Progestogens and androgens influence root morphology of angiosperms in a brassinosteroid-independent manner

. 2025 Sep ; 123 (5) : e70459.

Jazyk angličtina Země Velká Británie, Anglie Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40924936

Grantová podpora
CZ.02.01.01/00/22_008/0004581 ERDF Programme Johannes Amos Comenius
IP 2022-13 Impulseproject University Jena

Progestogens and androgens are steroids found in a wide range of plants, but little is known about their physiological functions. In this study, we sowed seeds of angiosperms on progestogen- and androgen-containing medium and analysed their morphological effects. We further investigated the effects of progesterone and testosterone on brassinosteroid profiles and gene expression in A. thaliana. Additionally, we examined the effects of progesterone and testosterone on A. thaliana plants overexpressing the steroid 5α-reductase DET2. We found that progestogens and androgens have strong negative effects on root length, especially in Brassicaceae species. In addition, these steroids led to uncoordinated cell growth and increased lateral root formation. We failed to detect an effect on endogenous brassinosteroid levels and gene expression of brassinosteroid-regulated genes. The overexpression of DET2 led to increased root growth, but the effects of progesterone and testosterone were not reduced. We conclude that progestogens and androgens act in a brassinosteroid-independent manner. This suggests that progestogens and androgens could represent a potential new class of plant steroid signalling molecules.

Zobrazit více v PubMed

Ali, K. , Li, W. & Wu, G. (2024) Evolution, classification, structure, and functional diversification of steroid 5α‐reductase family in eukaryotes. Heliyon, 10, e34322. PubMed PMC

Almazrouei, B. , Islayem, D. , Alskafi, F. , Catacutan, M.K. , Amna, R. , Nasrat, S. et al. (2023) Steroid hormones in wastewater: sources, treatments, environmental risks, and regulations. Emerging Contaminants, 9, 100210.

Altschul, S.F. , Gish, W. , Miller, W. , Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410. PubMed

Appenroth, K.‐J. , Teller, S. & Horn, M. (1996) Photophysiology of Turion Formation and Germination in DOI

Appenroth, K.‐J. & Nickel, G. (2010) Turion formation in PubMed

Appenroth, K.‐J. , Sree, K.S. , Bog, M. , Ecker, J. , Seeliger, C. , Böhm, V. et al. (2018) Nutritional value of the duckweed species of the genus Wolffia (Lemnaceae) as human food. Frontiers in Chemistry, 6, 483. PubMed PMC

Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B: Methodological, 57, 289–300.

Bennett, R.D. & Heftmann, E. (1965) Progesterone: biosynthesis from pregnenolone in PubMed

Bennett, R.D. , Heftmann, E. & Winter, B.J. (1969) Conversion of sitosterol to progesterone by PubMed

Berardini, T.Z. , Mundodi, S. , Reiser, L. , Huala, E. , Garcia‐Hernandez, M. , Zhang, P. et al. (2004) Functional annotation of the PubMed PMC

Bhattacharya, B. & Gupta, K. (1981) Steroid hormone effects on growth and apical dominance of sunflower. Phytochemistry, 20, 989–991.

Bienert, S. , Waterhouse, A. , de, B.T.A.P. , Tauriello, G. , Studer, G. , Bordoli, L. et al. (2017) The SWISS‐MODEL repository‐new features and functionality. Nucleic Acids Research, 45, D313–D319. PubMed PMC

Bishop, G.J. & Koncz, C. (2002) Brassinosteroids and plant steroid hormone signaling. The Plant Cell, 14(Suppl), S97–S110. PubMed PMC

Calleja‐Cabrera, J. , Boter, M. , Oñate‐Sánchez, L. & Pernas, M. (2020) Root growth adaptation to climate change in crops. Frontiers in Plant Science, 11, 544. PubMed PMC

Carroll, E. , Ravi Gopal, B. , Raghavan, I. , Mukherjee, M. & Wang, Z.Q. (2023) A cytochrome P450 CYP87A4 imparts sterol side‐chain cleavage in digoxin biosynthesis. Nature Communications, 14, 4042. PubMed PMC

Chen, S. , Zhou, Y. , Chen, Y. & Gu, J. (2018) Fastp: an ultra‐fast all‐in‐one FASTQ preprocessor. Bioinformatics (Oxford, England), 34, i884–i890. PubMed PMC

