A Negative Feedback Loop Controlling bHLH Complexes Is Involved in Vascular Cell Division and Differentiation in the Root Apical Meristem

• Published in: Current biology 2015-12, Vol.25 (23), p.3144-3150
• Main Authors: Katayama, Hirofumi, Iwamoto, Kuninori, Kariya, Yuka, Asakawa, Tomohiro, Kan, Toshiyuki, Fukuda, Hiroo, Ohashi-Ito, Kyoko
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Basic Helix-Loop-Helix Transcription Factors - genetics; Basic Helix-Loop-Helix Transcription Factors - metabolism; Cell Differentiation; Cell Division; Gene Expression Regulation, Plant; Meristem - genetics; Meristem - growth & development; Meristem - metabolism; Plant Roots - genetics; Plant Roots - growth & development; Plant Roots - metabolism; Xylem - genetics; Xylem - growth & development; Xylem - metabolism
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2015.10.051

Controlling cell division and differentiation in meristems is essential for proper plant growth. Two bHLH heterodimers consisting of LONESOME HIGHWAY (LHW) and TARGET OF MONOPTEROS 5 (TMO5)/TMO5-LIKE1 (T5L1) regulate periclinal cell division in vascular cells in the root apical meristem (RAM) [1–5]. In this study, we further investigated the functions of LHW-T5L1, finding that in addition to controlling cell division, this complex regulates xylem differentiation in the RAM via a novel negative regulatory system. LHW-T5L1 upregulated the thermospermine synthase gene ACAULIS5 (ACL5), as well as SUPPRESSOR OF ACAULIS5 LIKE3 (SACL3), which encodes a bHLH protein, in the RAM. The SACL3 promoter sequence contains a conserved upstream open reading frame (uORF) [6], which blocked translation of the main SACL3 ORF in the absence of thermospermine. Thermospermine eliminated the negative effect of uORF and enhanced SACL3 production. Further genetic and molecular biological analyses indicated that ACL5 and SACL3 suppress the function of LHW-T5L1 through a protein-protein interaction between LHW and SACL3. Finally, we showed that a negative feedback loop consisting of LHW-T5L1, ACL5, SACL3, and LHW-SACL3 contributes to maintain RAM size and proper root growth. These findings suggest that a negative feedback loop regulates the LHW-T5L1 output level to coordinate cell division and differentiation in a cell-autonomous manner. •LHW-T5L1 upregulates the thermospermine synthase gene ACL5, as well as SACL3•Thermospermine increases the production of SACL3, a bHLH protein•SACL3 physically interacts with LHW and inhibits LHW-T5L1 functions•This negative feedback loop is involved in vascular cell division and differentiation Katayama et al. show a novel negative feedback loop regulating a bHLH complex LHW-T5L1 in the Arabidopsis root apical meristem. LHW-T5L1 is a key regulator of xylem differentiation and vascular cell proliferation. This negative feedback mechanism contributes to coordinate vascular cell division and differentiation in the root apical meristem.