Identification of genetic variants controlling diosgenin content in Dioscorea zingiberensis tuber by genome-wide association study.
Dioscorea Zingiberensis
Breeding
Diosgenin
Enzyme
P450
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
13 Jun 2024
13 Jun 2024
Historique:
received:
27
11
2023
accepted:
10
05
2024
medline:
14
6
2024
pubmed:
14
6
2024
entrez:
13
6
2024
Statut:
epublish
Résumé
Diosgenin is an important steroidal precursor renowned for its diverse medicinal uses. It is predominantly sourced from Dioscorea species, particularly Dioscorea zingiberensis. Dioscorea zingiberensis has an ability to accumulate 2-16% diosgenin in its rhizomes. In this study, a diverse population of 180 D. zingiberensis accessions was used to evaluate the genomic regions associated with diosgenin biosynthesis by the genome wide association study approach (GWAS). The whole population was characterized for diosgenin contents from tubers by gas chromatography mass spectrometry. The individuals were genotyped by the genotyping-by-sequencing approach and 10,000 high-quality SNP markers were extracted for the GWAS. The highest significant marker-trait-association was observed as an SNP transversion (G to T) on chromosome 10, with 64% phenotypic variance explained. The SNP was located in the promoter region of CYP94D144 which is a member of P450 gene family involved in the independent biosynthesis of diosgenin from cholesterol. The transcription factor (TF) binding site enrichment analysis of the promoter region of CYP94D144 revealed NAC TF as a potential regulator. The results were further validated through expression profiling by qRT-PCR, and the comparison of high and low diosgenin producing hybrids obtained from a bi-parental population. This study not only enhanced the understanding of the genetic basis of diosgenin biosynthesis but also serves as a valuable reference for future genomic investigations on CYP94D144, with the aim of augmenting diosgenin production in yam tubers.
Sections du résumé
BACKGROUND
BACKGROUND
Diosgenin is an important steroidal precursor renowned for its diverse medicinal uses. It is predominantly sourced from Dioscorea species, particularly Dioscorea zingiberensis. Dioscorea zingiberensis has an ability to accumulate 2-16% diosgenin in its rhizomes. In this study, a diverse population of 180 D. zingiberensis accessions was used to evaluate the genomic regions associated with diosgenin biosynthesis by the genome wide association study approach (GWAS).
RESULTS
RESULTS
The whole population was characterized for diosgenin contents from tubers by gas chromatography mass spectrometry. The individuals were genotyped by the genotyping-by-sequencing approach and 10,000 high-quality SNP markers were extracted for the GWAS. The highest significant marker-trait-association was observed as an SNP transversion (G to T) on chromosome 10, with 64% phenotypic variance explained. The SNP was located in the promoter region of CYP94D144 which is a member of P450 gene family involved in the independent biosynthesis of diosgenin from cholesterol. The transcription factor (TF) binding site enrichment analysis of the promoter region of CYP94D144 revealed NAC TF as a potential regulator. The results were further validated through expression profiling by qRT-PCR, and the comparison of high and low diosgenin producing hybrids obtained from a bi-parental population.
CONCLUSIONS
CONCLUSIONS
This study not only enhanced the understanding of the genetic basis of diosgenin biosynthesis but also serves as a valuable reference for future genomic investigations on CYP94D144, with the aim of augmenting diosgenin production in yam tubers.
Identifiants
pubmed: 38872080
doi: 10.1186/s12870-024-05133-1
pii: 10.1186/s12870-024-05133-1
doi:
Substances chimiques
Diosgenin
K49P2K8WLX
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
540Subventions
Organisme : Reserve Talents Project for Young and Middle-aged Academic and Technical Leaders of Yunnan Provincial Department of Science and Technology
ID : 202105AC160047
Informations de copyright
© 2024. The Author(s).
