Michael Holdsworth

Contact

• workRoom 301B South Lab
  Sutton Bonington Campus
  Sutton Bonington
  Leicestershire
  LE12 5RD
  UK
• work0115 951 6046
• michael.holdsworth@nottingham.ac.uk
• https://sites.google.com/site/michaelholdsworthlab/home

Research Summary

Current research programmes, recent publications etc are available on the Portal for the laboratory of Professor Holdsworth: HERE

Keywords: N-degron pathways, The N-end rule pathway of ubiquitin-mediated targeted proteolysis, protein degradation, proteostasis, oxygen sensing, hypoxia, , nitric oxide (NO) sensing, plant genetics

My research work in recent years has focused on understand the importance of oxygen sensing in plants, in particular discovering the roles that the N-degron pathways of ubiquitin-mediated proteolysis play in regulating plant growth and development, and response to the environment. This included the discovery that the branch of the pathway controlled by the E3 ligase PRT6 regulates ABA sensitivity of seed germination (PNAS 2009), acts as the molecular mechanism for oxygen sensing (Nature 2011) and nitric oxide sensing in flowering plants (Molecular Cell, 2014, Nature Comms 2019). We showed that oxygen sensing through this pathway controls skotomorphogenesis (Current Biology 2015), is a general regulator of plant abiotic (Current Biology 2017) and biotic (BMC Plant Biology 2016, New Phytologist 2019) stress responses, manipulation of the pathway leads to waterlogging tolerant barley (Plant Biotechnology Journal 2016) and the pathway controls the stability of multiple proteins (Nature Comms 2018, New Phytologist 2020).

Current areas of interest include:

• Characterisation of the plant N-degron pathways.
• Understanding the role of targeted proteolysis in sensing plant-environment interactions.
• Gasotransmitters and oxygen sensing.
• Providing molecular resources and conceptual frameworks that plant breeders and growers can use.

Research papers highlighting these areas:

The role of N-degron pathways of targeted proteolysis in the control of plant growth and development.

• Gibbs et al. Nature Communications (2018): Histone modifier VRN2 is an oxygen sensor.
• Vicente et al.Current Biology (2017): Discovery of the general role of the N-end rule pathway in sensing abiotic stresses.
• Gibbs et al. Molecular Cell (2014): Discovery of a general mechanism of nitric oxide sensing in plants.
• Gibbs et al. Nature (2011): Discovery of the mechanism of oxygen sensing in plants.

Systems approaches to understanding the control of seed germination and seedling establishment.

• Sanchez-Montesino et al. Molecular Plant (2019): Defining the role of the endosperm in seed germination.
• Bassel et al. PNAS (USA) (2014): 4D modelling of a germinating Arabidopsis embryo.
• Bassel et al. PNAS (USA) (2011): Genome wide network analysis of seed dormancy and germination.

Transfer of molecular genetic information from studies in model species, to address important agricultural problems associated with plant developmental biology and response to abiotic and biotic stress.

• Vicente et al. New Phytologist (2018) Enhancing plant immunity.
• Mendiondo et al. Plant Biotech. J. (2016) Making barley water-logging tolerant.
• Mendiondo et al. J. Ex. Bot. (2014) The function of COMATOSE in barley.

The Virtual Seed Web Resource vseed.nottingham.ac.uk:

This online resource provides queryable interfaces for Gene Networks associated with seed development, dormancy and germination. Users can zoom into networks, search and highlight genes of interest and download images of network representations.

Selected Publications

• MILLAR, A. HARVEY, HEAZLEWOOD, JOSHUA L., GIGLIONE, CARMELA, HOLDSWORTH, MICHAEL J., BACHMAIR, ANDREAS and SCHULZE, WALTRAUD X., 2019. The Scope, Functions, and Dynamics of Posttranslational Protein Modifications ANNUAL REVIEW OF PLANT BIOLOGY, VOL 70. 70, 119-151
• 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. and HOLDSWORTH, M. J., 2018. Oxygen-dependent proteolysis regulates the stability of angiosperm polycomb repressive complex 2 subunit VERNALIZATION 2 NATURE COMMUNICATIONS. 9,
• VICENTE J, MENDIONDO GM, MOVAHEDI M, PEIRATS-LLOBET M, JUAN YT, SHEN YY, DAMBIRE C, SMART K, RODRIGUEZ PL, CHARNG YY, GRAY JE and HOLDSWORTH MJ, 2017. The Cys-Arg/N-End Rule Pathway Is a General Sensor of Abiotic Stress in Flowering Plants. Current Biology. 27, 3183-3190
• GIBBS, D.J., LEE, S.C., ISA, N.M., GRAMUGLIA, .S, FUKAO, T., BASSEL, G.W., CORREIA, C.S., CORBINEAU, F., THEODOULOU, F.L., BAILEY-SERRES, J. and HOLDSWORTH, M.J., 2011. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature. 479(7373), 415-418

