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Evolutionary metabolomics of specialized metabolism diversification in the genus Nicotiana highlights N-acylnornicotine innovations.

ABSTRACT: Specialized metabolite (SM) diversification is a core process to plants' adaptation to diverse ecological niches. Here, we implemented a computational mass spectrometry-based metabolomics approach to exploring SM diversification in tissues of 20 species covering Nicotiana phylogenetics sections. To markedly increase metabolite annotation, we created a large in silico fragmentation database, comprising >1 million structures, and scripts for connecting class prediction to consensus substructures. Together, the approach provides an unprecedented cartography of SM diversity and section-specific innovations in this genus. As a case study and in combination with nuclear magnetic resonance and mass spectrometry imaging, we explored the distribution of N-acylnornicotines, alkaloids predicted to be specific to Repandae allopolyploids, and revealed their prevalence in the genus, albeit at much lower magnitude, as well as a greater structural diversity than previously thought. Together, the data integration approaches provided here should act as a resource for future research in plant SM evolution.

SUBMITTER: Elser D

PROVIDER: S-EPMC10456844 | biostudies-literature | 2023 Aug

REPOSITORIES: biostudies-literature

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Evolutionary metabolomics of specialized metabolism diversification in the genus Nicotiana highlights N-acylnornicotine innovations.

Elser David D Pflieger David D Villette Claire C Moegle Baptiste B Miesch Laurence L Gaquerel Emmanuel E

Science advances 20230825 34

Specialized metabolite (SM) diversification is a core process to plants' adaptation to diverse ecological niches. Here, we implemented a computational mass spectrometry-based metabolomics approach to exploring SM diversification in tissues of 20 species covering Nicotiana phylogenetics sections. To markedly increase metabolite annotation, we created a large in silico fragmentation database, comprising >1 million structures, and scripts for connecting class prediction to consensus substruc ...[more]

PMID: 37624884

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Project description:Despite the importance of diversification rates in the study of prokaryote evolution, they have not been quantitatively assessed for the majority of microorganism taxa. The investigation of evolutionary patterns in prokaryotes constitutes a challenge due to a very scarce fossil record, limited morphological differentiation and frequently complex taxonomic relationships, which make even species recognition difficult. Although the speciation models and speciation rates in eukaryotes have traditionally been established by analyzing the fossil record data, this is frequently incomplete, and not always available. More recently, several methods based on molecular sequence data have been developed to estimate speciation and extinction rates from phylogenies reconstructed from contemporary taxa. In this work, we determined the divergence time and temporal diversification of the genus Aeromonas by applying these methods widely used with eukaryotic taxa. Our analysis involved 150 Aeromonas strains using the concatenated sequences of two housekeeping genes (approximately 2,000 bp). Dating and diversification model analyses were performed using two different approaches: obtaining the consensus sequence from the concatenated sequences corresponding to all the strains belonging to the same species, or generating the species tree from multiple alignments of each gene. We used BEAST to perform a Bayesian analysis to estimate both the phylogeny and the divergence times. A global molecular clock cannot be assumed for any gene. From the chronograms obtained, we carried out a diversification analysis using several approaches. The results suggest that the genus Aeromonas began to diverge approximately 250 millions of years (Ma) ago. All methods used to determine Aeromonas diversification gave similar results, suggesting that the speciation process in this bacterial genus followed a rate-constant (Yule) diversification model, although there is a small probability that a slight deceleration occurred in recent times. We also determined the constant of diversification (λ) values, which in all cases were very similar, about 0.01 species/Ma, a value clearly lower than those described for different eukaryotes.

Project description:Background and aimsTo better understand C4 evolution in monocots, we characterized C3-C4 intermediate phenotypes in the grass genus Homolepis (subtribe Arthropogoninae).MethodsCarbon isotope ratio (δ13C), leaf gas exchange, mesophyll (M) and bundle sheath (BS) tissue characteristics, organelle size and numbers in M and BS tissue, and tissue distribution of the P-subunit of glycine decarboxylase (GLDP) were determined for five Homolepis species and the C4 grass Mesosetum loliiforme from a phylogenetic sister clade. We generated a transcriptome-based phylogeny for Homolepis and Mesosetum species to interpret physiological and anatomical patterns in an evolutionary context, and to test for hybridization.Key resultsHomolepis contains two C3 species (H. glutinosa, H. villaricensis), one species with a weaker form of C2 termed sub-C2 (H. isocalycia), and two C2 species (H. longispicula, H. aturensis). Homolepis longispicula and H. aturensis express over 85 % of leaf glycine in centripetal mitochondria within the BS, and have increased fractions of leaf chloroplasts, mitochondria and peroxisomes within the BS relative to H. glutinosa. Analysis of leaf gas exchange, cell ultrastructure and transcript expression show M. loliiforme is a C4 plant of the NADP-malic enzyme subtype. Homolepis comprises two sister clades, one containing H. glutinosa and H. villaricensis and the second H. longispicula and H. aturensis. Homolepis isocalycia is of hybrid origin, its parents being H. aturensis and a common ancestor of the C3 Homolepis clade and H. longispicula.ConclusionsPhotosynthetic activation of BS tissue in the sub-C2 and C2 species of Homolepis is similar to patterns observed in C3-C4 intermediate eudicots, indicating common evolutionary pathways from C3 to C4 photosynthesis in these disparate clades. Hybridization can diversify the C3-C4 intermediate character state and should be considered in reconstructing putative ancestral states using phylogenetic analyses.

Dataset Information

Evolutionary metabolomics of specialized metabolism diversification in the genus Nicotiana highlights N-acylnornicotine innovations.

Publications

Evolutionary metabolomics of specialized metabolism diversification in the genus <i>Nicotiana</i> highlights <i>N-</i>acylnornicotine innovations.

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