Mikhail Schepetilnikov

Plants perceive neighboring vegetation through an enrichment of far-red light (shade) in the environment. These changes in light quality trigger molecular and physiological responses aimed at outgrowing competitors, collectively known as the shade avoidance syndrome. In this study, we identify the TARGET OF RAPAMYCIN (TOR) complex 1 (TORC1), a major growth-regulating hub in eukaryotes, as a driver of shade-mediated growth responses in plants. Combining physiology, genetics, biochemistry, and proteomics, we show that TOR activity is rapidly enhanced upon shade perception and is required for proper shade responses, as TOR inhibition severely impairs shade-mediated elongation. Furthermore, we found that the control of shade-mediated elongation by TOR involves auxin-dependent mechanisms, requires efficient translation activity, and is closely linked to epidermal cell elongation capacity. Altogether, our work identifies TOR as a key integrator of light quality signals to control adaptive growth responses. Finally, we further highlight the conservation of shade-mediated TOR activation in tomato, with potential implications for engineering crop cultivars better suited to high-density planting.

Light is a central environmental signal that coordinates plant development, metabolism, and stress responses. By integrating external cues with internal programs, plants balance growth and resource allocation to adapt to fluctuating environments. Light-regulated signalling cascades drive morpho-physiological adaptations for optimized light capture, tuning photosynthetic efficiency, and source-sink dynamics. Key transcriptional hubs, regulated by master transcription factors such as ELONGATED HYPOCOTYL 5 (HY5), PHYTOCHROME INTERACTING FACTORS (PIFs), and GOLDEN 2-LIKE transcription factors (GLKs) coordinate photosynthesis, growth, and defence responses, driving adjustments and imposing balances for adaptation to shade, variable light, and stress. In addition to photosynthetic energy production, light signalling pathways influence carbon and nitrogen metabolism, leading to sugar allocation, starch turnover, and nutrient utilization—balancing trade-offs between growth, energy storage, and stress responses. Emerging evidence shows that light signalling pathways intersect with energy-monitoring cascades regulated by TARGET OF RAPAMYCIN (TOR), trehalose-6-phosphate (T6P), and SUCROSE NON-FERMENTING-RELATED PROTEIN KINASE 1 (SnRK1), linking the plant’s energy status to growth, immunity, and stress resilience. Sugar concentration and light signals can also jointly regulate responses to both biotic and abiotic stress, with TOR acting as a central integration hub for environmental and metabolic signals, including transcriptional and translational mechanisms. This review synthesizes our current understanding on the interplay between light and TOR-mediated networks in energy production and allocation, while highlighting knowledge gaps that limit translational potential for improving plant productivity and resilience.

Plant organogenesis requires matching the available metabolic resources to developmental programs. In Arabidopsis, the root system is determined by primary root‐derived lateral roots (LRs), and adventitious roots (ARs) formed from non‐root organs. Lateral root formation entails the auxin‐dependent activation of transcription factors ARF7, ARF19, and LBD16. Adventitious root formation relies on LBD16 activation by auxin and WOX11. The allocation of shoot‐derived sugar to the roots influences branching, but how its availability is sensed for LRs formation remains unknown. We combine metabolic profiling with cell‐specific interference to show that LRs switch to glycolysis and consume carbohydrates. The target‐of‐rapamycin (TOR) kinase is activated in the lateral root domain. Interfering with TOR kinase blocks LR initiation while promoting AR formation. The target‐of‐rapamycin inhibition marginally affects the auxin‐induced transcriptional response of the pericycle but attenuates the translation of ARF19, ARF7, and LBD16. TOR inhibition induces WOX11 transcription in these cells, yet no root branching occurs as TOR controls LBD16 translation. TOR is a central gatekeeper for root branching that integrates local auxin‐dependent pathways with systemic metabolic signals, modulating the translation of auxin‐induced genes.

Summary: Root hairs (RH) are excellent model systems for studying cell size and polarity since they elongate several hundred‐fold their original size. Their tip growth is determined both by intrinsic and environmental signals. Although nutrient availability and temperature are key factors for a sustained plant growth, the molecular mechanisms underlying their sensing and downstream signaling pathways remain unclear. We use genetics to address the roles of the cell surface receptor kinase FERONIA (FER) and the nutrient sensing TOR Complex 1 (TORC) in RH growth. We identified that low temperature (10°C) triggers a strong RH elongation response in Arabidopsis thaliana involving FER and TORC. We found that FER is required to perceive limited nutrient availability caused by low temperature. FERONIA interacts with and activates TORC‐downstream components to trigger RH growth. In addition, the small GTPase Rho of plants 2 (ROP2) is also involved in this RH growth response linking FER and TOR. We also found that limited nitrogen nutrient availability can mimic the RH growth response at 10°C in a NRT1.1‐dependent manner. These results uncover a molecular mechanism by which a central hub composed by FER‐ROP2‐TORC is involved in the control of RH elongation under low temperature and nitrogen deficiency.

