Integrated evolutionary pattern analyses reveal multiple origins of steroidal saponins in plants.
distribution
evolutionary mechanisms
origin
phylogenetic signal
plant-specialized metabolites
steroidal saponins
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
revised:
19
07
2023
received:
05
09
2022
accepted:
22
07
2023
medline:
23
10
2023
pubmed:
31
7
2023
entrez:
31
7
2023
Statut:
ppublish
Résumé
Steroidal saponins are a class of specialized metabolites essential for plant's response to biotic and abiotic stresses. They are also important raw materials for the industrial production of steroid drugs. Steroidal saponins are present in some monocots, such as Dioscorea and Paris, but their distribution, origin, and evolution in plants remain poorly understood. By reconstructing the evolutionary history of the steroidal saponin-associated module (SSAM) in plants, we reveal that the steroidal saponin pathway has its origin in Asparagus and Dioscorea. Through evaluating the distribution and evolutionary pattern of steroidal saponins in angiosperms, we further show that steroidal saponins originated multiple times in angiosperms, and exist in early diverged lineages of certain monocot lineages including Asparagales, Dioscoreales, and Liliales. In these lineages, steroidal saponins are synthesized through the high copy and/or high expression mechanisms of key genes in SSAM. Together with shifts in gene evolutionary rates and amino acid usage, these molecular mechanisms shape the current distribution and diversity of steroidal saponins in plants. Consequently, our results provide new insights into the distribution, diversity and evolutionary history of steroidal saponins in plants, and enhance our understanding of plants' resistance to abiotic and biotic stresses. Additionally, fundamental understanding of the steroidal saponin biosynthesis will facilitate their industrial production and pharmacological applications.
Substances chimiques
Saponins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
823-839Informations de copyright
© 2023 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Anwar, Z. & Hussain, F. (2017) Steroidal saponins: an overview of medicinal uses. International Journal of Chemical and Biochemical Sciences, 11, 20-24.
Augustin, J.M., Drok, S., Shinoda, T., Sanmiya, K., Nielsen, J.K., Khakimov, B. et al. (2012) UDP-glycosyltransferases from the UGT73C subfamily in Barbarea vulgaris catalyze sapogenin 3-O-glucosylation in saponin-mediated insect resistance. Plant Physiology, 160, 1881-1895.
Begum, T., Serrano-Serrano, M.L. & Robinson-Rechavi, M. (2021) Performance of a phylogenetic independent contrast method and an improved pairwise comparison under different scenarios of trait evolution after speciation and duplication. Methods in Ecology and Evolution, 12, 1875-1887.
Cai, W., Pei, J. & Grishin, N.V. (2004) Reconstruction of ancestral protein sequences and its applications. BMC Evolutionary Biology, 4, 1-23.
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540-552.
Chae, L., Kim, T., Nilo-Poyanco, R. & Rhee, S.Y. (2014) Genomic signatures of specialized metabolism in plants. Science, 344, 510-513.
Chae, L., Lee, I., Shin, J. & Rhee, S.Y. (2012) Towards understanding how molecular networks evolve in plants. Current Opinion in Plant Biology, 15, 177-184.
Challinor, V.L. & De Voss, J.J. (2013) Open-chain steroidal glycosides, a diverse class of plant saponins. Natural Product Reports, 30, 429-454.
Chen, K., Durand, D. & Farach-Colton, M. (2000) NOTUNG: a program for dating gene duplications and optimizing gene family trees. Journal of Computational Biology, 7, 429-447.
Christ, B., Xu, C., Xu, M., Li, F.S., Wada, N., Mitchell, A.J. et al. (2019) Repeated evolution of cytochrome P450-mediated spiroketal steroid biosynthesis in plants. Nature Communications, 10, 1-11.
Ciura, J., Szeliga, M., Grzesik, M. & Tyrka, M. (2018) Changes in fenugreek transcriptome induced by methyl jasmonate and steroid precursors revealed by RNA-seq. Genomics, 110, 267-276.
Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S. et al. (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics, 29, 15-21.
Du, M.Z., Liu, S., Zeng, Z., Alemayehu, L.A., Wei, W. & Guo, F.B. (2018) Amino acid compositions contribute to the proteins' evolution under the influence of their abundances and genomic GC content. Scientific Reports, 8, 1-9.
Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113.
Felsenstein, J. (1985) Phylogenies and the comparative method. The American Naturalist, 125, 1-15.
Felsenstein, J. (2005) Using the quantitative genetic threshold model for inferences between and within species. Philosophical Transactions of the Royal Society B: Biological Sciences, 360, 1427-1434.
Fritz, S.A. & Purvis, A. (2010) Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conservation Biology, 24, 1042-1051.
Gas-Pascual, E., Berna, A., Bach, T.J. & Schaller, H. (2014) Plant oxidosqualene metabolism: cycloartenol synthase-dependent sterol biosynthesis in Nicotiana benthamiana. PLoS One, 9, e109156.
Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I. et al. (2013) Trinity: reconstructing a full-length transcriptome without a genome from RNA-seq data. Nature Biotechnology, 29, 644-652.
Gu, Z., Gu, L., Eils, R., Schlesner, M. & Brors, B. (2014) Circlize implements and enhances circular visualization in R. Bioinformatics, 30, 2811-2812.
Harkess, A., Zhou, J., Xu, C., Bowers, J.E., Van Der Hulst, R., Ayyampalayam, S. et al. (2017) The asparagus genome sheds light on the origin and evolution of a young Y chromosome. Nature Communications, 8, 1279.
Huang, A.C., Jiang, T., Liu, Y.X., Bai, Y.C., Reed, J., Qu, B. et al. (2019) A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science, 364, 546.
Itkin, M., Heinig, U., Tzfadia, O., Bhide, A.J., Shinde, B., Cardenas, P.D. et al. (2013) Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science, 341, 175-179.
Johnson, L.S., Eddy, S.R. & Portugaly, E. (2010) Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics, 11, 431.
Kim, D., Paggi, J.M., Park, C., Bennett, C. & Salzberg, S.L. (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology, 37, 907-915.
Langfelder, P. & Horvath, S. (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9, 259.
Li, B. & Dewey, C.N. (2011) RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics, 12, 323.
Li, J., Liang, Q., Li, C., Liu, M. & Zhang, Y. (2018) Comparative transcriptome analysis identifies putative genes involved in dioscin biosynthesis in Dioscorea zingiberensis. Molecules, 23, 454.
Li, X.J., Wang, Y., Sun, J., Li, X., Zhao, C., Zhao, P. et al. (2020) Chemotaxonomic studies of 12 Dioscorea species from China by UHPLC-QTOF-MS/MS analysis. Phytochemical Analysis, 31, 164-182.
Li, Y., Tan, C., Li, Z., Guo, J., Li, S., Chen, X. et al. (2022) The genome of Dioscorea zingiberensis sheds light on the biosynthesis, origin and evolution of the medicinally important diosgenin saponins. Horticulture Research, 9, uhac165.
Li, Y., Yang, H., Li, Z., Li, S. & Li, J. (2023) Advances in the biosynthesis and molecular evolution of steroidal saponins in plants. International Journal of Molecular Sciences, 24, 2620.
Lichman, B.R., Godden, G.T. & Buell, C.R. (2020) Gene and genome duplications in the evolution of chemodiversity: perspectives from studies of Lamiaceae. Current Opinion in Plant Biology, 55, 74-83.
Losos, J.B. (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters, 11, 995-1003.
Love, M.I., Huber, W. & Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.
Mackenzie, P.I., Owens, I.S., Burchell, B., Bock, K.W., Bairoch, A., Bélanger, A. et al. (1997) The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics, 7, 255-269.
