Periodic Reporting for period 1 - MECHANOJAS (Unravelling biophysical signals governing phytohormone production and plant acclimation)
Periodo di rendicontazione: 2023-07-01 al 2025-12-31
Tissue injury leads to the production of powerful lipid-based signaling molecules in both animals and plants. In flowering plants like Arabidopsis thaliana, plastidial membranes are the source of oxygenated lipids that eventually result in Jasmoni Acid (JA) biosynthesis. The JA phytohormone pathway is essential for plant defense against various stresses, including insect attacks, pathogenic infections, physical injury, and drought. In fact, insect herbivory alone is responsible for over 20% of global crop losses, and plants that cannot activate JA signaling are highly vulnerable to chewing insects. Although the JA pathway has been well-characterized at the molecular level, it remains unclear how are damage signals transmitted to plastids to initiate hormone production, and what is the nature of these signals. Our previous research revealed that changes in turgor pressure caused by osmotic stress can also trigger JA biosynthesis. This led us to propose a new hypothesis: mechanical signals may travel through plant tissues and cells, altering plastidilial membrane properties in a way that enables JA biosynthesis enzymes to access their substrates. To investigate this, we are quantifying the mechanical forces and osmotic pressures needed to induce JA production. We are also studying how these stress signals are transmitted to plastids, how changes in plastid membrane properties affect JA precursor synthesis, and which genetic components are involved in sensing and interpreting these biophysical cues. By uncovering the cellular, biophysical, and genetic mechanisms that initiate JA biosynthesis, we aim to deepen our understanding of how plants perceive and respond to environmental stress, ultimately contributing to strategies that enhance plant resilience.
Significant progress has been made in developing a biosensor to measure JA-Ile hormone levels in living plants. A large number of sensor designs were screened computationally, leading to several promising candidates now undergoing experimental validation. These sensors are based on a hormone-dependent interaction mechanism and are being tested using advanced imaging techniques. To ensure reliable hormone quantification, a complementary ratiometric biosensor has already been successfully used to track JA-Ile production in response to osmotic stress. This tool revealed the cellular specificities of hormone biosynthesis with rapid activation occurring within minutes. Further achievements include the use of mechanoprobes in different root cell compartments. These experiments strengthen our observations that osmotic stress generates differential responses in different tissues. Transgenic lines expressing tensile stress markers have further shown that inner root tissues experience stronger mechanical stress, correlating with increased JA-Ile signalling. Volumetric analyses of cleared root tissues are underway to model and predict mechanical properties. Breakthroughs in isolated plastid experiments point towards plastid autonomy in stress sensing and downstream responses. Key enzymes involved in root JA-Ile biosynthesis have been identified, with ongoing studies into their activation mechanisms and membrane interactions. Finally, a large-scale genetic screen yielded several mutants with impaired JA-Ile responses, including candidates linked to cytoskeleton organization. These findings reinforce the hypothesis that mechanical signals are transmitted to plastids, possibly via the cytoskeleton, highlighting the central role of biomechanics in plant stress signalling.
This research programme has made several important advances that extend what we know about how plants sense and respond to environmental stress. Two key breakthroughs stand out: the creation of a new tool to track plant hormones in real time, and the discovery that a plant’s cytoskeleton can control when stress hormones are produced. We have been developing a positive sensor that can track the activity of the stress hormone JA-Ile inside living plants. This tool fills a long-standing gap: while sensors for other plant hormones exist, none have been available for JA-Ile. Once fully tested and further optimized, it will provide the plant science community with a powerful tool to track hormone responses as they happen, opening up new possibilities for understanding how plants grow and defend themselves under stress.
We also found that the way plant cells are physically organized plays a key role in inducing stress hormones. This was unexpected, as the literature predominantly suggest hormone activation is induced via small molecules and ligand-receptor interactions. This finding reveals a new connection between physical forces inside the plant and their ability to produce protective hormones. It opens an exciting line of research into how plants sense their environment and translate mechanical changes into survival strategies. Together, these advances create new tools and fresh ideas for plant science, with the potential to reshape how researchers study plant resilience and adaptation, including crops.
We also found that the way plant cells are physically organized plays a key role in inducing stress hormones. This was unexpected, as the literature predominantly suggest hormone activation is induced via small molecules and ligand-receptor interactions. This finding reveals a new connection between physical forces inside the plant and their ability to produce protective hormones. It opens an exciting line of research into how plants sense their environment and translate mechanical changes into survival strategies. Together, these advances create new tools and fresh ideas for plant science, with the potential to reshape how researchers study plant resilience and adaptation, including crops.