Publications

Please also see Dan's Google scholar page

Eckardt  et al.  (2024) The lowdown on breakdown: Open questions in plant proteolyis.  The Plant Cell.  doi.org/10.1093/plcell/koae193

• This multiauthored commentary, part of a special issue on plant proteostasis in The Plant Cell, discusses some open questions in the field. My contribution is centred on recent advances and ongoing questions linked to roles for protein N-terminal acetylation in protein turnover.

Etherington RD, Bailey M, Baptiste JB, Armbruster L, Cao X, Coates JC, Meinnel T, Wirtz M, Giglione C and Gibbs DJ (2023) Nt-acetylation-independent turnover of SQUALENE EPOXIDASE 1 by Arabidopsis DOA10-like E3 ligases. Plant Physiology. doi.org/10.1093/plphys/kiad406

• We show that, in contrast to mammals and yeast, targeting of Nt-acetylated proteins is not a major function of DOA10-like E3 ligases in Arabidopsis, and provide further insight into plant ERAD and the conservation of regulatory mechanisms controlling sterol biosynthesis in eukaryotes through showing that Arabidopsis DOA10s regulate the turnover of ER localised SQUALENE EPOXIDASE 1.

• What happens in plants stays in plants: Arabidopsis prime Ac/N-recognin candidates do not function as such - News and Vews in Plant Physiology by Manuel Gonzalez-Fuente

Gibbs DJ and Osborne R (2022) High on oxygen. Nature Plants. 

• This News and Views article highlights a recent study by Abbas et al in Nature that reveals angiopsperm adaptation to altitude through natural variation in sensitivity to oxygen.  

Chustecki J, Etherington R, Gibbs DJ, Johnston I (2022) Altered collective mitochondrial dynamics in the Arabidopsis msh1 mutant compromising organelle DNA maintenance. Journal of Experimental Botany. 

Gibbs DJ, Bailey M and Etherington RD (2022) A stable start: Cotranslational Nt-acetylation promotes proteome stability across kingdoms. Trends in Cell Biology. DOI:https://doi.org/10.1016/j.tcb.2022.02.004DOI:https://doi.org/10.1016/j.tcb.2022.02.004

• In this Spotlight article we highlight two recent studies, in humans and Arabidopsis, that show NATA-mediated Nt-acetylation of nascent proteins promotes protein stability by masking N-degron sequences that would otherwise trigger protein turnover.  These studies indicate that Nt-acetylation has complex and context-specific effects on protein half-lives in eukaryotes.

Barreto P, Dambire C, Sharma G, Vicente J, Osborne R, Yassitepe J, Gibbs DJ, Maia IG, Holdsworth MJ and Arruda P (2022) Mitochondial retrograde signalling through UCP1-mediated inhibition of the plant oxygen-sensing pathway. Current Biology. 32, 1-9.

• This study, led by Michael Holdsworth and Paulo Arruda, identifies a novel link between mitochondrial retrograde signalling and regulation of nuclear gene expression during development and stress response.  It is shown that the mitochondrial inner membrane protein UCP1 inhibits the PRT6 N-degron pathway to enhance ERFVII substrate stability to increase hypoxic gene expression and stress resilience.  This therefore uncovers a new mechanistic connection between the major site for oxygen consumption in the cell (the mitochondrion) and the cytoplasmic oxygen-sensing pathway. 

I:https://doi.org/10.1016/j.cub.2022.01.037

Huber M, Armbruster L, Etherington RD, Torre CDL, Hawkesford MJ, Sticht C, Gibbs DJ, Hell R, Wirtz M (2022)  Disruption of the Nα-Acetyltransferase NatB Causes Sensitivity to Reductive Stress in Arabidopsis thaliana. Frontiers in Plant Science. doi.org/10.3389/fpls.2021.799954

• This study, led by Markus Wirtz's group, uncovers a role for the N-terminal acetlytransferase NATB in regulating cellular redox status in Arabidopsis thaliana. 

Chustecki JM, Gibbs DJ, Bassel GW, Johnston IG (2021) Network analysis of Arabidopsis mitochondrial dynamics reveals a resolved tradeoff between physical distribution and social connectivity. Cell Systems. https://doi.org/10.1016/j.cels.2021.04.006

• This study, led by Jo Chustecki and Iain Johnston, uses single-cell live imaging of Arabidopsis to characterize ‘‘social’’ networks of encounters between mitochondria. Network analysis and modeling reveal a cellular tradeoff between maintaining the physical spacing of mitochondria and their social interactions for exchanging metabolic and genetic information.

