Periodic Reporting for period 4 - INSPIRE (System-wide discovery and analysis of inositol pyrophosphate signaling networks in plants)
Reporting period: 2023-12-01 to 2025-05-31
The growth and development of plants is strongly influenced by environmental conditions, such as the availability of nutrients. The INPIRE project studies how small molecule nutrient messengers called inositol pyrophosphates communicate with developmental and immune signaling pathways, enabling the plant to shape its growth and development in response to changes in nutrient availability. Since many nutrients are poorly available in soils understanding plant nutrient sensing and signaling may be of biotechnological relevance. Specifically, the project aims at understanding at the mechanistic and physiological level how inositol pyrophosphates are broken down in plants, how they regulate different light signaling and developmental pathways and how they modulate the function of the plant immune system.
Over the course of our project, we discovered that the amount of a small signaling molecule called inositol pyrophosphate inside plant cells directly reflects how well the plant is nourished. In simple terms, plants that have plenty of phosphorus and nitrogen show higher levels of this messenger, while nutrient-starved plants have much less. We also found that plants very carefully control both the production and breakdown of this messenger. In particular, three different groups of enzymes (phosphatases) are responsible for breaking it down, working together to keep its levels balanced in plants like Arabidopsis and Marchantia polymorpha (Laurent et al., https://doi.org/10.1371/journal.pgen.1011468(opens in new window)).
Beyond being just a signal of nutrient status, this messenger actively helps the plant manage its resources. It does so by binding to a receptor protein inside the cell. That receptor then interacts with a transcription factor, a kind of “molecular switch” that turns genes on or off. Some of these genes build transport proteins that allow roots to take up more phosphate from the soil. When the transcription factor is bound in this complex, it stays silent. But under nutrient starvation, the messenger gets broken down, the complex falls apart, and the transcription factor becomes active. This switch-on event launches the plant’s phosphate starvation response, a survival program that boosts phosphate uptake and helps the plant continue to grow (Ried et al., https://doi.org/10.1038/s41467-020-20681-4(opens in new window))
The receptor protein is not the only one that interacts with this nutrient messenger. We also identified other partners, including two families of kinase, enzymes that can “tag” other proteins with phosphate groups to control whether they are active or inactive. The nutrient messenger regulates these kinases as well, allowing plants to make important developmental decisions, such as when to begin flowering, in response to changing nutrient conditions.
Beyond being just a signal of nutrient status, this messenger actively helps the plant manage its resources. It does so by binding to a receptor protein inside the cell. That receptor then interacts with a transcription factor, a kind of “molecular switch” that turns genes on or off. Some of these genes build transport proteins that allow roots to take up more phosphate from the soil. When the transcription factor is bound in this complex, it stays silent. But under nutrient starvation, the messenger gets broken down, the complex falls apart, and the transcription factor becomes active. This switch-on event launches the plant’s phosphate starvation response, a survival program that boosts phosphate uptake and helps the plant continue to grow (Ried et al., https://doi.org/10.1038/s41467-020-20681-4(opens in new window))
The receptor protein is not the only one that interacts with this nutrient messenger. We also identified other partners, including two families of kinase, enzymes that can “tag” other proteins with phosphate groups to control whether they are active or inactive. The nutrient messenger regulates these kinases as well, allowing plants to make important developmental decisions, such as when to begin flowering, in response to changing nutrient conditions.
At the start of the project, we assumed that this nutrient messenger would connect with only a few specific “receptor” proteins in the cell, each triggering a narrow set of responses to changes in nutrient availability. But as the project unfolded, we discovered that plants actually have many different receptors for inositol pyrophosphates. Rather than controlling just a handful of processes, this messenger seems to sit at the center of a broad network of signaling proteins. Through this network, it influences how plants respond to nutrient shortages, how they grow and develop, and even how they interact with helpful partners (like symbiotic microbes) or defend themselves against insects and pathogens. Pinpointing the most important “hubs” in this network is an exciting challenge for future research.