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Nutrient-driven TOR signalling controls a chromatin-associated complex for orchestrating plant growth and stress tolerance

Nature Plants volume 11, pages 2115–2129 (2025)Cite this article

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Abstract

The conserved target of rapamycin (TOR) kinase acts as a master regulator of growth by integrating nutrient and environmental signals in eukaryotes. However, how TOR influences chromatin remains poorly understood. Here we identified a multi-subunit complex in Arabidopsis thaliana, termed the chromatin-associated complex for growth (CACG). Our findings indicate that under nutrient-rich conditions, active TOR kinase enhances CACG mRNA translation, which is facilitated by pyrimidine-rich motifs in their 5′ untranslated regions. CACG components co-occupy stress-responsive genes marked by histone acetylation, repressing their transcription to promote growth. Conversely, under nutrient-deficient conditions, inactive TOR reduces CACG mRNA translation, relieving transcriptional repression of stress-responsive genes and leading to increased stress tolerance but impaired growth. These results indicate that the CACG complex acts as a critical nutrient-responsive transcriptional regulator that is required for coordinating plant growth and stress tolerance in a TOR-dependent manner. The molecular mechanism revealed here could aid in developing high-yield crops capable of thriving in adverse environments.

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Fig. 1: Identification of a multi-subunit protein complex involved in nutrient-responsive growth.
Fig. 2: The TOR kinase is crucial for the nutrient-mediated dynamic regulation of CACG protein levels.
Fig. 3: Pyrimidine-rich motifs in the 5′ UTRs of CACG mRNAs facilitate target selection by TOR.
Fig. 4: The CACG complex suppresses the expression of stress-responsive genes to coordinate plant growth and stress tolerance.
Fig. 5: The CACG components co-occupy genes marked by histone acetylation and mediate transcription repression.
Fig. 6: Working model for the role of the nutrient–TOR–CACG axis in balancing plant growth and stress tolerance.

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Data availability

The raw RNA-seq and ChIP–seq data have been deposited in the Gene Expression Omnibus database under the accession code GSE276448. The gene symbols and locus codes of genes investigated in this study are as follows: WDR5A (AT3G49660), ZDP1 (AT1G09520), GTA1 (AT1G05860), GTA2 (AT3G53860), GTA3 (AT2G31600), TRB4 (AT1G17520), TRB5 (AT1G72740), GTE1 (AT2G34900), GTE6 (AT3G52280), CP2 (AT3G18210), GTB1 (AT4G37440), GTB2 (AT3G59670), GTB3 (AT3G50040), DP1 (AT1G09710), DRMY1 (AT1G58220), EMB1967 (AT3G54350), TOR (AT1G50030), DEAR5 (AT4G06746), DREB26 (AT1G21910), ERF1A (AT4G17500), ERF2 (AT5G47220), ERF018 (AT1G74930), ERF6 (AT4G17490), CBF2 (AT4G25470), ERF5 (AT5G47230), ERF104 (AT5G61600), DDF1 (AT1G12610), ERF13 (AT2G44840), ERF109 (AT4G34410), ERF022 (AT1G33760), ERF11 (AT1G28370) and CBF1 (AT4G25490). Source data are provided with this paper.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (grant numbers 32025003 and 32470628 to X.-J.H.).

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Authors and Affiliations

  1. College of Life Sciences, Beijing Normal University, Beijing, China

    Xin Wang & Xin-Jian He

  2. National Institute of Biological Sciences, Beijing, China

    Xin Wang, Zhen-Zhen Liu, Dan-Yang Yuan, Yu-Jia Lu, Lin Li, She Chen & Xin-Jian He

  3. Tsinghua Institute of Multidisciplinary Biomedical Research, Tsinghua University, Beijing, China

    Xin-Jian He

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Contributions

X.-J.H. and X.W. conceived the study and designed the experiments. X.W., Z.-Z.L., Y.-J.L., L.L. and S.C. performed the experiments. D.-Y.Y. performed the bioinformatics analyses. X.W. and X.-J.H. wrote the manuscript.

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Correspondence to Xin-Jian He.

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Extended data

Extended Data Fig. 1 Identification of the CACG components by AP-MS.

The heatmap indicates the identified components in CACG. The color gradient represents the NSAF values.

Extended Data Fig. 2 Determination of the interactions among CACG components by Y2H assays.

Yeast strains expressing the indicated GAL4-AD and GAL4-BD fusion proteins were cultivated on SD medium lacking Trp and Leu (SD-W-L) and on SD medium lacking Trp, Leu, and His (SD-W-L-H) supplemented with 3 mM 3-AT. Yeast strains containing empty GAL4-AD or GAL4-BD vectors (VEC) serve as negative controls. Positive strains indicating protein-protein interactions are highlighted with dashed boxes. The experiments were repeated independently twice and showed similar results.

Extended Data Fig. 3 Morphological phenotypes of single and multiple CACG mutants.

a - c, Morphological phenotypes of 20-day-old plants (a), 24-day-old plants (b), and 30-day-old plants (c). Scale bar, 1 cm. d, Statistical analysis of the days to bolting (n = 24, left) and the number of rosette leaves (n = 24, right). Values are mean ± SD. P values were determined by two-tailed Student’s t-test.

Extended Data Fig. 4 Analysis of lethal CACG mutants.

a, Phenotypes of mature siliques in the indicated mutants. b, The ratio of aborted seeds (n = 10). Values are mean ± SD. c, Genotypes of the progeny of self-bred gte1−/−gte6−/−trb4+/−trb5−/−, dp1−/−drmy1+/−, and emb1967+/−. P values were determined by chi-square test.

