TDIF peptides regulate root growth by affecting auxin homeostasis and PINs expression in Arabidopsis thaliana

TDIF and TDIF-like peptides in excess simultaneously facilitate primary root elongation and lateral root formation through regulating auxin distribution and transport. Tracheary element differentiation inhibitory factor (TDIF) plays key roles in mediating cell-cell communication and stem cell maintenance during vascular development. Recently, TDIF has also been linked to lateral root (LR) organogenesis through Brassinosteroid Insensitive 2 (BIN2) action. In this work, by comparing the in vitro and in vivo activities of AtCLE41-encoded TDIF and one poplar-derived TDIF-like peptide in Arabidopsis thaliana, we demonstrated that both TDIFs promoted primary root (PR) growth and stimulated LR formation. Without affecting auxin biosynthesis and catabolism, TDIFs suppressed the auxin maxima at PR apex but intensified the auxin accumulation at LR initiation sites along the longitudinal axis of PR. TDIF did not alter root sensitivity to exogenous auxin and mutants with varied endogenous auxin levels responded to TDIF peptides in a wild-type manner but to a lesser extent. Intriguingly, TDIF specifically upregulated the transcript abundance of PINs and multiple pin mutants displayed insensitivity to TDIF, demonstrating that PIN-mediated polar auxin transport (PAT) is indispensably required for the TDIF-induced root phenotypes. Taken together, our results revealed that TDIF might target PAT via mobilizing auxin efflux carriers to dynamically regulate the auxin signaling output and hence facilitate PR growth and LR formation.