Czech J. Genet. Plant Breed., 2023, 59(4):235-252 | DOI: 10.17221/16/2023-CJGPB

Transcriptome profiling of Sorghum bicolor reveals cultivar-specific molecular signatures associated with starch and phenolic compounds biosyntheses and accumulation during sorghum grain developmentOriginal Paper

Li Wang1, Derang Ni2, Fan Yang3, Lin Lin3, Yubo Yang3, Chongde Sun4, Xingqian Ye2, Jinping Cao5, Xiangli Kong4
1 Kweichow Moutai Group, Renhuai, P.R.China
2 College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou, P.R. China
3 Kweichow Moutai Corporation Limited, Renhuai, P.R. China
4 College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, P.R. China
5 The Rural Development Academy, Zhejiang University, Hangzhou, P.R. China

Sorghum is an important crop, and starch and phenolic compounds are major and important components in the sorghum grain. However, the underlying critical genetic elements contributing to the rich portfolio of nutrients in sorghum grains are largely unknown. Transcriptomic methods were employed to characterize the expression patterns at five different grain developmental stages of Hongyingzi (an important brewing sorghum), and another two grain sorghums, Jinuoliang 1 and Hongliangfeng 1, for comparison. The uniquely expressed genes were identified at each developmental stage of Hongyingzi when compared with the other two sorghum cultivars. The co-regulated genes at different developmental stages and the regulatory network were determined; the determinant genes and single-nucleotide polymorphisms located at the promoters of these genes involved in starch and phenolic compounds biosynthetic pathways were also identified. These results will provide insights into the potential regulatory network and further contribute to the clarification of the key determinant genes involved in the biosyntheses of starch and phenolic compounds. Meanwhile, some new transcripts and genes were identified at five different developmental stages of grains of the three sorghum cultivars. Our work can provide impetus for further study of the genes responsible for the biosynthesis of starch and phenolic compounds in the sorghum grain, and pave a way for functional validation of a batch of potential genes and single-nucleotide polymorphisms proposed in current work.

Keywords: biosynthesis; phenolic compounds; sorghum; starch; transcriptome profiling

Received: February 14, 2023; Revised: April 3, 2023; Accepted: April 11, 2023; Prepublished online: June 1, 2023; Published: September 11, 2023  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Wang L, Ni D, Yang F, Lin L, Yang Y, Sun C, et al.. Transcriptome profiling of Sorghum bicolor reveals cultivar-specific molecular signatures associated with starch and phenolic compounds biosyntheses and accumulation during sorghum grain development. Czech J. Genet. Plant Breed. 2023;59(4):235-252. doi: 10.17221/16/2023-CJGPB.
Download citation

Supplementary files:

Download fileWang_ESM.pdf

File size: 567.63 kB

References

  1. Adom K.K., Liu R.H. (2002): Antioxidant activity of grains. Journal of Agricultural and Food Chemistry, 50: 6182-6187. Go to original source... Go to PubMed...
  2. Bloom J.S., Khan Z., Kruglyak L., Singh M., Caudy A.A. (2009): Measuring differential gene expression by short read sequencing: Quantitative comparison to 2-channel gene expression microarrays. BMC Genomics, 10: 221. Go to original source... Go to PubMed...
  3. Bolger A.M., Lohse M., Usadel B. (2014): Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30: 2114-2120. Go to original source... Go to PubMed...
  4. Boyles R.E., Pfeiffer B.K., Cooper E.A., Rauh B.L., Zielinski K.J., Myers M.T., Brenton Z., Rooney W.L., Kresovich S. (2017): Genetic dissection of sorghum grain quality traits using diverse and segregating populations. Theoretical and Applied Genetics, 130: 697-716. Go to original source... Go to PubMed...
  5. Buchfink B., Xie C., Huson D.H. (2015): Fast and sensitive protein alignment using DIAMOND. Nature Methods, 12: 59-60. Go to original source... Go to PubMed...
  6. Campbell B.C., Gilding E.K., Mace E.S., Tai S., Tao Y., Prentis P.J., Thomelin P., Jordan D.R., Godwin I.D. (2016): Domestication and the storage starch biosynthesis pathway: Signatures of selection from a whole sorghum genome sequencing strategy. Plant Biotechnology Journal, 14: 2240-2253. Go to original source... Go to PubMed...
  7. Chen B.R., Wang C.Y., Wang P., Zhu Z.X., Xu N., Shi G.S., Yu M., Wang N., Li J.H., Hou J.M., Li S.J., Zhou Y.F., Gao S.J., Lu X.C., Huang R.D. (2019): Genome-wide association study for starch content and constitution in sorghum (Sorghum bicolor (L.) Moench). Journal of Integrative Agriculture, 18: 2446-2456. Go to original source...
  8. Chen Y., Chen Y., Shi C., Huang Z., Zhang Y., Li S., Li Y., Ye J., Yu C., Li Z., Zhang X., Wang J., Yang H., Fang L., Chen Q. (2018): SOAPnuke: A MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. Gigascience, 7: 1-6. Go to original source... Go to PubMed...
  9. de Morais Cardoso L., Pinheiro S.S., Martino H.S., Pinheiro-Sant'Ana H.M. (2017): Sorghum (Sorghum bicolor L.): Nutrients, bioactive compounds, and potential impact on human health. Critical Reviews in Food Science and Nutrition, 57: 372-390. Go to original source... Go to PubMed...
  10. Dong W., He F., Jiang H., Liu L., Qiu Z. (2021): Comparative transcriptome sequencing of taro corm development with a focus on the starch and sucrose metabolism pathway. Frontiers in Genetics, 12: 771081. Go to original source... Go to PubMed...
  11. Eddy S.R. (1998): Profile hidden Markov models. Bioinformatics, 14: 755-763. Go to original source... Go to PubMed...
  12. Habyarimana E., Dall'Agata M., De Franceschi P., Baloch F.S. (2019): Genome-wide association mapping of total antioxidant capacity, phenols, tannins, and flavonoids in a panel of Sorghum bicolor and S. bicolor × S. halepense populations using multi-locus models. PLoS ONE, 14: e0225979. Go to original source... Go to PubMed...
  13. Hu Z., Olatoye M.O., Marla S., Morris G.P. (2019): An integrated genotyping-by-sequencing polymorphism map for over 10,000 sorghum genotypes. Plant Genome, 12: 180044. Go to original source... Go to PubMed...
  14. James M.G., Denyer K., Myers A.M. (2003): Starch synthesis in the cereal endosperm. Current Opinion in Plant Biology, 6: 215-222. Go to original source... Go to PubMed...
  15. Ke F., Zhang K., Li Z., Wang J., Zhang F., Wu H., Zhang Z., Lu F., Wang Y., Duan Y., Liu Z., Zou J., Zhu K. (2022): Transcriptomic analysis of starch accumulation patterns in different glutinous sorghum seeds. Scientific Reports, 12: 11133. Go to original source... Go to PubMed...
  16. Kim D., Langmead B., Salzberg S.L. (2015): HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 12: 357-360. Go to original source... Go to PubMed...
  17. Kimani W., Zhang L.M., Wu X.Y., Hao H.Q., Jing H.C. (2020): Genome-wide association study reveals that different pathways contribute to grain quality variation in sorghum (Sorghum bicolor). BMC Genomics, 21: 112. Go to original source... Go to PubMed...
  18. Kong L., Zhang Y., Ye Z.Q., Liu X.Q., Zhao S.Q., Wei L., Gao G. (2007): CPC: Assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Research, 35: W345-349. Go to original source... Go to PubMed...
  19. Kumar L., Futschik E.M. (2007): Mfuzz: A software package for soft clustering of microarray data. Bioinformation, 2: 5-7. Go to original source... Go to PubMed...
  20. Langfelder P., Horvath S. (2008): WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 9: 559. Go to original source... Go to PubMed...
  21. Langmead B., Salzberg S.L. (2012): Fast gapped-read alignment with Bowtie 2. Nature Methods, 9: 357-359. Go to original source... Go to PubMed...
  22. Li B., Dewey C.N. (2011): RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12: 323. Go to original source... Go to PubMed...
  23. Margraf T., Karnopp A.R., Rosso N.D., Granato D. (2015): Comparison between Folin-Ciocalteu and Prussian blue assays to estimate the total phenolic content of juices and teas using 96-well microplates. Journal of Food Science, 80: C2397-2403. Go to original source... Go to PubMed...
  24. Marioni J.C., Mason C.E., Mane S.M., Stephens M., Gilad Y. (2008): RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Research, 18: 1509-1517. Go to original source... Go to PubMed...
  25. McKenna A., Hanna M., Banks E., Sivachenko A., Cibulskis K., Kernytsky A., Garimella K., Altshuler D., Gabriel S., Daly M., DePristo M.A. (2010): The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20: 1297-1303. Go to original source... Go to PubMed...