Labandera AM, Tedds H, Bailey M, Sprigg C, Etherington R, Akintewe O, Kalleechurn G, Holdsworth MJ and Gibbs DJ (2021) The PRT6 N-degron pathway restricts VERNALIZATION 2 to endogenous hypoxic niches to modulate plant development. New Phytologist. doi.org/10.1111/nph.16477  

• • • This study investigates how regulation of VRN2 stability by the PRT6 N-degron pathway modulates its functions during development.  We show that VRN2 is restricted to hypoxic mersitematic regions, where it regulates  flowering and root development, but is also stabilized outside of meristems in response to cold and exogenous hypoxia , where it adopts a different set of functions.

Holdsworth MJ and Gibbs DJ (2020) Comparative Biology of Oxygen Sensing in Plants and Animals. Current Biology. doi.org/10.1016/j.cub.2020.03.021

• • • In this review, Mike Holdsworth and I discuss plant and animal oxygen sensing systems.  We detail the similarities, differences, conservation and evolution of the molecular sensing and transduction mechanisms, highlight downstream processes, and describe how the pathways represent promising targets for for therapeutic benefit and stress resilience.

Parry G, Benitez-Alfonso Y, Gibbs DJ, Grant M, Harper A, Harrison CJ, Kaiserli E, Leonelli S, May S, McKim S, Spoel S, Turnbull T, van der Hoorn RAL, Murrray J (2020) How to build and effective research network: Lessons from two decades of the GARNet plant science community. Journal of Experimental Botany. https://doi.org/10.1093/jxb/eraa397

Orosa B, Ustun S, Calderon Villalobos LIA, Genschik P, Gibbs DJ, Holdsworth MJ, Isono E, Lois M, Trujillo M, Sadanandom A (2020) Plant Proteostasis - shaping the proteome: a research community aiming to understand molecular mechanisms that control protein abundance. New Phytologist. 227: 1028-1033

Gibbs DJ and Holdsworth MJ (2019) Every Breath You Take: New Insights into Plant and Animal Oxygen Sensing. Cell. doi.org/10.1016/j.cell.2019.10.043

• • • 2019 was an exciting year for oxygen sensing research; many new advances were made in both plants and animals, and the discovery of HIF-based oxygen sensing in animal cells was awarded the Nobel Prize for Physiology or Medicine. In this preview article, we discuss recent advances related to the differences, commonalities, and origins of oxygen sensing across kingdoms , with particular focus on the discovery of an oxygen sensing enzyme in animals that had previously only been observed in plants (Masson et al (2019) Science)

Hartman S, Liu Z. van Veen H, Vicente J, Reinen E, Martopawiro S, Zhang H, van DongenN, Bosman F, Bassel GW, Visser EJW, Bailey-Serres J, Theodoulou F, Hebelstrup K, Gibbs DJ, Holdsworth MJ, Sasidharan R, Voesenek LACJ (2019) Ethylene-mediated Nitric Oxide depletion pre-adapts plants to hypoxia stress. Nature Communications. 10, Article number: 4020 (2019) 

• • • This study, led by Sjon Hartman from the groups of Rens Voesenek and Rashmi Sasidharan at the University of Utrecht, shows that plants sense flooding stress early through accumulating ethylene, which triggers phytoglobin production to scavenge NO & stabilise ERFVII transcription factors before hypoxia sets in.  The study reveals a pre-priming mechanism that adds further insight into the importance of NO in relation to ERFVII homeostasis in stress contexts.

    • Press release

    • Ethylene signalling controls fast oxygen sensing in plants - Spotlight in Trends in Plant Science

    • F1000 recommendation

Lin CC, Chao YT, Chen WC, Ho HY, Chou MY, Li YR, Wu YL, Yang HA, Hsieh H, Lin CS, Wu FH, Chou SJ, Jen HC, Huang YH, Irene D, Wu WJ, Wu JL, Gibbs DJ, Ho MC, Shih MC (2019) Regulatory cascade involving transcriptional and N-end rule pathways in rice under submergence. PNAS (USA). doi: 10.1073/pnas.1818507116 

• • • This study, led by Ming-Che Shih and Meng-Chiao Ho, identifies two ERFVII transcription factors as downstream targets of SUB1A, and shows that they are substrates of N-end rule pathway that are stabilsied by hypoxia and contribute to submergence tolerance.   Structural and interaction studies also provide a potential explanaiton for SUB1A's evasion of the N-end rule pathway.

