Abstract
To over-top the neighbors, shade-intolerant plants trigger shade avoidance responses with increasing the elongation of stem-like organs at the expense of leaf development. Shade-induced elongation growth has been extensively studied, while the regulatory mechanisms underlying shade-suppressed leaf development remain poorly understood. Here we find sucrose can rescue shade-inhibited leaf development, which requires the functions of phytochrome A (phyA) and TARGET OF RAPAMYCIN (TOR) complex. We confirm an interaction between PHYA and LETHAL WITH SEC THIRTEEN 8 (LST8), a component of TOR complex. Shade and phyA affect TOR activity, in turn TOR affects the protein stability of PHYA. The sucrose–TOR mediated accumulation of PHYA requires CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1)/SUPPRESSOR OF PHYA-105 (SPA) complex. Transcriptome analysis further reveals that sucrose and phyA regulate the expression of leaf development-related genes under shade, particularly those involved in cytokinin metabolism. Our work uncovers a critical role for TOR and PHYA in linking light signaling with cellular energy status, a mechanism that fine-tunes leaf development specifically under shade conditions.
Similar content being viewed by others
Data availability
The raw and processed RNA-seq data generated in this study were deposited in the NCBI GEO database under accession code GSE291348. Previously published RNA-seq datasets used in this study are available in the NCBI GEO database under accession numbers GSE17845 and GSE104146. Phosphoproteomic data were deposited in the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PRIDE: PXD075951. Source data are provided with this paper (https://doi.org/10.6084/m9.figshare.30879302).
References
Casal, J. J. Shade avoidance. Arabidopsis Book 10, e0157 (2012).
Park, E. et al. Phytochrome B inhibits binding of phytochrome-interacting factors to their target promoters. Plant J. 72, 537–546 (2012).
Park, E., Kim, Y. & Choi, G. Phytochrome B requires PIF degradation and sequestration to induce light responses across a wide range of light conditions. Plant Cell 30, 1277–1292 (2018).
Pham, V. N., Kathare, P. K. & Huq, E. Phytochromes and phytochrome interacting factors. Plant Physiol. 176, 1025–1038 (2018).
Li, L. et al. Linking photoreceptor excitation to changes in plant architecture. Genes Dev. 26, 785–790 (2012).
Yang, C. et al. Phytochrome A negatively regulates the shade avoidance response by increasing Auxin/Indole acidic acid protein stability. Dev. Cell 44, 29–41 e24 (2018).
Song, B. et al. Phytochrome A inhibits shade avoidance responses under strong shade through repressing the brassinosteroid pathway in Arabidopsis. Plant J. 104, 1520–1534 (2020).
Fraser, D. P. et al. Phytochrome A elevates plant circadian-clock components to suppress shade avoidance in deep-canopy shade. Proc. Natl. Acad. Sci. USA. 118, e2108176118 (2021).
Hao, Y., Oh, E., Choi, G., Liang, Z. & Wang, Z. Y. Interactions between HLH and bHLH factors modulate light-regulated plant development. Mol. Plant 5, 688–697 (2012).
Hornitschek, P., Lorrain, S., Zoete, V., Michielin, O. & Fankhauser, C. Inhibition of the shade avoidance response by formation of non-DNA-binding bHLH heterodimers. Embo J. 28, 3893–3902 (2009).
Buti, S. et al. A gas-and-brake mechanism of bHLH proteins modulates shade avoidance. Plant Physiol. 184, 2137–2153 (2020).
Hong, S. Y. et al. A competitive peptide inhibitor KIDARI negatively regulates HFR1 by forming nonfunctional heterodimers in Arabidopsis photomorphogenesis. Mol. Cells 35, 25–31 (2013).
Ortiz-Alcaide, M. et al. Chloroplasts modulate elongation responses to canopy shade by retrograde pathways involving HY5 and abscisic acid. Plant Cell 31, 384–398 (2019).
Pacín, M., Legris, M. & Casal, J. J. COP1 re-accumulates in the nucleus under shade. Plant J. 75, 631–641 (2013).
Liu, Y., Jafari, F. & Wang, H. Integration of light and hormone signaling pathways in the regulation of plant shade avoidance syndrome. aBIOTECH 2, 131–145 (2021).
de Wit, M. et al. Changes in resource partitioning between and within organs support growth adjustment to neighbor proximity in Brassicaceae seedlings. Proc. Natl. Acad. Sci. USA. 115, E9953–E9961 (2018).
Carabelli, M. et al. Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes Dev. 21, 1863–1868 (2007).
