Google Scholar Web Page
2025:
Dalle Carbonare, L., van Veen, H., Shukla, V., Perri, M., Bui, L., *Holdsworth, M.J., *Licausi, F. (2025) ERFVIIs as transducers of oxygen-sensing in the evolution of land plant response to hypoxia. Molecular Plant, DOI: 10.1016/j.molp.2025.05.015
When and how did oxygen-sensing evolve in plants? Here we use phylotranscriptomics to scan the response to low oxygen in land plants, and assess the evolution of the ERFVII transcription factors as transducers of low oxygen stress. A fascinating collaboration with Francesco Licausi and Hans van Veen.
This paper is highlighted in a Spotlight article by Dan Gibbs and Lina Zhou in Molecular Plant.
Holdsworth, M.J., Liu, H., Castellana, S., Abbas, M., Liu,J., Perata, P. (2025) Geography, altitude, agriculture and hypoxia. Plant Physiology, 10.1093/plphys/kiae535
Here we review recent advances in understanding how genetic adaptation to tolerate low oxygen spans geographical and agricultural scales and environments.
2023:
Zubrycka, A., Dambire, C., Dalle Carbonare, L., Sharma, G., Boeckx, T., Swarup, K., Sturrock, C.J., Atkinson, B.S., Swarup, R., Corbineau, F., Oldham, N.J., Michael J. Holdsworth M.J. (2023) ERFVII action and modulation through oxygen-sensing in Arabidopsis thaliana. Nature Communications, 14, 4665
The PCO N-degron pathway is the only known mechanism for plant oxygen-sensing, but key aspects are unknown or not understood. In this manuscript we define new functions and components of the sensing mechanism that provide an understanding of biochemical changes required for sensing and molecular and physiological responses allowing plant roots to survive in the soil. These data provide novel opportunities to completely understand plant oxygen-sensing. The work includes the culmination of many years collaboration with Prof. Neil Oldham (University of Nottingham Chemistry) to find the nature of the N-terminus of ERFVIIs.
This paper is highlighted in Trends in Plant Science here (Unearthing the secrets of ERFVIIs: New insights into hypoxia signalling). Thanks to the authors Jagannath Swain, Vinay Shukla, Francesco Licausi and Kapuganti Jagadis Gupta for explaining the work so clearly and putting it in context.
Pitsili, E., Rodriguez-Treviño, R., Ruiz-Solani, N., Demir, F., Kastanaki, E., Dambier, C., de Pedro-Jové, R., Vercammen, D., Salguero Linares, J., Hall, H., Mantz, M., Schuler, M., Tuominen, H., Van Breusegem, F., Valls, M., Munné-Bosch, S., Holdsworth, M., Huesgen, P., Rodriguez-Villalon, A., Coll, N. (2023) A phloem-localized Arabidopsis metacaspase (AtMC3) improves drought tolerance. New Phytologist, 239, 1281-1299. doi: 10.1111/nph.19022
Really interesting work led by Núria Coll investigating the role of Metacaspase 3 in plant development and environmental responses.
2022:
Abbas, M., Sharma, G., Dambire, C., Marquez, J., Alonso-Blanco, C., Proaño, K., Holdsworth, M.J. (2022) An oxygen-sensing mechanism for angiosperm adaptation to altitude. Nature 606, 565–569. doi:10.1038/s41586-022-04740-y.
Altitude is an important component of plant ecology, at least 30% of plant species diversity is contained in mountains, and climate change is influencing the altitudinal range of important crop species. For life at high altitude it has been considered that plants need to adapt to many variables, including high UV light and lower temperatures. However, we identify a mechanism through which absolute elevation is perceived by plants. The adaptation involves sensing atmospheric oxygen levels (that decrease with altitude). We show that this mechanism works in diverse flowering plant species, providing a new paradigm for plant ecology. A fantastic collaboration with Carlos Alonso Blanco and Karina Proaño.
This paper is highlighted by Dan Gibbs and Rory Osborne, you can read their thoughts on it in Nature Plants here.
