The onset of plant life is characterized by a major phase transition. During early heterotrophic seedling establishment, seed storage reserves fuel metabolic demands, allowing the plant to switch to autotrophic metabolism. Although metabolic pathways leading to storage compound mobilization are well-described, the regulatory circuits remain largely unresolved. Using an inducible knockdown approach of the evolutionarily conserved energy master regulator Snf1-RELATED-PROTEIN-KINASE1 (SnRK1), phenotypic studies reveal its crucial function in Arabidopsis thaliana seedling establishment. Importantly, glucose feeding largely restores growth defects of the kinase mutant, supporting its major impact in resource mobilization. Detailed metabolite studies reveal sucrose as a primary resource early in seedling establishment, in a SnRK1-independent manner. Later, SnRK1 orchestrates catabolism of triacylglycerols and amino acids. Concurrent transcriptomic studies highlight SnRK1 functions in controlling metabolic hubs fuelling gluconeogenesis, as exemplified by cytosolic PYRUVATE ORTHOPHOSPHATE DIKINASE (cyPPDK). Here, SnRK1 establishes its function via phosphorylation of the transcription factor BASIC LEUCINE ZIPPER63 (bZIP63), which directly targets and activates the cyPPDK promoter. Taken together, our results disclose developmental and catabolic functions of SnRK1 in seed storage mobilization and describe a prototypic gene regulatory mechanism. As seedling establishment is important for plant vigor and crop yield, our findings are of agronomical importance.
Henninger, Markus
Pedrotti, Lorenzo
Krischke, Markus
Draken, Jan
Wildenhain, Theresa
Fekete, Agnes
Rolland, Filip
Muller, Martin J
Froschel, Christian
Weiste, Christoph
Droge-Laser, Wolfgang
eng
Research Support, Non-U.S. Gov't
England
2021/11/11
Plant Cell. 2022 Jan 20;34(1):616-632. doi: 10.1093/plcell/koab270.
%0 Journal Article
%1 henninger2022evolutionarily
%A Henninger, M.
%A Pedrotti, L.
%A Krischke, M.
%A Draken, J.
%A Wildenhain, T.
%A Fekete, A.
%A Rolland, F.
%A Muller, M. J.
%A Froschel, C.
%A Weiste, C.
%A Droge-Laser, W.
%D 2022
%J Plant Cell
%K & Arabidopsis/genetics/*growth development myOwn
%N 1
%P 616-632
%R 10.1093/plcell/koab270
%T The evolutionarily conserved kinase SnRK1 orchestrates resource mobilization during Arabidopsis seedling establishment
%U https://www.ncbi.nlm.nih.gov/pubmed/34755865
%V 34
%X The onset of plant life is characterized by a major phase transition. During early heterotrophic seedling establishment, seed storage reserves fuel metabolic demands, allowing the plant to switch to autotrophic metabolism. Although metabolic pathways leading to storage compound mobilization are well-described, the regulatory circuits remain largely unresolved. Using an inducible knockdown approach of the evolutionarily conserved energy master regulator Snf1-RELATED-PROTEIN-KINASE1 (SnRK1), phenotypic studies reveal its crucial function in Arabidopsis thaliana seedling establishment. Importantly, glucose feeding largely restores growth defects of the kinase mutant, supporting its major impact in resource mobilization. Detailed metabolite studies reveal sucrose as a primary resource early in seedling establishment, in a SnRK1-independent manner. Later, SnRK1 orchestrates catabolism of triacylglycerols and amino acids. Concurrent transcriptomic studies highlight SnRK1 functions in controlling metabolic hubs fuelling gluconeogenesis, as exemplified by cytosolic PYRUVATE ORTHOPHOSPHATE DIKINASE (cyPPDK). Here, SnRK1 establishes its function via phosphorylation of the transcription factor BASIC LEUCINE ZIPPER63 (bZIP63), which directly targets and activates the cyPPDK promoter. Taken together, our results disclose developmental and catabolic functions of SnRK1 in seed storage mobilization and describe a prototypic gene regulatory mechanism. As seedling establishment is important for plant vigor and crop yield, our findings are of agronomical importance.
@article{henninger2022evolutionarily,
abstract = {The onset of plant life is characterized by a major phase transition. During early heterotrophic seedling establishment, seed storage reserves fuel metabolic demands, allowing the plant to switch to autotrophic metabolism. Although metabolic pathways leading to storage compound mobilization are well-described, the regulatory circuits remain largely unresolved. Using an inducible knockdown approach of the evolutionarily conserved energy master regulator Snf1-RELATED-PROTEIN-KINASE1 (SnRK1), phenotypic studies reveal its crucial function in Arabidopsis thaliana seedling establishment. Importantly, glucose feeding largely restores growth defects of the kinase mutant, supporting its major impact in resource mobilization. Detailed metabolite studies reveal sucrose as a primary resource early in seedling establishment, in a SnRK1-independent manner. Later, SnRK1 orchestrates catabolism of triacylglycerols and amino acids. Concurrent transcriptomic studies highlight SnRK1 functions in controlling metabolic hubs fuelling gluconeogenesis, as exemplified by cytosolic PYRUVATE ORTHOPHOSPHATE DIKINASE (cyPPDK). Here, SnRK1 establishes its function via phosphorylation of the transcription factor BASIC LEUCINE ZIPPER63 (bZIP63), which directly targets and activates the cyPPDK promoter. Taken together, our results disclose developmental and catabolic functions of SnRK1 in seed storage mobilization and describe a prototypic gene regulatory mechanism. As seedling establishment is important for plant vigor and crop yield, our findings are of agronomical importance.},
added-at = {2024-02-15T15:08:22.000+0100},
author = {Henninger, M. and Pedrotti, L. and Krischke, M. and Draken, J. and Wildenhain, T. and Fekete, A. and Rolland, F. and Muller, M. J. and Froschel, C. and Weiste, C. and Droge-Laser, W.},
biburl = {https://www.bibsonomy.org/bibtex/2d633dfdf95a76e3f2cebb981f56ceb88/jvsi_all},
doi = {10.1093/plcell/koab270},
interhash = {e08dbfa25b1f9adeac29dec8c0c3c7e3},
intrahash = {d633dfdf95a76e3f2cebb981f56ceb88},
issn = {1532-298X (Electronic)
1040-4651 (Print)
1040-4651 (Linking)},
journal = {Plant Cell},
keywords = {& Arabidopsis/genetics/*growth development myOwn},
note = {Henninger, Markus
Pedrotti, Lorenzo
Krischke, Markus
Draken, Jan
Wildenhain, Theresa
Fekete, Agnes
Rolland, Filip
Muller, Martin J
Froschel, Christian
Weiste, Christoph
Droge-Laser, Wolfgang
eng
Research Support, Non-U.S. Gov't
England
2021/11/11
Plant Cell. 2022 Jan 20;34(1):616-632. doi: 10.1093/plcell/koab270.},
number = 1,
pages = {616-632},
timestamp = {2024-02-15T15:08:22.000+0100},
title = {The evolutionarily conserved kinase SnRK1 orchestrates resource mobilization during Arabidopsis seedling establishment},
type = {Journal Article},
url = {https://www.ncbi.nlm.nih.gov/pubmed/34755865},
volume = 34,
year = 2022
}