Chomczynski, P. (1993) A reagent for the single‐step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. BioTechniques, 15(532–4), 536–537. PubMed

Clough, S.J. & Bent, A.F. (1998) Floral dip: a simplified method for agrobacterium‐mediated transformation of PubMed

Coenye, T. (2021) Do results obtained with RNA‐sequencing require independent verification? Biofilm, 3, 100043. PubMed PMC

Damkjaer, K. , Weisser, J.J. , Msigala, S.C. , Mdegela, R. & Styrishave, B. (2018) Occurrence, removal and risk assessment of steroid hormones in two wastewater stabilization pond systems in Morogoro, Tanzania. Chemosphere, 212, 1142–1154. PubMed

Dorfner, M. , Klein, J. , Senkleiter, K. , Lanig, H. , Kreis, W. & Munkert, J. (2024) Addressing the evolution of cardenolide formation in iridoid‐synthesizing plants: site‐directed mutagenesis of PRISEs (progesterone‐5β‐reductase/iridoid synthase‐like enzymes) of PubMed PMC

Eberhardt, J. , Santos‐Martins, D. , Tillack, A.F. & Forli, S. (2021) AutoDock Vina 1.2.0: new docking methods, expanded force field, and python bindings. Journal of Chemical Information and Modeling, 61, 3891–3898. PubMed PMC

Erdal, S. & Dumlupinar, R. (2011) Mammalian sex hormones stimulate antioxidant system and enhance growth of chickpea plants. Acta Physiologiae Plantarum, 33, 1011–1017.

Felsenstein, J. (1985) Comfidence limits on phylogenies: an approach using the bootstrap. Evolution: International Journal of Organic Evolution, 39, 783–791. PubMed

Ferrer, A. , Altabella, T. , Arró, M. & Boronat, A. (2017) Emerging roles for conjugated sterols in plants. Progress in Lipid Research, 67, 27–37. PubMed

Gawienowski, A.M. & Gibbs, C.C. (1968) Identification of cholesterol and progesterone in apple seeds. Steroids, 12, 545–550. PubMed

Goeury, K. , Munoz, G. , Vo Duy, S. , Prévost, M. & Sauvé, S. (2022) Occurrence and seasonal distribution of steroid hormones and bisphenol a in surface waters and suspended sediments of Quebec, Canada. Environmental Advances, 8, 100199.

González, A. , Kroll, K.J. , Silva‐Sanchez, C. , Carriquiriborde, P. , Fernandino, J.I. , Denslow, N.D. et al. (2020) Steroid hormones and estrogenic activity in the wastewater outfall and receiving waters of the Chascomús chained shallow lakes system (Argentina). The Science of the Total Environment, 743, 140401. PubMed PMC

Goodstein, D.M. , Shu, S. , Howson, R. , Neupane, R. , Hayes, R.D. , Fazo, J. et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research, 40, D1178–D1186. PubMed PMC

Hartz, P. , Strohmaier, S.J. , El‐Gayar, B.M. , Abdulmughni, A. , Hutter, M.C. , Hannemann, F. et al. (2021) Resurrection and characterization of ancestral CYP11A1 enzymes. The FEBS Journal, 288, 6510–6527. PubMed

Hendriks, K.P. , Kiefer, C. , Al‐Shehbaz, I.A. , Bailey, C.D. , van Hooft Huysduynen, A. , Nikolov, L.A. et al. (2023) Global Brassicaceae phylogeny based on filtering of 1,000‐gene dataset. Current Biology: CB, 33, 4052–4068.e6. PubMed

Herl, V. , Frankenstein, J. , Meitinger, N. , Müller‐Uri, F. & Kreis, W. (2007) Delta 5‐3beta‐hydroxysteroid dehydrogenase (3 beta HSD) from Digitalis lanata. Heterologous expression and characterisation of the recombinant enzyme. Planta medica, 73, 704–710. PubMed

Iino, M. , Nomura, T. , Tamaki, Y. , Yamada, Y. , Yoneyama, K. , Takeuchi, Y. et al. (2007) Progesterone: its occurrence in plants and involvement in plant growth. Phytochemistry, 68, 1664–1673. PubMed

Janeczko, A. & Filek, W. (2002) Stimulation of generative development in partly vernalized winter wheat by animal sex hormones. Acta Physiologiae Plantarum, 24, 291–295.

