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Sugar signaling modulates SHOOT MERISTEMLESS expression and meristem function in Arabidopsis
Monday, 2024/09/16 | 07:58:06

Filipa L. LopesAlice MalivertLeonor MargalhaAna ConfrariaRegina FeilJohn E. LunnHenrik JönssonBenoît Landrein, Pau Formosa-Jordan and Elena Baena-González

PNAS; September 6, 2024; 121 (37) e2408699121

Significance

The shoot apical meristem (SAM) generates all the aboveground plant organs and is hence crucial for plant adaptation to the environment. However, little is known of how the SAM perceives environmental information and how this impacts meristem activity and plant growth. Here, we show that sugars promote the accumulation of SHOOT MERISTEMLESS (STM), a transcription factor necessary for stem cell identity and proliferation. This is counteracted by SUCROSE NON-FERMENTING1-RELATED KINASE 1 (SnRK1), which is activated when sugar levels decline, and interacts with STM. On the other hand, silencing SnRK1 in the SAM showed that it is needed for meristem integrity. Overall, our data support a dual function for SnRK1 in plant growth and a need to finely balance its activity.

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 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.

 

See https://www.pnas.org/doi/10.1073/pnas.2408699121

 

Figure 1: Effect of light on STM expression. (A–C), STM-VENUS expression in SAMs of pSTM::STM-VENUS plants grown under HL (170 μmol m−2 s−1) or LL (60 μmol m−2 s−1) conditions or transferred from HL to darkness (D) or kept under HL for the indicated times. (A) Representative STM-VENUS images of SAMs from HL and LL-grown plants and of plants transferred to D for 48 h. (Scale bar, 50 µm.) (B and C) Quantification of STM-VENUS signal. (B) Plots show SAM measurements of plants grown as three independent batches normalized by the mean of the HL condition of each batch (HL, n = 44; LL, n = 45). Student’s t test (P-value shown). (C) Plots show SAM measurements of plants grown as two to three independent batches normalized by the mean of the HL condition of each batch (0 h, n = 18; 24 h L, n = 19; 24 h D, n = 18; 48 h L, n = 19; 48 h D, n = 18; 72 h L, n = 9; 72 h D, n = 12). The 0 h sample serves as control for both L and D treatments. Different letters indicate statistically significant differences (Kruskal–Wallis with Dunn's test; P < 0.05). (D) Immunoblot analyses of STM and TUBULIN (TUB) protein levels in SAMs of pSTM::STM-VENUS plants grown under HL or LL conditions or grown in HL and transferred to D for 48 h. Ponceau staining serves as loading control. Numbers refer to mean STM-VENUS amounts in LL and D as compared to HL (n = 2; each a pool of five SAMs; in parentheses, SEM). (E) RT-qPCR analyses of STM and STM target genes AIL7 and HB25 in SAMs of pSTM::STM-VENUS plants grown in HL and transferred to D or kept in HL for 48 h. Graphs show the average of three independent samples, each consisting of a pool of five SAMs. Paired ratio t test (P-values shown).

 

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