MAC3A and MAC3B mediate degradation of the transcription factor ERF13 and thus promote lateral root emergence.

Lateral roots (LRs) increase root surface area and allow plants greater access to soil water and nutrients. LR formation is tightly regulated by the phytohormone auxin. Whereas the transcription factor ETHYLENE-RESPONSIVE ELEMENT BINDING FACTOR13 (ERF13) prevents LR emergence in Arabidopsis (Arabidopsis thaliana), auxin activates MITOGEN-ACTIVATED PROTEIN KINASE14 (MPK14), which leads to ERF13 degradation and ultimately promotes LR emergence. In this study, we discovered interactions between ERF13 and the E3 ubiquitin ligases MOS4-ASSOCIATED COMPLEX 3A (MAC3A) and MAC3B. As MAC3A and MAC3B gradually accumulate in the LR primordium, ERF13 levels gradually decrease. We demonstrate that MAC3A and MAC3B ubiquitinate ERF13, leading to its degradation and accelerating the transition of LR primordia from stage IV to stage V. Auxin enhances the MAC3A and MAC3B interaction with ERF13 by facilitating MPK14-mediated ERF13 phosphorylation. In summary, this study reveals the molecular mechanism by which auxin eliminates the inhibitory factor ERF13 through the MPK14-MAC3A and MAC3B signaling module, thus promoting LR emergence.

VIK-Mediated Auxin Signaling Regulates Lateral Root Development in Arabidopsis.

The crucial role of TIR1-receptor-mediated gene transcription regulation in auxin signaling has long been established. In recent years, the significant role of protein phosphorylation modifications in auxin signal transduction has gradually emerged. To further elucidate the significant role of protein phosphorylation modifications in auxin signaling, a phosphoproteomic analysis in conjunction with auxin treatment has identified an auxin activated Mitogen-activated Protein Kinase Kinase Kinase (MAPKKK) VH1-INTERACTING Kinase (VIK), which plays an important role in auxin-induced lateral root (LR) development. In the vik mutant, auxin-induced LR development is significantly attenuated. Further investigations show that VIK interacts separately with the positive regulator of LR development, LATERAL ORGAN BOUNDARIES-DOMAIN18 (LBD18), and the negative regulator of LR emergence, Ethylene Responsive Factor 13 (ERF13). VIK directly phosphorylates and stabilizes the positive transcription factor LBD18 in LR formation. In the meantime, VIK directly phosphorylates the negative regulator ERF13 at Ser168 and Ser172 sites, causing its degradation and releasing the repression by ERF13 on LR emergence. In summary, VIK-mediated auxin signaling regulates LR development by enhancing the protein stability of LBD18 and inducing the degradation of ERF13, respectively.

MPK14-mediated auxin signaling controls lateral root development via ERF13-regulated very-long-chain fatty acid biosynthesis.

Auxin plays a critical role in lateral root (LR) formation. The signaling module composed of auxin-response factors (ARFs) and lateral organ boundaries domain transcription factors mediates auxin signaling to control almost every stage of LR development. Here, we show that auxin-induced degradation of the APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factor ERF13, dependent on MITOGEN-ACTIVATED PROTEIN KINASE MPK14-mediated phosphorylation, plays an essential role in LR development. Overexpression of ERF13 results in restricted passage of the LR primordia through the endodermal layer, greatly reducing LR emergence, whereas the erf13 mutants showed an increase in emerged LR. ERF13 inhibits the expression of 3-ketoacyl-CoA synthase16 (KCS16), which encodes a fatty acid elongase involved in very-long-chain fatty acid (VLCFA) biosynthesis. Overexpression of KCS16 or exogenous VLCFA treatment rescues the LR emergence defects in ERF13 overexpression lines, indicating a role downstream of the auxin-MPK14-ERF13 signaling module. Collectively, our study uncovers a novel molecular mechanism by which MPK14-mediated auxin signaling modulates LR development via ERF13-regulated VLCFA biosynthesis.