MYB68 orchestrates cork differentiation by regulating stem cell proliferation and suberin deposition

Abstract

Plants have developed specialized barriers to protect and isolate the inner tissues from the environment while maintaining homeostasis. Different barriers are present in various organs and at different growth stages. During secondary growth, the periderm acts as the protective tissue, covering roots, stems, and branches as they become thick. The periderm is a dynamic barrier comprising a stem cell niche known as the cork cambium, which bifacially divides to generate the phelloderm inward and the cork outward. Cork cells have a unique cell wall impregnated with suberin and lignin polymers, essential for the barrier function. Despite its importance, the differentiation process that forms new cork cells from the stem cell is largely unknown. In this work, we identify members of the MYB36-subclade transcription factors as key regulators of cork differentiation. On the one hand, this set of transcription factors promotes suberin deposition by inducing the expression of enzymes involved in all steps of suberin biosynthesis, including the recently discovered suberin-polymerizing enzymes GDS Lipases; on the other hand, it represses cork cambium proliferation. Furthermore, we demonstrated that suberin deposition in the cork is a robust process regulated by a complex network of transcription factors, including other MYB transcription factors that activate suberin deposition in the endodermis. However, only members of the MYB36 subclade can repress cell proliferation in different developmental contexts, highlighting general and specific functions for MYB transcription factors. These findings have broad applicability, as tissue-specific manipulation of MYB activity has the potential for improving traits of biotechnological interest, such as thicker periderms and more suberized cork layers, and for assessing how these traits affect plant performance in response to stresses.