschel2. Curr Protoc Plant Biol 3:e20076. https://doi.org/10.1002/cppb.20076
Ng TL, Karim R, Tan YS, Teh HF, Danial AD, Ho LS, Khalid N, Appleton DR, Harikrishna JA (2016) Amino acid and secondary metabolite production in embryogenic and non-embryogenic callus of fingerroot ginger (Boesenbergia rotunda). PLoS ONE 11:e0156714. https://doi.org/10.1371/journal.pone.0156714
Nishimura A, Ashikari M, Lin S, Takashi T, Angeles ER, Yamamoto T, Matsuoka M (2005) Isolation of a rice regeneration quantitative trait loci gene and its application to transformation systems. Proc Natl Acad Sci USA 102:11940–11944. https://doi.org/10.1073/pnas.0504220102
Palovaara J, Hallberg H, Stasolla C, Hakman I (2010) Comparative expression pattern analysis of WUSCHEL-related homeobox 2 (WOX2) and WOX8/9 in developing seeds and somatic embryos of the gymnosperm Picea abies. New Phytol 188:122–135. https://doi.org/10.1111/j.1469-8137.2010.03336.x
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Rahman M, Ware D, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The sorghum bicolor genome and the diversification of grasses. Nature 457:551–556. https://doi.org/10.1038/nature07723
Phat DT, Lee H, Mookkan M, Folk WR, Zhangyuan ZJ (2016) Rapid and efficient Agrobacterium-mediated transformation of sorghum (Sorghum bicolor) employing standard binary vectors and bar gene as a selectable marker. Plant Cell Rep 35:2065–2076. https://doi.org/10.1007/s00299-016-2019-6
Ritter H, Schulz GE (2004) Structural basis for the entrance into the phenylpropanoid metabolism catalyzed by phenylalanine ammonia-lyase. Plant Cell 16:3426–3436. https://doi.org/10.1105/tpc.104.025288
Scully ED, Gries T, Palmer NA, Sarath G, Funnell-Harris DL, Baird L, Twigg P, Seravalli J, Clemente TE, Sattleret SE (2018) Overexpression of SbMyb60 in Sorghum bicolor impacts both primary and secondary metabolism. New Phytol 217:82–104. https://doi.org/10.1111/nph.14815
Srinivasan C, Liu Z, Heidmann I, Supena ED, Fukuoka H, Joosen R, Lambalk J, Angenent G, Scorza R, Custers JB, Boutilier K (2007) Heterologous expression of the Baby Boom AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.). Planta 225:341–351. https://doi.org/10.1007/s00425-006-0358-1
Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) Leafy Cotyledon2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–11811. https://doi.org/10.1073/pnas.201413498
Sussex IM (2008) The scientific roots of modern plant biotechnology. Plant Cell 20:1189–1198. https://doi.org/10.1105/tpc.108.058735
Tetreault HM, Scully ED, Gries T, Palmer NA, Funnell-Harris DL, Baird L, Seravalli J, Dien BS, Sarath G, Clemente TE, Sattler SE (2018) Overexpression of the sorghum bicolor SbCCoAOMT alters cell wall associated hydroxycinnamoyl groups. PLoS ONE 13:e0204153. https://doi.org/10.1371/journal.pone.0204153
Verma DC, Dougall DK (1977) Influence of carbohydrates on quantitative aspects of growth and embryo formation in wild carrot suspension cultures. Plant Physiol 59:81–85. https://doi.org/10.1104/pp.59.1.81
Wang X, Yang Z, Wang M, Meng L, Jiang Y, Han Y (2014) The Branching Enzyme1 gene, encoding a glycoside hydrolase family 13 protein, is required for in vitro plant regeneration in Arabidopsis. Plant Cell Tissue Organ Cult 117:279–291. https://doi.org/10.1007/s11240-014-0439-y
Weis BL, Kovacevic J, Missbach S, Schleiff E (2015) Plant-specific features of ribosome biogenesis. Trends Plant Sci 20:729–740. https://doi.org/10.1016/j.tplants.2015.07.003
Wu E, Zhao ZY (2017) Agrobacterium-mediated sorghum transformation. Methods Mol Biol 1669:355–364. https://doi.org/10.1007/978-1-4939-7286-9_26
Xu L (2018) De novo root regeneration from leaf explants: wounding, auxin, and cell fate transition. Curr Opin Plant Biol 41:39–45. https://doi.org/10.1016/j.pbi.2017.08.004
Xu L, Huang H (2014) Genetic and epigenetic controls of plant regeneration. Curr Top Dev Biol 108:1–33. https://doi.org/10.1016/B978-0-12-391498-9.00009-7
Zhang Y, Peng L, Wu Y, Shen Y, Wu X, Wang J (2014) Analysis of global gene expression profiles to identify differentially expressed genes critical for embryo development in Brassica rapa. Plant Mol Biol 86:425–442. https://doi.org/10.1007/s11103-014-0238-1
Zhang X, Wang Y, Yan Y, Peng H, Long Y, Zhang Y, Jiang Z, Liu P, Zou C, Peng H, Pan G, Shen Y (2019) Transcriptome sequencing analysis of maize embryonic callus during early redifferentiation. BMC Genomics 20:159. https://doi.org/10.1186/s12864-019-5506-7
Acknowledgements
We thank Dr. Hongwei Cai (China Agricultural University) for providing Hiro-1 seeds. The seeds of Hiro-1, a variety of sorghum with small grains from Japan (Han et al. 2015), used in this study were provided by Dr. Hongwei Cai of China Agricultural University (Yuanmingyuan West Road, Beijing, 100193, China). We thank Xiang Peng (China Three Gorges University) for collecting RNA-seq samples. This work was supported by funds from the National Natural Science Foundation of China grants 31900427 (to CZ) and 31371596 (to DZ), the Natural Science Foundation of Hubei Provincial Department of Education (Q20191207) to CZ, the Initial Project for High-Level Personnel of China Three Gorges University to CZ, the Open Project of Hubei Key Laboratory of Wudang Local Chinese Medicine Research (Hubei University of Medicine) (Grant No. WDCM2019009) to CZ, and the Principle Investigator Program (HBMUPI202104) to YZ.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Anastasios Melis.
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
Zhou, C., Wang, S., Zhou, H. et al. Transcriptome sequencing analysis of sorghum callus with various regeneration capacities. Planta 254, 33 (2021). https://doi.org/10.1007/s00425-021-03683-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-021-03683-4