Références
Sonawane PD, Pollier J, Panda S, Szymanski J. Plant cholesterol biosynthetic pathway overlaps with phytosterol metabolism. Nat Plants. 2016;3(1):16205. https://doi.org/10.1038/nplants.2016.205 .
doi: 10.1038/nplants.2016.205
pubmed: 28005066
Chaturvedi HC, Kidwai MJNR. Cloning of medicinal plants through tissue culture–a review. Indian J Exp Biol. 2007;45(11):937–48.
pubmed: 18072537
Wang Y, Zhang Y, Zhu Z, Zhu S. Exploration of the correlation between the structure, hemolytic activity, and cytotoxicity of steroid saponins. Bioorg Med Chem. 2007;15(7):2528–32.
doi: 10.1016/j.bmc.2007.01.058
pubmed: 17306549
Bertrand J, Liagre B, Bégaud-Grimaud G, Jauberteau MO. Analysis of relationship between cell cycle stage and apoptosis induction in K562 cells by sedimentation field-flow fractionation. J Chromatogr B. 2009;877(11):1155–61.
doi: 10.1016/j.jchromb.2009.02.064
Zhang R, Li P, Xu L, Chen Y. Enhancement of diosgenin production in Dioscorea zingiberensis cell culture by oligosaccharide elicitor from its endophytic fungus fusarium oxysporum Dzf17. Nat Prod Commun. 2009;4(11):1459–62.
pubmed: 19967973
He Z, Tian Y, Zhang X, Bing B. Anti-tumour and immunomodulating activities of diosgenin, a naturally occurring steroidal saponin. Nat Prod Res. 2012;26(23):2243–6. https://doi.org/10.1080/14786419.2011.648192 .
doi: 10.1080/14786419.2011.648192
pubmed: 22235932
Liu L, Dong YS, Xiu ZL. three-liquid-phase extraction of diosgenin and steroidal saponins from fermentation of Dioscorea Zingibernsis CH Wright. Process Biochem. 2010;45(5):752–6.
doi: 10.1016/j.procbio.2010.01.013
Hua W, Kong W, Cao X, Chen C. Transcriptome analysis of Dioscorea zingiberensis identifies genes involved in diosgenin biosynthesis. Genes Genomics. 2017;39(5):509–20. https://doi.org/10.1007/s13258-017-0516-9 .
doi: 10.1007/s13258-017-0516-9
Minato D, Li B, Zhou D, Shigeta Y. Synthesis and antitumor activity of des-AB analogue of steroidal saponin OSW-1. Tetrahedron. 2013;69(37):8019–24.
doi: 10.1016/j.tet.2013.06.105
Yi T, Fan LL, Chen HL, Zhu GY. Comparative analysis of diosgenin in Dioscorea species and related medicinal plants by UPLC-DAD-MS. BMC Biochem. 2014;15:19.
doi: 10.1186/1471-2091-15-19
pubmed: 25107333
pmcid: 4131487
Sautour M, Mitaine-OfferM A-C, Lacaille-Dubois A. The Dioscorea genus: a review of bioactive steroid saponins. J Nat Med. 2007;61(2):91–101.
doi: 10.1007/s11418-006-0126-3
Shen L, Xu J, Luo L, Hu H. Predicting the potential global distribution of diosgenin-contained Dioscorea species. Chin Med. 2018;13(1):58. https://doi.org/10.1186/s13020-018-0215-8 .
doi: 10.1186/s13020-018-0215-8
pubmed: 30479655
pmcid: 6245757
Zhang X, Liang J, Liu J, Zhao Y. Quality control and identification of steroid saponins from Dioscorea Zingiberensis C. H. Wright by fingerprint with HPLC-ELSD and HPLC-ESI-Quadrupole/Time-of-fight tandem mass spectrometry. J Pharm Biomed Anal. 2014;91:46–59 (PMID: PMC3924326).
doi: 10.1016/j.jpba.2013.11.023
pubmed: 24418811
Bai Y, Zhang L, Jin W, Wei M. in situ high-valued utilization and transformation of sugars from Dioscorea Zingiberensis C.H. Wright for clean production of diosgenin. Bioresour Technol. 2015;196:642–7. https://www.sciencedirect.com/science/article/pii/S0960852415011141 .
doi: 10.1016/j.biortech.2015.08.010
pubmed: 26299979
Jinreng W, ZhiZunQ D, Huizhen Q. A phytogeographical study on the family Dioscoreaceae. Acta Botanica Boreali-occidentalia Sinica. 1994;14(2):128–35.
