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Secondary growth in woody plants generates new cells and tissues via the activity of the vascular cambium and drives the radial expansion of stems and roots. It is regulated by a series of endogenous factors, especially transcription factors. Here, we cloned the basic helix–loop–helix (bHLH) transcription factor gene UNFERTILIZED EMBRYO SAC12 (UNE12) from poplar (Populus alba × Populus glandulosa Uyeki) and used biochemical, molecular, and cytological assays to investigate the biological functions and regulatory mechanism of PagUNE12. PagUNE12 mainly localized in the nucleus and possessed transcriptional activation activity. It was widely expressed in vascular tissues, including primary phloem and xylem and secondary phloem and xylem. Poplar plants overexpressing PagUNE12 showed significantly reduced plant height, shorter internodes, and curled leaves compared with wild-type plants. Optical microscopy and transmission electron microscopy revealed that overexpressing PagUNE12 promoted secondary xylem development, with thicker secondary cell walls than wild-type poplar. Fourier transform infrared spectroscopy, confocal Raman microscopy, and 2D Heteronuclear Single Quantum Correlation analysis indicated that these plants also had increased lignin contents, with a lower relative abundance of syringyl lignin units and a higher relative abundance of guaiacyl lignin units. Therefore, overexpressing PagUNE12 promoted secondary xylem development and increased the lignin contents of secondary xylem in poplar, suggesting that this gene could be used to improve wood quality in the future.

Cell wall lignification is a key step in forming functional endodermis and protoxylem (PX) in plant roots. Lignified casparian strips (CS) in endodermis and tracheary elements of PX are essential for selective absorption and transport of water and nutrients. Although multiple key regulators of CS and PX have been identified, the spatial information that drives the developmental shift to root lignification remains unknown. Here, we found that brassinosteroid (BR) signaling plays a key role in inhibiting root lignification in the root elongation zone. The inhibitory activity of BR signaling occurs partially through the direct binding of BRASSINAZOLE-RESISTANT 1 (BZR1) to SHORT-ROOT (SHR), repressing the SHR-mediated activation of downstream genes that are involved in root lignification. Upon entering the mature root zone, BR signaling declines rapidly, which releases SHR activity and initiates root lignification. Our results provide a mechanistic view of the developmental transition to cell wall lignification in Arabidopsis thaliana roots.

Vascular tissues are surrounded by an apoplastic barrier formed by endodermis that is vital for selective absorption of water and nutrients. Lignification and suberization of endodermal cell walls are fundamental processes in establishing the apoplastic barrier. Endodermal suberization in Arabidopsis (Arabidopsis thaliana) roots is presumed to be the integration of developmental regulation and stress responses. In root endodermis, the suberization level is enhanced when the Casparian strip, the lignified structure, is defective. However, it is not entirely clear how lignification and suberization interplay and how they interact with stress signaling. Here, in Arabidopsis, we constructed a hierarchical network mediated by SHORT-ROOT (SHR), a master regulator of endodermal development, and identified 13 key MYB transcription factors (TFs) that form multiple sub-networks. Combined with functional analyses, we further uncovered MYB TFs that mediate feedback or feed-forward loops, thus balancing lignification and suberization in Arabidopsis roots. In addition, sub-networks comprising nine MYB TFs were identified that interact with abscisic acid signaling to integrate stress response and root development. Our data provide insights into the mechanisms that enhance plant adaptation to changing environments.