Metabolomic and gene expression approaches reveal the developmental and environmental regulation of the secondary metabolism of yac\xf3n (Smallanthus sonchifolius, Asteraceae)

Guillermo F. Padilla-González,Javier Gómez-Zeledón,Maximilian Frey,Otmar Spring,Fernando B. Da Costa

doi:10.1038/s41598-019-49246-2

Guillermo F. Padilla-González, Javier Gómez-Zeledón + Show 3 more

Open Access

https://doi.org/10.1038/s41598-019-49246-2

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Abstract

Acting as chemical defense or signaling compounds, secondary metabolites (SMs) play an essential role in the evolutionary success of many angiosperm plant families. However, the adaptive advantages that SMs confer, and the influence of environmental and developmental factors on SMs expression, remains poorly understood. A study of taxa endemic to the variable Andean climate, using a metabolomics approach, may provide further insight. By analyzing gene expression patterns and metabolic fingerprints, we report herein the developmental and environmental regulation of the secondary metabolism of Smallanthus sonchifolius (yacón), a medicinal Andean plant. Our results demonstrate a clear developmental stage dependent regulation of the secondary metabolism of yacón leaves wherein the metabolic diversity increases with plant age. However, environmental factors seem to regulate biosynthetic pathways, creating differences in the expression of chemical classes, pointing to an association between transcription levels of relevant genes and the relative amounts of more than 40 different metabolites. This study suggests that the secondary metabolism of yacón is regulated by a complex interplay between environmental factors and developmental stage and provides insight into the regulatory factors and adaptive roles of SMs in Andean taxa.

Highlights

With more than 23,000 species currently described and a global distribution, Asteraceae represents one of the largest angiosperm plant families
In conducting metabolic fingerprinting via ultra-high-performance liquid chromatography coupled to UV and high-resolution mass spectrometry (UHPLC-UV-HRMS) of yacón leaves collected in different developmental stages (Fig. 2a), 1,562 and 1,353 mass signals were recorded in the positive and negative ionization modes, respectively
We found that metabolic differences in leaves of yacón are related to developmental and environmental factors and that different classes of secondary metabolites respond differently to such factors

Summary

Introduction

With more than 23,000 species currently described and a global distribution, Asteraceae represents one of the largest angiosperm plant families. Given its remarkable adaptive success in diverse environments and rapid growth, yacón can be considered as a model organism to use in elucidating the influence of intrinsic (e.g., plant developmental stage) and extrinsic environmental factors on the biosynthesis and accumulation of secondary metabolites in Andean groups. By using modern analytical platforms and computational methods, this relatively new research field has promoted a broader analysis of plant metabolism, leading to a better understanding of the interactions of organisms with their environments[31] In this context, metabolomics constitutes an interesting approach to the study of the influence of abiotic environmental factors on the metabolism of higher plants[10], including Andean taxa. Given the ecological significance and medicinal importance of chlorogenic acids (CGAs), flavonoids and STLs, their expression levels were monitored, at different developmental stages, using key genes involved in their biosynthetic pathway; (hydroxycinnamoyl CoA: quinate hydroxycinnamoyl transferase (HQT), chalcone synthase (CHS) and germacrene A oxidase (GAO), respectively (Fig. 1)

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