Hussain, E., Romanowski, A. & Halliday, K. J. PIF7 controls leaf cell proliferation through an AN3 substitution repression mechanism. Proc. Natl. Acad. Sci. USA. 119, e2115682119 (2022).
Liu, Y. et al. Target of Rapamycin (TOR): a master regulator in plant growth, development, and stress responses. Annu. Rev. Plant. Biol. 21, 190–205 (2025).
Wu, Y. et al. Integration of nutrient, energy, light, and hormone signalling via TOR in plants. J. Exp. Bot. 70, 2227–2238 (2019).
Chen, G. H., Liu, M. J., Xiong, Y., Sheen, J. & Wu, S. H. TOR and RPS6 transmit light signals to enhance protein translation in deetiolating Arabidopsis seedlings. Proc. Natl. Acad. Sci. USA 115, 12823–12828 (2018).
Li, X. et al. Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes. Proc. Natl. Acad. Sci. USA. 114, 2765–2770 (2017).
Xiong, Y. et al. Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496, 181–186 (2013).
Zhang, Z. et al. TOR signaling promotes the accumulation of BZR1 to balance growth with carbon availability in Arabidopsis. Curr. Biol. 26, 1854–1860 (2016).
Liu, Z. et al. Phytochrome interacting factors (PIFs) are essential regulators for sucrose-induced hypocotyl elongation in Arabidopsis. J. Plant Physiol. 168, 1771–1779 (2011).
Simon, N. M. L. et al. The energy-signaling hub SnRK1 is important for sucrose-induced hypocotyl elongation. Plant Physiol. 176, 1299–1310 (2018).
Mahfouz, M. M., Kim, S., Delauney, A. J. & Verma, D. P. Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18, 477–490 (2006).
Moreau, M. et al. Mutations in the Arabidopsis homolog of LST8/GβL, a partner of the target of Rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell 24, 463–481 (2012).
Van Leene, J. et al. Capturing the phosphorylation and protein interaction landscape of the plant TOR kinase. Nat. Plants 5, 316–327 (2019).
Fu, L. et al. The TOR-EIN2 axis mediates nuclear signalling to modulate plant growth. Nature 591, 288–292 (2021).
Qi, H., Xia, F. N. & Xiao, S. Autophagy in plants: physiological roles and post-translational regulation. J. Integr. Plant Biol. 63, 161–179 (2021).
Thompson, A. R., Doelling, J. H., Suttangkakul, A. & Vierstra, R. D. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 138, 2097–2110 (2005).
Ohama, N. et al. MEDIATOR15 destabilizes DELLA protein to promote gibberellin-mediated plant development. N. Phytol. 245, 2665–2680 (2025).
Franklin, K. A. & Quail, P. H. Phytochrome functions in Arabidopsis development. J. Exp. Bot. 61, 11–24 (2010).
Legris, M., Ince, Y. C. & Fankhauser, C. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat. Commun. 10, 5219 (2019).
Seo, H. S., Watanabe, E., Tokutomi, S., Nagatani, A. & Chua, N. H. Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev. 18, 617–622 (2004).
Saijo, Y. et al. Arabidopsis COP1/SPA1 complex and FHY1/FHY3 associate with distinct phosphorylated forms of phytochrome A in balancing light signaling. Mol. Cell 31, 607–613 (2008).
Kozuka, T. et al. Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol. 153, 1608–1618 (2010).
Hung, W. F., Chen, L. J., Boldt, R., Sun, C. W. & Li, H. M. Characterization of Arabidopsis glutamine phosphoribosyl pyrophosphate amidotransferase-deficient mutants. Plant Physiol. 135, 1314–1323 (2004).
Fujikura, U., Horiguchi, G., Ponce, M. R., Micol, J. L. & Tsukaya, H. Coordination of cell proliferation and cell expansion mediated by ribosome-related processes in the leaves of Arabidopsis thaliana. Plant J. 59, 499–508 (2009).
Wang, Y. et al. Crucial role of SWL1 in chloroplast biogenesis and development in Arabidopsis thaliana. Plant Cell Rep. 43, 135 (2024).
Ito, T., Kim, G. T. & Shinozaki, K. Disruption of an Arabidopsis cytoplasmic ribosomal protein S13-homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J. 22, 257–264 (2000).
Romanowski, A., Furniss, J. J., Hussain, E. & Halliday, K. J. Phytochrome regulates cellular response plasticity and the basic molecular machinery of leaf development. Plant Physiol. 186, 1220–1239 (2021).
Martinez-Garcia, J. F. et al. The shade avoidance syndrome in Arabidopsis: the antagonistic role of phytochrome A and B differentiates vegetation proximity and canopy shade. PLoS ONE 9, e109275 (2014).
