Auxin mediates the touch-induced mechanical stimulation of adventitious root formation under windy conditions in Brachypodium distachyon

Abstract

Background: It is widely perceived that mechanical or thigmomorphogenic stimuli, such as rubbing and bending by passing animals, wind, raindrop, and flooding, broadly influence plant growth and developmental patterning. In particular, wind-driven mechanical stimulation is known to induce the incidence of radial expansion and shorter and stockier statue. Wind stimulation also affects the adaptive propagation of the root system in various plant species. However, it is unknown how plants sense and transmit the wind-derived mechanical signals to launch appropriate responses, leading to the wind-adaptive root growth. Results: Here, we found that Brachypodium distachyon, a model grass widely used for studies on bioenergy crops and cereals, efficiently adapts to wind-mediated lodging stress by forming adventitious roots (ARs) from nonroot tissues. Experimental dissection of wind stimuli revealed that not bending of the mesocotyls but physical contact of the leaf nodes with soil particles triggers the transcriptional induction of a group of potential auxin-responsive genes encoding WUSCHEL RELATED HOMEOBOX and LATERAL ORGAN BOUNDARIES DOMAIN transcription factors, which are likely to be involved in the induction of AR formation. Conclusions: Our findings would contribute to further understanding molecular mechanisms governing the initiation and development of ARs, which will be applicable to crop agriculture in extreme wind climates.

The wild grass Brachypodium distachyon as a developmental model system

“…Depending on environmental conditions, the genetic background of specific accessions and tiller proximity to the soil, the above-ground leaf node can form adventitious roots, too (Hardtke and Pacheco-Villalobos, 2016). In fact, wind-stimulated B. distachyon shoots formed leaf node roots at tiller positions in proximity to soil and this process could be significantly inhibited when auxin transport was inhibited in wind-stimulated plants (Nam et al, 2020). Both seminal and adventitious roots can form lateral roots and root hairs (Hardtke and Pacheco-Villalobos, 2016).…”

Mechanical stress acclimation in plants: Linking hormones and somatic memory to thigmomorphogenesis

“…Mechanical stimulation induced by rotational shaker enhanced proline and Δ 1 pyrroline 5‐carboxylate synthetase (P5CS) to promote the survival of tobacco suspension cells under chilling (1°C) conditions (Z. G. Li & Gong, 2012) and the rubbing of P. vulgaris stem increased ABA concentration three‐fold during drought to improve recovery (Jaffe & Biro, 1979; Suge, 1980). In Brachypodium distachyon , wind stimulation increased adventitious root formation via auxin‐mediated pathways to enable efficient adaptation to wind‐induced lodging (Nam et al, 2020). In a hydrodynamic environment, the continuous twisting and bending of aquatic plant Egeria densa by fast‐flowing water‐induced thigmomorphogenetic traits and promoted lignin, cellulose and silica accumulation to compensate for structural integrity challenges (Miler et al, 2012; Schoelynck et al, 2015).…”

Touch signaling and thigmomorphogenesis are regulated by complementary CAMTA3- and JA-dependent pathways

“…Repeated mechanostimulation leads to severe alterations of the plant morphology, like dwarfism, pithiness, altered mechanical properties of stem, delayed flowering, improved anchorage strength of roots, and reduced stomatal aperture, which is collectively termed as thigmomorphogenesis (3). These morphological changes improve the mechanical safety of plants against strong wind, which often causes lodging due to anchorage failure and stem breakage (4)(5)(6). In addition to this, it has been noted that repetitive mechanical stimulation improves plant performance in stressful environments like pathogen attack, drought, salinity, and cold (4,(7)(8)(9).…”