Expansin-mediated developmental and adaptive responses: A matter of cell wall biomechanics?

Abstract

Biomechanical properties of the cell wall (CW) are important for many developmental and adaptive responses in plants. Expansins were shown to mediate pH-dependent CW enlargement via a process called CW loosening. Here, we provide a brief overview of expansin occurrence in plant and non-plant species, their structure and mode of action including the role of hormone-regulated CW acidification in the control of expansin activity. We depict the historical as well as recent CW models, discuss the role of expansins in the CW biomechanics and address the developmental importance of expansin-regulated CW loosening in cell elongation and new primordia formation. We summarise the data published so far on the role of expansins in the abiotic stress response as well as the rather scarce evidence and hypotheses on the possible mechanisms underlying expansin-mediated abiotic stress resistance. Finally, we wrap it up by highlighting possible future directions in expansin research.

Keywords: biomechanics; cell wall loosening; cell wall remodelling; development; expansin; plant.

Graphical abstract

Fig. 1.

(a) Structure of AtEXPA1 determined by the AlphaFold algorithm. N-terminal six-stranded double-psi (ω) β-barrel D1 domain related to family 45 glycoside hydrolases (GH45) (green/blue, left) and C-terminal β-sandwich fold D2 domain related to group-2 grass pollen allergens resembling the carbohydrate binding module (CBM) family 63 (red/orange, right); the unstructured signal peptide is not shown. (b) Upon binding the load-bearing cellulose microfibril (CMF) network laterally interconnected with possible xyloglucan contribution (grey), expansins induce CW expansion via CW creep. By interfering with CW remodelling enzymes via binding to xylan and/or pectin or through transcriptional feedback regulations in a response to changed CW biomechanics, expansins might contribute to CW remodelling, too. (c) Expansin expression and localization is regulated during plant development, ensuring expansin action in a manner that is specific to their dose and the particular developmental context. Conversely, expansin action on CW biomechanics affects plant development and growth responses by regulating cell elongation and/or primordia specification/outgrowth. Expansins are activated in response to various stresses associated with ROS production. Expansin expression might be mediated by developmental- and stress-regulated hormone production, controlling expansin activity also via spatial-specific CW acidification. Expansins could mitigate ROS effects by upregulating CW peroxidases. In turn, ROS also contribute to the regulation of CW biomechanical properties. While short-term or low-level ROS production leads to growth inhibition by inducing crosslinking of CW components, high ROS levels/long-term ROS production leads to OH°-radical formation that was hypothesised to allow restoration of cell expansion via polymer cleavage, leading to CW weakening. See the main text for a more detailed description.