Gibbs DJ*, Tedds HM, Labandera A-M, Bailey M, White MD, Hartman S, Sprigg C, Mogg SL, Osborne R, Dambire C, Boeckx T, Paling Z, Voesenek LACJ, Flashman E, Holdsworth MJ* (2018) Oxygen-dependent proteolysis regulates the stability of angiosperm Polycomb Repressive Complex 2 subunit VERNALIZATION 2. Nature Communications. 9:5438 DOI:10.1038/s41467-018-07875-7 *Corresponding authors

• • • This study identifies the angiosperm-specific PRC2 subunit VRN2 as an oxygen and nitric oxide regulated substrate of the N-end rule pathway, uncovering a biochemical link between environment-derived signals and VRN2 protein levels.  This suggests that oxygen availability may control epigenetic regulation of gene expression through controlling VRN2 stability.  We also provide evidence that VRN2 was specifically co-opted to the N-end rule pathway in the flowering plant lineage, following gene duplication and N-terminal truncation of an ancient homolog.

    • Press release

    • Spotlight at plantae.org

Zhang H, Gannon L, Jones PD, Rundle CA, Hassall KL, Gibbs DJ, Holdsworth MJ, Theodoulou FL (2018) Genetic interactions between ABA signalling and the Arg/N-end rule pathway during Arabidopsis seedlings establishment.  Scientific Reports. 8(1):15192

• • • This study, led by Freddie Theodoulou, reveals that the N-end rule regulated stabilisation of a subset of ERFVII transcription factors controls sugar sensitivity and oil body breakdown during seedling establishment, through ABA-dependent and independent routes. 

Vicente J, Mendiondo GM, Pauwels J, Pastor V, Izquierdo Y, Naumann C, Movahedi M, Rooney D, Gibbs DJ, Smart K, Bachmair A, Gray JE, Dissmeyer N, Castresana C, Ray RV, Gevaert K and Holdsworth MJ (2018) Distinct branches of the N‐end rule pathway modulate the plant immune response. New Phytologist: DOI:10.1111/nph.15387

• • • This study led from the lab of Michael Holdsworth describes how distinct subdivisions of the Arg/N-end rule pathway modulate the immune response in both Arabidopsis and barley.  Along with previous studies connecting the pathway to abiotic stress, this work reveals that the N-end rule is a key regulator of diverse environmental responses.

Meitha K, Agudelo-Romero P, Signorelli S, Gibbs DJ, Considine JA, Foyer CH, Considine MJ (2018) Developmental control of hypoxia during bud burst in grapevine. Plant, Cell and Environment. doi: 10.1111/pce.13141

• • • This study, led by Mick Considine, used detailed RNA-seq and protein analyses to uncover an important developmental function for oxygen-dependent signalling in determining the timing and effective coordination of bud burst in grapevine, which may be regulated via post-translational control of ERFVII transcription factor stability.

Dissmeyer N, Graciet E, Holdsworth MJ, Gibbs DJ (2018) N-term 2017: Proteostasis via the N-terminus.  Trends in Biochemical Sciences doi.org/10.1016/j.tibs.2017.11.006

• • • A meeting report: N-term 2017 was the first international meeting to bring together researchers from diverse disciplines with a shared interest in protein N-terminal modifications and the N-end rule pathway of ubiquitin-mediated proteolysis, providing a platform for interdisciplinary cross-kingdom discussions and collaborations, as well as strengthening the visibility of this growing scientific community.

Zhang H, Gannon L, Hassall, KL, Deery M., Gibbs DJ, Holdsworth MJ, van der Hoorn RAL, Lilley KS, Theodoulou FL. (2017) N-terminomics reveals control of Arabidopsis seed storage proteins and proteases by the Arg/N-end rule pathway.  New Phytologist DOI: 10.1111/nph.14909

• • • This study, led by Freddie Theodoulou at Rothamsted, used large scale N-terminomics to investigate the impact of the Arg/N-end rule on the Arabidopsis prtoteome, which revealed that the pathway regulated protease activities and optimises storage reserve mobilisation during seed to seedlings trasnition, which is largely co ordinated by the ERFVII transcription factors.  

