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1.
Proc Natl Acad Sci U S A ; 121(7): e2313343121, 2024 Feb 13.
Article in English | MEDLINE | ID: mdl-38315839

ABSTRACT

Plants tightly control growth of their lateral organs, which led to the concept of apical dominance. However, outgrowth of the dormant lateral primordia is sensitive to the plant's nutritional status, resulting in an immense plasticity in plant architecture. While the impact of hormonal regulation on apical dominance is well characterized, the prime importance of sugar signaling to unleash lateral organ formation has just recently emerged. Here, we aimed to identify transcriptional regulators, which control the trade-off between growth of apical versus lateral organs. Making use of locally inducible gain-of-function as well as single and higher-order loss-of-function approaches of the sugar-responsive S1-basic-leucine-zipper (S1-bZIP) transcription factors, we disclosed their largely redundant function in establishing apical growth dominance. Consistently, comprehensive phenotypical and analytical studies of S1-bZIP mutants show a clear shift of sugar and organic nitrogen (N) allocation from apical to lateral organs, coinciding with strong lateral organ outgrowth. Tissue-specific transcriptomics reveal specific clade III SWEET sugar transporters, crucial for long-distance sugar transport to apical sinks and the glutaminase GLUTAMINE AMIDO-TRANSFERASE 1_2.1, involved in N homeostasis, as direct S1-bZIP targets, linking the architectural and metabolic mutant phenotypes to downstream gene regulation. Based on these results, we propose that S1-bZIPs control carbohydrate (C) partitioning from source leaves to apical organs and tune systemic N supply to restrict lateral organ formation by C/N depletion. Knowledge of the underlying mechanisms controlling plant C/N partitioning is of pivotal importance for breeding strategies to generate plants with desired architectural and nutritional characteristics.


Subject(s)
Basic-Leucine Zipper Transcription Factors , Plant Breeding , Basic-Leucine Zipper Transcription Factors/genetics , Basic-Leucine Zipper Transcription Factors/metabolism , Plants/metabolism , Signal Transduction/genetics , Sugars , Gene Expression Regulation, Plant , Plant Proteins/genetics , Plant Proteins/metabolism
2.
Plant Cell ; 34(1): 616-632, 2022 01 20.
Article in English | MEDLINE | ID: mdl-34755865

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.


Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis/growth & development , Seedlings/genetics , Transcription Factors/genetics , Arabidopsis/genetics , Arabidopsis Proteins/metabolism , Gene Expression Regulation, Plant , Seedlings/growth & development , Transcription Factors/metabolism
3.
RNA Biol ; 16(7): 972-987, 2019 07.
Article in English | MEDLINE | ID: mdl-31043113

ABSTRACT

CsrA is a widely conserved, abundant small RNA binding protein that has been found in E. coli and other Gram-negative bacteria where it is involved in the regulation of carbon metabolism, biofilm formation and virulence. CsrA binds to single-stranded GGA motifs around the SD sequence of target mRNAs where it inhibits or activates translation or influences RNA processing. Small RNAs like CsrB or CsrC containing 13-22 GGA motifs can sequester CsrA, thereby abrogating the effect of CsrA on its target mRNAs. In B. subtilis, CsrA has so far only been found to regulate one target, hag mRNA and to be sequestered by a protein (FliW) and not by an sRNA. Here, we employ a combination of in vitro and in vivo methods to investigate the effect of CsrA on the small regulatory RNA SR1 from B. subtilis, its primary target ahrC mRNA and its downstream targets, the rocABC and rocDEF operons. We demonstrate that CsrA can promote the base-pairing interactions between SR1 and ahrC mRNA, a function that has so far only been found for Hfq or ProQ. Abbreviations: aa, amino acid; bp, basepair; nt, nucleotide; PAA, polyacrylamide; SD, Shine Dalgarno.


Subject(s)
Bacillus subtilis/metabolism , Bacterial Proteins/metabolism , RNA, Bacterial/metabolism , Arginine/pharmacology , Bacillus subtilis/drug effects , Bacillus subtilis/genetics , Bacillus subtilis/growth & development , Base Pairing/genetics , Base Sequence , Carbon/pharmacology , Gene Expression Regulation, Bacterial , Mutation/genetics , Nucleic Acid Conformation , Promoter Regions, Genetic/genetics , Protein Binding , Protein Biosynthesis , RNA Stability/genetics , RNA, Bacterial/chemistry , RNA, Bacterial/genetics , RNA, Messenger/chemistry , RNA, Messenger/genetics , RNA, Messenger/metabolism , Ribonucleases/metabolism , Transcription, Genetic
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