Abstract
Main conclusion
Genome-wide screening of short-chain dehydrogenases/reductases (SDR) family reveals functional diversification of borneol dehydrogenase (BDH) in Wurfbainia villosa.
Abstract
Wurfbainia villosa is an important medicinal plant, the fruits of which accumulate abundant terpenoids, especially bornane-type including borneol and camphor. The borneol dehydrogenase (BDH) responsible for the conversion of borneol to camphor in W. villosa remains unknown. BDH is one member of short-chain dehydrogenases/reductases (SDR) family. Here, a total of 115 classical WvSDR genes were identified through genome-wide screening. These WvSDRs were unevenly distributed on different chromosomes. Seven candidate WvBDHs based on phylogenetic analysis and expression levels were selected for cloning. Of them, four BDHs can catalyze different configurations of borneol and other monoterpene alcohol substrates to generate the corresponding oxidized products. WvBDH1 and WvBDH2, preferred (+)-borneol to (−)-borneol, producing the predominant ( +)-camphor. WvBDH3 yielded approximate equivalent amount of (+)-camphor and (−)-camphor, in contrast, WvBDH4 generated exclusively (+)-camphor. The metabolic profiles of the seeds showed that the borneol and camphor present were in the dextrorotatory configuration. Enzyme kinetics and expression pattern in different tissues suggested WvBDH2 might be involved in the biosynthesis of camphor in W. villosa. All results will increase the understanding of functional diversity of BDHs.
This is a preview of subscription content, log in via an institution to check access.
Data availability
All data described in the study have been provided as Supplementary Material.
Abbreviations
- BAT:
-
Borneol acetyltransferase
- BDH:
-
Borneol dehydrogenase
- BPPS:
-
Bornyl diphosphate synthase
- DAF:
-
Days after flowering
- SDR:
-
Short-chain dehydrogenases/reductases
References
Alexander R, Alamillo JM, Salamini F, Bartels D (1994) A novel embryo-specific barley cDNA clone encodes a protein with homologies to bacterial glucose and ribitol dehydrogenase. Planta 192(4):519–525. https://doi.org/10.1007/BF00203590
Allam M, Bhavani AKD, Mudiraj A et al (2018) Synthesis of pyrazolo[3,4-d]pyrimidin-4(5H)-ones tethered to 1,2,3-triazoles and their evaluation as potential anticancer agents. Eur J Med Chem 156:43–52. https://doi.org/10.1016/j.ejmech.2018.06.055
Alphey MS, Yu W, Byres E et al (2005) Structure and reactivity of human mitochondrial 2,4-dienoyl-CoA reductase. J Biol Chem 280:3068–3077. https://doi.org/10.1074/jbc.M411069200
Anjaneyulu B, Sangeeta SN (2021) A study on camphor derivatives and its applications: a review. Curr Org Chem 25:1404–1428. https://doi.org/10.2174/1385272825666210608115750
Ao H, Wang J, Chen L et al (2019) Comparison of volatile oil between the fruits of Amomum villosum Lour. and Amomum villosum Lour. Var. xanthioides T. L. Wu et Senjen based on GC-MS and chemometric techniques. Molecules 24:1663. https://doi.org/10.3390/molecules24091663
Bachem CWB, Horvath B, Trindade L et al (2001) A potato tuber-expressed mRNA with homology to steroid dehydrogenases affects gibberellin levels and plant development: Gibberellin and plant development in potato tuber. Plant J 25:595–604. https://doi.org/10.1046/j.1365-313x.2001.00993.x
Beaudoin F, Wu X, Li F et al (2009) Functional characterization of the Arabidopsis β -ketoacyl-coenzyme a reductase candidates of the fatty acid elongase. Plant Physiol 150:1174–1191. https://doi.org/10.1104/pp.109.137497
Benach J, Atrian S, Gonzàlez-Duarte R, Ladenstein R (1999) The catalytic reaction and inhibition mechanism of Drosophila alcohol dehydrogenase: observation of an enzyme-bound NAD-ketone adduct at 1.4 Å resolution by X-ray crystallography. J Mol Biol 289:335–355. https://doi.org/10.1006/jmbi.1999.2765
Brock A, Brandt W, Dräger B (2008) The functional divergence of short-chain dehydrogenases involved in tropinone reduction. Plant J 54:388–401. https://doi.org/10.1111/j.1365-313X.2008.03422.x
