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Dickinson, A. J.

Publications and source records attributed to Dickinson, A. J..

5 recordsLinked to original sources

Computational method for mapping mass signatures along developmental gradients reveals a novel role for a monosaccharide tetrose in maize salt-stress response.

Metabolic processes are essential for regulating and maintaining developmental transitions, from stem cell quiescence through differentiation. However, the distinct metabolite-driven mechanisms that are critical for development remain poorly characterized due to inherent challenges in measuring their production, localization, and function in situ. We employed desorption electrospray ionization mass spectrometry imaging (DESI-MSI) to map metabolites in the developing maize root, which has a well-characterized longitudinal gradient that encompasses developmental transitions from quiescence through proliferation and maturation. DESI-MSI enables in situ analysis of the chemical composition of tissue sections with high spatial resolution ([~]50-100 {micro}m). To identify metabolites with specific developmental enrichment patterns, we developed a computational approach called Developmental Imaging Mass Spectrometry Pipeline for Linear Evaluation (DIMPLE). DIMPLE processes mass signatures along linear gradients, generating clusters of metabolites with specific developmental enrichment patterns in the maize root. We employed this method to compare developmental enrichment of metabolites in a salt-resilient maize variety, Oaxacan Green, and a salt-susceptible variety, B73. DIMPLE identifies specific differences in the mass signatures and the overall enrichment patterns between these varieties. DIMPLE also revealed a metabolite, D-erythrose, that had different localization patterns in these varieties. We found that in salt-sensitive maize varieties, treatment with D-erythrose improves stress tolerance by increasing primary root length. Overall, DIMPLE enables comprehensive and rapid analysis of metabolite patterns along a linear gradient, revealing new biology in plant growth and stress response.

plant biology↗

Chemical Imaging Reveals Diverse Functions of Tricarboxylic Acid Metabolites in Root Growth and Development

Understanding how plants grow is critical for agriculture and fundamental for illuminating principles of multicellular development 1. Here, we apply chemical mapping of the developing maize root using desorption electrospray ionization mass spectrometry imaging (DESI-MSI) 2. This technique reveals a range of small molecule distribution patterns across the gradient of stem cell differentiation in the root. To understand the developmental logic of these patterns, we examined tricarboxylic acid (TCA) cycle metabolites. In both Arabidopsis and maize, TCA metabolites are enriched in developmentally opposing regions, suggesting that stem-cell specific TCA metabolite localization may be conserved in evolutionarily divergent species. We find that these metabolites, particularly succinate, aconitate, citrate, and -ketoglutarate, control root development in diverse and distinct ways. Critically, the effects of metabolites on stem cell behavior can be independent of their canonical role in ATP production. These results present new insights into development and suggest practical means for controlling plant growth.

plant biology↗

A plant lipocalin is required for retinal-mediated de novo root organogenesis

Branching of root systems enables the exploration and colonization of the soil environment. In Arabidopsis roots, de novo organogenesis of lateral roots is patterned by an oscillatory mechanism called the root clock, which is dependent on metabolites derived from the {beta}-carotene pathway1, 2. Retinoids are {beta}-carotene-derived regulators of organogenesis in the animal kingdom. To determine if retinoids function in plant development, we conducted time-lapse imaging of a chemical reporter for retinoid binding proteins. We found that it oscillates with a comparable frequency to the root clock and accurately predicts sites of lateral root organogenesis. Exogenous application of retinal to wild-type plants is sufficient to induce root clock oscillations and lateral root organogenesis. A homology search yielded a potential Arabidopsis homolog, TEMPERATURE INDUCED LIPOCALIN (TIL) to vertebrate retinoid binding proteins. Genetic analysis indicates that TIL is necessary for normal lateral root development and a til mutant has decreased retinal sensitivity. TIL expression in a heterologous system conferred retinal binding activity, suggesting that it may directly interact with this molecule. Together, these results demonstrate an essential role for retinal and for plant retinal binding proteins in lateral root organogenesis.

plant biology↗

Anchorene is an endogenous diapocarotenoid required for anchor root formation in Arabidopsis

Arabidopsis root development is predicted to be regulated by yet unidentified carotenoid-derived metabolite(s). In this work, we screened known and putative carotenoid cleavage products and identified anchorene, a predicted carotenoid-derived dialdehyde (diapocarotenoid) that triggers anchor root development. Anchor roots are the least characterized type of root in Arabidopsis. They form at the root-shoot junction, particularly upon damage to the root apical meristem. Using Arabidopsis reporter lines, mutants and chemical inhibitors, we show that anchor roots originate from pericycle cells and that the development of this root type is auxin-dependent and requires carotenoid biosynthesis. Transcriptome analysis and treatment of auxin-reporter lines indicate that anchorene triggers anchor root development by modulating auxin homeostasis. Exogenous application of anchorene restored anchor root development in carotenoid-deficient plants, indicating that this compound is the carotenoid-derived signal required for anchor root development. Chemical modifications of anchorene led to a loss of anchor root promoting activity, suggesting that this compound is highly specific. Furthermore, we demonstrate by LC-MS analysis that anchorene is a natural, endogenous Arabidopsis metabolite. Taken together, our work reveals a new member of the family of carotenoid-derived regulatory metabolites and hormones.\n\nSignificanceUnknown carotenoid-derived compounds are predicted to regulate different aspects of plant development. Here, we characterize the development of anchor roots, the least characterized root type in Arabidopsis, and show that this process depends on auxin and requires a carotenoid-derived metabolite. We identified a presumed carotenoid-derivative, anchorene, as the likely, specific signal involved in anchor root formation. We further show that anchorene is a natural metabolite that occurs in Arabidopsis. Based on the analysis of auxin reporter lines and transcriptome data, we provide evidence that anchorene triggers the growth of anchor roots by modulating auxin homeostasis. Taken together, our work identifies a novel carotenoid-derived growth regulator with a specific developmental function.

plant biology↗

β-cyclocitral is a natural root growth regulator

Natural compounds capable of increasing root depth and branching are desirable tools for enhancing stress tolerance in crops. We devised a sensitized screen to identify natural metabolites capable of regulating root traits in Arabidopsis. {beta}-cyclocitral, an endogenous root compound, was found to promote cell divisions in root meristems and stimulate lateral root branching. {beta}-cyclocitral rescued meristematic cell divisions in ccd1ccd4 biosynthesis mutants and {beta}-cyclocitral-driven root growth was found to be independent of auxin, brassinosteroid, and ROS signaling pathways. {beta}-cyclocitral had a conserved effect on root growth in tomato and rice and generated significantly more compact crown root systems in rice. Moreover, {beta}-cyclocitral treatment enhanced plant vigor in rice plants exposed to salt-contaminated soil. These results indicate that {beta}-cyclocitral is a broadly effective root growth promoter in both monocots and eudicots and could be a valuable tool to enhance crop vigor under environmental stress.\n\nOne Sentence Summary{beta}-cyclocitral is a metabolite of {beta}-carotene that was identified using a sensitized chemical screen and acts broadly across plants to enhance root growth and branching.

developmental biology↗