Four MYB transcription factors regulate suberization and nonlocalized lignification at the root endodermis in rice

Abstract

In response to variable environments, rice (Oryza sativa) roots have developed lignified and suberized diffusion barriers at the endodermis to permit selective nutrient uptake for optimal growth. Here, we demonstrate that endodermal suberization and nonlocalized lignification are redundantly regulated by 4 MYB transcription factors: OsMYB39a, OsMYB41, OsMYB92a, and OsMYB92b. These transcription factors function downstream of the OsMYB36a/b/c, CASPARIAN STRIP INTEGRITY FACTOR (OsCIF)-SCHENGEN3 (OsSGN3), and stress-inducible signaling pathways in rice. Knockout of all 4 MYB genes resulted in the complete absence of endodermal suberin lamellae (SL) and almost no lignin deposition between the Casparian strip and the cortex-facing lignified band at cell corners under all conditions examined. In contrast, endodermis-specific overexpression of any of these MYB genes was sufficient to induce strong endodermal suberization and nonlocalized lignification near the root tip. Furthermore, OsMYB92a-overexpressing lines showed an altered ionomic profile and enhanced salinity tolerance. Transcriptome analysis identified 152 downstream genes regulated by OsMYB39a/41/92a/92b, including the key SL formation gene OsCYP86A1 and other genes involved in endodermal lignification and suberization under normal and stress conditions. Our results provide important insights into the molecular mechanisms underlying suberization and nonlocalized lignification at the root endodermis and their physiological significance in ion homeostasis and acclimation to environmental stress.