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

Abstract

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

Mechanically induced localization of SECONDARY WALL INTERACTING bZIP is associated with thigmomorphogenic and secondary cell wall gene expression

“…Following touch, most of these genes become significantly upregulated. This activity is consistent with our observations of increased lignin staining in touched SWIZ-OE peduncles, and aligns with the compositional data presented by Gladala-Kostarz et al (2020). This activation may be a result of direct binding of SWIZ to modulate expression, or an indirect effect from another transcriptional regulator such as the NAC transcription factor SWN5, capable of activating the full developmental program for secondary cell wall synthesis (Valdivia et al, 2013), which is significantly upregulated in SWIZ-OE following touch.…”

“…While these studies highlight the importance of stem strength and associated cell wall defects, they do relatively little to elucidate the mechanosensitive response. Recent work by Gladala-Kostarz et al (2020) describes grass touch response to both wind and direct mechanical treatment, with an emphasis on cell walls and stem anatomy. Touch treatment significantly increased lignin content, and also altered the relative abundance of wall bound hydroxycinnamates.…”

“…Stem elongation comes from cellular division and elongation in a discrete series of intercalary meristems, called nodes, with one internode region elongating and pushing up subsequent nodes. Detailed studies of thigmomorphogenesis have been conducted almost exclusively in eudicots However, recent work in the model cereal grass Brachypodium distachyon shows general overlap with conventional dicot thigmomorphogenesis, albeit with some notable differences, such as no change in stem diameter and increased flowering time (Gladala-Kostarz et al, 2020).…”

Cell wall remodeling under salt stress: Insights into changes in polysaccharides, feruloylation, lignification, and phenolic metabolism in maize

“…Plant cell walls are highly dynamic and responsive structures that can be remodelled during plant growth, development and in response to various abiotic and biotic stresses (Cesarino, 2019; Gladala‐Kostarz, Doonan, & Bosch, 2020; Le Gall et al, 2015; Tenhaken, 2014; Voiniciuc, Pauly, & Usadel, 2018). The complex arrangement of cell wall polymers provides mechanical and structural integrity to each cell, sustains differential growth during cell division and expansion, and serves as a sensory interface between the plant and its environment (Burton, Gidley, & Fincher, 2010; Vaahtera, Schulz, & Hamann, 2019).…”

Mechanostimulation: a promising alternative for sustainable agriculture practices

“…In addition, plants exposed to repeated external mechanical stimulation exhibit thigmomorphogenesis (Jaffe, 1973), which, in extreme cases, leads to severe alterations of the plant morphology, such as dwarfism, pithiness, delayed flowering, and reduction in stomatal aperture (Chehab et al, 2009(Chehab et al, , 2011. Moreover, it has been reported to greatly alter the biomechanical and structural traits in a wide range of plant species, from an aquatic macrophyte to trees (Kern et al, 2005;Paul-Victor and Rowe, 2011;Schoelynck et al, 2015;Gladala-Kostarz et al, 2020). Mechanical stimulation (e.g.…”