The dynamics of touch-responsive gene expression in cereals

Wind, rain, herbivores, obstacles, neighbouring plants, etc. provide important mechanical cues to steer plant growth and survival. Mechanostimulation to stimulate yield and stress resistance of crops is of significant research interest, yet a molecular understanding of transcriptional responses to touch is largely absent in cereals. To address this, we performed whole-genome transcriptomics following mechanostimulation of wheat, barley, and the recent genome-sequenced oat. The largest transcriptome changes occurred +/- 25 min after touching, with most of the genes being upregulated. While most genes returned to basal expression level by 1-2 h in oat, many genes retained high expression even 4 h post-treatment in barley and wheat. Functional categories such as transcription factors, kinases, phytohormones, and Ca2+ regulation were affected. In addition, cell wall-related genes involved in (hemi)cellulose, lignin, suberin, and callose biosynthesis were touch-responsive, providing molecular insight into mechanically induced changes in cell wall composition. Furthermore, several cereal-specific transcriptomic footprints were identified that were not observed in Arabidopsis. In oat and barley, we found evidence for systemic spreading of touch-induced signalling. Finally, we provide evidence that both the jasmonic acid-dependent and the jasmonic acid-independent pathways underlie touch-signalling in cereals, providing a detailed framework and marker genes for further study of (a)biotic stress responses in cereals.

Automated summary

Wind, rain, herbivores, obstacles, and neighbouring plants provide important mechanical cues for plant growth and survival. However, there is still a lack of molecular understanding of transcriptional responses to touch in cereals. By performing whole-genome transcriptomics on wheat, barley, and oat, we found that touch-induced changes in the transcriptome occurred mainly within +/- 25 min after touching, with most genes being upregulated. Many touch-responsive genes remained highly expressed even 4 h post-treatment in barley and wheat. Functional categories such as transcription factors, kinases, phytohormones, and cell wall-related genes were affected by touch. Additionally, evidence for systemic spreading of touch-induced signaling was observed in oat and barley.