Short, T. W. Overexpression of Arabidopsis phytochrome B inhibits phytochrome A function in the presence of sucrose. Plant Physiol. 119, 1497–1506 (1999).
Klepikova, A. V., Kasianov, A. S., Gerasimov, E. S., Logacheva, M. D. & Penin, A. A. A high-resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. Plant J. 88, 1058–1070 (2016).
Ye, R. et al. Glucose-driven TOR-FIE-PRC2 signalling controls plant development. Nature 609, 986–993 (2022).
Feng, Z. et al. Liquid-liquid phase separation of TZP promotes PPK-mediated phosphorylation of the phytochrome A photoreceptor. Nat. Plants 10, 798–814 (2024).
Zhou, Y. et al. Hinge region of Arabidopsis phyA plays an important role in regulating phyA function. Proc. Natl. Acad. Sci. USA 115, E11864–E11873 (2018).
Li, K. L., Xue, H., Tang, R. J. & Luan, S. TORC pathway intersects with a calcium sensor kinase network to regulate potassium sensing in Arabidopsis. Proc. Natl. Acad. Sci. USA 120, e2316011120 (2023).
Lin, F. et al. Phosphorylation and negative regulation of CONSTITUTIVELY PHOTOMORPHOGENIC 1 by PINOID in Arabidopsis. Proc. Natl. Acad. Sci. USA 114, 6617–6622 (2017).
Lindback, L. N., Hu, Y., Ackermann, A., Artz, O. & Pedmale, U. V. UBP12 and UBP13 deubiquitinases destabilize the CRY2 blue light receptor to regulate Arabidopsis growth. Curr. Biol. 32, 3221–3231 e3226 (2022).
Fonseca, B. D. et al. The ever-evolving role of mTOR in translation. Semin Cell Dev. Biol. 36, 102–112 (2014).
Patel, D. et al. Temperature-dependent shade avoidance involves the receptor-like kinase ERECTA. Plant J. 73, 980–992 (2013).
Han, X. et al. Phytochrome A and B regulate primary metabolism in Arabidopsis leaves in response to light. Front Plant Sci. 8, 1394 (2017).
Yang, D., Seaton, D. D., Krahmer, J. & Halliday, K. J. Photoreceptor effects on plant biomass, resource allocation, and metabolic state. Proc. Natl. Acad. Sci. USA 113, 7667–7672 (2016).
Chen, F. et al. Arabidopsis phytochrome A directly targets numerous promoters for individualized modulation of genes in a wide range of pathways. Plant cell 26, 1949–1966 (2014).
Park, J. et al. CYTOKININ-RESPONSIVE GROWTH REGULATOR regulates cell expansion and cytokinin-mediated cell cycle progression. Plant Physiol. 186, 1734–1746 (2021).
Riou-Khamlichi, C., Huntley, R., Jacqmard, A. & Murray, J. A. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283, 1541–1544 (1999).
Reed, J. W., Nagatani, A., Elich, T. D., Fagan, M. & Chory, J. Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiol. 104, 1139–1149 (1994).
Jamsheer, K. M. et al. A negative feedback loop of TOR signaling balances growth and stress-response trade-offs in plants. Cell Rep. 39, 110631 (2022).
Li, F., Wang, J., Wang, P. & Li, L. Dephosphorylation of bZIP59 by PP2A ensures appropriate shade avoidance response in Arabidopsis. Dev. Cell 60, 551–566.e6 (2024).
Zhang, Y. et al. Structural insights into plant phytochrome A as a highly sensitized photoreceptor. Cell Res. 33, 806–809 (2023).
Acknowledgments
The work was supported by the National Natural Science Foundation of China (32030018) to L.L. We thank Prof. Yan Xiong (Fujian Agriculture and Forestry University, Fujian, China) for sharing plant materials tor-es, pCYCB1;1::GUS and the valuable anti-TOR antibody. We also thank Prof. Jizong Wang (Peking University, Beijing, China) for sharing the purified AtphyA protein.
Author information
Authors and Affiliations
Contributions
J.W., F.L., and L.L. designed the experiments. J.W., F.L., and C.L. performed the experiments. L.L wrote the paper.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Communications thanks the anonymous reviewer(s) for their contribution to the peer review of this work. A peer review file is available.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
About this article
Cite this article
Wang, J., Li, F., Lu, C. et al. Sucrose-activated TOR and phyA signaling alleviates shade-mediated inhibition of leaf development in Arabidopsis. Nat Commun (2026). https://doi.org/10.1038/s41467-026-71841-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s41467-026-71841-x


