Genome-wide association of the metabolic shifts underpinning dark-induced senescence in Arabidopsis

Author:

Zhu Feng12ORCID,Alseekh Saleh23ORCID,Koper Kaan4ORCID,Tong Hao235ORCID,Nikoloski Zoran235ORCID,Naake Thomas2ORCID,Liu Haijun67ORCID,Yan Jianbing6ORCID,Brotman Yariv28ORCID,Wen Weiwei1ORCID,Maeda Hiroshi4ORCID,Cheng Yunjiang1ORCID,Fernie Alisdair R23ORCID

Affiliation:

1. National R&D Center for Citrus Preservation, Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan 430070, China

2. Max-Planck-Institut für Molekulare Pflanzenphysiologie, Potsdam-Golm 14476, Germany

3. Center of Plant Systems Biology and Biotechnology, Plovdiv 4000, Bulgaria

4. Department of Botany, University of Wisconsin–Madison, Madison, Wisconsin 53706, USA

5. Bioinformatics, Institute of Biochemistry and Biology, University of Potsdam, Potsdam 14476, Germany

6. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China

7. Gregor Mendel Institute, Austrian Academy of Sciences, Vienna 1030, Austria

8. Department of Life Sciences, Ben-Gurion University of the Negev, Beersheba, Israel

Abstract

Abstract Dark-induced senescence provokes profound metabolic shifts to recycle nutrients and to guarantee plant survival. To date, research on these processes has largely focused on characterizing mutants deficient in individual pathways. Here, we adopted a time-resolved genome-wide association-based approach to characterize dark-induced senescence by evaluating the photochemical efficiency and content of primary and lipid metabolites at the beginning, or after 3 or 6 days in darkness. We discovered six patterns of metabolic shifts and identified 215 associations with 81 candidate genes being involved in this process. Among these associations, we validated the roles of four genes associated with glycine, galactinol, threonine, and ornithine levels. We also demonstrated the function of threonine and galactinol catabolism during dark-induced senescence. Intriguingly, we determined that the association between tyrosine contents and TYROSINE AMINOTRANSFERASE 1 influences enzyme activity of the encoded protein and transcriptional activity of the gene under normal and dark conditions, respectively. Moreover, the single-nucleotide polymorphisms affecting the expression of THREONINE ALDOLASE 1 and the amino acid transporter gene AVT1B, respectively, only underlie the variation in threonine and glycine levels in the dark. Taken together, these results allow us to present a very detailed model of the metabolic aspects of dark-induced senescence, as well as the process itself.

Funder

National Key R&D Program of China

European Union’s Horizon 2020 Research and Innovation Programme

US Department of Energy

Deutsche Forschungsgemeinschaft in the framework of Deutsche Israeli Project

Publisher

Oxford University Press (OUP)

Subject

Cell Biology,Plant Science

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