Considine MJ, Diaz-Vivancoz P, Kerchev P, Signorelli S, Agudelo-Romero P, Gibbs DJ, Foyer CH (2017) Learning to breathe: Developmental Phase transitions in oxygen status. Trends in Plant Science. DOI: http://dx.doi.org/10.1016/j.tplants.2016.11.013

• • • Plants are developmentally disposed to significant changes in oxygen availability, but our understanding of the importance of hypoxia is almost entirely limited to stress biology.  In this opinion piece we discuss recent advances in our understanding of the role of oxygen availability, and associated changes in ROS and NO, during development.

Gibbs DJ, Bailey M, Tedds HM, Holdsworth MJ (2016) From start to finish: amino-terminal protein modifications as degradation signals in plants. New Phytologist.DOI: 10.1111/nph.14105 

• • • In this invited insight article, we review recent advances in our understanding of the relationship between the nature of protein N-termini, Nt-processing events and proteolysis in plants. 

Moody LA, Saidi Y, Gibbs DJ, Choudhary A, Holloway D, Vesty EF, Bansal KK, Bradshaw SJ, Coates JC (2016) An ancient and conserved function for Armadillo-related proteins in the control of spore and seed germination by abscisic acid. New Phytologist. DOI:10.1111/nph.13938

• • • This paper investigates functions for Armadillo-related proteins across 450 my of plant evolution, identifying a conserved role for these proteins in regulating ABA-responsive spore and seed germination in mosses and Arabidopsis.

Gibbs DJ (2015) Emerging functions for N-terminal protein acetylation in plants. Trends in Plant Science. DOI:  http://dx.doi.org/10.1016/j.tplants.2015.08.008

• • • This spotlight article discusses recent studies that shed light onto the proteome-wide dynamics and protein-specific consequences of Nt-acetylation in relation to plant development, stress-response, and protein stability, identifying this modification as a key regulator of diverse aspects of plant growth and behaviour.  The potential presence of the acetylation-dependent branch of the N-end rule (Ac/N-end rule) in plants is also discussed.

Abbas M, Berckhan S, Rooney DJ, Gibbs DJ, Vicente Conde J, Sousa Correia C, Bassel GW, Marín-de la Rosa N, León J, Alabadí D, Blázquez MA and Holdsworth MJ (2015) Oxygen sensing coordinates photomorphogenesis to facilitate seedling survival.  Current Biology. DOI: http://dx.doi.org/10.1016/j.cub.2015.03.060  

• • • In this paper we show that oxygen sensing via N-end rule mediated degradation of group VII ERF transcription factors coordinates photomorphogenesis to facilitate seedling survival.  Remarkably, hypoxia acts as a beneficial cue, repressing photomorphogenesis and protecting seedlings from photo oxidative damage following extended darkness, which dramatically improves establishment and survival once light is perceived.

    • Commentary by Potuschak and Bachmair in Current Biology

    • News and Views by Voesenek and Bailey-Serres in Nature Plants

Gibbs DJ*, Vicente Conde J, Berckhan S, Mendiondo GM, Prasad G and Holdsworth MJ* (2015) Group VII ethlyene response factors co-ordinate oxygen and nitric oxide signal transduction and stress responses in plants. Plant Physiology. DOI:10.1104/pp.15.00338  *corresponding authors 

• • • In this invited update we discusses recent advances in our understanding of group VII ERF regulation and function in plants, highlighting their role as central regulators of gaseous signal transduction at the interface of oxygen, NO and phytohormone signalling.

Mendiondo GM, Gibbs DJ, Szurman-Zubrzycka M, Korn A, Marquez J, Szarejko I, Maluszynski M, King J, Axcell B, Smart K, Corbineau F, and Holdsworth MJ (2015) Enhanced waterlogging tolerance in barley by manipulation of expression of the N-end rule pathway E3 ligase PROTEOLYSIS6. Plant Biotechnology Journal. doi: 10.1111/pbi.12334

• • • In this paper we show that N-end rule regulation of the hypoxia response is conserved in barley.  Downregulation of barley PROTEOLYSIS6 activity using RNAi and TILLING approaches produces plants that have enhanced tolerance to waterlogging, demonstrating that the N-end rule pathway represents a promising target for the development of crops with improved flooding resistance, a major focus for food security.

