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

Abstract

Due to its detrimental effect on plant growth, salinity is an increasing worldwide problem for agriculture. To understand the molecular mechanisms activated in response to salt in Arabidopsis, we investigated the Catharanthus roseus Receptor like Kinase 1 Like family, containing sensors previously shown to be involved in sensing the structural integrity of the cell walls. We found that herk1the1-4 double mutants, lacking the function of HERKULES1 (HERK1) combined with a gain-of-function allele of THESEUS1 (THE1), strongly respond to salt application, resulting in an intense activation of stress responses, similarly to plants lacking FERONIA (FER) function. We report that salt triggers pectin methyl esterase (PME) activation and show its requirement for the activation of several salt-dependent responses. Because chemical inhibition of PMEs alleviates these salt-induced responses, we hypothesize a model where salt directly leads to cell wall modifications through the activation of PMEs. Responses to salt partly require the functionality of FER alone or the HERK1/THE1 combination to attenuate salt effects, highlighting the complexity of the salt sensing mechanisms that rely on the cell wall integrity.

Endoreplication mediates cell size control via mechanochemical signaling from cell wall

“…5A and fig. S9A), presumably due to redundancy with related receptor-like protein kinases (RLKs) such as HERCULES1 (HERK1), as shown for other responses ( 26 ). Consistently, endoreplication asymmetry was not affected by loss of function the1-1 (fig.…”

“…Therefore, we next investigated potential mediators of endoreplication responsive mechanochemical feedback in the regulation of cell elongation during hook development. THESEUS1 (THE1), a receptor-like kinase that monitors cell wall integrity, was targeted because it mediates changes in HG methylesterification ( 26 ). The loss-of-function mutant allele the1-1 does not cause discernible hook defects ( Fig.…”

The cell biology of primary cell walls during salt stress

“…More recently, two other cell wall sensors, the FER-related CrRLK1Ls HERKULES1 (HERK1) and THESEUS1 (THE1), have also been reported to contribute to salt-induced responses. Indeed, the double mutant herk1 the1-4 (a loss of function allele of HERK1 combined with a gain-of-function allele of THE1 ) exhibits a similar phenotype to fer under salt stress ( Gigli-Bisceglia et al, 2022 ). In this study, the authors proposed a model in which these sensors might mitigate salt stress sensitivity by alleviating salt-induced responses through the negative regulation of MAPK6, a MAPK protein involved in regulating many cellular processes, including salt stress response ( Colcombet and Hirt, 2008 ; Komis et al, 2011 ).…”

“…It is thought that excessive Na + in apoplastic region competes with Ca 2+ to bind to pectin, which in turn disturbs the cross-linking of pectin ( Manunza et al, 1998 ; Figure 3 ). However, salt stress might also directly trigger PME activation, resulting in a decrease in pectin methylation, thus affecting cell wall properties ( Gigli-Bisceglia et al, 2022 ). Consistently, application of exogenous Ca 2+ , which inhibits PME activity, decreased certain salt-induced responses, furthering the notion that the pectin status is important during salt stress signaling ( Gigli-Bisceglia et al, 2022 ).…”

“…However, salt stress might also directly trigger PME activation, resulting in a decrease in pectin methylation, thus affecting cell wall properties ( Gigli-Bisceglia et al, 2022 ). Consistently, application of exogenous Ca 2+ , which inhibits PME activity, decreased certain salt-induced responses, furthering the notion that the pectin status is important during salt stress signaling ( Gigli-Bisceglia et al, 2022 ). Salt stress induces GALACTAN SYNTHASE 1 (GALS1) in roots, leading to the accumulation of ß-1,4 galactan, a major component of pectins ( Yan et al, 2021 ), which reduces root growth.…”