Chánique AM, Dimos N, Drienovská I et al (2021) A structural view on the stereospecificity of plant borneol-type dehydrogenases. ChemCatChem 13:2262–2277. https://doi.org/10.1002/cctc.202100110
Chen LX, Lai YF, Zhang WX et al (2020) Comparison of volatile compounds in different parts of fresh Amomum villosum Lour. from different geographical areas using cryogenic grinding combined HS–SPME–GC–MS. Chin Med 15:97. https://doi.org/10.1186/s13020-020-00377-z
Cheng WH, Endo A, Zhou L et al (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14:2723–2743. https://doi.org/10.1105/tpc.006494
Collin MA, Clarke TH, Ayoub NA, Hayashi CY (2018) Genomic perspectives of spider silk genes through target capture sequencing: Conservation of stabilization mechanisms and homology-based structural models of spidroin terminal regions. Int J Biol Macromol 113:829–840. https://doi.org/10.1016/j.ijbiomac.2018.02.032
Contreras Á, Merino I, Álvarez E et al (2021) A poplar short-chain dehydrogenase reductase plays a potential key role in biphenyl detoxification. Proc Natl Acad Sci USA 118(35):e2103378118. https://doi.org/10.1073/pnas.2103378118
Cui L, Yang G, Yan J et al (2019) Genome-wide identification, expression profiles and regulatory network of MAPK cascade gene family in barley. BMC Genomics 20(1):750. https://doi.org/10.1186/s12864-019-6144-9
DeLong A, Calderon-Urrea A, Dellaporta SL (1993) Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74(4):757–768. https://doi.org/10.1016/0092-8674(93)90522-r
Drienovská I, Kolanović D, Chánique A et al (2020) Molecular cloning and functional characterization of a two highly stereoselective borneol dehydrogenases from Salvia officinalis L. Phytochemistry 172:112227. https://doi.org/10.1016/j.phytochem.2019.112227
Filling C, Berndt KD, Benach J et al (2002) Critical residues for structure and catalysis in short-chain dehydrogenases/reductases. J Biol Chem 277:25677–25684. https://doi.org/10.1074/jbc.M202160200
González-Guzmán M, Apostolova N, Bellés JM et al (2002) The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell 14:1833–1846. https://doi.org/10.1105/tpc.002477
Hofer M, Diener J, Begander B et al (2021) Engineering of a borneol dehydrogenase from P. putida for the enzymatic resolution of camphor. Appl Microbiol Biotechnol 105:3159–3167. https://doi.org/10.1007/s00253-021-11239-5
Hörmann F, Küchler M, Sveshnikov D et al (2004) Tic32, an essential component in chloroplast biogenesis. J Biol Chem 279:34756–34762. https://doi.org/10.1074/jbc.M402817200
Kallberg Y, Oppermann U, Persson B (2010) Classification of the short-chain dehydrogenase/reductase superfamily using hidden Markov models: SDR classification using HMM. FEBS J 277:2375–2386. https://doi.org/10.1111/j.1742-4658.2010.07656.x
Kavanagh KL, Jrnvall H, Persson B et al (2008) The SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell Mol Life Sci 65:3895–3906. https://doi.org/10.1007/s00018-008-8588-y
Khine AA, Yang M-Y, Hu A et al (2020) Production of optically pure (–)-borneol by Pseudomonas monteilii TCU-CK1 and characterization of borneol dehydrogenase involved. Enzyme Microbiol Technol 139:109586. https://doi.org/10.1016/j.enzmictec.2020.109586
Kihara A, Igarashi Y (2004) FVT-1 is a mammalian 3-ketodihydrosphingosine reductase with an active site that faces the cytosolic side of the endoplasmic reticulum membrane. J Biol Chem 279:49243–49250. https://doi.org/10.1074/jbc.M405915200
Koutsompogeras P, Kyriacou A, Zabetakis I (2010) Characterization of NAD-dependent alcohol dehydrogenase enzymes of strawberry’s achenes (Fragaria x ananassa cv. Elsanta) and comparison with respective enzymes from Methylobacterium extorquens. LWT-Food Sci Technol 43:828–835. https://doi.org/10.1016/j.lwt.2010.01.017
