Does the Phytochemical Diversity of Wild Plants Like the Erythrophleum genus Correlate with Geographical Origin?

Secondary metabolites are essential for plant survival and reproduction. Wild undomesticated and tropical plants are expected to harbor highly diverse metabolomes. We investigated the metabolomic diversity of two morphologically similar trees of tropical Africa, Erythrophleum suaveolens and E. ivorense, known for particular secondary metabolites named the cassaine-type diterpenoids. To assess how the metabolome varies between and within species, we sampled leaves from individuals of different geographic origins but grown from seeds in a common garden in Cameroon. Metabolites were analyzed using reversed phase LC-HRMS(/MS). Data were interpreted by untargeted metabolomics and molecular networks based on MS/MS data. Multivariate analyses enabled us to cluster samples based on species but also on geographic origins. We identified the structures of 28 cassaine-type diterpenoids among which 19 were new, 10 were largely specific to E. ivorense and five to E. suaveolens. Our results showed that the metabolome allows an unequivocal distinction of morphologically-close species, suggesting the potential of metabolite fingerprinting for these species. Plant geographic origin had a significant influence on relative concentrations of metabolites with variations up to eight (suaveolens) and 30 times (ivorense) between origins of the same species. This shows that the metabolome is strongly influenced by the geographical origin of plants (i.e., genetic factors).

[1]  X. Tong,et al.  [Quality evaluation of different Berberidis Cortex species based on ~1H-NMR metabolomics and anti-diabetic activity]. , 2020, Zhongguo Zhong yao za zhi = Zhongguo zhongyao zazhi = China journal of Chinese materia medica.

[2]  M. Beniddir,et al.  Five new cassane diterpenes from the seeds and bark of Erythrophleum suaveolens. , 2020, Fitoterapia.

[3]  Kazuki Saito,et al.  Editorial: The Origin of Plant Chemodiversity – Conceptual and Empirical Insights , 2020, Frontiers in Plant Science.

[4]  Masanori Arita,et al.  Systematic Multi-Omics Integration (MOI) Approach in Plant Systems Biology , 2020, Frontiers in Plant Science.

[5]  Milen I Georgiev,et al.  Authenticity and quality evaluation of different Rhodiola species and commercial products based on NMR-spectroscopy and HPLC. , 2020, Phytochemical analysis : PCA.

[6]  U. Albuquerque,et al.  The chemical ecology approach to modern and early human use of medicinal plants , 2020, Chemoecology.

[7]  Simon Rogers,et al.  Feature-Based Molecular Networking in the GNPS Analysis Environment , 2019, Nature Methods.

[8]  Christine M. Aceves,et al.  Reproducible molecular networking of untargeted mass spectrometry data using GNPS , 2019, Nature Protocols.

[9]  Vanessa V Phelan,et al.  Feature-Based Molecular Networking for Metabolite Annotation. , 2020, Methods in molecular biology.

[10]  J. Doucet,et al.  Seed and pollen dispersal distances in two African legume timber trees and their reproductive potential under selective logging , 2019, Molecular ecology.

[11]  N. Son.  Genus Erythrophleum: Botanical description, traditional use, phytochemistry and pharmacology , 2019, Phytochemistry Reviews.

[12]  M. Beniddir,et al.  New cassane diterpenoids from the root bark of Erythrophleum suaveolens , 2019, Phytochemistry Letters.

[13]  Joe Wandy,et al.  MolNetEnhancer: Enhanced Molecular Networks by Integrating Metabolome Mining and Annotation Tools , 2019, bioRxiv.

[14]  F. Liu,et al.  Comparative analysis of proteomic and metabolomic profiles of different species of Paris. , 2019, Journal of proteomics.

[15]  Ying Wang,et al.  Naturally occurring cassane diterpenoids (CAs) of Caesalpinia: A systematic review of its biosynthesis, chemistry and pharmacology. , 2019, Fitoterapia.

[16]  A. Fernie,et al.  Exploring the Diversity of Plant Metabolism. , 2019, Trends in plant science.

[17]  Marc Litaudon,et al.  MetGem Software for the Generation of Molecular Networks Based on the t-SNE Algorithm. , 2018, Analytical chemistry.

[18]  Lei Wang,et al.  Cassaine diterpenoids from the seeds of Erythrophleum fordii and their cytotoxic activities. , 2018, Fitoterapia.

[19]  P. Steenkamp,et al.  Leishmanicidal activity of the root bark of Erythrophleum Ivorense (Fabaceae) and identification of some of its compounds by ultra-performance liquid chromatography quadrupole time of flight mass spectrometry (UPLC-QTOF-MS/MS). , 2018, Journal of ethnopharmacology.

[20]  Yann Guitton,et al.  Create, run, share, publish, and reference your LC-MS, FIA-MS, GC-MS, and NMR data analysis workflows with the Workflow4Metabolomics 3.0 Galaxy online infrastructure for metabolomics. , 2017, The international journal of biochemistry & cell biology.

[21]  Jeong Ah Kim,et al.  Cytotoxic and apoptosis-inducing activities against human lung cancer cell lines of cassaine diterpenoids from the bark of Erythrophleum fordii. , 2017, Bioorganic & medicinal chemistry letters.

[22]  Kazuki Saito,et al.  Integrated omics analysis of specialized metabolism in medicinal plants. , 2017, The Plant journal : for cell and molecular biology.

[23]  Jian‐Kang Zhu.  Abiotic Stress Signaling and Responses in Plants , 2016, Cell.

[24]  Kristian Fog Nielsen,et al.  Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking , 2016, Nature Biotechnology.

