Periodic Reporting for period 1 - TIME_FOR_SHADE (Circadian Clock Gating of the Shade Avoidance Response Optimises Plant Fitness)
Reporting period: 2021-09-01 to 2023-08-31
Light limitation due to long-term shading by neighbouring plants is a major threat to food security, as it decreases overall yield. At high vegetation densities, shade-intolerant plants switch to a survival growth strategy known as the shade avoidance syndrome (SAS), which reconfigures overall architecture for optimal light capture. Of the diverse light-sensing photoreceptors that plants possess, phytochrome photoreceptors are exquisitely tuned to detect spectral changes indicative of nearby vegetation. These changes in light quality activate the phytochrome surveillance system, which in turn initiates compensatory changes in plant architecture and reproductive timing to suit more crowded conditions. Plants exhibiting SAS are characterised by elongation of growth of stem-like tissue, at the expense of harvestable organs (leaves, fruits, seeds, etc.). In nature, the SAS response is critical for plant survival, but it is troublesome for farmers, as it impacts crop robustness and yield. Interestingly, we have shown that the SAS response is tissue and developmental time-specific. For example, if shading occurs early in leaf development it leads to reduced cell numbers in leaf blades, and increased cell numbers in the leaf petioles. Whereas if this happens later in a leaf's life, it reduces the cell size in leaf blades and increases it in leaf petioles. Overall, the plant uses two alternative strategies to obtain the same result: small leaf blades and elongated petioles.
Several lines of research indicate that the shade signal is only perceived by plants at dusk, through a mechanism known as ‘gating’. Gating is controlled by the plant’s internal clock – namely the circadian clock. This endogenous timing mechanism allows a plant to fine-tune its physiology to a cyclical environment. Furthermore, proper internal timing that matches the environment is beneficial for plants and leads to optimised fitness and survival. However, almost nothing is known about how gating affects SAS plant fitness. Our data indicate that disruption of different elements that make up the clock results in plants that have an architecture very similar to SAS-affected plants. Furthermore, as the clock has been tied to the cell cycle, this suggests a possible mechanism through which the clock could be directly controlling the SAS leaf cellular response. Additionally, using a powerful bioinformatics approach we discovered an unexpected and potentially new avenue through which the clock and the phytochrome photoreceptors could be coordinately regulating leaf size, ultimately impacting biomass (a key predictor of crop yield).
TIME_FOR_SHADE is an innovative project, using genetic, bioinformatics, and dynamic imaging techniques to study how circadian clock gating affects plant fitness under light-limiting conditions and explore the mechanism that links the clock to the SAS leaf cellular response. Moreover, during the course of this action, we have established pennycress as a direct translational model. Identification of novel genetic targets to optimise plant yield under light-limiting conditions will be translated into pennycress, a newly domesticated oilseed crop. This will likely lead to increased crop yield and will inform other crop improvement efforts.
Initially, we assessed whether a plant's circadian clock offers a competitive advantage in shaded conditions. Experiments, including leaf size assessment, cellular analysis, biomass measurements, and bioinformatics, identified specific clock components influencing leaf traits and overall plant fitness under simulated shade. These findings deepen our understanding of how the clock affects a plant's response to shade and unveil promising genetic targets.
Subsequently, we investigated the direct regulation of the leaf cell cycle by phytochrome B (phyB) and TOC1. Our research expanded beyond TOC1, leading to the establishment of a Förster resonance energy transfer (FRET) library to examine interactions among key light signaling components, the central regulator of leaf cell proliferation (AN3), and various clock components under diverse environmental conditions.
Our inquiry also explored ribosome biogenesis's potential role in shaded leaf development, though further research is necessary for a comprehensive understanding.
Lastly, we leveraged knowledge from Arabidopsis to advance pennycress as a model crop. We made significant progress in cultivating pennycress under conditions mirroring Arabidopsis. Collaborations were formed, research grants secured, and infrastructure established for future translational work.
In summary, our research unraveled the interplay between a plant's circadian clock and light conditions, shaping architecture and biomass, particularly under shade. We identified specific clock components as key players in this process, setting the stage for practical applications to improve crop fitness and productivity, starting with pennycress and potentially extending to other crops.
This project has been instrumental in Dr. Andres Romanowski's career, enabling him to establish his own research path and secure an independent PI position at Wageningen University. It has also fostered collaborations that will help accelerate future research in his lab. The results obtained in this project serve as the foundation for future grant applications, ensuring that the discoveries made here will continue to benefit the field of plant science.
With regards to the wider societal implications, TIME_FOR_SHADE has the potential to boost plant productivity, which is crucial for crops grown in conditions where sunlight is limited, such as densely planted fields. By gaining a deeper understanding of how light and the plant's internal clock interact, we can uncover new factors that could be applied in biotechnology or breeding efforts to enhance the performance of various crops, including a promising cover crop called pennycress and related plant species. In essence, this research has far-reaching implications for improving agriculture and ensuring a more sustainable food supply.