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lang PT, Harned AM, Wissinger JE (2011) Oxidation of borneol to camphor using oxone and catalytic sodium chloride: a green experiment for the undergraduate organic chemistry laboratory. J Chem Educ 88:652–656. https://doi.org/10.1021/ed100853f
Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:W293–W296. https://doi.org/10.1093/nar/gkab301
Liang H, Lin X, Yang P et al (2022) Genome-wide identification of BAHD superfamily and functional characterization of bornyl acetyltransferases involved in the bornyl acetate biosynthesis in Wurfbainia villosa. Front Plant Sci 13:860152. https://doi.org/10.3389/fpls.2022.860152
Lüddeke F, Wülfing A, Timke M et al (2012) Geraniol and geranial dehydrogenases induced in anaerobic monoterpene degradation by castellaniella defragrans. Appl Environ Microbiol 78:2128–2136. https://doi.org/10.1128/AEM.07226-11
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155. https://doi.org/10.1126/science.290.5494.1151
Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473. https://doi.org/10.1093/genetics/154.1.459
Lynch M, O’Hely M, Walsh B, Force A (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159:1789–1804. https://doi.org/10.1093/genetics/154.1.459
Ma R, Su P, Jin B et al (2021) Molecular cloning and functional identification of a high-efficiency (+)-borneol dehydrogenase from Cinnamomum camphora (L.) Presl. Plant Physiol Biochem 158:363–371. https://doi.org/10.1016/j.plaphy.2020.11.023
Mikláš R, Miklášová N, Bukovský M, Devínsky F (2014) Synthesis and antimicrobial properties of camphorsulfonic acid derived imidazolium salts. Acta Fac Pharm Univ Comenianae 61:42–48. https://doi.org/10.2478/afpuc-2014-0007
Moore RC, Purugganan MD (2003) The early stages of duplicate gene evolution. Proc Natl Acad Sci USA 100:15682–15687. https://doi.org/10.1073/pnas.2535513100
Moummou H, Kallberg Y, Tonfack LB et al (2012) The plant short-chain dehydrogenase (SDR) superfamily: genome-wide inventory and diversification patterns. BMC Plant Biol 12:219. https://doi.org/10.1186/1471-2229-12-219
Nys KD, Meyhi E, Mannaerts GP et al (2001) Characterisation of human peroxisomal 2,4-dienoyl-CoA reductase. Biochim Biophys Acta 1533(1):66–72. https://doi.org/10.1016/s1388-1981(01)00141-x
Persson B, Kallberg Y (2013) Classification and nomenclature of the superfamily of short-chain dehydrogenases/reductases (SDRs). Chem Biol Interact 202(1–3):111–115. https://doi.org/10.1016/j.cbi.2012.11.009
Persson B, Kallberg Y, Bray JE et al (2009) The SDR (short-chain dehydrogenase/reductase and related enzymes) nomenclature initiative. Chem Biol Interact 178(1–3):94–98. https://doi.org/10.1016/j.cbi.2008.10.040
Polichuk DR, Zhang Y, Reed DW et al (2010) A glandular trichome-specific monoterpene alcohol dehydrogenase from Artemisia annua. Phytochemistry 71:1264–1269. https://doi.org/10.1016/j.phytochem.2010.04.026
Ringer KL, Davis EM, Croteau R (2005) Cloning, expression, and characterization of (-)-isopiperitenol/(-)-carveol dehydrogenase of peppermint and spearmint. Plant Physiol 137(3):863–872. https://doi.org/10.1104/pp.104.053298
Sarker LS, Galata M, Demissie ZA, Mahmoud SS (2012) Molecular cloning and functional characterization of borneol dehydrogenase from the glandular trichomes of Lavandula x intermedia. Arch Biochem Biophys 528(2):163–170. https://doi.org/10.1016/j.abb.2012.09.013
Sato-Masumoto N, Ito M (2014) Isolation and characterization of isopiperitenol dehydrogenase from piperitenone-type Perilla. Biol Pharm Bull 37(5):847–852. https://doi.org/10.1248/bpb.b14-00090
Schrödinger L, DeLano W (2020) PyMOL. Retrieved from http://www.pymol.org/pymol
Shanati T, Lockie C, Beloti L et al (2019) Two enantiocomplementary ephedrine dehydrogenases from Arthrobacter sp. TS-15 with broad substrate specificity. ACS Catal 9:6202–6211. https://doi.org/10.1021/acscatal.9b00621
Shimura K, Okada A, Okada K et al (2007) Identification of a biosynthetic gene cluster in rice for momilactones. J Biol Chem 282(47):34013–34018. https://doi.org/10.1074/jbc.M703344200
