Mechanical signaling in plant morphogenesis

Zhao, Feng; Chen, Wenqian; Traas, Jan

doi:10.1016/j.gde.2018.04.001

Cited by 18 publications

(21 citation statements)

References 42 publications

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“…The mechanical properties of cell walls have been proposed to play a key role in plant morphogenesis and the control of organ outgrowth [ 7 , 109 , 110 ]. Organ morphogenesis requires a transition from isotropic growth of undifferentiated cells to anisotropic growth pattern, which is dependent on local cell wall loosening and stiffening by e.g., modification of cell wall components.…”

Section: Role Of Pmeis In Developmentmentioning

confidence: 99%

The Multifaceted Role of Pectin Methylesterase Inhibitors (PMEIs)

Wormit

Usadel

2018

IJMS

164

126

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Plant cell walls are complex and dynamic structures that play important roles in growth and development, as well as in response to stresses. Pectin is a major polysaccharide of cell walls rich in galacturonic acid (GalA). Homogalacturonan (HG) is considered the most abundant pectic polymer in plant cell walls and is partially methylesterified at the C6 atom of galacturonic acid. Its degree (and pattern) of methylation (DM) has been shown to affect biomechanical properties of the cell wall by making pectin susceptible for enzymatic de-polymerization and enabling gel formation. Pectin methylesterases (PMEs) catalyze the removal of methyl-groups from the HG backbone and their activity is modulated by a family of proteinaceous inhibitors known as pectin methylesterase inhibitors (PMEIs). As such, the interplay between PME and PMEI can be considered as a determinant of cell adhesion, cell wall porosity and elasticity, as well as a source of signaling molecules released upon cell wall stress. This review aims to highlight recent updates in our understanding of the PMEI gene family, their regulation and structure, interaction with PMEs, as well as their function in response to stress and during development.

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Section: Role Of Pmeis In Developmentmentioning

confidence: 99%

The Multifaceted Role of Pectin Methylesterase Inhibitors (PMEIs)

Wormit

Usadel

2018

IJMS

164

126

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“…Among these first constitutive barriers, the cell wall has traditionally been considered a passive defense barrier. However, an increasingly large body of evidence suggests that the cell wall, through its associated receptor kinases, provides active signaling toward mounting defense responses against a variety of stresses and controlling plant development (Gallego-Giraldo et al, 2011bWolf et al, 2012Wolf et al, , 2014Miedes et al, 2014;Kohorn, 2015;Tenhaken, 2015;Bethke et al, 2016;Voxeur and Höfte, 2016;Feng et al, 2018;Zhao et al, 2018). Modification of lignin quantity and quality can lead to cell wall remodeling and ectopic release of signal molecules that are recognized by cell wall receptors and turn on a variety of defense responses (Gallego-Giraldo et al, 2011b.…”

Section: Tradeoffs Between Growth and Defense In Monolignol Pathway Mmentioning

confidence: 99%

Ectopic Defense Gene Expression Is Associated with Growth Defects in Medicago truncatula Lignin Pathway Mutants

Fine

Bhatia

et al. 2019

Plant Physiol.

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Lignin provides essential mechanical support for plant cell walls but decreases the digestibility of forage crops and increases the recalcitrance of biofuel crops. Attempts to modify lignin content and/or composition by genetic modification often result in negative growth effects. Although several studies have attempted to address the basis for such effects in individual transgenic lines, no common mechanism linking lignin modification with perturbations in plant growth and development has yet been identified. To address whether a common mechanism exists, we have analyzed transposon insertion mutants resulting in independent loss of function of five enzymes of the monolignol pathway, as well as one double mutant, in the model legume Medicago truncatula. These plants exhibit growth phenotypes from essentially wild type to severely retarded. Extensive phenotypic, transcriptomic, and metabolomics analyses, including structural characterization of differentially expressed compounds, revealed diverse phenotypic consequences of lignin pathway perturbation that were perceived early in plant development but were not predicted by lignin content or composition alone. Notable phenotypes among the mutants with severe growth impairment were increased trichome numbers, accumulation of a variety of triterpene saponins, and extensive but differential ectopic expression of defense response genes. No currently proposed model explains the observed phenotypes across all lines. We propose that reallocation of resources into defense pathways is linked to the severity of the final growth phenotype in monolignol pathway mutants of M. truncatula, although it remains unclear whether this is a cause or an effect of the growth impairment.

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“…For instance, strong winds induce stem breakage (Eloy, 2011; Moore et al, 2018). Accordingly, perception of mechanical forces may have emerged from the need to maintain the physical integrity of cells and organisms (Moulia et al, 2015), which would in turn influence growth and morphogenesis (Mirabet et al, 2011; Zhao et al, 2018). There are numerous examples of plant responses to mechanical forces, from molecular and cellular level – reorganization of the cytoskeleton (Landrein and Hamant, 2013; Robinson and Kuhlemeier, 2018), calcium influx (Trewavas and Knight, 1994; Monshausen and Haswell, 2013), and changes in protein polarity or in gene expression (Lee et al, 2005; Bringmann and Bergmann, 2017) – to tissue and organism levels – organogenesis (Ditengou et al, 2008; Hamant et al, 2008; Heisler et al, 2010; Nakayama et al, 2012; Landrein et al, 2015), fast movements (Poppinga et al, 2016), formation of tension and compression wood (Okuyama et al, 1994) and control of plant posture (Eloy, 2011; Moore et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants

2019

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Mechanical signals have recently emerged as a major cue in plant morphogenesis, notably influencing cytoskeleton organization, gene expression, protein polarity, or cell division. Although many putative mechanosensing proteins have been identified, it is unclear what mechanical cue they might sense and how this would occur. Here we briefly explain the notions of mechanical stress and strain. We present the challenges to understand their sensing by plants, focusing on the cell wall and the plasma membrane, and we review putative mechanosensing structures. We propose minimal biophysical models of mechanosensing, revealing the modes of mechanosensing according to mechanosensor lifetime, threshold force for mechanosensor dissociation, and type of association between the mechanosensor and the cell wall, as the sensor may be associated to a major load-bearing structure such as cellulose or to a minor load-bearing structure such as pectins or the plasma membrane. Permanent strain, permanent expansion, and relatively slow variations thereof are sensed in all cases; variations of stress are sensed in all cases; permanent stress is sensed only in the following specific cases: sensors associated to minor load-bearing structures slowly relaxing in a growing wall, long-lived sensors with high dissociation force and associated to major-load-bearing structures, and sensors with low dissociation force associated to major-load-baring structures behaving elastically. We also find that all sensors respond to variations in the composition or the mechanical properties of the cell wall. The level of sensing is modulated by the properties of all of mechanosensor, cell wall components, and plasma membrane. Although our models are minimal and not fully realistic, our results yield a framework to start investigating the possible functions of putative mechanosensors.

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Mechanical signaling in plant morphogenesis

Cited by 18 publications

References 42 publications

The Multifaceted Role of Pectin Methylesterase Inhibitors (PMEIs)

The Multifaceted Role of Pectin Methylesterase Inhibitors (PMEIs)

Ectopic Defense Gene Expression Is Associated with Growth Defects in Medicago truncatula Lignin Pathway Mutants

Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants

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