Tissue and cell type specific response to cold stress in maize roots

Maize is a highly cold sensitive species due to its tropical origin. Low temperature events frequently occur early after planting in temperate climates, thereby decreasing yield in modern maize. European flint maize landraces provide a unique genetic resource for study cold adaptation and acclimation. However, the unique response of specific root cell types at different developmental stages to cold have not yet been comprehensively studied. Here, we explored tissue- and cell type- specific transcriptomic dynamics of maize roots under mild and moderate cold stresses. In response to cold, maize roots exhibited a high degree of tissue and cell-type specific transcriptomic pattern irrespective of stress intensity and duration. Moreover, cell type transcriptomes, particularly in xylem-pole-pericycle cells and epidermis, were more affected by different cold temperatures in comparison with whole roots or different root tissues. Furthermore, moderate cold temperature induced the largest quantity of cold responsive genes in the epidermis and stimulated root hair extension. A focused analysis provided evidence that auxin and ethylene responsive genes were dynamically regulated by cold. Differentially gene expression analysis and functional characterization identified members of HSF transcription factor family playing a key role linking cold stress response to other signaling. Finally, gene co-expression analysis defined cell wall-related gene expression changes across tissues and cell types associated root phenotypic changes. An interplay between auxin-, ethylene- and cell wall-related genes might associate with root phenotypic adaptations and tissue- or cell type- specific cold tolerance. Overall, this study provides a systemic transcriptomic landscape of maize roots in response to cold stress from the whole organ to the single cell type level.