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Sainsbury Laboratory

I have long been fascinated by how plants change their physiology and development to suit dynamic environments without a centralised information processing system. In particular, I’ve spent my scientific career investigating how a suite of mobile small molecules, the phytohormones, serve as both signal-integrators and program activators in plants.

After undergraduate research on the phytohormone auxin (with Judy Callis, UC Davis), my PhD was focused on the role of the immune hormone salicylic acid (SA) in both root development and in crosstalk between host plants and a bacterial pathogen that synthesizes SA (with Mary Wildermuth, UC Berkeley). In one project, I developed a promoter-reporter line that is highly sensitive to SA and found evidence of a transient accumulation of SA in the Arabidopsis root tip. In conjunction with my investigations of the mechanism of root growth inhibition by SA, I hypothesized that root tip localized SA carries out an unknown function in root development. In a second project centred on the question of how the pathogen acquires iron from plants, I found that the bacterium has three high-affinity iron acquisition systems. Because a mutant lacking all three remained fully pathogenic, I hypothesized that, unlike many mammalian pathosystems, the pathogen’s environment is relatively iron replete. In both projects, progress on my new hypotheses stalled because I was unable directly quantify the levels of SA or iron with the necessary spatiotemporal resolution using available technologies.

These challenges inspired me to pursue enabling technologies during my postdoc with Wolf Frommer (Department of Plant Biology, Carnegie Institution for Science). I first developed a platform for accelerated engineering of FRET biosensors. Using this platform, I screened over 1,500 biosensor designs and succeeded in generating both an Abscisic Acid Concentration and Uptake Sensor (ABACUS) and Gibberellin Perception Sensor (GPS). A key early finding was determining, for the first time, cell-type and timing of specific ABA dynamics and GA distribution patterns in actively growing Arabidopsis roots.

Biosensor imaging of root tip measuring GA gradient, showing a substantial GA increase in the elongation zone.

Also during my postdoc, I led the completion and analysis of a large-scale protein interactome project (Associomics.org). During the network analysis, bioinformatics, and hypothesis testing phases of the project, the Associomics team in the Frommer lab and seven additional collaborating labs analysed the results of millions of protein-protein interaction tests. Many of our analyses and biological discoveries focused on hormone biology (e.g. hormone receptor trafficking, hormone transporter regulation, and hormone-related interaction networks). The resulting Membrane-based Interactome Network Database added greatly to our knowledge of individual protein-protein interactions and also the characteristics of interactome networks generally (Associomics.org).

My research group at the Sainsbury Laboratory, Cambridge University investigates how plant hormones serve as signal integrators and master regulators of physiology and development. In multicellular organisms, these functions are crucial for the coordination of the activities of individual cells – each having an independently tuneable hormone level and hormone response – into an ensemble behaviour appropriate for the organism as a whole. Our recent advent of ABACUS and GPS biosensors permits analysis of ABA and GA levels with cellular resolution and we are now observing hormone patterns that were previously unknown. We also continue to develop new technologies for high-resolution sensing and perturbation of plant hormones in vivo.

Jones Research Group Website

 

 

Image: Analysis of a gibberellin biosensor expressed in nuclei of an etiolated Arabidopsis seedling.

 

Publications

Walia A*, Carter R*, Wightman R, Meyerowitz EM, Jönsson H†, Jones AM† (2024) Differential growth is an emergent property of mechanochemical feedback mechanisms in curved plant organs. Developmental Cell revisedSSRN: https://ssrn.com/abstract=4677553

Griffiths J, Rizza A, Tang B, Feng L, Frommer WB, Jones AM† (2024) Gibberellin Perception Sensors 1 and 2 reveal the genesis of cellular GA dynamics necessary but not sufficient to pattern hypocotyl cell elongation. Plant Cell accepted. BioRxivhttps://doi.org/10.1101/2023.11.06.565859

Drapek C, Rizza A, Mohd-Radzman N, Schiessl K, Dos Santos Barbosa F, Wen J, Oldroyd GED†, Jones AM† (2024) Cellular gibberellin dynamics govern indeterminate nodule development, morphology and function. Plant Cell accepted BioRxivhttps://doi.org/10.1101/2023.09.09.556959

Rosa-Diaz I, Rowe JH, Cayuela-Lopez A, Arbona V, Diaz I, Jones AM† (2024) Spider mite herbivory induces an abscisic acid-driven stomatal defense. Plant Physiologyhttps://doi.org/10.1093/plphys/kiae215

Larsen, B., Hofmann, R., Camacho, I.S., Clarke, R.W., Lagarias, J.C., Jones, A.R., Jones A.M. (2023) Highlighter is an optogenetic actuator for light-mediated, high resolution gene expression control in plants. PLOS Biologydoi.org/10.1371/journal.pbio.3002303

Rowe, J., Grangé-Guermente, M., Exposito-Rodriguez, M., Wimalasekera, R., Lenz, M., Shetty, K., Cutler, S.R., Jones, A.M. (2023) Next-generation ABACUS biosensors reveal cellular ABA dynamics driving root growth at low aerial humidity. Nature Plantsdoi.org/10.1038/s41477-023-01447-4.