Lou, S., Guo, X., Liu, L., Song, Y., Zhang, L., Jiang, Y., Zhang, L., Sun, P., Liu, B., Tong, S., Chen, N., Liu, M., Zhang, H., Liang, R., Feng, X., Zheng, Y., *Liu, H., *Holdsworth, M.J., *Liu, J. (2022) Allelic shift in cis-elements of the transcription factor RAP2.12 underlies adaptation associated with humidity in Arabidopsis thaliana. Science Advances 8, Article number: 8281; doi:10.1126/sciadv.abn8281.
How do widespread species adapt to differing abiotic stresses throughout their geographical range? In this collaboration led by Professor Jianquan Liu, Sichuan University, we show that within the species Arabidopsis thaliana allelic changes in the promoter of a key oxygen-regulated transcription factor RAP2.12 underlie adaptation related to humidity. We also solve the conundrum of why RAP2.12 appears to be the dominant ERFVII in accession Columbia-0 for hypoxia studies!
Barreto, P., Dambire, C., Sharma, G., Vicente, J., Osborne, R., Yassitepe, J., Gibbs, D.J., Maia, I.G., *Holdsworth, M.J. and *Arruda, P. (2022) Mitochondrial retrograde signalling through UCP1-mediated inhibition of the plant oxygen-sensing pathway. Current Biology 32, 1403-1411. doi:10.1016/j.cub.2022.01.037
In collaboration with Paulo Arruda we show that oxygen-sensing is part of mitochondrial retrograde signalling during normal plant development and that this interaction influences abiotic stress tolerance.
This paper is highlighted by Prof. Dr. Nico Dissmeyer, you can read his thoughts on it in Current Biology here.
Kozlic, A., Winter, N., Telser, T., Reimann, J., Rose. K,, Nehlin, L., Berckhan, S., Sharma, G., Dambire. C,, Boeckx, T., Holdsworth. M.J., and Bachmair. A, (2022) A Yeast-Based Functional Assay to Study Plant N-Degron–N-Recognin Interactions. Front. Plant Sci. 12:806129. doi: 10.3389/fpls.2021.806129
A collaboration led by Andreas Bachmair, revealing new plant Met-Cys substrates and a method for functional analysis of plant N-degron components in yeast.
2021:
Labandera, A.M., Tedds, H.M., Bailey, M., Sprigg, C., Etherington, R.D., Akintewe, O., Kalleechurn, G., Holdsworth M.J., Gibbs, D.J. (2020) The PRT6 N-degron pathway restricts VERNALIZATION 2 to endogenous hypoxic niches to modulate plant development. New Phytologist: 229: 126-139. doi: 10.1111/nph.16477
In collaboration with @DJ_Gibbs we continue our quest to understand the reach of oxygen-sensing in plants. Here we deepen our understanding of the influence of oxygen on the stability of the PRC2 component VRN2, and of the influence of this on the biology of VRN2 function in relation to plant hypoxic niches.
2020:
Holdsworth M.J., Gibbs, D.J. (2020) Comparative biology of oxygen sensing in plants and animals. Current Biology: 30, Issue 8, Pages R362-R369. DOI: 10.1016/j.cub.2020.03.021
An review of the comparative biology of oxygen sensing in advanced multicellular eukaryotes.
Orosa, B., Üstün, S., Calderón Villalobos, L.I.A., Genschik, P., Gibbs, D.J., Holdsworth, M.J., 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. doi:10.1111/nph.16664
Happy to have been involved in a small way in helping write this report of a fantastic meeting.
Gibbs, D.J., Holdsworth, M.J. (2020) Every Breath You Take: New Insights into Plant and Animal Oxygen Sensing. Cell: 180 (1), 22-24; DOI:10.1016/j.cell.2019.10.043
@DJ_Gibbs and I highlight the discovery in animals of an N-terminal cysteine oxidase (Masson et al Science 2019), and discuss what it says about the evolution of oxygen-sensing.
2019:
Till, C., Vicente, J., Zhang, H., Oszvald, M., Deery, M., Pastor, V., Lilley, K., Ray, R., Theodoulou, F., Holdsworth M.J. (2019) The Arabidopsis E3 ligase N-recognin PROTEOLYSIS1 influences the immune response. Plant Direct: 3, e00194, doi:10.1002/pld3.194
The first plant N-recognin to be genetically identified (back in 1998) was PRT1. Here we show that PRT1 influences the plant immune system, providing molecular information about possible functions.