Janeczko, A. , Tóbiás, I. , Skoczowski, A. , Dubert, F. , Gullner, G. & Barna, B. (2013) Progesterone moderates damage in

Jauković, Z. , Grujić, S. , Bujagić, I.M. , Petković, A. & Laušević, M. (2022) Steroid‐based tracing of sewage‐sourced pollution of river water and wastewater treatment efficiency: dissolved and suspended water phase distribution. The Science of the Total Environment, 846, 157510. PubMed

Jones, D.T. , Taylor, W.R. & Thornton, J.M. (1992) The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences: CABIOS, 8, 275–282. PubMed

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. PubMed PMC

Klein, J. (2024) Progesterone metabolism in digitalis and other plants ‐ 60 years research and recent results. Plant & Cell Physiology. Available from: 10.1093/pcp/pcae006 PubMed DOI

Klein, J. , Appenroth, K.‐J. & Sree, K.S. (2025) Duckweeds: Model Organisms for Research on Plant Sterols and Steroids. Plant Biology. Available from: 10.1111/plb.70095 PubMed DOI

Klein, J. , Ernst, M. , Christmann, A. , Tropper, M. , Leykauf, T. , Kreis, W. et al. (2021) Knockout of PubMed PMC

Klein, J. , Horn, E. , Ernst, M. , Leykauf, T. , Leupold, T. , Dorfner, M. et al. (2021) RNAi‐mediated gene knockdown of progesterone 5β‐reductases in PubMed PMC

Korbei, B. & Luschnig, C. (2021) Plants on (brassino)steroids. Nature Plants, 7, 548–549. PubMed

Kreis, W. (2017) The foxgloves ( PubMed

Kunert, M. , Langley, C. , Lucier, R. , Ploss, K. , Rodríguez López, C.E. , Serna Guerrero, D.A. et al. (2023) Promiscuous CYP87A enzyme activity initiates cardenolide biosynthesis in plants. Nature Plants, 9, 1607–1617. PubMed PMC

Leykauf, T. , Klein, J. , Ernst, M. , Dorfner, M. , Ignatova, A. , Kreis, W. et al. (2023) Overexpression and RNAi‐mediated knockdown of two 3β‐hydroxy‐Δ5‐steroid dehydrogenase genes in PubMed

Li, H. , Chen, L. , Chen, H. , Xue, R. , Wang, Y. & Song, J. (2022) The role of plant progesterone in regulating growth, development, and biotic/abiotic stress responses. International Journal of Molecular Sciences, 23, 10945. PubMed PMC

Li, H. , Handsaker, B. , Wysoker, A. , Fennell, T. , Ruan, J. , Homer, N. et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078–2079. Available from: 10.1093/bioinformatics/btp352 PubMed DOI PMC

Li, J. , Biswas, M.G. , Chao, A. , Russell, D.W. & Chory, J. (1997) Conservation of function between mammalian and plant steroid 5alpha‐reductases. Proceedings of the National Academy of Sciences of the United States of America, 94, 3554–3559. PubMed PMC

Liao, Y. , Smyth, G.K. & Shi, W. (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics (Oxford, England), 30, 923–930. PubMed

Lindemann, P. (2015) Steroidogenesis in Plants – Biosynthesis and Conversions of Progesterone and Other Pregnane Derivatives. Steroids, 103, 145–152. PubMed

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. PubMed PMC

Lynch, J.P. (2019) Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. New Phytologist, 223, 548–564. PubMed

Lynch, J.P. (2022) Harnessing root architecture to address global challenges the. Plant Journal, 109(415), 431. PubMed PMC

McKinney, W. (2010) Data structures for statistical computing in python. In: proceedings of the 9th python in science conference. SciPy, 56–61.

