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Lateral root initiation requires the accumulation of auxin in lateral root founder cells, yielding a local auxin maximum. The positioning of auxin maxima along the primary root determines the density and spacing of lateral roots. The GOLVEN6 (GLV6) and GLV10 signaling peptides and their receptors have been established as regulators of lateral root spacing via their inhibitory effect on lateral root initiation in Arabidopsis. However, it was unclear how these GLV peptides interfere with auxin signaling or homeostasis. Here, we show that GLV6/10 signaling regulates the expression of a subset of auxin response genes, downstream of the canonical auxin signaling pathway, while simultaneously inhibiting the establishment of auxin maxima within xylem-pole pericycle cells that neighbor lateral root initiation sites. We present genetic evidence that this inhibitory effect relies on the activity of the PIN3 and PIN7 auxin export proteins. Furthermore, GLV6/10 peptide signaling was found to enhance PIN7 abundance in the plasma membranes of xylem-pole pericycle cells, which likely stimulates auxin efflux from these cells. Based on these findings, we propose a model in which the GLV6/10 signaling pathway serves as a negative feedback mechanism that contributes to the robust patterning of auxin maxima along the primary root. [ABSTRACT FROM AUTHOR]

Summary: Indole‐3‐acetic acid (IAA) controls a plethora of developmental processes. Thus, regulation of its concentration is of great relevance for plant performance. Cellular IAA concentration depends on its transport, biosynthesis and the various pathways for IAA inactivation, including oxidation and conjugation.Group II members of the GRETCHEN HAGEN 3 (GH3) gene family code for acyl acid amido synthetases catalysing the conjugation of IAA to amino acids. However, the high degree of functional redundancy among them has hampered thorough analysis of their roles in plant development.In this work, we generated an Arabidopsis gh3.1,2,3,4,5,6,9,17 (gh3oct) mutant to knock out the group II GH3 pathway. The gh3oct plants had an elaborated root architecture, showed an increased tolerance to different osmotic stresses, including an IAA‐dependent tolerance to salinity, and were more tolerant to water deficit. Indole‐3‐acetic acid metabolite quantification in gh3oct plants suggested the existence of additional GH3‐like enzymes in IAA metabolism. Moreover, our data suggested that 2‐oxindole‐3‐acetic acid production depends, at least in part, on the GH3 pathway. Targeted stress‐hormone analysis further suggested involvement of abscisic acid in the differential response to salinity of gh3oct plants.Taken together, our data provide new insights into the roles of group II GH3s in IAA metabolism and hormone‐regulated plant development. [ABSTRACT FROM AUTHOR]

Summary: The levels of the important plant growth regulator indole‐3‐acetic acid (IAA) are tightly controlled within plant tissues to spatiotemporally orchestrate concentration gradients that drive plant growth and development. Metabolic inactivation of bioactive IAA is known to participate in the modulation of IAA maxima and minima.IAA can be irreversibly inactivated by oxidation and conjugation to aspartate and glutamate. Usually overlooked because of its reversible nature, the most abundant inactive IAA form is the IAA‐glucose (IAA‐glc) conjugate.Glycosylation of IAA in Arabidopsis thaliana is reported to be carried out by UDP‐glycosyltransferase 84B1 (UGT84B1), while UGT74D1 has been implicated in the glycosylation of the irreversibly formed IAA catabolite oxIAA.Here we demonstrated that both UGT84B1 and UGT74D1 modulate IAA levels throughout plant development by dual IAA and oxIAA glycosylation. Moreover, we identified a novel UGT subfamily whose members redundantly mediate the glycosylation of oxIAA and modulate skotomorphogenic growth. [ABSTRACT FROM AUTHOR]

Summary: The plant hormone auxin is a key factor for regulation of plant development, and this function was probably reinforced during the evolution of early land plants. We have extended the available toolbox to allow detailed studies of how auxin biosynthesis and responses are regulated in moss reproductive organs, their stem cells and gametes to better elucidate the function of auxin in the morphogenesis of early land plants.We measured auxin metabolites and identified IPyA (indole‐3‐pyruvic acid) as the main biosynthesis pathway in Physcomitrium (Physcomitrella) patens and established knock‐out, overexpressor and reporter lines for biosynthesis genes which were analyzed alongside previously reported auxin‐sensing and transport reporters.Vegetative and reproductive apical stem cells synthesize auxin. Sustained stem cell activity depends on an inability to sense the auxin produced while progeny of the stem cells respond to the auxin, aiding in the control of cell division, expansion and differentiation. Gamete precursors are dependent on a certain degree of auxin sensing, while the final differentiation is a low auxin‐sensing process.Tha data presented indicate that low auxin activity may represent a conserved hallmark of land plant gametes, and that local auxin biosynthesis in apical stem cells may be part of an ancestral mechanism to control focal growth. [ABSTRACT FROM AUTHOR]

Summary: Dynamic regulation of the concentration of the natural auxin (IAA) is essential to coordinate most of the physiological and developmental processes and responses to environmental changes. Oxidation of IAA is a major pathway to control auxin concentrations in angiosperms and, along with IAA conjugation, to respond to perturbation of IAA homeostasis. However, these regulatory mechanisms remain poorly investigated in conifers. To reduce this knowledge gap, we investigated the different contributions of the IAA inactivation pathways in conifers.MS‐based quantification of IAA metabolites under steady‐state conditions and after perturbation was investigated to evaluate IAA homeostasis in conifers. Putative Picea abies GH3 genes (PaGH3) were identified based on a comprehensive phylogenetic analysis including angiosperms and basal land plants. Auxin‐inducible PaGH3 genes were identified by expression analysis and their IAA‐conjugating activity was explored.Compared to Arabidopsis, oxidative and conjugative pathways differentially contribute to reduce IAA concentrations in conifers. We demonstrated that the oxidation pathway plays a marginal role in controlling IAA homeostasis in spruce. By contrast, an excess of IAA rapidly activates GH3‐mediated irreversible conjugation pathways.Taken together, these data indicate that a diversification of IAA inactivation mechanisms evolved specifically in conifers. [ABSTRACT FROM AUTHOR]

