The emerging role of TARGET OF RAPAMYCIN in the shade-induced susceptibility in plants.

Light is a key parameter for plant growth and survival. Plants absorb blue and red light (R) to fuel photosynthesis and reflect far-red light (FR) back to their surroundings. The reflection and subsequent accumulation of FR leads to a decrease in the ratio between R and FR (low R:FR) in the canopy. Low R:FR is sensed by a set of specialized photoreceptors called phytochromes and constitutes an early warning signal for close neighbouring vegetation (shade). Low R:FR perception by phytochromes triggers strong and rapid growth responses, known as the shade avoidance syndrome, mostly driven by the growth hormone auxin and allowing plants to grow taller than their neighbours. In addition to eliciting growth responses, low R:FR promote plant susceptibility to pathogen attacks. Indeed, shade strongly dampens defence hormone signalling; a process referred to as shade-induced susceptibility. Interestingly, this dampening of plant defence by low R:FR has long been attributed to a direct interplay between light and defence hormone signalling. However, other mechanisms, also affected by shade, have not yet been considered as potential components of the shade-induced susceptibility.

Recently, we found that plants experiencing low R:FR accumulate glucose, which is closely associated with faster lesion development by pathogens. Yet, the molecular mechanism behind how glucose accumulation leads to increased pathogen susceptibility remains elusive. In a recent RNA-sequencing study, we found that TARGET OF RAPAMYCIN (TOR) is upregulated in response to low R:FR. In eukaryotes, TOR is a master growth regulator activated by glucose and auxin, both strongly elevated in shaded plants, too. I am currently investigating if and how shade signals could promote growth at the expense of defence in a TOR-dependent manner. The gained insights will be instrumental for understanding how plants respond to shade to engineer pathogen-resilient crops, which can be grown at higher densities.

Research:

Plants have developed advanced strategies to react and adapt to environmental changes, including competition with other organisms, even within their own species. Neighbor proximity in plants is perceived via a reduction of the red to far-red ratio (R:FR) in the light environment. As a result of low R:FR perception by phytochromes photoreceptors, plants trigger a set of molecular and physiological responses referred to as the "shade avoidance syndrome"; a process meant to outgrow neighboring vegetation. In addition to exhibiting strong growth responses, plants experiencing low R:FR display lower resistance capacities towards pathogens. However, the exact molecular components, triggered by low R:FR, leading to the onset of shade avoidance and associated with the reduced defense capacities remain to be found.

Based on previous RNA-sequencing data, we identified TARGET OF RAPAMYCIN (TOR) as a potential regulator of the growth-defense tradeoff in plants. By coupling biochemistry, omics and physiology, we are currently investigating if and how low R:FR perception regulates TOR activity and signaling thereby promoting growth at the expense of defense in Arabidopsis. Given the conserved nature of the TOR pathway throughout green lineages, this work ultimately aims to unravel TOR-(in)dependent molecular pathways regulating the growth-defense tradeoff in plants, which could help develop more climate and pest resilient crops in the future.

Keywords:

Light, TARGET OF RAPAMYCIN, growth, defense, auxin, Arabidopsis.

Selected publications:

1. Farming Goes Dynamic: Potential improvements in resource use efficiency, product quality, and profitability Kaiser E., Kusuma P., Vialet-Chabrand S., Folta K., Liu Y., Poorter H., Woning N., Shrestha S., Ciarreta A., van Brenk J., Karpe M., Ji Y., David S., Zepeda C., Zhu X-G.,  Huntenburg K., Verdonk J. C., Woltering E., Gauthier P., Courbier S., Taylor G. and Marcelis L.F.M. (2024) Vertical (accepted in Frontiers in Science)
2. Paradise by the far-red light: Far-red and red:blue ratios independently affect yield, pigments, and carbohydrate production in lettuce, Lactuca sativa. Van Brenk J.B.*, Courbier S.*, Kleijweg C.L., Verdonk J.C., and Marcelis L.F.M. (2024) Frontiers in Plant Science doi: 10.3389/fpls.2024.1383100
3. Mechanisms of far-red light-mediated dampening of defense against Botrytis cinerea in tomato leaves. Courbier S., Snoek B. L., Kajala K., Li L., van Wees S. C. M. and Pierik R. (2021) Plant Physiology187: 1250–1266.
4. Far-red light enhances soluble sugar levels and Botrytis cinerea disease development in tomato leaves in a jasmonate-dependent manner.Courbier S., Grevink S., Sluijs E., Bonhomme P. O., Kajala K., Van Wees S. C. M. and Pierik R. (2020) Plant, Cell and Environment6: 1-13.
5. Canopy light quality modulates stress responses in plants.Courbier, S.and Pierik, R. (2019) iScience 22:441-452.
6. Far-red radiation increases dry mass partitioning to fruits but reduces Botrytis cinerea resistance in tomato. Ji, Y., Ouzounis, T., Courbier, S., Kaiser, E., Nguyen, P.T., Schouten H.J., Visser, R.G.F, Pierik, R., Marcelis, L.F.M., Heuvelink, E. (2019) Environmental and Experimental Botany 168: 103889.
7. Bringing together Europe’s young plant scientists. van der Horst S., van Butselaar T., Zhang H., Steenbergen M., Courbier S., Neilen, M., Küpers, J.J. (2019) New Phytologist 222: 29–32
8. Genomics analysis of Aphanomyces spp. identifies a new class of oomycete effector associated with host adaptation. Gaulin E., Pel M. J. C., Camborde L., San-Clémente H., Courbier S., Dupouy MA, Lengellé J, Veyssiere M, Le Ru A, Grandjean F, et al. (2018) BMC Biology16:43.

*shared first authorship