Analysis of the growth and orientation of roots of Arabidopsis mutants with differing root cap sizes and shapes indicates that the form of the cap affects root responses to variations in the strength of the growth medium.

Plants can attenuate their molecular response to repetitive mechanical stimulation as a function of their mechanical history. For instance, a single bending of stem is sufficient to attenuate the gene expression in poplar plants to the subsequent mechanical stimulation, and the state of desensitization can last for several days. The role of histone modifications in memory gene expression and modulating plant response to abiotic or biotic signals is well known. However, such information is still lacking to explain the attenuated expression pattern of mechano-responsive genes in plants under repetitive stimulation. Using poplar as a model plant in this study, we first measured the global level of H3K9/14ac and H3K4me3 marks in the bent stem. The result shows that a single mild bending of the stem for 6 seconds is sufficient to alter the global level of the H3K9/14ac mark in poplar, highlighting the fact that plants are extremely sensitive to mechanical signals. Next, we analyzed the temporal dynamics of these two active histone marks at attenuated (PtaZFP2, PtaXET6, and PtaACA13) and non-attenuated (PtaHRD) mechano-responsive loci during the desensitization and resensitization phases. Enrichment of H3K9/14ac and H3K4me3 in the regulatory region of attenuated genes correlates well with their transient expression pattern after the first bending. Moreover, the levels of H3K4me3 correlate well with their expression pattern after the second bending at desensitization (3 days after the first bending) as well as resensitization (5 days after the first bending) phases. On the other hand, H3K9/14ac status correlates only with their attenuated expression pattern at the desensitization phase. The expression efficiency of the attenuated genes was restored after the second bending in the histone deacetylase inhibitor-treated plants. While both histone modifications contribute to the expression of attenuated genes, mechanostimulated expression of the non-attenuated PtaHRD gene seems to be H3K4me3 dependent.

During root progression in soil, root cap cells are the first to encounter obstacles. The root cap is known to sense environmental cues, making it a relevant candidate for a mechanosensing site. An original two-layer medium was developed in order to study root responses to growth medium strength and the importance of the root cap in the establishment of these responses. Root growth and trajectory of primary roots of Arabidopsis thaliana seedlings were investigated using in vivo image analysis. After contact with the harder layer, the root either penetrated it or underwent rapid curvature, enabling reorientation of the root primary growth. The role of the root cap in tip reorientation was investigated by analyzing the responses of Arabidopsis mutant roots with altered caps. The primary root of fez-2 mutant lines, which has fewer root cap cell layers than wild-type roots, showed impaired penetration ability. Conversely, smb-3 roots of mutant lines, which display a higher number of root cap cells, showed enhanced penetration abilities. This work highlights that alterations in root cap shape and size affect the root responses to medium strength.HighlightThe analysis of the growth and orientation of Arabidopsis thaliana mutant roots affected in root cap size and shape showed that properly formed root cap is required to trigger the root responses to medium strength.AbbreviationsCOLcolumella;LRCLateral Root Cap;SISharpness Index;SMBSOMBRERO.