Mohammadi, M., Mashayekh, T., Rashidi-Monfared, S., Ebrahimi, A. & Abedini, D. (2020) New insights into diosgenin biosynthesis pathway and its regulation in Trigonella foenum-graecum L. Phytochemical Analysis, 31, 229-241.
Moreno-Hagelsieb, G. & Latimer, K. (2008) Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics, 24, 319-324.
Moses, T., Papadopoulou, K.K. & Osbourn, A. (2014) Metabolic and functional diversity of saponins, biosynthetic intermediates and semi-synthetic derivatives. Critical Reviews in Biochemistry and Molecular Biology, 49, 439-462.
Nakayasu, M., Kawasaki, T., Lee, H.J., Sugimoto, Y., Onjo, M., Muranaka, T. et al. (2015) Identification of furostanol glycoside 26-O-β-glucosidase involved in steroidal saponin biosynthesis from Dioscorea esculenta. Plant Biotechnology, 32, 299-308.
Nasrollahi, V., Mirzaie-Asl, A., Piri, K., Nazeri, S. & Mehrabi, R. (2014) The effect of drought stress on the expression of key genes involved in the biosynthesis of triterpenoid saponins in liquorice (Glycyrrhiza glabra). Phytochemistry, 103, 32-37.
Nelson, D.R. (2009) The cytochrome P450 homepage. Human Genomics, 4, 59-65.
Nguyen, L.T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268-274.
Paradis, E., Claude, J. & Strimmer, K. (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289-290.
Park, C., Chen, X., Yang, J.R. & Zhang, J. (2013) Differential requirements for mRNA folding partially explain why highly expressed proteins evolve slowly. Proceedings of the National Academy of Sciences of the United States of America, 110, E678-E686.
Prall, W., Hendy, O. & Thornton, L.E. (2016) Utility of a phylogenetic perspective in structural analysis of CYP72A enzymes from flowering plants. PLoS One, 11, e0163024.
Randall, R.N., Radford, C.E., Roof, K.A., Natarajan, D.K. & Gaucher, E.A. (2016) An experimental phylogeny to benchmark ancestral sequence reconstruction. Nature Communications, 7, 12847.
Revell, L.J. (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217-223.
Sahu, N.P., Banerjee, S., Mondal, N.B. & Mandal, D. (2008) Steroidal saponins. In: Kinghorn, A.D., Falk, H., Liu, J.-K., Gibbons, S., Asakawa, Y. & Dirsch, V.M. (Eds.) Progress in the chemistry of organic natural products. Vienna: Springer Vienna, pp. 45-141.
Shen, L., Xu, J., Luo, L., Hu, H., Meng, X., Li, X. et al. (2018) Predicting the potential global distribution of diosgenin-contained Dioscorea species. Chinese Medicine, 13, 58.
Song, W., Zhang, C., Wu, J., Qi, J., Hua, X., Kang, L. et al. (2022) Characterization of three Paris polyphylla glycosyltransferases from different UGT families for steroid functionalization. ACS Synthetic Biology, 11, 1669-1680.
Szakiel, A., Pączkowski, C. & Henry, M. (2011) Influence of environmental abiotic factors on the content of saponins in plants. Phytochemistry Reviews, 10, 493-502.
Tian, L.W., Zhang, Z., Long, H.L. & Zhang, Y.J. (2017) Steroidal saponins from the genus Smilax and their biological activities. Natural Products and Bioprospecting, 7, 283-298.
Unruh, S.A., McKain, M.R., Lee, Y.I., Yukawa, T., McCormick, M.K., Shefferson, R.P. et al. (2018) Phylotranscriptomic analysis and genome evolution of the Cypripedioideae (Orchidaceae). American Journal of Botany, 105, 631-640.
Upadhyay, S., Jeena, G.S., Shikha & Shukla, R.K. (2018) Recent advances in steroidal saponins biosynthesis and in vitro production. Planta, 248, 519-544.
