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  Perturbations in plant energy homeostasis prime lateral root initiation via SnRK1-bZIP63-ARF19 signaling

Muralidhara, P., Weiste, C., Collani, S., Krischke, M., Kreisz, P., Draken, J., et al. (2021). Perturbations in plant energy homeostasis prime lateral root initiation via SnRK1-bZIP63-ARF19 signaling. Proceedings of the National Academy of Sciences of the United States of America, 118(37): e2106961118. doi:10.1073/pnas.2106961118.

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Muralidhara, Prathibha1, Author
Weiste, Christoph1, Author
Collani, Silvio1, Author
Krischke, Markus1, Author
Kreisz, Philipp1, Author
Draken, Jan1, Author
Feil, R.2, Author              
Mair, Andrea1, Author
Teige, Markus1, Author
Müller, Martin J.1, Author
Schmid, Markus1, Author
Becker, Dirk1, Author
Lunn, J. E.2, Author              
Rolland, Filip1, Author
Hanson, Johannes1, Author
Dröge-Laser, Wolfgang1, Author
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1External Organizations, ou_persistent22              
2System Regulation, Department Stitt, Max Planck Institute of Molecular Plant Physiology, Max Planck Society, ou_1753327              

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 Abstract: Plant architecture is highly plastic and known to respond sensitively to nutritional changes. Although of great agronomic importance, the underlying molecular mechanisms that sense and transduce these cues into plant development and growth are poorly understood. Applying diverse genetic, biochemical, and microscopic approaches, we disclosed that signaling via the central, evolutionarily conserved fuel-sensor kinase Snf1-RELATED KINASE1 (SnRK1) initiates lateral root (LR) primordia formation in response to transient metabolic perturbations. This is accomplished by SnRK1-mediated activation of a signaling cascade involving the pivotal LR regulator AUXIN RESPONSE FACTOR19 (ARF19). We propose that this developmental priming strategy represents a cost-efficient approach to ensure rapid growth recovery after stress release, providing in competitive ecosystems a clear advantage in terms of Darwinian fitness.Plants adjust their energy metabolism to continuous environmental fluctuations, resulting in a tremendous plasticity in their architecture. The regulatory circuits involved, however, remain largely unresolved. In Arabidopsis, moderate perturbations in photosynthetic activity, administered by short-term low light exposure or unexpected darkness, lead to increased lateral root (LR) initiation. Consistent with expression of low-energy markers, these treatments alter energy homeostasis and reduce sugar availability in roots. Here, we demonstrate that the LR response requires the metabolic stress sensor kinase Snf1-RELATED-KINASE1 (SnRK1), which phosphorylates the transcription factor BASIC LEUCINE ZIPPER63 (bZIP63) that directly binds and activates the promoter of AUXIN RESPONSE FACTOR19 (ARF19), a key regulator of LR initiation. Consistently, starvation-induced ARF19 transcription is impaired in bzip63 mutants. This study highlights a positive developmental function of SnRK1. During energy limitation, LRs are initiated and primed for outgrowth upon recovery. Hence, this study provides mechanistic insights into how energy shapes the agronomically important root system.All study data are included in the article and/or supporting information.

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Language(s): eng - English
 Dates: 2021-09-14
 Publication Status: Published in print
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 Identifiers: DOI: 10.1073/pnas.2106961118
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Title: Proceedings of the National Academy of Sciences of the United States of America
  Other : PNAS
  Other : Proceedings of the National Academy of Sciences of the USA
  Abbreviation : Proc. Natl. Acad. Sci. U. S. A.
Source Genre: Journal
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Publ. Info: Washington, D.C. : National Academy of Sciences
Pages: - Volume / Issue: 118 (37) Sequence Number: e2106961118 Start / End Page: - Identifier: ISSN: 0027-8424
CoNE: https://pure.mpg.de/cone/journals/resource/954925427230