Shi, B., Felipo-Benavent, A., Cerutti, G., Galvan-Ampudia, C., Jilli, L., Brunoud, G., Mutterer, J., Sakvarelidze-Achard, L., Davière, J-M., Navarro-Galiano, A., Walia, A., Lazary, S., Legrand, J., Weinstein, R., Jones, A., Prat, S., Achard, P.†, Vernoux, T.† (2024) A quantitative gibberellin signalling biosensor reveals a role for gibberellins in internode specification at the shoot apical meristem. Nature Comms. https://doi.org/10.1038/s41467-024-48116-4

Kubalová, M., Müller, K.,Dobrev, P.I., Rizza, A., Jones, A.M., Fendrych, M.† (2024) Auxin coreceptor IAA17/AXR3 controls cell elongation in Arabidopsis thaliana root by modulation of auxin and gibberellin perception. New Phytologist. doi.org/10.1111/nph.19557

Dao, T. Q., Drapek, C., Jones, A.M., Leiboff, S. †(2023) Comparing hormone dynamics in cereal crops via transient expression of hormone sensors. In revision. bioRxiv. doi.org/10.1101/2023.11.14.567063

Albuquerque-Martins, R., Szakonyi, D., Rowe, J., *Jones, A.M. and *Duque P. (2022), ABA signaling prevents phosphodegradation of the Arabidopsis SR45 splicing factor to negatively autoregulate inhibition of early seedling development. Plant Communicationsdoi.org/10.3390/life13061386

Mehra, P., Pandey, B.K., Melebari, D., Banda, J., Leftley, N., Couveur, V., Rowe, J., Anfang, M., De Gernier, H., Morris, E., Sturrock, C.J., Mooney, S.J., Swarup, R., Faulkner, C., Beeckman, T., Bhalerao, R.P., Shani, E., Jones, A.M., Dodd, I.C., Sharp, R.E., Sadanandom, A., Draye, X., Bennett, M. J. (2022) Hydraulic flux responsive hormone redistribution determines root branching. Science. 378(6621):762-768. doi.org/10.1126/science.add3771

Pablo Albertos, Tanja Wlk, Jayne Griffiths, Maria J Pimenta Lange, Simon J Unterholzner, Wilfried Rozhon, Theo Lange, Alexander M Jones, Brigitte Poppenberger (2022) Brassinosteroid-regulated bHLH transcription factor CESTA induces the gibberellin 2-oxidase GA2ox7Plant Physiology, Volume 188, Issue 4, April 2022, Pages 2012–2025, doi.org/10.1093/plphys/kiac008

James H Rowe, Annalisa Rizza, Alexander M Jones (2022) Quantifying Phytohormones in Vivo with FRET Biosensors and the FRETENATOR Analysis Toolset. In: Duque, P., Szakonyi, D. (eds) Environmental Responses in Plants. Methods in Molecular Biology, vol 2494. Humana, New York, NY. doi.org/10.1007/978-1-0716-2297-1_17

Martin Balcerowicz, Kartika N. Shetty, Alexander M. Jones (2021) Fluorescent biosensors illuminating plant hormone research, Plant Physiology, Volume 187, Issue 2, October 2021, Pages 590–602, doi.org/10.1093/plphys/kiab278

Cesar L Cuevas-Velazquez, Tamara Vellosillo, Karina Guadalupe, Hermann Broder Schmidt, Feng Yu, David Moses, Jennifer AN Brophy, Dante Cosio-Acosta, Alakananda Das, Lingxin Wang, Alexander M Jones, Alejandra A Covarrubias, Shahar Sukenik, José R Dinneny (2021) Intrinsically disordered protein biosensor tracks the physical-chemical effects of osmotic stress on cells. Nat Commun 12, 5438. doi.org/10.1038/s41467-021-25736-8

