Metabolome plasticity in 241 Arabidopsis thaliana accessions reveals evolutionary cold adaptation processes

Author(s)
Jakob Weiszmann, Dirk Walther, Pieter Clauw, Georg Back, Joanna Gunis, Ilka Reichardt, Stefanie Koemeda, Jakub Jez, Magnus Nordborg, Jana Schwarzerova, Iro Pierides, Thomas Nägele, Wolfram Weckwerth
Abstract

Acclimation and adaptation of metabolism to a changing environment are key processes for plant survival and reproductive success. In the present study, 241 natural accessions of Arabidopsis (Arabidopsis thaliana) were grown under two different temperature regimes, 16 °C and 6 °C, and growth parameters were recorded, together with metabolite profiles, to investigate the natural genome × environment effects on metabolome variation. The plasticity of metabolism, which was captured by metabolic distance measures, varied considerably between accessions. Both relative growth rates and metabolic distances were predictable by the underlying natural genetic variation of accessions. Applying machine learning methods, climatic variables of the original growth habitats were tested for their predictive power of natural metabolic variation among accessions. We found specifically habitat temperature during the first quarter of the year to be the best predictor of the plasticity of primary metabolism, indicating habitat temperature as the causal driver of evolutionary cold adaptation processes. Analyses of epigenome- and genome-wide associations revealed accession-specific differential DNA-methylation levels as potentially linked to the metabolome and identified FUMARASE2 as strongly associated with cold adaptation in Arabidopsis accessions. These findings were supported by calculations of the biochemical Jacobian matrix based on variance and covariance of metabolomics data, which revealed that growth under low temperatures most substantially affects the accession-specific plasticity of fumarate and sugar metabolism. Our findings indicate that the plasticity of metabolic regulation is predictable from the genome and epigenome and driven evolutionarily by Arabidopsis growth habitats.

Organisation(s)
Research Platform Vienna Metabolomics Center, Research Group Bioinformatics and Computational Biology, Functional and Evolutionary Ecology
External organisation(s)
Max-Planck-Institut für Molekulare Pflanzenphysiologie, Österreichische Akademie der Wissenschaften (ÖAW), Max-Planck-Institut für molekulare Zellbiologie und Genetik, Vienna BioCenter , Brno University of Technology, Gregor Mendel-Gesellschaft-Wien, Universität Wien, Ludwig-Maximilians-Universität München
Journal
Plant Physiology
Volume
193
Pages
980-1000
No. of pages
21
ISSN
0032-0889
DOI
https://doi.org/10.1093/plphys/kiad298
Publication date
10-2023
Peer reviewed
Yes
Austrian Fields of Science 2012
106057 Metabolomics, 106031 Plant physiology, 106005 Bioinformatics, 106002 Biochemistry
Keywords
ASJC Scopus subject areas
Physiology, Genetics, Plant Science
Portal url
https://ucris.univie.ac.at/portal/en/publications/metabolome-plasticity-in-241-arabidopsis-thaliana-accessions-reveals-evolutionary-cold-adaptation-processes(3e71775f-73d9-4473-9870-a0cfb89df5fa).html