Holdsworth, M.J., Vicente, J., Sharma, G., Abbas, M., Zubrycka. A. (2019) The plant N-degron pathways of ubiquitin-mediated proteolysis. Journal of Integrative Plant Biology: 62 (1) 70-89; DOI:10.1111/jipb.12882
A review from the lab about the current staging of knowledge about the N-degron pathways in plants.
Hartman, S., Liu, Z., van Veen, H., Vicente Conde, J., Reinen, E., Martopawiro, S., Zhang, H., van Dongen, N., Bosman, Bassel, G.W., Visser, E.J.W., Bailey-Serres, J., Theodoulou, F.L., Hebelstrup, K.H., Gibbs, D.J., *Holdsworth, M.J., *Sasidharan, R., *Voesenek, L.C.J. (2019) Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nature Communications: 10, Article number: 4020. DOI:10.1038/s41467-019-12045-4
A tale of three gases; We knew previously that both oxygen and nitric oxide (NO) are required for destabilisation of ERFVIIs. Here a great collaboration led by Rens Voesenek (started by an MSc visit by Sjon Hartman @SjonHartman) elegantly elucidates the molecular mechanism that plants use, by responding to three gases, ethylene, oxygen and NO, to enhance survival of flooding.
Millar, A.H., Heazlewood, J.L., Giglione, C., Holdsworth,M.J., Bachmair, A., Schulze, W.X. (2019), The Scope, Functions, and Dynamics of Posttranslational Protein Modifications. Annual Review of Plant Biology: 70, 119-151. DOI:10.1146/annurev-arplant-050718-100211
Here we review the vast world of post-translational modifications in plants. We combine four perspectives on PTMs and their roles by considering five classes of PTMs as examples of the broader context of PTMs. These include modifications of the N terminus, glycosylation, phosphorylation, oxidation, and N-terminal and protein modifiers linked to protein degradation.
Vicente, J. , Mendiondo, G. M., Pauwels, J. , Pastor, V. , Izquierdo, Y. , Naumann, C. , Movahedi, M. , Rooney, D. , Gibbs, D. J., Smart, K. , Bachmair, A. , Gray, J. E., Dissmeyer, N. , Castresana, C. , Ray, R. V., Gevaert, K. and Holdsworth, M. J. (2019), Distinct branches of the N‐end rule pathway modulate the plant immune response. New Phytologist: 221 (2), 988-1000. DOI:10.1111/nph.15387
Here we show that the N-end rule pathway influences the plant immune response. In particular we show a role for substrate(s) of amino-terminal Gln amidase NTAQ1 in enhancing plant immunity.
Sánchez-Montesino R., Bouza-Morcillo L., Marquez J., Ghita M., Duran-Nebreda S., Gómez L., Holdsworth M.J., Bassel G., and Oñate-Sánchez L. (2019) A regulatory module controlling GA-mediated endosperm cell expansion is critical for seed germination in Arabidopsis. Molecular Plant: 12(1) 71-85. DOI: 10.1016/j.molp.2018.10.009.
A key role for the endosperm in regulating embryo growth and germination. Great collaboration led by Luis Oñate Sánchez with George Bassel. My last paper from research focussed on germination?
2018:
Gibbs, D.J., Tedds, H.M., Labandera, A-M., Bailey, M., White, M.D., Hartman, S., Sprigg, C., Mogg, S.L., Osborne, R., Dambire, C., Boeckx, T., Paling, Z., Voesenek, L.A.C.J., Flashman, E., Holdsworth, M.J. (2018) Oxygen-dependent proteolysis regulates the stability of angiosperm Polycomb Repressive Complex 2 subunit VERNALIZATION2. Nature Communications. 9:5438 DOI: 10.1038/s41467-018-07875-7.
Fantastic collaboration with @DJ_Gibbs and many others, showing that the stability of Polycomb Repressive Complex (PRC)2 component VERNALISATION2 is restricted by oxygen and cold, controlled by the N-end rule pathway, and evolved in angiosperms.
Zhang, H., Gannon, L., Jones, P.D., Rundle, C.A., Hassall, K.L., Gibbs, D.J., Holdsworth, M.J., Theodoulou, F.L. (2018) Genetic interactions between ABA signalling and the Arg/N-end rule pathway during Arabidopsis seedling establishment. Scientific Reports 8:15192. DOI:10.1038/s41598-018-33630-5
Work led by Freddie Theodoulou shows the importance of the PRT6 N-end rule pathway and ERFVIIs in early seedling development.
