Feeling stretched or compressed? The multiple mechanosensitive responses of wood formation to bending

Roignant, Jeanne; Badel, Éric; Leblanc‐Fournier, Nathalie; Brunel-Michac, Nicole; Ruelle, Julien; Moulia, Bruno; Decourteix, Mélanie

doi:10.1093/aob/mcx211

Cited by 28 publications

(45 citation statements)

References 49 publications

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“…Although the treatment responses in terms of many of the macroscopic and biochemical traits tended to be similar between the two accessions, a notable exception were those involving the vascular system. Mechanical stimulation affects architectural and anatomical features in dicot stems (Paul‐Victor & Rowe, ; Rigo, ; Roignant et al, ), which may influence their mechanical properties (Shah, Reynolds, & Ramage, ). Mechanical stimulation has been reported to increase xylem tissue in a range of dicots (Hepworth & Vincent, ; Hunt & Jaffe, ; Jaffe, , ), but the situation in rice may be more complex.…”

Section: Discussionmentioning

confidence: 99%

“…Expression studies in Arabidopsis have shown that genes encoding cell wall‐associated proteins are enriched in response to mechanical stimulation (Lee et al, ), suggesting that changes in cell wall composition and architecture are involved in thigmomorphogenesis. A recent work reported that mechanical perturbations affect cell wall properties in trees (Roignant et al, ) and cell wall‐related traits play an important role in lodging resistance of rice (Fan et al, ; Li, Liu, Xu, & Xu, ; Ookawa et al, ) and wheat (Zheng et al, ). However, few studies have looked at cell wall‐related changes induced by more moderate wind and/or mechanical treatments (MTs).…”

Section: Introductionmentioning

confidence: 99%

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Mechanical stimulation in Brachypodium distachyon: Implications for fitness, productivity, and cell wall properties

Gladala-Kostarz

Doonan

Bosch

2020

Plant Cell & Environment

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Mechanical stimulation, including exposure to wind, is a common environmental variable for plants. However, knowledge about the morphogenetic response of the grasses (Poaceae) to mechanical stimulation and impact on relevant agronomic traits is very limited. Two natural accessions of Brachypodium distachyon were exposed to wind and mechanical treatments. We surveyed a wide range of stem-related traits to determine the effect of the two treatments on plant growth, development, and stem biomass properties. Both treatments induced significant quantitative changes across multiple scales, from the whole plant down to cellular level. The two treatments resulted in shorter stems, reduced biomass, increased tissue rigidity, delayed flowering, and reduced seed yield in both accessions. Among changes in cell wallrelated features, a substantial increase in lignin content and pectin methylesterase activity was most notable. Mechanical stimulation also reduced the enzymatic sugar release from the cell wall, thus increasing biomass recalcitrance. Notably, treatments had a distinct and opposite effect on vascular bundle area in the two accessions, suggesting genetic variation in modulating these responses to mechanical stimulation.Our findings highlight that exposure of grasses to mechanical stimulation is a relevant environmental factor affecting multiple traits important for their utilization in food, feed, and bioenergy applications. K E Y W O R D S biomass, Brachypodium distachyon, cell wall, fitness, grasses, growth and development, mechanical stress, plant morphology, thigmomorphogenesis, wind

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Mechanical stimulation in Brachypodium distachyon: Implications for fitness, productivity, and cell wall properties

Gladala-Kostarz

Doonan

Bosch

2020

Plant Cell & Environment

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“…The wood formed at the opposite side in each case is referred to as opposite wood (OW) and it is subjected to tensile and compressive forces in gymnosperms and angiosperms, respectively. In addition, wood formed in stems growing upright is subjected solely to vertical gravitational forces with respect to the long axis of xylogenic cells and it is often referred to as normal wood (NW), featuring intermediate MFA values when compared to RW and OW [7,40,41].…”

Section: Mfa As a Key Feature Of Scw Formationmentioning

confidence: 99%

The Cytoskeleton and Its Role in Determining Cellulose Microfibril Angle in Secondary Cell Walls of Woody Tree Species

Tobias

Spokevicius

McFarlane

et al. 2020

Plants

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Recent advances in our understanding of the molecular control of secondary cell wall (SCW) formation have shed light on molecular mechanisms that underpin domestication traits related to wood formation. One such trait is the cellulose microfibril angle (MFA), an important wood quality determinant that varies along tree developmental phases and in response to gravitational stimulus. The cytoskeleton, mainly composed of microtubules and actin filaments, collectively contribute to plant growth and development by participating in several cellular processes, including cellulose deposition. Studies in Arabidopsis have significantly aided our understanding of the roles of microtubules in xylem cell development during which correct SCW deposition and patterning are essential to provide structural support and allow for water transport. In contrast, studies relating to SCW formation in xylary elements performed in woody trees remain elusive. In combination, the data reviewed here suggest that the cytoskeleton plays important roles in determining the exact sites of cellulose deposition, overall SCW patterning and more specifically, the alignment and orientation of cellulose microfibrils. By relating the reviewed evidence to the process of wood formation, we present a model of microtubule participation in determining MFA in woody trees forming reaction wood (RW).

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“…Finally, wind-induced mechanical strains have been proved a major driver of wood growth rate 323 (Bonnesoeur et al 2016) and of wood anatomy (Roignant et al 2018). 324…”

Section: Discussion 251mentioning

confidence: 99%

Modelling the spatial crosstalk between two biochemical signals explains wood formation dynamics and tree-ring structure

Hartmann

Rathgeber

Badel

et al. 2020

Preprint

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HighlightA dynamical model proves that two interacting signals (auxin, plus a cytokinin or the TDIF peptide) can drive wood formation dynamics and tree-ring structure development in conifers. AbstractIn conifers, xylogenesis produces during a growing season a very characteristic tree-ring structure: large thin-walled earlywood cells followed by narrow thick-walled latewood cells. Although many factors influence the dynamics of differentiation and the final dimensions of xylem cells, the associated patterns of variation remain very stable from one year to the next. While radial growth is characterised by an S-shaped curve, the widths of xylem differentiation zones exhibit characteristic skewed bell-shaped curves. These elements suggest a strong internal control of xylogenesis. It has long been hypothesised that much of this regulation relies on a morphogenetic gradient of auxin.However, recent modelling works have shown that while this hypothesis could account for the dynamics of stem radial growth and the zonation of the developing xylem, it failed to reproduce the characteristic tree-ring structure. Here we investigated the hypothesis of a regulation by a crosstalk between auxin and a second biochemical signal, using dynamical modelling. We found that, in conifers, such a crosstalk is sufficient to simulate the characteristic features of wood formation dynamics, as well as the resulting tree-ring structure. In this model, auxin controls cell enlargement rates while another signal (e.g., cytokinin, TDIF) drives cell division and auxin polar transport.

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Feeling stretched or compressed? The multiple mechanosensitive responses of wood formation to bending

Cited by 28 publications

References 49 publications

Mechanical stimulation in Brachypodium distachyon: Implications for fitness, productivity, and cell wall properties

Mechanical stimulation in Brachypodium distachyon: Implications for fitness, productivity, and cell wall properties

The Cytoskeleton and Its Role in Determining Cellulose Microfibril Angle in Secondary Cell Walls of Woody Tree Species

Modelling the spatial crosstalk between two biochemical signals explains wood formation dynamics and tree-ring structure

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