[25]  Philippe Rinaudo,et al.  biosigner: A New Method for the Discovery of Significant Molecular Signatures from Omics Data , 2016, Front. Mol. Biosci..

[26]  Prakash P. Kumar,et al.  Plant hormone-mediated regulation of stress responses , 2016, BMC Plant Biology.

[27]  K. Halliday,et al.  Molecular and genetic control of plant thermomorphogenesis , 2016, Nature Plants.

[28]  G. Komlaga,et al.  Cassane diterpenoids from stem bark of Erythrophleum suaveolens [(Guill. et Perr.), Brenan] , 2015 .

[29]  Daniel Jacob,et al.  Workflow4Metabolomics: a collaborative research infrastructure for computational metabolomics , 2014, Bioinform..

[30]  P. Retailleau,et al.  Four new cassane diterpenoid amides from Erythrophleum suaveolens [(Guill. et Perr.), Brenan] , 2014 .

[31]  Jeong Ah Kim,et al.  Cassaine diterpene alkaloids from Erythrophleum fordii and their anti-angiogenic effect. , 2014, Bioorganic & medicinal chemistry letters.

[32]  J. Doucet,et al.  Large-scale pattern of genetic differentiation within African rainforest trees: insights on the roles of ecological gradients and past climate changes on the evolution of Erythrophleum spp (Fabaceae) , 2013, BMC Evolutionary Biology.

[33]  A. Gómez-Cadenas,et al.  Metabolomics as a Tool to Investigate Abiotic Stress Tolerance in Plants , 2013, International journal of molecular sciences.

[34]  Joost J. B. Keurentjes,et al.  Multi-dimensional regulation of metabolic networks shaping plant development and performance. , 2012, Journal of experimental botany.

[35]  P. Yadav,et al.  A review on cassane and norcassane diterpenes and their pharmacological studies. , 2012, Fitoterapia.

[36]  Xiao-guang Chen,et al.  Cytotoxic cassaine diterpenoid-diterpenoid amide dimers and diterpenoid amides from the leaves of Erythrophleum fordii. , 2010, Phytochemistry.

[37]  Matej Oresic,et al.  MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data , 2010, BMC Bioinformatics.

[38]  J. Keurentjes,et al.  Metabolomics: the chemistry between ecology and genetics , 2010, Molecular ecology resources.

[39]  C. Fankhauser,et al.  Light-regulated plant growth and development. , 2010, Current topics in developmental biology.

[40]  Jing Qu,et al.  Rapid structural determination of new trace cassaine-type diterpenoid amides in fractions from Erythrophleum fordii by liquid chromatography-diode-array detection/electrospray ionization tandem mass spectrometry and liquid chromatography/nuclear magnetic resonance. , 2007, Rapid communications in mass spectrometry : RCM.

[41]  Jing Liu,et al.  Progress on Cassaine-Type Diterpenoid Ester Amines and Amides (Erythrophleum Alkaloids) , 2006 .

[42]  Richard A Dixon,et al.  Phytochemistry meets genome analysis, and beyond. , 2003, Phytochemistry.

[43]  L. Verotta,et al.  Chemical and pharmacological characterization of Erythrophleum lasianthum alkaloids. , 1995, Planta medica.

[44]  J. Mann.  Fortschritte der Chemie organischer Naturstoffe/Progress in the Chemistry of Organic Natural Products , 2011 .

[45]  F. Sandberg.  Medicinal and toxic plants from Equatorial Africa: a pharmacologic approach. , 1980, Journal of ethnopharmacology.

[46]  A. Cronlund.  The botanical and phytochemical differentiation between Erythrophleum suaveolens and E. ivorense. , 1976, Planta Medica.

[47]  R. Coates.  Biogenetic-type rearrangements of terpenes. , 1976, Fortschritte der Chemie organischer Naturstoffe = Progress in the chemistry of organic natural products. Progres dans la chimie des substances organiques naturelles.

[48]  J. Loder,et al.  3β-acetoxynorerythrosuamine, a highly cytotoxic alkaloid from erythrophleum chlorostachys , 1975 .

[49]  A. Cronlund,et al.  Alkaloids from the bark of Erythrophleum couminga. , 1975, Acta pharmaceutica Suecica.

[50]  A. Cronlund.  Two new alkaloids from bark of Erythrophleum ivorense. , 1971, Acta pharmaceutica Suecica.

[51]  C. Culvenor,et al.  Isolation of norcassamidide and authentic norcassamidine from erythrophleum chlorostachys. Structural revision of the alkaloids previously known as norcassamidine, norcassamine, norethythrosuamine and dehydro-norerythrosuamine. , 1972 .

[52]  G. Spiteller,et al.  [Use of mass spectrum analysis for structure elucidation of alkaloids. X. New alkaloids from Erythrophleum guineense and about Muawin]. , 1971, Chemische Berichte.

[53]  A. Ronco,et al.  Zur Kenntnis der Erythrophleum‐Alkaloide. 17. Mitteilung. Über einige für die Konstitutionsbestimmung von Cassamin wichtige Derivate der Cassan‐19‐säure , 1961 .

[54]  V. Arya,et al.  Zur Kenntnis der Erythrophleum‐Alkaloide. 18. Mitteilung. Die Struktur des Cassamins und des Erythrophlamins , 1961 .

[55]  G. Dalma.  Chapter 36 The Erythrophleum Alkaloids , 1954 .

[56]  A. Ronco.  Zur Kenntnis der Erythrophleum-Alkaloide , 1945 .