Xu DP, Hu CY, Pang LWZJ. [Isolation and structure determination of steroidal saponin from Dioscorea Zingiberensis]. Yao Xue Xue Bao. 2007;42(11):1162–5.
pubmed: 18300473
Li X, Shi JMY. Research progress and prospects of dioscorea and diosgenin. Chem Ind for Prod. 2010;30(2):107–12.
Li H, Huang W, Wen Y, Gong G. Anti-thrombotic activity and chemical characterization of steroidal saponins from Dioscorea Zingiberensis C.H. Wright. Fitoterapia. 2010;81(8):1147–56.
doi: 10.1016/j.fitote.2010.07.016
pubmed: 20659537
Qin Y, Wu X, Huang W, Gong G. Acute toxicity and sub-chronic toxicity of steroidal saponins from Dioscorea Zingiberensis C.H.Wright in rodents. J Ethnopharmacol. 2009;126(3):543–50.
doi: 10.1016/j.jep.2009.08.047
pubmed: 19735710
Heping H, Shanlin G, Lanlan C, Xiaoke J. In vitro induction and identification of autotetraploids of Dioscorea zingiberensis. In Vitro Cellular & Developmental Biology - Plant. 2008;44(5):448–55. https://doi.org/10.1007/s11627-008-9177-3 .
doi: 10.1007/s11627-008-9177-3
Dansi A, Mignouna HD, Zoundjihékpon J, Sangare A. morphological diversity, cultivar groups and possible descent in the cultivated yams (Dioscorea cayenensis/D. rotundata) complex in Benin Republic. Genet Resour Crop Evol. 1999;46(4):371–88. https://doi.org/10.1023/A:1008698123887 .
doi: 10.1023/A:1008698123887
Viruel J, Segarra-Moragues PCatalánJG. Latitudinal Environmental Niches and Riverine barriers shaped the phylogeography of the central Chilean endemic Dioscorea Humilis (Dioscoreaceae). PLoS One. 2014;9(10):e110029. https://doi.org/10.1371/journal.pone.0110029 .
doi: 10.1371/journal.pone.0110029
pubmed: 25295517
pmcid: 4190404
Ondo Ovono P, Dommes CKJ. Effects of planting methods and tuber weights on growth and yield of yam cultivars (Dioscorea rotundata Poir.) in Gabon. Int Res J Agri Sci Soil Sci. 2016;6:32.
Wang Z, Li B, XiaoD JL, Jiang C. [Regionalization study of Dioscorea Nipponica in Jilin province based on MaxEnt and ArcGIS]. Zhongguo Zhong Yao Za Zhi. 2017;42(22):4373–7.
pubmed: 29318838
Mehrafarin A, Ghaderi A, Rezazadeh S. Bioengineering of important secondary metabolites and metabolic pathways in fenugreek (Trigonella foenum-graecum L). J Med Plants. 2010;9:1–18.
Ye Y, Wang R, Jin L, Shen J. Molecular cloning and differential expression analysis of a squalene synthase gene from Dioscorea zingiberensis, an important pharmaceutical plant. Mol Biol Rep. 2014;41(9):6097–104.
doi: 10.1007/s11033-014-3487-9
pubmed: 24996285
lshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011;6(5). https://doi.org/10.1371/journal.pone.0019379 .