Meents, A.K. , Furch, A.C.U. , Almeida‐Trapp, M. , Özyürek, S. , Scholz, S.S. , Kirbis, A. et al. (2019) Beneficial and pathogenic Arabidopsis root‐interacting fungi differently affect auxin levels and responsive genes during early infection. Frontiers in Microbiology, 10, 380. PubMed PMC

Meitinger, N. , Geiger, D. , Augusto, T.W. , Maia de Pádua, R. & Kreis, W. (2015) Purification of Δ(5)‐3‐ketosteroid isomerase from PubMed

Meitinger, N. , Munkert, J. , Maia de Pádua, R. , de Souza Filho, J.D. , Maid, H. , Bauer, W. et al. (2016) The catalytic mechanism of the 3‐ketosteroid isomerase of

Miyaji, T. , Yamagami, A. , Nakamura, Y. , Nishida, K. , Tachibana, R. , Surina, S. et al. (2024) BIL7 enhances plant growth by regulating the transcription factor BIL1/BZR1 during brassinosteroid signaling‡. The Plant Journal, 121, e17212. Available from: 10.1111/tpj.17212 PubMed DOI PMC

Munkert, J. , Ernst, M. , Müller‐Uri, F. & Kreis, W. (2014) Identification and stress‐induced expression of three 3β‐hydroxysteroid dehydrogenases from PubMed

Mußmann, V. , Serek, M. & Winkelmann, T. (2011) Selection of transgenic

Nelson, S.E. (2009) Persephone's seeds: abortifacients and contraceptives in ancient Greek medicine and their recent scientific appraisal. Pharmacy in History, 51(57), 68. PubMed

Noguchi, T. , Fujioka, S. , Takatsuto, S. , Sakurai, A. , Yoshida, S. , Li, J. et al. (1999) PubMed PMC

Normington, K. & Russell, D.W. (1992) Tissue distribution and kinetic characteristics of rat steroid 5 alpha‐reductase isozymes. Evidence for distinct physiological functions Journal of Biological Chemistry, 267(19548), 19554. PubMed

Oklešťková, J. , Tarkowská, D. , Eyer, L. , Elbert, T. , Marek, A. , Smržová, Z. et al. (2017) Immunoaffinity chromatography combined with tandem mass spectrometry: a new tool for the selective capture and analysis of brassinosteroid plant hormones. Talanta, 170(432), 440. PubMed

Oktay, C. , Shiko, G. , Liebl, M. , Feistel, F. , Mußbach, S. , Körber, K.L. et al. (2025) PubMed DOI

Pasaribu, B. , Acosta, K. , Aylward, A. , Liang, Y. , Abramson, B.W. , Colt, K. et al. (2023) Genomics of turions from the greater duckweed reveal its pathways for dormancy and re‐emergence strategy. New Phytologist, 239(116), 131. PubMed

Pauli, G.F. , Friesen, J.B. , Gödecke, T. , Farnsworth, N.R. & Glodny, B. (2010) Occurrence of Progesterone and Related Animal Steroids in Two Higher Plants. Journal of Natural Products, 73, 338–345. PubMed

Peres, A.L.G.L. , Soares, J.S. , Tavares, R.G. , Righetto, G. , Zullo, M.A.T. , Mandava, N.B. et al. (2019) Brassinosteroids, the sixth class of phytohormones: a molecular view from the discovery to hormonal interactions in plant development and stress adaptation. International Journal of Molecular Sciences, 20, 331. Available from: 10.3390/ijms20020331 PubMed DOI PMC

Pettersen, E.F. , Goddard, T.D. , Huang, C.C. , Couch, G.S. , Greenblatt, D.M. , Meng, E.C. et al. (2004) UCSF Chimera–A Visualization System for Exploratory Research and Analysis. Journal of Computational Chemistry, 25, 1605–1612. PubMed

Retzer, K. , Akhmanova, M. , Konstantinova, N. , Malínská, K. , Leitner, J. , Petrášek, J. et al. (2019) Brassinosteroid signaling delimits root gravitropism via sorting of the PubMed PMC

Rogowska, A. & Szakiel, A. (2020) The role of sterols in plant response to abiotic stress. Phytochemistry Reviews, 19(1525), 1538.

Schaller, H. (2004) New aspects of sterol biosynthesis in growth and development of higher plants. Plant Physiology and Biochemistry: PPB, 42(465), 476. PubMed

Shiko, G. , Paulmann, M.‐J. , Feistel, F. , Ntefidou, M. , Hermann‐Ene, V. , Vetter, W. et al. (2023) Occurrence and conversion of progestogens and androgens are conserved in land plants. New Phytologist, 240, 318–337. PubMed

Simerský, R. , Novák, O. , Morris, D.A. , Pouzar, V. & Strnad, M. (2009) Identification and Quantification of Several Mammalian Steroid Hormones in Plants by UPLC‐MS/MS. Journal of Plant Growth Regulation, 28, 125–136.

