Sugar signaling modulates SHOOT MERISTEMLESS expression and meristem function in Arabidopsis
(2024) In Proceedings of the National Academy of Sciences of the United States of America 121(37).- Abstract
In plants, development of all above-ground tissues relies on the shoot apical meristem (SAM) which balances cell proliferation and differentiation to allow life-long growth. To maximize fitness and survival, meristem activity is adjusted to the prevailing conditions through a poorly understood integration of developmental signals with environmental and nutritional information. Here, we show that sugar signals influence SAM function by altering the protein levels of SHOOT MERISTEMLESS (STM), a key regulator of meristem maintenance. STM is less abundant in inflorescence meristems with lower sugar content, resulting from plants being grown or treated under limiting light conditions. Additionally, sucrose but not light is sufficient to... (More)
In plants, development of all above-ground tissues relies on the shoot apical meristem (SAM) which balances cell proliferation and differentiation to allow life-long growth. To maximize fitness and survival, meristem activity is adjusted to the prevailing conditions through a poorly understood integration of developmental signals with environmental and nutritional information. Here, we show that sugar signals influence SAM function by altering the protein levels of SHOOT MERISTEMLESS (STM), a key regulator of meristem maintenance. STM is less abundant in inflorescence meristems with lower sugar content, resulting from plants being grown or treated under limiting light conditions. Additionally, sucrose but not light is sufficient to sustain STM accumulation in excised inflorescences. Plants overexpressing the α1-subunit of SUCROSE-NON-FERMENTING1-RELATED KINASE 1 (SnRK1) accumulate less STM protein under optimal light conditions, despite higher sugar accumulation in the meristem. Furthermore, SnRK1α1 interacts physically with STM and inhibits its activity in reporter assays, suggesting that SnRK1 represses STM protein function. Contrasting the absence of growth defects in SnRK1α1 overexpressors, silencing SnRK1α in the SAM leads to meristem dysfunction and severe developmental phenotypes. This is accompanied by reduced STM transcript levels, suggesting indirect effects on STM. Altogether, we demonstrate that sugars promote STM accumulation and that the SnRK1 sugar sensor plays a dual role in the SAM, limiting STM function under unfavorable conditions but being required for overall meristem organization and integrity under favorable conditions. This highlights the importance of sugars and SnRK1 signaling for the proper coordination of meristem activities.
(Less)
- author
- Lopes, Filipa L. ; Formosa-Jordan, Pau ; Malivert, Alice ; Margalha, Leonor ; Confraria, Ana ; Feil, Regina ; Lunn, John E. ; Jönsson, Henrik LU ; Landrein, Benoît and Baena-González, Elena
- organization
- publishing date
- 2024-09
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- Arabidopsis thaliana, plant development, shoot apical meristem, sugar signaling
- in
- Proceedings of the National Academy of Sciences of the United States of America
- volume
- 121
- issue
- 37
- article number
- e2408699121
- publisher
- National Academy of Sciences
- external identifiers
-
- pmid:39240964
- scopus:85203419917
- ISSN
- 0027-8424
- DOI
- 10.1073/pnas.2408699121
- language
- English
- LU publication?
- yes
- id
- 8a4b5e89-6d56-4329-9191-0d7bd6d8401b
- date added to LUP
- 2024-11-22 14:55:49
- date last changed
- 2025-05-10 04:34:37
@article{8a4b5e89-6d56-4329-9191-0d7bd6d8401b,
abstract = {{<p>In plants, development of all above-ground tissues relies on the shoot apical meristem (SAM) which balances cell proliferation and differentiation to allow life-long growth. To maximize fitness and survival, meristem activity is adjusted to the prevailing conditions through a poorly understood integration of developmental signals with environmental and nutritional information. Here, we show that sugar signals influence SAM function by altering the protein levels of SHOOT MERISTEMLESS (STM), a key regulator of meristem maintenance. STM is less abundant in inflorescence meristems with lower sugar content, resulting from plants being grown or treated under limiting light conditions. Additionally, sucrose but not light is sufficient to sustain STM accumulation in excised inflorescences. Plants overexpressing the α1-subunit of SUCROSE-NON-FERMENTING1-RELATED KINASE 1 (SnRK1) accumulate less STM protein under optimal light conditions, despite higher sugar accumulation in the meristem. Furthermore, SnRK1α1 interacts physically with STM and inhibits its activity in reporter assays, suggesting that SnRK1 represses STM protein function. Contrasting the absence of growth defects in SnRK1α1 overexpressors, silencing SnRK1α in the SAM leads to meristem dysfunction and severe developmental phenotypes. This is accompanied by reduced STM transcript levels, suggesting indirect effects on STM. Altogether, we demonstrate that sugars promote STM accumulation and that the SnRK1 sugar sensor plays a dual role in the SAM, limiting STM function under unfavorable conditions but being required for overall meristem organization and integrity under favorable conditions. This highlights the importance of sugars and SnRK1 signaling for the proper coordination of meristem activities.</p>}},
author = {{Lopes, Filipa L. and Formosa-Jordan, Pau and Malivert, Alice and Margalha, Leonor and Confraria, Ana and Feil, Regina and Lunn, John E. and Jönsson, Henrik and Landrein, Benoît and Baena-González, Elena}},
issn = {{0027-8424}},
keywords = {{Arabidopsis thaliana; plant development; shoot apical meristem; sugar signaling}},
language = {{eng}},
number = {{37}},
publisher = {{National Academy of Sciences}},
series = {{Proceedings of the National Academy of Sciences of the United States of America}},
title = {{Sugar signaling modulates SHOOT MERISTEMLESS expression and meristem function in Arabidopsis}},
url = {{http://dx.doi.org/10.1073/pnas.2408699121}},
doi = {{10.1073/pnas.2408699121}},
volume = {{121}},
year = {{2024}},
}