Plants post-embryonic organogenesis requires matching the available metabolic resources to the developmental programs. The root system is determined by the formation of lateral roots (LR), which in Arabidopsis thaliana entails the auxin-induced activation of founder cells located in the pericycle. While the allocation of sugars to roots influences root branching, how sugar availability is sensed for auxin-triggered formation of LRs remains unknown. Here, we combine metabolic profiling with cell-specific genetic interference to show that LR formation is an important sink for carbohydrate accompanied by a switch to glycolysis. We show that the target-of-rapamycin (TOR) kinase is locally activated in the pericycle and the founder cells and that both chemical and genetic inhibition of TOR kinase lead to a block of LR initiation. TOR marginally affects the auxin-induced transcriptional response of the pericycle but modulates the translation of ARF19, ARF7 and LBD16, three key targets of auxin signalling. These data place TOR as a gatekeeper for post-embryonic LR formation that integrates local auxin-dependent pathways with systemic metabolic signals, modulating the translation of auxin induced gene expression.

Root hairs (RH) are excellent model systems for studying cell size and polarity since they elongate several hundred-fold their original size. Their tip growth is determined both by intrinsic and environmental signals. Although nutrient availability and temperature are key factors for a sustained plant growth, the molecular mechanisms underlying their sensing and downstream signaling pathways remain unclear. Here, we identified that low temperature (10°C) triggers a strong RH elongation response involving the cell surface receptor kinase FERONIA (FER) and the nutrient sensing TOR Complex 1 (TORC). In this study, we found that FER is required to perceive limited nutrient availability caused by low temperature. FER interacts with and activates TORC downstream components to trigger RH growth. In addition, the small GTPase Rho-related protein from plants 2 (ROP2) is also involved in this RH growth response linking FER and TOR. We also found that limited nitrogen nutrient availability can mimic the RH growth response at 10°C in a NRT1.1-dependent manner. These results uncover a molecular mechanism by which a central hub composed by FER-ROP2-TORC is involved in the control of RH elongation under low temperature and nitrogen deficiency.

Reinitiation supporting protein, RISP, interacts with 60S (60S ribosomal subunit) and eIF3 (eukaryotic initiation factor 3) in plants. TOR (target-of-rapamycin) mediates RISP phosphorylation at residue Ser267, favoring its binding to eL24 (60S ribosomal protein L24). In a viral context, RISP, when phosphorylated, binds the CaMV transactivator/ viroplasmin, TAV, to assist in an exceptional mechanism of reinitiation after long ORF translation. Moreover, we show here that RISP interacts with eIF2 via eIF2β and TOR downstream target 40S ribosomal protein eS6. A RISP phosphorylation knockout, RISP-S267A, binds preferentially eIF2β, and both form a ternary complex with eIF3a in vitro. Accordingly, transient overexpression in plant protoplasts of RISP-S267A, but not a RISP phosphorylation mimic, RISP-S267D, favors translation initiation. In contrast, RISP-S267D preferentially binds eS6, and, when bound to the C-terminus of eS6, can capture 60S in a highly specific manner in vitro, suggesting that it mediates 60S loading during reinitiation. Indeed, eS6-deficient plants are highly resistant to CaMV due to their reduced reinitiation capacity. Strikingly, an eS6 phosphomimic, when stably expressed in eS6-deficient plants, can fully restore the reinitiation deficiency of these plants in cellular and viral contexts. These results suggest that RISP function in translation (re)initiation is regulated by phosphorylation at Ser267.

RNA silencing is a conserved mechanism in eukaryotes and is involved in development, heterochromatin maintenance and defense against viruses. In plants, ARGONAUTE1 (AGO1) protein plays a central role in both microRNA (miRNA) and small interfering RNA (siRNA)-directed silencing and its expression is regulated at multiple levels. Here, we report that the F-box protein FBW2 targets proteolysis of AGO1 by a CDC48-mediated mechanism. We found that FBW2 assembles an SCF complex that recognizes the MID-PIWI domain of AGO1 and requires its C-terminal domain containing a GW motif for AGO1 turnover. We showed that FBW2 prefers the unloaded and some mutated forms of AGO1 protein. While FBW2 loss of function does not lead to strong growth or developmental defects, it significantly increases RNA silencing activity. Interestingly, under conditions in which small RNA production or accumulation is affected, the failure to degrade AGO1 in fbw2 mutants becomes more deleterious for the plant. Hence, the non-degradable AGO1 protein assembles high molecular weight complexes and binds illegitimate small RNA leading to the cleavage of new target genes that belong to stress responses and cellular metabolic processes. Therefore, the control of AGO1 homeostasis by ubiquitin ligases plays an important role in quality control to avoid off-target cleavage.

TOR signaling regulates plant translation via a specific translation initiation mechanism: reinitiation.