Tomanov, K., Nukarinen, E., Vicente, J., Mendiondo, G.M.M., Winter, N., Nehlin, L., Weckwerth, W., Holdsworth, M.J., Teige, M., Bachmair A. (2018) Sumoylation and phosphorylation: hidden and overt links, Journal of Experimental Botany, ery167, https://doi.org/10.1093/jxb/ery167
A review, led by Andreas Bachmair, addresses the cross-talk between phosphorylation and sumoylation in plants and how this affects growth, development and environmental interactions.
Pearce, S.P., King, J.R., Steinbrecher, T., Leubner-Metzger, G., Everitt, N.M., Holdsworth, M.J. (2018) Finite indentation of highly curved elastic shells. Proceedings of the Royal Society Series A 474: 20170482. DOI: 10.1098/rspa.2017.0482
Taking as a biological cue the stretching and rupture of the endosperm during seed germination, work led by Simon Pearce defines mathematical terms required to define a model to represent this system, work carried out as part of the vSEED ERANET consortium project.
2017:
Dissmeyer N., Graciet E., Holdsworth M.J., Gibbs D.J. (2017) N-term 2017: Proteostasis via the N-terminus. Trends in Biochem Sci. DOI: 10.1016/j.tibs.2017.11.006
N-term-17 Conference report; the first time the community of biologists working on protein modifications and function at the amino-terminus got together.
Zhang, H., Gannon, L., Hassall, K.L., Deery, M.J., Gibbs, D.J., Holdsworth, M.J., van der Hoorn, R.A.L., Lilley, K.S., Theodoulou, F.L. (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
Work led by Freddie Theodoulou shows that the PRT6 branch of the N-end rule pathway, via ERFVIIs, regulates protease activities in a complex manner optimising storage reserve mobilisation during seedling establishment.
Vicente, J., Mendiondo, G.G., Movahedi, M., Peirats-Llobet, M., Juan, Y., Shen, Y., Dambire, C., Smart, K., Rodriguez, P.L., Charng, Y., Gray, J.E., Holdsworth, M.J. (2017) The Cys-Arg/N-end rule pathway is a general sensor of abiotic stress in flowering plants. Current Biology 27, 3183-3190; doi:10.1016/j.cub.2017.09.006
This work, a collaboration with Julie Gray, Pedro Rodriguez and Yee-yung Charng, shows that the N-end rule pathway, via its effect on ERFVII activity, influences responses to many abiotic stresses.
Holdsworth, M. J. (2017) First hints of new sensors. Nature Plants 3, 767–768; doi:10.1038/s41477-017-0031-7
Are there undiscovered sensors of hypoxia? Analysis of three recent papers appears to show that there are...
Sasidharan, R., Bailey-Serres, J., Ashikari, M., Atwell, B. J., Colmer, T. D., Fagerstedt, K., Fukao, T., Geigenberger, P., Hebelstrup, K. H., Hill, R. D., Holdsworth, M. J., Ismail, A. M., Licausi, F., Mustroph, A., Nakazono, M., Pedersen, O., Perata, P., Sauter, M., Shih, M.-C., Sorrell, B. K., Striker, G. G., van Dongen, J. T., Whelan, J., Xiao, S., Visser, E. J. W. and Voesenek, L. A. C. J. (2017), Community recommendations on terminology and procedures used in flooding and low oxygen stress research. New Phytologist 214: 1403–1407;doi:10.1111/nph.14519
Now you know how to do your experiments correctly!
2016 and before.....:
Gravot, A., Richard, G., Lime, T., Lemarié, S., Jubault, M., Lariagon C., Lemoine J., Vincente, J., Robert-Seilaniantz, A., Holdsworth, M.J., Manzanares-Dauleux M.J. (2016) Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot. BMC Plant Biology 16 (1): 251; doi:10.1186/s12870-016-0941-y
In work led by Antoine Gravot we show that Plasmodiophora brassicae userps the N-end rule pathway in Arabidopsis to enhance infection and the development of clubroot.
