Plants are necessarily highly competitive and have finely tuned mechanisms to adjust growth and development in accordance with opportunities and limitations in their environment. Sugars from photosynthesis form an integral part of this growth control process, acting as both an energy source and as signaling molecules in areas targeted for growth. The plant hormone auxin similarly functions as a signaling molecule and a driver of growth and developmental processes. Here, we show that not only do the two act in concert but that auxin metabolism is itself regulated by the availability of free sugars. The regulation of the biosynthesis and degradation of the main auxin, indole-3-acetic acid (IAA), by sugars requires changes in the expression of multiple genes and metabolites linked to several IAA biosynthetic pathways. The induction also involves members of the recently described central regulator PHYTOCHROME-INTERACTING FACTOR transcription factor family. Linking these three known regulators of growth provides a model for the dynamic coordination of responses to a changing environment.

Significance: Understanding how hormones like auxin control plant growth and development has fascinated scientists since Darwin. The past two decades have seen breakthroughs in elucidating the molecular basis of auxin transport, perception, and response, but little is known about how auxin is metabolized or its homeostasis is controlled. We report that the DIOXYGENASE FOR AUXIN OXIDATION 1 ( AtDAO1 ) enzyme represents the major pathway for auxin oxidation in Arabidopsis . Disrupting AtDAO1 function elevates levels of auxin conjugates between ∼50- and 280-fold, but auxin levels remain close to the WT, helping explain why mutant phenotypes are relatively weak. We conclude that AtDAO1 and auxin conjugation pathways play highly redundant roles and reveal a level of regulation of auxin abundance in plants.

The plant hormone auxin plays a crucial role in regulating plant development and plant architecture. The directional auxin distribution within tissues depends on PIN transporters that are polarly localized on the plasma membrane. The PIN polarity and the resulting auxin flow directionality are mediated by the antagonistic actions of PINOID kinase and protein phosphatase 2A. However, the contribution of the PIN phosphorylation to the polar PIN sorting is still unclear. Here, we identified an evolutionarily conserved phosphorylation site within the central hydrophilic loop of PIN proteins that is important for the apical and basal polar PIN localizations. Inactivation of the phosphorylation site in PIN1(Ala) resulted in a predominantly basal targeting and increased the auxin flow to the root tip. In contrast, the outcome of the phosphomimic PIN1(Asp) manipulation was a constitutive, PINOID-independent apical targeting of PIN1 and an increased auxin flow in the opposite direction. Furthermore, the PIN1(Asp) functionally replaced PIN2 in its endogenous expression domain, revealing that the phosphorylation-dependent polarity regulation contributes to functional diversification within the PIN family. Our data suggest that PINOID-independent PIN phosphorylation at one single site is adequate to change the PIN polarity and, consequently, to redirect auxin fluxes between cells and provide the conceptual possibility and means to manipulate auxin-dependent plant development and architecture.

Organ formation in animals and plants relies on precise control of cell state transitions to turn stem cell daughters into fully differentiated cells. In plants, cells cannot rearrange due to shared cell walls. Thus, differentiation progression and the accompanying cell expansion must be tightly coordinated across tissues. PLETHORA (PLT) transcription factor gradients are unique in their ability to guide the progression of cell differentiation at different positions in the growing Arabidopsis thaliana root, which contrasts with well-described transcription factor gradients in animals specifying distinct cell fates within an essentially static context. To understand the output of the PLT gradient, we studied the gene set transcriptionally controlled by PLTs. Our work reveals how the PLT gradient can regulate cell state by region-specific induction of cell proliferation genes and repression of differentiation. Moreover, PLT targets include major patterning genes and autoregulatory feedback components, enforcing their role as master regulators of organ development.