Thakral V, Yadav H, Padalkar G, Kumawat S, Raturi G, Kumar V, Mandlik R, Rajora N, Singh M. Recent Advances and Applicability of GBS, GWAS, and GS in Polyploid Crops. In Genotyping by Sequencing for Crop Improvement (eds H. Sonah, V. Goyal, S.M. Shivaraj and R.K. Deshmukh). 2022. https://doi.org/10.1002/9781119745686.ch15 .
Chen Y, Zhou X, Ma L, Lin Y, Huang X. Chinese yam yield is affected by soil nutrient levels and interactions among N P K Fertilizers. Chin Herb Med. 2023;15(4):588–93. https://doi.org/10.1016/j.chmed.2022.11.006 .
doi: 10.1016/j.chmed.2022.11.006
pubmed: 38094011
pmcid: 10715871
Huang C, Hang Y, Zhou Y, Guo K. Analysis on quality of some main populations of Dioscorea zingiberensis in China. Chem Indus for Prod. 2003;23(2):68–72.
Deschamps S, May VLGD. Genotyping-by-sequencing in plants. Biology. 2012;1(3):460–83.
doi: 10.3390/biology1030460
pubmed: 24832503
pmcid: 4009820
Glaubitz JC, Casstevens TM, Lu F, Harriman J. A high capacity genotyping by sequencing analysis Pipeline. PLoS One. 2014;9(2):e90346. https://doi.org/10.1371/journal.pone.0090346 .
doi: 10.1371/journal.pone.0090346
pubmed: 24587335
pmcid: 3938676
Li Y, Tan C, Li Z, Guo J, et al. The genome of Dioscorea zingiberensis sheds light on the biosynthesis, origin and evolution of the medicinally important diosgenin saponins. Hortic Res. 2022;9:uhac165. https://doi.org/10.1093/hr/uhac165 . (Haut du formulaire Bas du formulaire).
doi: 10.1093/hr/uhac165
pubmed: 36204203
pmcid: 9531337
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007;23(19):2633–5. https://doi.org/10.1093/bioinformatics/btm308 .
doi: 10.1093/bioinformatics/btm308
pubmed: 17586829
VanRaden PM. Efficient methods to compute genomic predictions. J Dairy Sci. 2008;91(11):4414–23. https://doi.org/10.3168/jds.2007-0980 .
doi: 10.3168/jds.2007-0980
pubmed: 18946147
Lipka AE, Tian F, Wang Q, Peiffer J. GAPIT: genome association and prediction integrated tool. Bioinformatics. 2012;28(18):2397–9. https://doi.org/10.1093/bioinformatics/bts444 .
doi: 10.1093/bioinformatics/bts444
pubmed: 22796960
Husson F, Josse J, Le S, Mazet J. 2017. FactoMineR: Multivariate Exploratory Data Analysis and Data Mining. https://CRAN.R-project.org/package=FactoMineR . https://www.sciencedirect.com/science/article/pii/S0167715296000892 .
Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14:2611–20. https://doi.org/10.1111/j.1365-294X.2005.02553.x .
doi: 10.1111/j.1365-294X.2005.02553.x
pubmed: 15969739
Kumar S, Stecher G, Li M, Knyaz C. Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–9 (PMID: PMC5967553).
doi: 10.1093/molbev/msy096
pubmed: 29722887
pmcid: 5967553
Rashid MAR, Zhao Y, Azeem F, Zhao Y. Unveiling the genetic architecture for lodging resistance in rice (Oryza sativa L) by genome-wide association analyses. Front Genet. 2022;13:960007.
doi: 10.3389/fgene.2022.960007
pubmed: 36147492
pmcid: 9486067
Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008;3:1101–8. https://doi.org/10.1038/nprot.2008.73 .
doi: 10.1038/nprot.2008.73
pubmed: 18546601
Semwal P, Painuli S, Abu-Izneid T, Rauf A. Diosgenin: an updated pharmacological review and therapeutic perspectives. Oxidative Med Cell Longev. 2022;2022(1035441):1.
