Search

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]

In Arabidopsis thaliana , local wounding and herbivore feeding provoke leaf-to-leaf propagating Ca2+ waves that are dependent on the activity of members of the glutamate receptor-like channels (GLRs). In systemic tissues, GLRs are needed to sustain the synthesis of jasmonic acid (JA) with the subsequent activation of JA-dependent signaling response required for the plant acclimation to the perceived stress. Even though the role of GLRs is well established, the mechanism through which they are activated remains unclear. Here, we report that in vivo , the amino-acid-dependent activation of the At GLR3.3 channel and systemic responses require a functional ligand-binding domain. By combining imaging and genetics, we show that leaf mechanical injury, such as wounds and burns, as well as hypo-osmotic stress in root cells, induces the systemic apoplastic increase of L-glutamate (L-Glu), which is largely independent of At GLR3.3 that is instead required for systemic cytosolic Ca2+ elevation. Moreover, by using a bioelectronic approach, we show that the local release of minute concentrations of L-Glu in the leaf lamina fails to induce any long-distance Ca2+ waves. [Display omitted] • Plant glutamate receptor-like channel At GLR3.3 is gated by exogenous amino acids • At GLR3.3 ligand-binding domain is essential for channel activation • Leaf injury and osmotic stress induce L-Glu systemic elevation activating At GLR3.3 • Local activation of GLRs does not trigger long-distance Ca2+ waves In Arabidopsis thaliana , mechanical stresses induce long-distance Ca2+ signals mediated by the glutamate receptor-like 3.3 channel. Grenzi et al. show that the stress-induced systemic increase of apoplastic L-glutamate, in a submillimolar range of concentrations, gates the At GLR3.3 through its ligand-binding domain. [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]