Dekkers, B.J.W., Pearce, S.P., van Bolderen-Veldkamp, R.P.M., Holdsworth, M.J., Bentsink, L. (2016) Dormant and after-Ripened Arabidopsis thaliana Seeds are Distinguished by Early Transcriptional Differences in the Imbibed State. Front. Plant Sci. 7 Article 1323, doi: 10.3389/fpls.2016.01323
A vSEED initiated study led by Bas and Simon that analyses the transcriptome changes associated with imbibed dormant and after-ripened seeds. An associated web tool for analysis of gene expression is available at http://www.wageningenseedlab.nl/resources
Gibbs, D.J., Bailey, M., Tedds, H.M. and Holdsworth M.J. (2016) From start to finish: amino-terminal protein modifications as degradation signals in plants; Tansley Insight. New Phytologist 211, (4): 1188–1194. DOI: 10.1111/nph.14105
We review the really exciting emerging field of plant protein N-terminal modifications, plenty more to come...
Shorinola, O., Bird, N., Simmonds, J., Berry, S., Henriksson, T., Jack, P., Werner, P., Gerjets, T., Scholefield, D., Balcárková, B., Valárik, M., Holdsworth, M. J., Flintham, J., Uauy, C. (2016) The wheat Phs-A1 pre-harvest sprouting resistance locus delays the rate of seed dormancy loss and maps 0.3 cM distal to the PM19 genes in UK germplasm. Journal of Experimental Botany, 67 (14): 4169-4178. doi: 10.1093/jxb/erw194
Mendiondo, G.M., Gibbs, D.J., Szurman-Zubrzycka, M., Korn, A., Marquez, J., Szarejko, I., Maluszynski, M., King, J., Axcell, B., Smart, K., Corbineau, F., and Holdsworth, M.J. (2016) Enhanced waterlogging tolerance in barley by manipulation of expression of the N-end rule pathway E3 ligase PROTEOLYSIS6. Plant Biotechnology Journal, 14 (1). 40–50: doi: 10.1111/pbi.12334
Here we show that the N-end rule pathway controls the response of barley to waterlogging, demonstrating that it should be possible therefore to improve tolerance of crops to flooding by manipulating this pathway.
Abbas, M., Berckhan, S., Rooney, D., Gibbs, D.J., Vicente Conde, J., Sousa Correia, C., Bassel, G.W., Marin-de la Rosa, N., León, J., Alabadí, D., Blázquez, M.A. and Holdsworth, M.J. (2015) Oxygen sensing coordinates photomorphogenesis to facilitate seedling survival. Current Biology, 25: 1483–1488
This paper demonstrates that oxygen sensing is a key component of photomorphogenesis in eudicot flowering plants. Hypoxia is a positive signal during early seedling growth, sensed via oxygen-controlled conditional stability of ERFVII transcription factors, that alters development in the dark enhancing subsequent survival during photomorphogenesis.
Gibbs, D.J., Vicente Conde, J., Berckhan, S., Mendiondo, G.M., Prasad, G., Holdsworth M.J. (2015) Group VII Ethylene Response Factors co-ordinate oxygen and nitric oxide signal transduction and stress responses in plants. Plant Physiology 169: 23–31; doi:10.1104/pp.15.00338
This Update for Plant Physiology describes the important role of ERFVII transcription factors in plant environment interactions, regulated via conditional protein stability that is controlled by NO and oxygen sensing through the N-end rule pathway.
Wilson M.H., Holman T.J., Sørensen I., Cancho-Sanchez E., Wells D.M., Swarup R., Knox P., Willats W.G., Ubeda-Tomas S., Holdsworth M., Bennett M., Vissenberg K. and Hodgman T.C. (2015). Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone. Front. Cell Dev. Biol. 3:10. doi: 10.3389/fcell.2015.00010
Scheler, C., Weitbrecht, K., Pearce, S.P., Hampstead, A., Büttner-Mainik, A., Lee, K., Voegele, A., Oracz, K., Dekkers, B., Wang, X., Wood, A., Bentsink, L., King, J., Knox, P., *Holdsworth, M.J., *Müller, K., *Leubner, G. (2015) Promotion of Testa Rupture during Lepidium sativum Germination Involves Seed Compartment-Specific Expression and Activity of Pectin Methylesterases. Plant Physiology 167: 200-215. *Joint senior authors.