  26. Mitchell G.A. (1990): Methods of Starch Analysis. Starch-Stärke, 42: 131-134. Go to original source...
  27. Nesi N., Debeaujon I., Jond C., Stewart A.J., Jenkins G.I., Caboche M., Lepiniec L. (2002): The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell, 14: 2463-2479. Go to original source... Go to PubMed...
  28. Pertea M., Pertea G.M., Antonescu C.M., Chang T.C., Mendell J.T., Salzberg S.L. (2015): StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology, 33: 290-295. Go to original source... Go to PubMed...
  29. Rice P., Longden I., Bleasby A. (2000): EMBOSS: The European Molecular Biology Open Software Suite. Trends in Genetics, 16: 276-277. Go to original source... Go to PubMed...
  30. Sanseverino W., Roma G., De Simone M., Faino L., Melito S., Stupka E., Frusciante L., Ercolano M.R. (2010): PRGdb: A bioinformatics platform for plant resistance gene analysis. Nucleic Acids Research, 38: D814-821. Go to original source... Go to PubMed...
  31. Scully E.D., Gries T., Sarath G., Palmer N.A., Baird L., Serapiglia M.J., Dien B.S., Boateng A.A., Ge Z., Funnell-Harris D.L., Twigg P., Clemente T.E., Sattler S.E. (2016): Overexpression of SbMyb60 impacts phenylpropanoid biosynthesis and alters secondary cell wall composition in Sorghum bicolor. Plant Journal, 85: 378-395. Go to original source... Go to PubMed...
  32. Shen S., Park J.W., Lu Z.X., Lin L., Henry M.D., Wu Y.N., Zhou Q., Xing Y. (2014): rMATS: Robust and flexible detection of differential alternative splicing from replicate RNA-Seq data. Proceedings of the National Academy of Sciences of the USA, 111: E5593-5601. Go to original source... Go to PubMed...
  33. Shen S., Huang R., Li C., Wu W., Chen H., Shi J., Chen S., Ye X. (2018): Phenolic compositions and antioxidant activities differ significantly among sorghum grains with different applications. Molecules, 23: 1203. Go to original source... Go to PubMed...
  34. Shi L., Wang J., Liu Y., Ma C., Guo S., Lin S., Wang J. (2021): Transcriptome analysis of genes involved in starch biosynthesis in developing Chinese chestnut (Castanea mollissima Blume) seed kernels. Scientific Reports, 11: 3570. Go to original source... Go to PubMed...
  35. Singleton V.L., Orthofer R., Lamuela-Raventós R.M. (1999): Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology, 229: 152-178. Go to original source...
  36. Tetlow I.J., Morell M.K., Emes M.J. (2004): Recent developments in understanding the regulation of starch metabolism in higher plants. Journal of Experimental Botany, 55: 2131-2145. Go to original source... Go to PubMed...
  37. Tetlow I.J., Beisel K.G., Cameron S., Makhmoudova A., Liu F., Bresolin N.S., Wait R., Morell M.K., Emes M.J. (2008): Analysis of protein complexes in wheat amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiology, 146: 1878-1891. Go to original source... Go to PubMed...
  38. Trapnell C., Roberts A., Goff L., Pertea G., Kim D., Kelley D.R., Pimentel H., Salzberg S.L., Rinn J.L., Pachter L. (2012): Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols, 7: 562-578. Go to original source... Go to PubMed...
  39. Wang L., Feng Z., Wang X., Wang X., Zhang X. (2010). DEGseq: An R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics, 26: 136-138. Go to original source... Go to PubMed...
  40. Wu Y., Li X., Xiang W., Zhu C., Lin Z., Wu Y., Li J., Pandravada S., Ridder D.D., Bai G., Wang M. L., Trick H.N., Beane S.R., Tuinstra M.R., Tesso T.T., Yu J. (2012): Presence of tannins in sorghum grains is conditioned by different natural alleles of Tannin1. Proceedings of the National Academy of Sciences of the USA, 109: 10281-10286. Go to original source... Go to PubMed...
  41. Wu Y., Guo T., Mu Q., Wang J., Li X., Wu Y., Tian B., Wang M.L., Bai G., Perumal R., Trick H.N., Bean S.R., Dweikat I.M., Tuinstra M.R., Morris G., Tesso T.T., Yu J., Li X. (2019): Allelochemicals targeted to balance competing selections in African agroecosystems. Nature Plants, 5: 1229-1236. Go to original source... Go to PubMed...
  42. Xiong Y., Zhang P., Warner R.D., Fang Z. (2019): Sorghum grain: from genotype, nutrition, and phenolic profile to its health benefits and food applications. Comprehensive Reviews in Food Science and Food Safety, 18: 2025-2046. Go to original source... Go to PubMed...
  43. Xu W., Bobet S., Le Gourrierec J., Grain D., De Vos D., Berger A., Salsac F., Kelemen Z., Boucherez J., Rolland A., Mouille G., Routaboul J.M., Lepiniec L., Dubos C. (2017): TRANSPARENT TESTA 16 and 15 act through different mechanisms to control proanthocyanidin accumulation in Arabidopsis testa. Journal of Experimental Botany, 68: 2859-2870. Go to original source... Go to PubMed...
  44. Yang Q., Yuan Y., Liu J., Han M., Li J., Jin F., Feng B. (2023): Transcriptome analysis reveals new insights in the starch biosynthesis of non-waxy and waxy broomcorn millet (Panicum miliaceum L.). International Journal of Biological Macromolecules, 230: 123155. Go to original source... Go to PubMed...
  45. Yin H., Chen L., Li X.Y., Chen Q.M., Yi M.F. (2008): Analysis and improvement of high-quality RNA extraction in leaves of lily. Journal of China Agricultural University, 13: 41-45. (in Chinese)
  46. Zhou Y., Lv J., Yu Z., Wang Z., Li Y., Li M., Deng Z., Xu Q., Cui F., Zhou W. (2022): Integrated metabolomics and transcriptomic analysis of the flavonoid regulatory networks in Sorghum bicolor seeds. BMC Genomics, 23: 619. Go to original source... Go to PubMed...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.