Extended Data Fig. 5 Growth defects observed in the CACG mutants.

a, Morphological phenotypes of 40-day-old plants. Scale bar, 1 cm. b, Statistical analyses of plant height of 40-day-old plants (n = 20, left), fresh weight of 20-day-old plants (n = 20, middle), and primary root length of 12-day-old plants (n = 20, right). Values are mean ± SD. P values were determined by two-tailed Student’s t-test. c, Phenotypic observation of siliques from 40-day-old plants (left) and rosette leaves from 28-day-old plants (right) in CACG mutants. Scale bar, 1 cm. d, Statistical analysis of the silique length in 40-day-old plants. Values are mean ± SD. P values were determined by two-tailed Student’s t-test. e, Statistical analysis of CACG mutant growth rates. Seedlings were initially cultivated in solid MS for 12 days before transferring to soil. The daily count of rosette leaves was recorded after transplanting (n = 20). Values are mean ± SD.

Extended Data Fig. 6 Morphological phenotypes of gtb1 gtb2 gtb3, trb4 trb5-c, and their complementation lines.

a, The morphological defects in gtb1 gtb2 gtb3 and trb4 trb5-c were complemented by the GTB1-Flag and TRB5-Myc transgenes, respectively. Scale bar, 1 cm. b, Immunoblot analysis shows the protein levels of GTB1-Flag and TRB5-Myc in the transgenic lines. The actin protein level is shown as a loading control. The experiments were independently repeated twice and showed similar results.

Source data

Extended Data Fig. 7 Effect of different nutrient components on CACG protein levels.

a, The protein levels of CACG in response to treatment with different nutrient components. Twelve-day-old plants grown on solid MS medium were transferred into liquid MS medium lacking macroelements, microelements, and/or vitamins. The protein levels of indicated CACG components were detected by immunoblot analysis after the plants were incubated for 4 days. Ma, macroelements; Mi, microelements; V, vitamins. The actin protein level is shown as a loading control. TOR activity was monitored by the phosphorylation state of S6K. The experiments were independently repeated twice and showed similar results. b, Statistical analysis of pS6K protein levels. Actin was used as a loading control. Each black dot represents an independent biological replicate.

Source data

Extended Data Fig. 8 The protein levels of CACG components were not influenced by inhibitors of proteasome or autophagy.

a, Immunoblot analysis shows the effect of the proteasome inhibitor MG132 on the protein levels of CACG components. Twelve-day-old plants grown in solid MS medium were transferred to H2O, liquid MS, or H2O containing 50 µM MG132 for 4 days. The actin protein level is shown as a loading control. b, Immunoblot analysis shows the effect of the autophagy inhibitor 3-MA on the protein levels of CACG components. Twelve-day-old plants grown in solid MS medium were incubated in H2O, liquid MS, or H2O containing 5 mM 3-MA for 4 days. The actin protein level is shown as a loading control. The experiments in (a) and (b) were independently repeated twice and showed similar results.

Source data

Extended Data Fig. 9 Pyrimidine-rich motifs in the 5’ UTRs of GTE1 and DP1 mRNAs facilitate target selection by TOR.

a, The expression of LUC driven by wild-type GTE1 and DP1 promoters along with wild-type or modified 5’ UTRs (5’ UTR-GTE1-R and 5’ UTR-DP1-R) were determined by luminescence imaging in tobacco leaves. Agrobacterium strains carrying the indicated plasmids were injected into tobacco leaves, either with (right) or without 6 µM AZD8055 (left). b, c, Statistical analysis of the expression levels of LUC driven by the wild-type GTE1 and DP1 promoters, along with their wild-type or modified 5’-UTRs. Protein (b) and transcript (c) levels were determined by luminescence imaging and quantitative RT-PCR, respectively. Each black dot represents an independent biological replicate. Values are mean ± SD from three independent biological replicates. P values were determined by two-tailed Student’s t-test.

Extended Data Fig. 10 The bromodomain-containing protein GTE1 exhibits a higher affinity for acetylated histone peptides than non-acetylated peptides.

a, The interaction of GTE1 and its bromodomain mutant with the indicated histone peptides was determined by pull-down assays. The experiments were independently repeated three times and showed similar results. b, Statistical analyses of the affinity of GTE1 with the indicated histone peptides. Values are means ± SD of three independent biological replicates. P values were determined by two-tailed Student’s t-test.

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Supplementary Figs. 1–7.

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Supplementary Data 1 (download XLSX )

Full list of co-purified proteins as determined by AP–MS.

Supplementary Data 2 (download XLSX )

DEGs in gte1 gte6, gta1 gta2 gta3, gtb1 gtb2 gtb3, drmy1 and wdr5a-r mutants relative to the wild type.

Supplementary Data 3 (download XLSX )

DEGs in Col-H2O, Col-AZD, drmy1-MS and gtb1 gtb2 gtb3-MS relative to Col-MS.

Supplementary Data 4 (download XLSX )

DEGs in Col-H2O, Col-AZD, drmy1-MS and gtb1 gtb2 gtb3-MS relative to Col-MS.

Supplementary Data 5 (download XLSX )

Primers used in this study.

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Wang, X., Liu, ZZ., Yuan, DY. et al. Nutrient-driven TOR signalling controls a chromatin-associated complex for orchestrating plant growth and stress tolerance. Nat. Plants 11, 2115–2129 (2025). https://doi.org/10.1038/s41477-025-02107-5

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