As part of the vSEED consortium, work co-ordinated by Gerd at RHUC using transcriptomics, mathematical modelling and biochemistry investigates the role of Pectin methylesterase (PME) in germination in Lepidium sativum.
Marin-de la Rosa, N., Sotillo, B., Miskolczi, P., Gibbs, D.J., Vicente, J., Carbonero, P., Onate-Sanchez, L., Holdsworth, M.J., Bhalerao, R., Alabadi, D., Blazquez, M.A. (2014) Large-scale identification of gibberellin-related transcription factors defines Group VII ERFs as functional DELLA partners. Plant Physiology, 166: 1022-1032.
Work led by David and Miguel at the IBMCP in Valencia shows with our help that Group VII ERFs are functional DELLA partners.
Mendiondo, G.M., Medhurst, A., van Roermund, C.W., Zhang, X., Devonshire, J., Scholefield, D., Fernandez, J., Axcell, B., Ramsay, L., Waterham, H.R., Waugh, R., L Theodoulou, F.L., Holdsworth, M.J. (2014) Barley has two peroxisomal ABC transporters with multiple functions in beta-oxidation. Journal of Experimental Botany, 65 (17): 4833-4847.
Peroxisomal ABC transporters have been studied extensively in Arabidopsis but not in monocotyledonous species. Using barley, it is shown that their biochemical functions are conserved in flowering plants.
Bassel, G.W., Stamm, P., Mosca, G., Barbier de Reuille, P., Gibbs, D.J., Winter, R.C., Janka, A., Holdsworth, M.J., Smith, R.S. (2014) Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo. PNAS (USA), 111 (23), 8685–8690.
Work led by George and Richard has produced the first 'virtual' seedling. Using a combination of genetics, cell biology and 3D finite-element modelling the paper demonstrates that the size, shape, and arrangement of plant cells all influence their ability to grow in response to growth-promoting gene expression.
Gibbs, D.J., Bacardit, J., Bachmair, A., Holdsworth, M.J. (2014) The eukaryotic N-end rule pathway: conserved mechanisms and diverse functions. Trends in Cell Biology, 24, 603–611.
We review what is currently known about the eukaryotic N-end rule pathway, in particular recent papers that show that almost all of the naturally occurring amino-acids can act as destabilising residues at the amino-terminus of a protein. Food for thought!
Gibbs, D.J., Isa, N.M., Movahedi, M., Lozano- Juste, J., Mendiondo, G.M., Berckhan, S., Marín-de la Rosa, N., Vicente Conde, J., Sousa Correia, C., Pearce, S.P., Bassel, G.W., Hamali, B., Talloji, P., Tomé, D.F.A., Coego, A., Beynon, J., Alabadí, D., Bachmair, A., León, J., Gray, J.E., Theodoulou, F.L., Holdsworth, M.J. (2014) Nitric oxide sensing in plants is mediated by proteolytic control of Group VII ERF transcription factors. Molecular Cell; 53 no. 3, 369-379.
In this paper we elucidate a general molecular mechanism for nitric oxide sensing in plants. We show that Group VII ERFs act as nitric oxide sensors via the N-end rule pathway. Group VII ERFs are shown to mediate cross-talk between nitric oxide and Abscisic Acid. We also show that the N-end rule regulates nitric oxide homeostasis through Group VII ERFs.
- Dekkers, B.J.W., Pearce, S., van Bolderen-Veldkamp, R.P.M., Marshall, A., Widera, P., Gilbert, J., Drost, H-G., Bassel, G.W., Müller, K., King, J.R., Wood, A.T.A., Grosse, I., Quint, M., Krasnogor, N., *Leubner-Metzger, G., *Holdsworth, M.J., *Bentsink, L. (2013) Transcriptional Dynamics of Two Seed Compartments with Opposing Roles in Arabidopsis Seed Germination. Plant Physiology 163 no. 1, 205-215
*Joint senior authors.
This paper describes the temporal and spatial changes in genome expression during seed germination in Arabidopsis. It is an output of the vSEED ERANET-PG funded European consortium. Web based resources associated with the paper can be found at vseed.nottingham.ac.uk.