Simons, R.G. & Grinwich, D.L. (1989) Immunoreactive detection of four mammalian steroids in plants. Canadian Journal of Botany, 67(288), 296.

Sinnecker, G.H.G. , Hiort, O. , Dibbelt, L. , Albers, N. , Dörr, H.G. , Hauß, H. et al. (1996) Phenotypic classification of male pseudohermaphroditism due to steroid 5α‐reductase 2 deficiency. American Journal of Medical Genetics, 63, 223–230. PubMed

Song, L. , Shi, Q.‐M. , Yang, X.‐H. , Xu, Z.‐H. & Xue, H.‐W. (2009) Membrane Steroid‐Binding Protein 1 (MSBP1) Negatively Regulates Brassinosteroid Signaling by Enhancing the Endocytosis of BAK1. Cell Research, 19, 864–876. PubMed

Tamura, K. , Stecher, G. & Kumar, S. (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(3022), 3027. PubMed PMC

Tarkowská, D. , Novák, O. , Oklešťková, J. & Strnad, M. (2016) The determination of 22 natural brassinosteroids in a minute sample of plant tissue by UHPLC‐ESI‐MS/MS. Analytical and Bioanalytical Chemistry, 408(6799), 6812. PubMed

Trott, O. & Olson, A.J. (2010) AutoDock Vina: Improving the Speed and Accuracy of Docking with a New Scoring Function, Efficient Optimization, and Multithreading. Journal of Computational Chemistry, 31, 455–461. PubMed PMC

Vriet, C. , Russinova, E. & Reuzeau, C. (2013) From squalene to brassinolide: the steroid metabolic and signaling pathways across the plant kingdom. Molecular Plant, 6(1738), 1757. PubMed

Vukašinović, N. , Wang, Y. , Vanhoutte, I. , Fendrych, M. , Guo, B. , Kvasnica, M. et al. (2021) Local brassinosteroid biosynthesis enables optimal root growth. Nature Plants, 7(619), 632. PubMed

Waterhouse, A. , Bertoni, M. , Bienert, S. , Studer, G. , Tauriello, G. , Gumienny, R. et al. (2018) SWISS‐MODEL: homology modelling of protein structures and complexes. Nucleic Acids Research, 46, W296–W303. PubMed PMC

Wobbrock, J.O. , Findlater, L. , Gergle, D. & Higgins, J.J. (2011) The aligned rank transform for nonparametric factorial analyses using only anova procedures. In: Tan, D. , Fitzpatrick, G. , Gutwin, C. , Begole, B. & Kellogg, W.A. (Eds.) Proceedings of the SIGCHI Conference on Human Factors in Computing Systems. New York, NY, USA: ACM, pp. 143–146.

Xu, W. , Zheng, B. , Bai, Q. , Wu, L. , Liu, Y. & Wu, G. (2019) Functional study of the brassinosteroid biosynthetic genes from PubMed PMC

Yang, X.‐H. , Xu, Z.‐H. & Xue, H.‐W. (2005) PubMed PMC

Yang, X. , Song, L. & Xue, H.‐W. (2008) Membrane steroid binding protein 1 (MSBP1) stimulates tropism by regulating vesicle trafficking and auxin redistribution. Molecular Plant, 1, 1077–1087. PubMed

Yao, B. , Li, R. , Yan, S. , Chan, S.‐A. & Song, W. (2018) Occurrence and estrogenic activity of steroid hormones in Chinese streams: a nationwide study based on a combination of chemical and biological tools. Environment International, 118, 1–8. PubMed

Younkin, G.C. , Alani, M.L. , Züst, T. & Jander, G. (2024) Four enzymes control natural variation in the steroid core of DOI

Zhang, X. , Lin, K. & Li, Y. (2020) Highlights to phytosterols accumulation and equilibrium in plants: Biosynthetic pathway and feedback regulation. Plant physiology and biochemistry: PPB, 155(637), 649. PubMed

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...