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GWAS on multiple traits identifies mitochondrial ACONITASE3 as important for acclimation to submergence stress

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posted on 2022-09-16, 01:50 authored by X Meng, L Li, J Pascual, M Rahikainen, Changyu YiChangyu Yi, Ricarda JostRicarda Jost, Cunman He, A Fournier-Level, J Borevitz, S Kangasjärvi, James WhelanJames Whelan, Oliver BerkowitzOliver Berkowitz
Flooding causes severe crop losses in many parts of the world. Genetic variation in flooding tolerance exists in many species; however, there are few examples for the identification of tolerance genes and their underlying function. We conducted a genome-wide association study (GWAS) in 387 Arabidopsis (Arabidopsis thaliana) accessions. Plants were subjected to prolonged submergence followed by desubmergence, and seven traits (score, water content, Fv/Fm, and concentrations of nitrate, chlorophyll, protein, and starch) were quantified to characterize their acclimation responses. These traits showed substantial variation across the range of accessions. A total of 35 highly significant single-nucleotide polymorphisms (SNPs) were identified across the 20 GWA datasets, pointing to 22 candidate genes, with functions in TCA cycle, DNA modification, and cell division. Detailed functional characterization of one candidate gene, ACONITASE3 (ACO3), was performed. Chromatin immunoprecipitation followed by sequencing showed that a single nucleotide polymorphism in the ACO3 promoter co-located with the binding site of the master regulator of retrograde signaling ANAC017, while subcellular localization of an ACO3-YFP fusion protein confirmed a mitochondrial localization during submergence. Analysis of mutant and overexpression lines determined changes in trait parameters that correlated with altered submergence tolerance and were consistent with the GWAS results. Subsequent RNA-seq experiments suggested that impairing ACO3 function increases the sensitivity to submergence by altering ethylene signaling, whereas ACO3 overexpression leads to tolerance by metabolic priming. These results indicate that ACO3 impacts submergence tolerance through integration of carbon and nitrogen metabolism via the mitochondrial TCA cycle and impacts stress signaling during acclimation to stress.


This work was supported by the facilities of the Australian Research Council Centre of Excellence Program (CE140100008, ARC Centre of Excellence in Plant Energy Biology; J.W.; ARC Discovery Grant DP200102452; J.W.). X.M., L.L., and C.Y. were supported by a La Trobe University postgraduate research scholarship. X.M. was supported by the China Postdoctoral Science Foundation (2020M672156) and the Natural Science Foundation of Shandong Province (ZR2021QC028), L.L. was supported by the China Postdoctoral Science Foundation (2020M672046) and S.K., J.P., and M.R. were supported by Academy of Finland project 307719 and 345071, post-doctoral grant 325122, and the Center of Excellence program 307335.


Publication Date



Plant Physiology






20p. (p. 2039-2058)


Oxford University Press



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© The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (, which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial reuse, please contact