- Gonzalez-Guzman, M., Pizzio, G., Antoni, R., Vera-Sirera, F., Merilo, E., Bassel, G., Fernandez, M., Holdsworth, M.J., Perez-Amador, M., Kollist, H., Rodriguez P. (2012) Arabidopsis PYR/PYL/RCAR Receptors Play a Major Role in Quantitative Regulation of Stomatal Aperture and Transcriptional Response to Abscisic Acid. Plant Cell 24 no. 6, 2483-2496
This paper provides a detailed understanding of the role of the ABA PYR/PYL/RCAR receptors in the regulation of plant growth and development, showing them to be the major components of ABA perception.
- Middleton, A.M., Úbeda Tomás, S., Griffiths, J., Holman, T., Hedden, P., Thomas, S.G., Phillips, A.L., Holdsworth, M.J., Bennett, M.J., King, J.R., Owen, M.R. (2012) Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signalling. PNAS (USA), 109 no. 19, 7571–7576.
Mathematical modelling approaches used to understand GA biosynthesis, perception and signalling. CPIB paper.
- Bailey-Serres, J., Fukao, T., Gibbs, D.J., Holdsworth, M.J., Lee, S.C., Licausi, F., Perata, P., Voesenek, L.A.C.J., van Dongen, J.T. (2012) Making sense of low oxygen sensing. Trends in Plant Science, 17, 1360-1385. (Review article)
Here we review current knowledge in the area of plant low oxygen sensing, focussing on our recent discoveries of the role of the N-end rule pathway in regulating low-oxygen sensing through Group VII ERF transcription factors.
- Gibbs, D.J., Lee, S.C., Isa, N.M., Gramuglia, S., Fukao, T., Bassel, G.W., Sousa Correia, C., Corbineau, F., Theodoulou, F.L., Bailey-Serres, J., Holdsworth, M.J. (2011) Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature, 479, 415–418. [UKPMC+] web reference.
We identify a molecular mechanism through which low oxygen (hypoxia) is sensed in plants, a determinant of crop survival of root waterlogging and foliage submergence. This mechanism relates stability of hypoxia-associated transcription factors to the N-end rule pathway of targeted proteolysis, thus identifying the first plant N-end rule pathway substrates. Stability is related to the sequence of the protein N-terminus. Rice orthologue proteins, including the key regulator of submergence tolerance, exhibit different stabilities due to N-terminal variations. This mechanism is homeostatic: Prior to hypoxia the substrates are degraded, during hypoxia they accumulate, and following return to normoxia they decline.
- Bassel, G.W., Glaab, E., Marquez, J., *Holdsworth, M.J., *Bacardit, J. (2011) Functional Network Construction in Arabidopsis Using Rule-Based Machine Learning on Large-Scale Datasets. The Plant Cell, 23: 3101-3116.
*Joint senior authors.
A genome-wide network model generated using rule-based machine learning. Functional associations between genes are established by the collective ability to come together and form "rules" that accurately predict developmnetal outcome in seeds.
- Dupeux, F., Santiago, J., Betz, K., Twycross, J., Park, S-Y., Rodriguez, L., Gonzalez-Guzman, M., Jensen, M., Krasnogor, N., Holdsworth, M.J., Blackledge, M., Cutler, S., Rodriguez P. and Marquez, J. (2011) A Thermodynamic Switch Modulates Abscisic Acid Receptor Sensitivity. EMBO Journal 30: 4171 - 4184.
In this paper we significantly advance understanding of the role that ABA receptor dimerization plays in the modulation of the ABA response. We develop and validate a computational model of the interaction of receptors, hormone and phosphatases. Analysis of the dynamics of this model shows that competition for ABA binding between monomeric and dimeric receptors leads to preferential activation of monomeric receptors. Monomeric receptors provide strong and rapid response to ABA, while dimeric receptors provide weaker and slower response. By varying relative concentrations receptors, the overall ABA response can be modulated.
- Bassel, G.W., Holdsworth, M.J., Provart, N. (2011) Seed Bioinformatics. Methods in Molecular Biology 773 (8) 403-419, DOI: 10.1007/978-1-61779-231-1_23.
In this article we discuss the current tools available for seed bioinformatics.
