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Biology subjects

Band, L. R.

Publications and source records attributed to Band, L. R..

4 recordsLinked to original sources

Mathematical modeling of SUMOylation reveals tissue-specific and dynamic responses to abiotic stress

SUMOylation is an essential and evolutionarily conserved post-translational modification that enables rapid cellular adaptation to environmental stress. Despite its importance, how the SUMOylation machinery controls its dynamics remains poorly understood. Here, we integrated a mathematical model of the plant SUMO cycle with quantitative imaging and biochemical data to decode the regulatory logic of SUMOylation dynamics. The model reveals a fundamental principle: steady-state SUMOylation levels are determined not by the full complement of SUMO-cycle components, but by the abundance of SUMO modifier proteins and E1 enzymes, together with SUMO protease abundance and activity. Strikingly, when we integrated fluorescence measurements from reporters for SUMO-cycle components in Arabidopsis roots after three hours of abiotic stress, the model predicted decreased SUMOylation levels across several tissues, contrary to prevailing evidence. Motivated by this unexpected prediction, we performed time-resolved imaging to better characterize the dynamics of key SUMO-cycle components after salt and osmotic stress. These data revealed highly dynamic component levels within the first three hours of stress that were not captured in the previous measurements. Incorporating this temporal data into the model uncovered a twin-peaked SUMOylation response to salt stress: an early surge underpinned by protease dynamics, followed by a decline and a second peak driven by elevated SUMO modifier and E2 levels. Western blot analysis revealed a corresponding twin-peaked pattern of SUMOylation. Together, our findings demonstrate that the plant SUMO cycle is a highly dynamic system that achieves tissue- and stress-specific control of SUMOylation through the coordinated interplay of multiple SUMO-cycle components.

plant biology↗

Water stress adaptive responses in plants require movement of ABA and AB-aldehyde from vascular to target tissues

Vascular plants rapidly coordinate root and shoot responses to water stress. Abscisic acid (ABA) mediates these adaptations; however, it remains unclear which cells produce ABA, whether ABA synthesis shifts during stress, and whether ABA movement is required for its adaptive functions. Here, we map ABA biosynthesis at cellular resolution in Arabidopsis and report that water-stress adaptive responses in roots and shoots require movement of ABA and its precursor AB-aldehyde from vascular tissues to target cells. We suggest that ABA accumulation arises from two parallel routes: (i) ABA synthesized in the vasculature via ABA2 and AAO3, then moving to guard cells, and (ii) phloem-derived AB-aldehyde being converted to ABA in the epidermis or bundle sheath by AAO1 and AAO2. Finally, we predict that tightly packed cells beneath leaf veins facilitate efficient ABA delivery to guard cells, an anatomical arrangement that has enabled angiosperms to evolve the use of ABA to rapidly close stomata.

plant biology↗

Elucidating tissue and sub-cellular specificity of the entire SUMO network reveals how stress responses are fine-tuned in a eukaryote

SUMOylation is essential in plant and animal cells, but it remains unknown how SUMO components act in concert to modify specific targets in response to environmental stresses. In this study we characterise every SUMO component in the Arabidopsis root to create the first complete SUMO Cell Atlas in eukaryotes. This unique resource reveals wide spatial variation, where SUMO proteins and proteases have sub-functionalized in both their expression and subcellular localisation. During stress SUMO conjugation is mainly driven by tissue specific regulation of the SUMO E2 ligase. Stress-specific modulation of the SUMO pathway reveals unique combinations of Proteases being targeted for regulation in distinct root tissues by salt, osmotic and biotic signals. Our SUMO Cell Atlas resources reveal how this PTM influences cellular and tissue scale adaptations during root development and stress responses. We provide the first comprehensive study elucidating how multiple stress inputs can regulate an entire PTM system.

plant biology↗

A balance of metabolism and diffusion articulates a gibberellin hormone gradient in the Arabidopsis root

The plant hormone gibberellin (GA4) regulates numerous developmental processes. Within the root, GA4 controls growth, in part, by controlling the extent of cell elongation. The nlsGPS1 FRET biosensor revealed a GA4 gradient within the Arabidopsis root growth zones, with GA4 levels correlating with cell length. We developed a multiscale mathematical model to understand how biosynthesis, catabolism and transport create the GA4 distribution within the root growth zones. The model showed that phloem delivery of the biosynthetic intermediate GA12 contributes to higher levels of bioactive GA4 in the elongation zone, with the GA4 synthesis pattern being further modified by local GA12 synthesis in the quiescent centre region and the spatial distribution of biosynthesis enzymes (GA20ox and GA3ox). Model predictions revealed that whilst GA20ox and GA3ox transcript is present throughout the growth zones, these enzymes are inactive in the dividing cells, which explains steep GA4 gradients observed in GA20ox and GA3ox over-expression lines, and improves agreement between model predictions and data in wildtype, ga20ox and ga3ox lines. The model revealed that the GA4 gradient also depends a balance of diffusion through plasmodesmata and catabolism. Both model predictions and biosensor data demonstrated that plasmodesmatal diffusion enables a more gradual GA4 gradient, with higher diffusion antagonizing the GA4 gradient. Model predictions suggested that catabolism limits GA4 levels, which we validated via biosensor imaging in the ga2oxhept mutant. We concluded that GA4 distribution mediates root growth programming via local GA4 synthesis combining with diffusion and catabolism to create a spatial gradient that provides positional information and patterns cell elongation.

plant biology↗