    • Press release

Gibbs DJ*, Bacardit J, Bachmair A, Holdsworth MJ* (2014) The eukaryotic N-end rule pathway: conserved mechanisms and diverse functions. Trends in Cell Biology. http://dx.doi.org/10.1016/j.tcb.2014.05.001. *corresponding authors

• • • This review discusses the diverse functions of the eukaryotic N-end rule pathway, with a particular focus on recently identified branches of the pathway, and its conserved role in oxygen and nitric oxide sensing in higher eukaryotes via kingdom-specific substrates

Marín-de la Rosa N, Sotillo B, Miskolczi P, Gibbs DJ, Vicente Conde J, Carbonero P, Oñate-Sánchez  L, Holdsworth MJ, Bhalerao R, Alabadí D, Blázquez MA (2014) Large-scale identification of gibberellin-related transcription factors defines Group VII ERFs as functional DELLA partners. Plant Physiology. doi:10.1104/pp.114.244723

• • • A large scale GAI-protein interactome reveals that DELLAs bind a wide range of functionally and structurally diverse transcription factors. The physical interaction between DELLAs and group VII ERFs is functionally investigated within the context of apical hook development, validating the network and revealing a novel mode of crosstalk between GA, ethylene and NO/O2 signalling.

Bassel GW, Stamm P, Mosca G, Barbier de Reuille P, Gibbs DJ, Winter RM, Janka A, Holdsworth MJ, Smith RS (2014) Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo.  PNAS (USA). doi/10.1073/pnas.1404616111

• • • Using cell biology, imaging and 3D computer modelling, this work identifies an important role for cell size, shape and arrangement in modulating plant morphogenesis, which explains why observed growth does not always correlate with patterns of growth-promoting gene expression

Gibbs DJ, Voss U, Harding SA, Fannon J, Moody LA, Yamada E, Swarup K, Nibau C, Bassel GW, Choudhary A, Lavenus J, Bradshaw SJ, Stekel DJ, Bennett MJ, Coates JC (2014) AtMYB93 is a novel negative regulator of lateral root development in Arabidopsis. New Phytologist. DOI: 10.1111/nph.12879  

• • • We identify the AtMYB93 transcription factor as a novel auxin induced negative regulator of lateral root development in Arabidopsis. AtMYB93 expression is restricted to the few endodermal cells overlying developing lateral root primordia, and represents a potential target for manipulating root system architecture in crop species.

    • BBSRC Press release

Gibbs DJ and Coates JC (2014) AtMYB93 is an endodermis-specific transcriptional regulator of lateral root development in Arabidopsis.  Plant Signaling and Behaviour. http://dx.doi.org/10.4161/psb.29808

• • • In this addendum article, we discuss the emerging role of the endodermis as a key tissue regulating lateral root morphogenesis, and present several models explaining how the recently identified AtMYB93 transcription factor may regulate this process.

Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LA, van Dongen JT (2012) Making sense of low oxygen sensing. Trends in Plant Science.17(3):129-38

• • • This review details recent advances in our understanding of oxygen sensing and signalling in plants, with respect to normal oxygen availabilities during growth and also submergence-induced hypoxia 

Bassel GW, Lan H, Glaab E, Gibbs DJ, Gerjets T, Krasnogor N, Bonner AJ, Holdsworth MJ, Provart NJ (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. PNAS (USA). 108(23):9709-14

• • • This paper describes the global gene co-expression network regulating seed dormancy, germination and the transition between both states.  A conserved set of genes regulating different life-phase transitions is identified.

    • Press release

Nibau C, Gibbs DJ, Bunting KA, Moody LA, Smiles EJ, Tubby JA, Bradshaw SJ, Coates JC (2011) ARABIDILLO proteins have a novel and conserved domain structure important for the regulation of their stability. Plant Molecular Biology. 75(1-2):77-92.

• • • This paper describes the proteolytic control of a key regulator of lateral root branching in Arabidopsis

Nibau C*, Gibbs DJ*, Coates JC (2008) Branching out in new directions: the control of root architecture by lateral root formation. New Phytologist. 179(3):595-614. *Joint first author.

• • • This invited review provides a comprehensive discussion of the endogenous factors and environmental signals that regulate root system architecture in plants, with a particular focus on lateral root development.