The phytohormone auxin controls many processes in plants, at least in part through its regulation of cell expansion¹. The acid growth hypothesis has been proposed to explain auxin-stimulated cell expansion for five decades, but the mechanism that underlies auxin-induced cell-wall acidification is poorly characterized. Auxin induces the phosphorylation and activation of the plasma membrane H⁺-ATPase that pumps protons into the apoplast², yet how auxin activates its phosphorylation remains unclear. Here we show that the transmembrane kinase (TMK) auxin-signalling proteins interact with plasma membrane H⁺-ATPases, inducing their phosphorylation, and thereby promoting cell-wall acidification and hypocotyl cell elongation in Arabidopsis. Auxin induced interactions between TMKs and H⁺-ATPases in the plasma membrane within seconds, as well as TMK-dependent phosphorylation of the penultimate threonine residue on the H+-ATPases. Our genetic, biochemical and molecular evidence demonstrates that TMKs directly phosphorylate plasma membrane H⁺-ATPase and are required for auxin-induced H⁺-ATPase activation, apoplastic acidification and cell expansion. Thus, our findings reveal a crucial connection between auxin and plasma membrane H⁺-ATPase activation in regulating apoplastic pH changes and cell expansion through TMK-based cell surface auxin signalling.

The developmental plasticity of plants relies on the remarkable ability of the meristems to integrate nutrient and energy availability with environmental signals. Meristems in root and shoot apexes share highly similar molecular players but are spatially separated by soil. Whether and how these two meristematic tissues have differential activation requirements for local nutrient, hormone, and environmental cues (e.g., light) remain enigmatic in photosynthetic plants. Here, we report that the activation of root and shoot apexes relies on distinct glucose and light signals. Glucose energy signaling is sufficient to activate target of rapamycin (TOR) kinase in root apexes. In contrast, both the glucose and light signals are required for TOR activation in shoot apexes. Strikingly, exogenously applied auxin is able to replace light to activate TOR in shoot apexes and promote true leaf development. A relatively low concentration of auxin in the shoot and high concentration of auxin in the root might be responsible for this distinctive light requirement in root and shoot apexes, because light is required to promote auxin biosynthesis in the shoot. Furthermore, we reveal that the small GTPase Rho-related protein 2 (ROP2) transduces light-auxin signal to activate TOR by direct interaction, which, in turn, promotes transcription factors E2Fa,b for activating cell cycle genes in shoot apexes. Consistently, constitutively activated ROP2 plants stimulate TOR in the shoot apex and cause true leaf development even without light. Together, our findings establish a pivotal hub role of TOR signaling in integrating different environmental signals to regulate distinct developmental transition and growth in the shoot and root. Significance The modulation of growth and development is central to sessile plants. Shoot and root meristems share almost identical molecular machineries but are responsible for different types of aboveground and underground organogenesis. How two such highly similar biological systems respond to different environmental cues and regulate distinct developmental programs remains largely unknown. We report that, in harmony with nature, the shoot, but not the root, demands light for the activation of cell proliferation during organogenesis. We decipher the underlying mechanism that light is necessary for continuous auxin biosynthesis only in the shoot, but not the root, to activate target of rapamycin (TOR) kinase signaling. We further elucidate an auxin-Rho-related protein 2 (ROP2)-TOR-transcription factors E2Fa,b signaling cascade that integrates different environmental signals to orchestrate plant growth and development.

Protein phosphorylation modification is crucial for signaling transduction in plant development and environmental adaptation. By precisely phosphorylating crucial components in signaling cascades, plants can switch on and off the specific signaling pathways needed for growth or defense. Here, we have summarized recent findings of key phosphorylation events in typical hormone signaling and stress responses. More interestingly, distinct phosphorylation patterns on proteins result in diverse biological functions of these proteins. Thus, we have also highlighted latest findings that show how the different phosphosites of a protein, also named phosphocodes, determine the specificity of downstream signaling in both plant development and stress responses.

Age and wounding are two major determinants for regeneration. In plants, the root regeneration is triggered by wound-induced auxin biosynthesis. As plants age, the root regenerative capacity gradually decreases. How wounding leads to the auxin burst and how age and wound signals collaboratively regulate root regenerative capacity are poorly understood. Here, we show that the increased levels of three closely-related miR156-targeted Arabidopsis (Arabidopsis thaliana) SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors, SPL2, SPL10, and SPL11, suppress root regeneration with age by inhibiting wound-induced auxin biosynthesis. Mechanistically, we find that a subset of APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) transcription factors including ABSCISIC ACID REPRESSOR1 and ERF109 is rapidly induced by wounding and serves as a proxy for wound signal to induce auxin biosynthesis. In older plants, SPL2/10/11 directly bind to the promoters of AP2/ERFs and attenuates their induction, thereby dampening auxin accumulation at the wound. Our results thus identify AP2/ERFs as a hub for integration of age and wound signal for root regeneration.

Significance: Development in multicellular organisms consists of a series of cell divisions followed by cell expansions, which are tightly controlled both spatially and temporally. Disorganized cell division causes serious growth defects in both animals and plants. Auxin has been repeatedly implicated in regulating cell division patterns during organogenesis in plants; however, the underlying mechanisms remain to be further investigated. Here, we demonstrate that auxin signaling controls cell division pattern by activating Mitogen-Activated Protein Kinase (MAPK)-signaling cascade during lateral root development. Our work reveals how signal transduction pathways regulate cell division pattern and also provides a connection between auxin signaling and MAPK signaling in plants.