A question of turgor pressure: mechanical compression triggers Jasmonate production.
The phytohormone jasmonate-isoleucine (JA-Ile) is a crucial coordinator of plant growth and stress responses. It not only ensures successful reproductive development, but is also essential to protect plants against chewing herbivores and necrotrophic pathogens. In spite of regulating such a wide-range of fundamental plant processes, it is still unknown how exactly is JA-Ile biosynthesis initiated. IPB scientists have now provided compelling genetic evidence that mechanical and osmotic regulation of turgor pressure represents a key elicitor of JA-Ile biosynthesis. Dr. Debora Gasperini and her team have found that in roots, enlarged plant cells with weak cell walls compress neighbouring tissues and thus stimulate the production of the decisive stress hormone.
Unlike animals, plant cells have a high turgor pressure (0.1-5 MPa) that is generated by the gradient of osmotic potential across the plasma membrane and is mainly counterbalanced by cellulose microfibrils of plant cell walls. Plant cells with impaired cellulose production can no longer efficiently counteract the high intracellular turgor pressure, often resulting in swollen cells. To understand what causes JA-Ile production, the Halle scientists used an Arabidopsis mutant in KORRIGAN 1 (kor1) with compromised cellulose biosynthesis and constitutively high JA-Ile levels in the early differentiation zone of the primary root. Stefan Mielke, the first author of the paper, noticed that kor1 roots are significantly thicker and have considerably larger cortex cells compared to wild-type controls. He then found that constitutive JA-Ile biosynthesis in kor1 roots does not occur in swollen cortex cells but in adjacent inner endodermal and pericycle cells. The team therefore hypothesized that JA-Ile production may derive from enlarged cortex cells mechanically squeezing inner tissues.
Indeed, reducing cortex cell size in three independent manners complitely abolished constitutive JA-Ile production and validated their assumption. First, the kor1 high JA-Ile levels were suppressed when restoring wild-type KOR1 function in the cortex, but not when restoring it in endodermal or pericycle cells. Second, they identified a genetic suppressor of kor1 affecting cell wall properties. Third, by reducing kor1 turgor pressure with hyperosmotic treatments, enlarged cortex cells and JA signalling were fully restored to wild-type levels. Conversely, hypoosmotic treatments leading to cell enlargement activated JA-Ile signalling in similar locations as in kor1 roots. Interestingly, these findings may be relevant for other stresses such as mechanical wounding and herbivory, which also alter osmotic potentials and turgor pressure.
Remarkably, the scientists found that constitutive JA-Ile production in the mutant was beneficial to guide root growth towards greater water availability. Although the team still needs to elucidate the molecular mechanisms governing this process, they think the results may have beneficial impacts on strategies aimed at increasing plant drought tolerance.