Morphological variation is the basis of natural diversity and adaptation. For example, angiosperms (flowering plants) evolved during the Cretaceous period more than 100 mya and quickly colonized terrestrial habitats [ 1 ]. A major reason for their astonishing success was the formation of fruits, which exist in a myriad of different shapes and sizes [ 2 ]. Evolution of organ shape is fueled by variation in expression patterns of regulatory genes causing changes in anisotropic cell expansion and division patterns [ 3–5 ]. However, the molecular mechanisms that alter the polarity of growth to generate novel shapes are largely unknown. The heart-shaped fruits produced by members of the Capsella genus comprise an anatomical novelty, making it particularly well suited for studies on morphological diversification [ 6–8 ]. Here, we show that post-translational modification of regulatory proteins provides a critical step in organ-shape formation. Our data reveal that the SUMO protease, HEARTBREAK (HTB), from Capsella rubella controls the activity of the key regulator of fruit development, INDEHISCENT (CrIND in C. rubella), via de-SUMOylation. This post-translational modification initiates a transduction pathway required to ensure precisely localized auxin biosynthesis, thereby facilitating anisotropic cell expansion to ultimately form the heart-shaped Capsella fruit. Therefore, although variation in the expression of key regulatory genes is known to be a primary driver in morphological evolution, our work demonstrates how other processes—such as post-translational modification of one such regulator—affects organ morphology. • HTB encodes a SUMO protease required for fruit shape in Capsella • Anisotropic cell growth is suppressed in the fruit valves of the htb mutant • HTB stabilizes CrIND through de-SUMOylation to facilitate local auxin biosynthesis Dong et al. reveal post-translational modification as a so-far-undisclosed driver of morphological diversity. They show that the SUMO protease HEARTBREAK is required to de-SUMOylate a key regulator of fruit-shape determination in Capsella , thereby initiating a transduction pathway leading to local auxin biosynthesis and anisotropic cell growth. [ABSTRACT FROM AUTHOR]

Pollen grains become increasingly independent of the mother plant as they reach maturity through poorly understood developmental programs. We report that the hormone auxin is essential during barley pollen maturation to boost the expression of genes encoding almost every step of heterotrophic energy production pathways. Accordingly, auxin is necessary for the flux of sucrose and hexoses into glycolysis and to increase the levels of pyruvate and two tricarboxylic (TCA) cycle metabolites (citrate and succinate). Moreover, bioactive auxin is synthesized by the pollen-localized enzyme HvYUCCA4, supporting that pollen grains autonomously produce auxin to stimulate a specific cellular output, energy generation, that fuels maturation processes such as starch accumulation. Our results demonstrate that auxin can shift central carbon metabolism to drive plant cell development, which suggests a direct mechanism for auxin's ability to promote growth and differentiation. • Barley pollen autonomously produces high auxin levels to control its maturation • The cereal-specific enzyme HvYUCCA4 synthesizes bioactive auxin in barley pollen • Auxin is required to enhance the expression of central carbon metabolism genes • Increased flux of energy production pathways fuels pollen starch accumulation As cereal pollen grains reach maturity, they form large starch deposits that later nourish them on their way to fertilization. Amanda et al. show that barley pollen produces the hormone auxin to control starch accumulation by enhancing central carbon metabolism pathways that generate energy as ATP, a limiting factor in the synthesis of starch. [ABSTRACT FROM AUTHOR]

Summary Evolution of gene-regulatory sequences is considered the primary driver of morphological variation [ 1–3 ]. In animals, the diversity of body plans between distantly related phyla is due to the differential expression patterns of conserved "toolkit" genes [ 4 ]. In plants, variation in expression domains similarly underlie most of the reported diversity of organ shape both in natural evolution and in the domestication of crops [ 5–9 ]. The heart-shaped fruit from members of the Capsella genus is a morphological novelty that has evolved after Capsella diverged from Arabidopsis ∼8 mya [ 10 ]. Comparative studies of fruit growth in Capsella and Arabidopsis revealed that the difference in shape is caused by local control of anisotropic growth [ 11 ]. Here, we show that sequence variation in regulatory domains of the fruit-tissue identity gene, INDEHISCENT (IND), is responsible for expansion of its expression domain in the heart-shaped fruits from Capsella rubella. We demonstrate that expression of this CrIND gene in the apical part of the valves in Capsella contributes to the heart-shaped appearance. While studies on morphological diversity have revealed the importance of cis -regulatory sequence evolution, few examples exist where the downstream effects of such variation have been characterized in detail. We describe here how CrIND exerts its function on Capsella fruit shape by binding sequence elements of auxin biosynthesis genes to activate their expression and ensure auxin accumulation into highly localized maxima in the fruit valves. Thus, our data provide a direct link between changes in expression pattern and altered hormone homeostasis in the evolution of morphological novelty. Highlights • Fruit-shape defect observed in crind mutant is rescued by exogenous auxin application • Auxin dynamics are perturbed in crind mutant • CrIND directly controls expression of auxin-biosynthesis genes in fruit valves • CrIND regulatory sequences contribute to the morphological novelty of Capsella fruits Dong et al. demonstrate that diversification of INDEHISCENT expression in the Capsella genus has contributed to morphological changes of the heart-shaped fruit compared to the cylindrical Arabidopsis fruit and that INDEHISCENT mediates its effect via localized activation of auxin-biosynthesis genes. [ABSTRACT FROM AUTHOR]