Turning plants from passive to active material: FERONIA and microtubules independently contribute to mechanical feedback

Abstract

To survive, cells must constantly resist mechanical stress. In plants, this involves the reinforcement of cell walls, notably through microtubule-dependent cellulose deposition, and thus wall sensing. Several receptor-like kinases have been proposed to act as mechanosensors. Here we tested whether the microtubule response to stress acts downstream of known wall sensors. Using a multi-step screen with eleven mutant lines, we identify FERONIA as the primary candidate for controlling the microtubule response to stress. However, when performing mechanical perturbations, we show that the microtubule response to stress can be independent from FER. We reveal that the feronia phenotype can be partially rescued by reducing tensile stress levels. Conversely, in the absence of both microtubules and FER, cells swell and burst like soap bubbles. Altogether, this shows that the microtubule response to stress acts as an independent pathway to resist stress, in parallel to FER. We propose that both pathways are key components to turn plant cells from passive to active material.

Brassinosteroid recruits FERONIA to safeguard cell expansion in Arabidopsis

“…In particular, the fer mutants show altered responses to many hormones, and FER is considered a central node that mediates crosstalk among multiple phytohormones (28). However, our study supports the notion that some of the pleiotropic phenotypes of fer may reflect the consequence of losing mechanical sensing and wall integrity rather than a direct role of FER in the specific signaling pathways controlling the phenotypes (29).…”

Mechano-transduction via the pectin-FERONIA complex activates ROP6 GTPase signaling in Arabidopsis pavement cell morphogenesis

“…In addition to cell expansion and morphogenesis, FER has also been shown to maintain cell wall integrity under salt stress or conditions that increase tensile stress and in root hairs. 45,49,65 Interestingly, the role for FER in the maintenance of cell wall integrity appears to be independent of microtubule rearrangements induced by mechanical stress. 65 Several FER homologs in the CrRLK1L subfamily, such as ANX1/2 and BUPS1/2, have been shown to maintain cell wall integrity in the rapidly growing cells, such as pollen tubes.…”

“…45,49,65 Interestingly, the role for FER in the maintenance of cell wall integrity appears to be independent of microtubule rearrangements induced by mechanical stress. 65 Several FER homologs in the CrRLK1L subfamily, such as ANX1/2 and BUPS1/2, have been shown to maintain cell wall integrity in the rapidly growing cells, such as pollen tubes. 66,67 Interestingly, BUPS1 also binds pectin and participates in the sensing and/or signaling of mechanical stress to ROPs to control cell wall integrity of pollen tubes by promoting the accumulation of highly demethylesterified pectin in the cell wall during their penetrative growth with the pistil.…”

THESEUS1 modulates cell wall stiffness and abscisic acid production in Arabidopsis thaliana

“…This suggests that some form of redundancy compensates for loss of THE1 and that THE1 has more specialized and different functions than FER, even if both FER and THE1 contribute to stress-induced, cell wall dependent processes. Redundancy could be mediated by other molecular components involved in mechano-perception or coordination between the cell wall and cellular components (3,4,23,46). Reduced JA induction in rlp12 seedlings after ISX treatment and ISX-induced, osmosensitive RLP12 expression in the same region of the root like THE1 indicate that RLP12 is required for CWI maintenance.…”