Shokova EA, Kim JK, Kovalev VV (2016) Camphor and its derivatives. Unusual transformations and biological activity. Russ J Org Chem 52:459–488. https://doi.org/10.1134/S1070428016040011
Smith AG, Margolis G (1954) Camphor poisoning; anatomical and pharmacologic study; report of a fatal case; experimental investigation of protective action of barbiturate. Am J Pathol 30(5):857–869
Sonawane PD, Heinig U, Panda S et al (2018) Short-chain dehydrogenase/reductase governs steroidal specialized metabolites structural diversity and toxicity in the genus Solanum. Proc Natl Acad Sci USA 115:E5419–E5428. https://doi.org/10.1073/pnas.1804835115
Tetsurou T, Nobutaka T, Kouichiro U et al (1998) Roles of the Ser146, Tyr159, and Lys163 residues in the catalytic action of 7alpha-hydroxysteroid dehydrogenase from Escherichia coli. J Biochem 124(3):634–641. https://doi.org/10.1093/oxfordjournals.jbchem.a022159
Tian N, Tang Y, Xiong S et al (2015) Molecular cloning and functional identification of a novel borneol dehydrogenase from Artemisia annua L. Ind Crops Prod 77:190–195. https://doi.org/10.1016/j.indcrop.2015.08.049
Tonfack LB, Moummou H, Latché A et al (2011) The plant SDR superfamily: involvement in primary and secondary metabolism. Curr Top Plant Biol 12:41–53. https://doi.org/10.3390/ijms22179498
Tsang HL, Huang JL, Lin YH et al (2016) Borneol dehydrogenase from Pseudomonas sp. strain TCU-HL1 catalyzes the oxidation of (+)-borneol and its isomers to camphor. Appl Environ Microbiol 82:6378–6385. https://doi.org/10.1128/AEM.01789-16
Wang Y, Tang H, Debarry JD et al (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40(7):e49. https://doi.org/10.1093/nar/gkr1293
Wang H, Ma D, Yang J et al (2018) An integrative volatile terpenoid profiling and transcriptomics analysis for gene mining and functional characterization of AvBPPS and AvPS involved in the monoterpenoid biosynthesis in Amomum villosum. Front Plant Sci 9:846. https://doi.org/10.3389/fpls.2018.00846
Waterhouse A, Bertoni M, Bienert S et al (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46:W296–W303. https://doi.org/10.1093/nar/gky427
Wong WC, Yap CK, Eisenhaber B, Eisenhaber F (2015) DissectHMMER: a HMMER-based score dissection framework that statistically evaluates fold-critical sequence segments for domain fold similarity. Biol Direct 10:39. https://doi.org/10.1186/s13062-015-0068-3
Yang P, Zhao HY, Wei JS et al (2022) Chromosome-level genome assembly and functional characterization of terpene synthases provide insights into the volatile terpenoid biosynthesis of Wurfbainia villosa. Plant J 112:630–645. https://doi.org/10.1111/tpj.15968
Zhao X, Zhang ZW, Cui W et al (2015) Identification of camphor derivatives as novel M2 ion channel inhibitors of influenza a virus. MedChemComm 6:727–731. https://doi.org/10.1039/C4MD00515E
Zhao H, Li M, Zhao Y et al (2021) A comparison of two monoterpenoid synthases reveals molecular mechanisms associated with the difference of bioactive monoterpenoids between Amomum villosum and Amomum longiligulare. Front Plant Sci 12:695551. https://doi.org/10.3389/fpls.2021.695551
Ziegler J, Facchini PJ, Geißler R et al (2009) Evolution of morphine biosynthesis in opium poppy. Phytochemistry 70(15–16):1696–1707. https://doi.org/10.1016/j.phytochem.2009.07.006
Funding
This work is financially supported by National Natural Science Foundation of China (no. 81303163) and Key-Area Research and Development Program of Guangdong Province (no.2020B20221001).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Dorothea Bartels.
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
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
Lin, X., Huang, L., Liang, H. et al. Genome-wide identification and functional characterization of borneol dehydrogenases in Wurfbainia villosa. Planta 258, 69 (2023). https://doi.org/10.1007/s00425-023-04221-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04221-0