doi: 10.1155/2022/1035441
Cheng J, Chen J, Liu X, Li X. The origin and evolution of the diosgenin biosynthetic pathway in yam. Plant Commun. 2021;2(1):100079 ( https://www.sciencedirect.com/science/article/pii/S2590346220301024 ).
doi: 10.1016/j.xplc.2020.100079
pubmed: 33511341
Xu X, Wang Z, Xu S, Xu M. Identifying loci controlling total starch content of leaf in Nicotiana tabacum through genome-wide association study. Funct Integr Genom. 2022;22(4):537–52. https://doi.org/10.1007/s10142-022-00851-x .
doi: 10.1007/s10142-022-00851-x
Zhao Y, Zhang H, Xu J, Jiang C. Loci and natural alleles underlying robust roots and adaptive domestication of upland ecotype rice in aerobic conditions. PLoS Genet. 2018;14(8):e1007521. https://doi.org/10.1371/journal.pgen.1007521
doi: 10.1371/journal.pgen.1007521
pubmed: 30096145
pmcid: 6086435
Bredeson JV, Lyons JB, Oniyinde IO, Okereke NR. Chromosome evolution and the genetic basis of agronomically important traits in greater yam. Nat Commun. 2022;13(1):2001. https://doi.org/10.1038/s41467-022-29114-w .
doi: 10.1038/s41467-022-29114-w
pubmed: 35422045
pmcid: 9010478
Schönhals EM, Ding J, Ritter E, Paulo MJ. Physical mapping of QTL for tuber yield, starch content and starch yield in tetraploid potato (Solanum tuberosum L.) by means of genome wide genotyping by sequencing and the 8.3 K SolCAP SNP array. BMC Genomics. 2017;18(1):642. https://doi.org/10.1186/s12864-017-3979-9 .
doi: 10.1186/s12864-017-3979-9
pubmed: 28830357
pmcid: 5567664
Dossa K, Morel A, Houngbo ME, Mota AZ, Malédon E, Irep J-L, Diman J-L, Mournet P, Causse S, Van KN, Cornet D, Chair H. Genome-wide association studies reveal novel loci controlling tuber flesh color and oxidative browning in Dioscorea alata. J Sci Food Agric. 2024. https://doi.org/10.1002/jsfa.12721 .
Yano K, Yamamoto E, Aya K, Takeuchi H. Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nat Genet. 2016;48(8):927–34. https://doi.org/10.1038/ng.3596 .
doi: 10.1038/ng.3596
pubmed: 27322545
Vaidya K, Ghosh A, Kumar V, Chaudhary S. De Novo Transcriptome sequencing in Trigonella foenum-graecum L. to identify genes involved in the biosynthesis of Diosgenin. Plant Genome. 2013;6(2):plantgenome2012.08.0021. https://doi.org/10.3835/plantgenome2012.08.0021 .
doi: 10.3835/plantgenome2012.08.0021
Li J, Liang Q, Li C, Liu M. Comparative transcriptome analysis identifies putative genes involved in Dioscin Biosynthesis in Dioscorea zingiberensis. Molecules. 2018;23(2):454.
doi: 10.3390/molecules23020454
pubmed: 29463020
pmcid: 6017347
Souza CM, Schwabe TME, Pichler H, Ploier B. A stable yeast strain efficiently producing cholesterol instead of ergosterol is functional for tryptophan uptake, but not weak organic acid resistance. Metab Eng. 2011;13(5):555–69.
doi: 10.1016/j.ymben.2011.06.006
pubmed: 21741494
Christ B, Xu C, Xu M, Li F-S. Repeated evolution of cytochrome P450-mediated spiroketal steroid biosynthesis in plants. Nat Commun. 2019;10(1):3206. https://doi.org/10.1038/s41467-019-11286-7 .
doi: 10.1038/s41467-019-11286-7
pubmed: 31324795
pmcid: 6642093