Upadhyay, S., Phukan, U.J., Mishra, S. & Shukla, R.K. (2014) De novo leaf and root transcriptome analysis identified novel genes involved in steroidal sapogenin biosynthesis in Asparagus racemosus. BMC Genomics, 15, 746.
Ur Rahman, S., Ismail, M., Khurram, M., Ullah, I., Rabbi, F. & Iriti, M. (2017) Bioactive steroids and saponins of the genus Trillium. Molecules, 22, 2156.
Wang, Y., Gao, W., Li, X., Wei, J., Jing, S. & Xiao, P. (2013) Chemotaxonomic study of the genus Paris based on steroidal saponins. Biochemical Systematics and Ecology, 48, 163-173.
Wei, C., Yang, H., Wang, S., Zhao, J., Liu, C., Gao, L. et al. (2018) Draft genome sequence of Camellia sinensis var. sinensis provides insights into the evolution of the tea genome and tea quality. Proceedings of the National Academy of Sciences of the United States of America, 115, E4151-E4158.
Xia, E.H., Zhang, H.B., Sheng, J., Li, K., Zhang, Q.J., Kim, C. et al. (2017) The tea tree genome provides insights into tea flavor and independent evolution of caffeine biosynthesis. Molecular Plant, 10, 866-877.
Yang, J., Wang, P., Wu, W., Zhao, Y., Idehen, E. & Sang, S. (2016) Steroidal saponins in oat bran. Journal of Agricultural and Food Chemistry, 64, 1549-1556.
Yang, Z. (2007) PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24, 1586-1591.
Ye, T., Song, W., Zhang, J.J., An, M., Feng, S., Yan, S. et al. (2017) Identification and functional characterization of DzS3GT, a cytoplasmic glycosyltransferase catalyzing biosynthesis of diosgenin 3-O-glucoside in Dioscorea zingiberensis. Plant Cell, Tissue and Organ Culture, 129, 399-410.
Yin, X., Liu, J., Kou, C., Lu, J., Zhang, H., Song, W. et al. (2023) Deciphering the network of cholesterol biosynthesis in Paris polyphylla laid a base for efficient diosgenin production in plant chassis. Metabolic Engineering, 76, 232-246.
Zanne, A.E., Tank, D.C., Cornwell, W.K., Eastman, J.M., Smith, S.A., Fitzjohn, R.G. et al. (2014) Three keys to the radiation of angiosperms into freezing environments. Nature, 506, 89-92.
Zhang, Y., Deng, T., Sun, L., Landis, J.B., Moore, M.J., Wang, H. et al. (2021) Phylogenetic patterns suggest frequent multiple origins of secondary metabolites across the seed-plant “tree of life”. National Science Review, 8, nwaa105.
Zhao, P., Zhao, C., Li, X., Gao, Q., Huang, L., Xiao, P. et al. (2018) The genus Polygonatum: a review of ethnopharmacology, phytochemistry and pharmacology. Journal of Ethnopharmacology, 214, 274-291.
Zhao, Q., Yang, J., Cui, M.Y., Liu, J., Fang, Y., Yan, M. et al. (2019) The reference genome sequence of Scutellaria baicalensis provides insights into the evolution of wogonin biosynthesis. Molecular Plant, 12, 935-950.
Zheng, Y., Jiao, C., Sun, H., Rosli, H.G., Pombo, M.A., Zhang, P. et al. (2016) iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Molecular Plant, 9, 1667-1670.
Zhou, C., Yang, Y., Tian, J., Wu, Y., An, F., Li, C. et al. (2022) 22R- but not 22S-hydroxycholesterol is recruited for diosgenin biosynthesis. The Plant Journal, 109, 940-951.
Zou, Z. & Zhang, J. (2019) Amino acid exchangeabilities vary across the tree of life. Science Advances, 5, eaax3124.