- Pearce, S.P., King, J.R., Holdsworth, M.J. (2011) Axisymmetric indentation of curved elastic membranes by a convex rigid indenter. International Journal of Non-Linear Mechanics, 46 (9) 1128-1138
Using germination (specifically the biomechanics of endosperm rupture) as an example, this paper looks at how an elastic membrane deforms when a rigid indenter is pushed into it. The membrane is allowed to have an arbitrary shape and elastic properties, while the indenter may also take any convex shape.
- Bassel, G.W., Lan, H., Glaab, E., Gibbs, D.J., Gerjets, T., Krasnogor, N., Bonner, A.J., Holdsworth, M.J., Provart, N.J. (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. PNAS (USA), 108 (23) 9709-9714.
Front cover of PNAS features the SeedNet network.
In this manuscript we generated and analysed a genome-wide network model using publicly available data that describes global transcriptional interactions in Arabidopsis seeds that we term “SeedNet”, and show that SeedNet represents a step-change in our understanding of the regulation of germination.
- Lucas, M., Swarup, R., Paponov, I.A., Swarup, K., Casimiro, I., Lake, D., Péret, B., Zappala, S., Mairhofer, S., Whitworth, M., Wang, J.H., Ljung, K., Marchant, A., Sandberg, G., Holdsworth, M.J., Palme, K., Pridmore, T., Mooney, S., Bennett, M.J. (2011) SHORT-ROOT regulates primary, lateral and adventitious root development in Arabidopsis. Plant Physiology, 155: 384-398
- Holman, T.J, Wilson, M.H., Kenobi, K., Dryden, I.L., Hodgman, T.C., Wood, A.T.A., Holdsworth M. J. (2010) Statistical evaluation of transcriptomic data generated using the Affymetrix one-cycle, two-cycle and IVT-Express RNA labelling protocols with the Arabidopsis ATH1 microarray. Plant Methods, 6:9
- Gerjets, T., Scholefield, D., Foulkes, M.J., Lenton J.R., Holdsworth, M.J. (2010) An analysis of dormancy, ABA responsiveness, after-ripening and pre-harvest sprouting in hexaploid wheat (Triticum aestivum L.) caryopses. Journal of Experimental Botany, 61(2): 597-607
Front cover of The Journal of Experimental Botany features wheat ears showing Pre-Harvest Sprouting (PHS).
- Foulkes M.J., Hawkesford M.J., Barraclough P.B., Holdsworth M.J., Kerr S., Kightly S., Shewry P.R. (2009) Identifying traits to improve the nitrogen economy of wheat: recent advances and future prospects. Field Crops Research, 114(3): 329-342. Review Article.
- Holman, T., Jones, P.J., Russell, L., Medurst, A., Úbeda Tomás, S., Talloji, P., Marquez, J., Schmuths, H., Tung, S-A., Taylor, I., Footitt, S., Bachmair, A., Theodoulou, F., Holdsworth, M.J. (2009) The N-end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis. PNAS (USA), 106(11): 4549-4554.
- De Marcos Lousa, C., Dietrich, D., Johnson, B., Baldwin, S.A., Holdsworth, M.J., Theodoulou, F.L., Baker, A. (2009) The NBDs that wouldn't die: A cautionary tale of the use of isolated nucleotide binding domains of ABC transporters. Commun Integr Biol, 2(2): 97-9. Opinion Article.
- Dietrich, D., Schmuths, H., DeMarcos L. C., Baldwin, J., Baldwin, S., Baker, A., Theodoulou, F., Holdsworth, M. (2009) Mutations in the Arabidopsis ABC transporter COMATOSE allow differentiation between multiple functions in planta: insights from an allelic series. Mol Biol Cell, 20: 530 –543.
- Holdsworth, M.J., Soppe, W.S., Bentsink, L. (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New phytologist, 179(1), 33-54. Invited Tansley Review.
- Holdsworth, M.J., Finch-Savage, W.E., Grappin, P., Job, D. (2008) Post-genomics dissection of seed dormancy and germination. Trends in Plant Science, 13(1): 7-13. Opinion Article.
- Carrera, E., Holman, T., Medhurst, A., Dietrich, D., Footitt, S., Theodoulou, F.L., Holdsworth, M.J. (2008) Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. The Plant Journal 53(2): 214-224.
Front cover of The Plant Journal features the output of the TAGGIT ontological classification of seed transcriptomes in different germinative states.