Rizza A, Tang B, Stanley CE, Grossmann G, Owen MR, Band LR, Jones AM (2021) Differential biosynthesis and cellular permeability explain longitudinal gibberellin gradients in growing roots. PNAS doi.org/10.1073/pnas.1921960118

Jayne Griffiths, Roberto Hofmann, Alexander M Jones. Signals| Gibberellin Signaling in Plants. Elsevier 2021 doi.org/10.1016/B978-0-12-819460-7.00322-4

James H Rowe, Alexander M Jones. Focus on biosensors: Looking through the lens of quantitative biology. Quantitative Plant Biology 2021 doi.org/10.1017%2Fqpb.2021.10

Martin Balcerowicz, Kartika N Shetty, Alexander M Jones. O auxin, where art thou? Nat Plants 2021. https://doi.org/10.1038/s41477-021-00921-1

Bihai Shi, Amelia Felipo-Benavent, Guillaume Cerutti, Carlos Galvan-Ampudia, Lucas Jilli, Geraldine Brunoud, Jérome Mutterer, Lali Sakvarelidze-Achard, Jean-Michel Davière, Alejandro Navarro-Galiano, Ankit Walia, Shani Lazary, Jonathan Legrand, Roy Weinstein, Alexander M Jones, Salomé Prat, Patrick Achard, Teva Vernoux. A quantitative gibberellin signalling biosensor reveals a role for gibberellins in internode specification at the shoot apical meristem. bioRxiv 2021 https://doi.org/10.1101/2021.06.11.448154

Annalisa Rizza, Alexander M Jones. The makings of a gradient: spatiotemporal distribution of gibberellins in plant development. Current Opinion in Plant Biology 2019. https://doi.org/10.1016/j.pbi.2018.08.001

Annalisa Rizza, Ankit Walia, Bijun Tang, Alexander M Jones. Visualizing Cellular Gibberellin Levels Using the nlsGPS1 Förster Resonance Energy Transfer (FRET) Biosensor. J. Vis. Exp. 2019 (143) https://dx.doi.org/10.3791/58739

Ankit Walia, Rainer Waadt, Alexander Jones. Genetically encoded biosensors in plants: pathways to discovery. Annual Reviews 2018  https://doi.org/10.1146/annurev-arplant-042817-040104

Rizza A, Walia A, Lanquar V, Frommer WB, Jones AM. In vivo gibberellin gradients visualized in rapidly elongating tissues. Nature Plants 2017rdcu.be/wnOh 

Alexander M Jones. A new look at stress: abscisic acid patterns and dynamics at high-resolution. New Phytologist 2015. https://doi.org/10.1111/nph.13552

Alexander M Jones, Yuanhu Xuan, Meng Xu, Rui-Sheng Wang et al. Border control – a membrane-linked interactome of Arabidopsis. Science 2014. https://doi.org/10.1126/science.1251358

Alexander M Jones, Danielson JA, ManojKumar S, Lanquar V, Grossman G, Frommer WB. Abscisic acid dynamics in roots detected with genetically encoded FRET biosensors. eLife 2014. https://doi.org/10.7554/elife.01741

            Highlighted in eLife Insight article: Choi W-G, Gilroy S. eLife. 2014; 3: e02763.

            Highlighted in TheScientist Modus Operandi article: Williams R. Stressing and FRETing. August 1st 2014.

Alexander M Jones*, Grossman G*, Frommer WB. In vivo biochemistry: Applications for small molecule biosensors in plant biology. Current Opinion in Plant Biology 2013. https://doi.org/10.1016%2Fj.pbi.2013.02.010 *equal contribution

Okumoto S*, Alexander M Jones*, Frommer WB. Quantitative imaging with fluorescent biosensors. Annu Rev Plant Biol. 2012.  https://doi.org/10.1146/annurev-arplant-042110-103745 *equal contribution

Alexander Jones, Wildermuth MC. The phytopathogen Pseudomonas syringae pv tomato DC3000 has three high-affinity iron-scavenging systems functional under iron limitation conditions but dispensable for pathogenesis. J Bacteriol. 2011.  https://doi.org/10.1128/jb.00069-10

Alexander M Jones, Lindow SE, Wildermuth MC. Salicylic acid, yersiniabactin, and pyoverdin production by the model phytopathogen Pseudomonas syringae pv tomato DC3000: synthesis, regulation, and impact on tomato and Arabidopsis host plants. J Bacteriol. 2007.  https://doi.org/10.1128/jb.00827-07

Research Group Leader
Dr Alexander  Jones

Contact Details

Sainsbury Laboratory
University of Cambridge
47 Bateman Street
Cambridge
CB2 1LR