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

Abstract

Plant cells can be distinguished from animal cells by their cell walls and high-turgor pressure. Although changes in turgor and the stiffness of cell walls seem coordinated, we know little about the mechanism responsible for coordination. Evidence has accumulated that plants, like yeast, have a dedicated cell wall integrity maintenance mechanism. It monitors the functional integrity of the wall and maintains integrity through adaptive responses induced by cell wall damage arising during growth, development, and interactions with the environment. These adaptive responses include osmosensitive induction of phytohormone production, defense responses, as well as changes in cell wall composition and structure. Here, we investigate how the cell wall integrity maintenance mechanism coordinates changes in cell wall stiffness and turgor in Arabidopsis thaliana. We show that the production of abscisic acid (ABA), the phytohormone-modulating turgor pressure, and responses to drought depend on the presence of a functional cell wall. We find that the cell wall integrity sensor THESEUS1 modulates mechanical properties of walls, turgor loss point, ABA biosynthesis, and ABA-controlled processes. We identify RECEPTOR-LIKE PROTEIN 12 as a component of cell wall integrity maintenance–controlling, cell wall damage–induced jasmonic acid (JA) production. We propose that THE1 is responsible for coordinating changes in turgor pressure and cell wall stiffness.

Arabidopsis root responses to salinity depend on pectin modification and cell wall sensing

“…In recent years, a mechanism required to monitor CW structure, namely CW integrity (CWI) maintenance, has been described in plants. In this mechanism, several proteins belonging to the CrRLK1L subfamily were described to function as CW sensors ( Bacete et al, 2022 ; Engelsdorf et al, 2018 ; Gigli-Bisceglia et al, 2020 ; Vaahtera et al, 2019 ). In our attempt to understand the role of CrRLK1Ls in regulating salt stress responses, we studied the double herk1 the1-4 mutant, which was originally reported to lack the function of both the CrRLK1Ls THE1 and HERK1, and only later characterized for being a combination of herk1 loss-of-function and the1-4 gain-of-function alleles ( Merz et al, 2017 ).…”

“…It is likely that PM-localized CrRLK1Ls (such as THE1, HERK1 and FER) regulate similar metabolic and cellular responses. For example, it has recently been reported that THE1, similarly to FER, functions as negative regulator of ABA synthesis in response to osmotic stress ( Bacete et al, 2022 ; Zhao et al, 2021 ). Whether HERK1 together with THE1 would affect ABA metabolism and/or synthesis and would contribute to altering salt stress responses remains to be determined, but certain salt-induced FER-dependent phenotypes, such as stunted growth in salt, seem to be abolished upon disruption of ABA biosynthesis or ROS accumulation ( Zhao et al, 2021 ).…”

“…In plants, THE1 has been hypothesized to function in a similar manner as the yeast WSC1, being required to activate responses induced by cellulose impairment-induced cell swelling. Recent evidence showed that, not only signaling, but also CW strength, might be altered in the1 mutants ( Bacete et al, 2022 ), suggesting that CrRLK1Ls might not only regulate the intracellular responses to CW damage, but also the structural architecture of the CW. Here, we show that changes in CW elasticity observed in response to salt ( Feng et al, 2018 ) might be the result of modifications in the degree of methyl esterification of homogalacturonan, as wt seedlings treated with salt showed enhanced PME activity and increased de-methyl esterified epitopes of pectin compared with the mock controls ( Fig.…”

“…fertility, mechanical stress and immune responses), whereas THESEUS1 (THE1), HERKULES 1/2 (HERK1/2) and CURVY (CVY1) appear to be essential for cell elongation and cell morphology-related processes ( Guo et al, 2009 ; Nissen et al, 2016 ; Voxeur and Höfte, 2016 ). THE1 has been described to be responsible for sensing CW alterations and mechanical stress responses upon cellulose impairment ( Engelsdorf et al, 2018 ; Gigli-Bisceglia et al, 2018b ), but at the same time appears to be essential for controlling the mechanical properties of cell walls that affect turgor pressure in plants ( Bacete et al, 2022 ). Several proteins have been characterized to play a role in CWI signaling, including stretch-activated PM-localized Ca 2+ channels (MCAs) and the NITRATE REDUCTASE 1 and 2 (NIA1/2), the latter having been recently described to play an essential role in CW damage (CWD)-dependent cell cycle regulation ( Engelsdorf et al, 2018 ; Gigli-Bisceglia et al, 2018b ; 2020 ; Vaahtera et al, 2019 ).…”

Arabidopsis Leucine Rich Repeat-Malectin Receptor Kinases in immunity triggered by cellulose and mixed-linked glucan oligosaccharides

“…However, MLG43, and in a lower extend CEL3, have been described to be perceived by cereals suggesting that additional receptors to LRR-MAL RLKs (e.g., LysM-RLKs for MLGs in rice) would be involved in these perception mechanisms (32,33). MLG-and cellulose-derived oligosaccharides can be also released upon alteration of plant cell wall integrity triggered by other stresses (e.g., salt or drought) or during plant development (e.g., cell wall remodelling: (71,72)). During these processes plant endogenous enzymes can hydrolase cell wall polysaccharides, as described recently for a maize GH17 licheninase that releases MLG43 and other oligosaccharides from MLGs (73).…”