• View all publications

• OROSA, BEATRIZ, UESTUEN, SUAYIB, CALDERON VILLALOBOS, LUZ I. A., GENSCHIK, PASCAL, GIBBS, DANIEL, HOLDSWORTH, MICHAEL JOHN, ISONO, ERIKA, LOIS, MARIA, TRUJILLO, MARCO and SADANANDOM, ARI, 2020. Plant proteostasis - shaping the proteome: a research community aiming to understand molecular mechanisms that control protein abundance NEW PHYTOLOGIST. 227(4), 1028-1033
• HOLDSWORTH, MICHAEL J. and GIBBS, DANIEL J., 2020. Comparative Biology of Oxygen Sensing in Plants and Animals CURRENT BIOLOGY. 30(8), R362-R369
• LABANDERA, ANNE-MARIE, TEDDS, HANNAH M., BAILEY, MARK, SPRIGG, COLLEEN, ETHERINGTON, ROSS D., AKINTEWE, OLUNWATUNMISE, KALLEECHURN, GEETIKA, HOLDSWORTH, MICHAEL J. and GIBBS, DANIEL J., 2020. The PRT6 N-degron pathway restricts VERNALIZATION 2 to endogenous hypoxic niches to modulate plant development NEW PHYTOLOGIST.
• HOLDSWORTH, MICHAEL JOHN, VICENTE, JORGE, SHARMA, GUNJAN, ABBAS, MOHAMAD and ZUBRYCKA, AGATA, 2020. The plant N-degron pathways of ubiquitin-mediated proteolysis JOURNAL OF INTEGRATIVE PLANT BIOLOGY. 62(1), 70-89
• HARTMAN S, LIU Z, VAN VEEN H, VICENTE J, REINEN E, MARTOPAWIRO S, ZHANG H, VAN DONGEN N, BOSMAN F, BASSEL GW, VISSER EJW, BAILEY-SERRES J, THEODOULOU FL, HEBELSTRUP KH, GIBBS DJ, HOLDSWORTH MJ, SASIDHARAN R and VOESENEK LACJ, 2019. Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nature communications. 10(1), 4020
• MILLAR, A. HARVEY, HEAZLEWOOD, JOSHUA L., GIGLIONE, CARMELA, HOLDSWORTH, MICHAEL J., BACHMAIR, ANDREAS and SCHULZE, WALTRAUD X., 2019. The Scope, Functions, and Dynamics of Posttranslational Protein Modifications ANNUAL REVIEW OF PLANT BIOLOGY, VOL 70. 70, 119-151
• PEARCE, S. P., KING, J. R., STEINBRECHER, T., LEUBNER-METZGER, G., EVERITT, N. M. and HOLDSWORTH, M. J., 2018. Finite indentation of highly curved elastic shells PROCEEDINGS OF THE ROYAL SOCIETY A-MATHEMATICAL PHYSICAL AND ENGINEERING SCIENCES. 474(2209),
• TOMANOV K, NUKARINEN E, VICENTE J, MENDIONDO GM, WINTER N, NEHLIN L, WECKWERTH W, HOLDSWORTH MJ, TEIGE M and BACHMAIR A, 2018. Sumoylation and phosphorylation: hidden and overt links. Journal of experimental botany. 69(19), 4583-4590
• 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. 221, 988–1000
• SANCHEZ-MONTESINO, R., BOUZA-MORCILLO, L., MARQUEZ, J., GHITA, M., DURAN-NEBREDA, S., GOMEZ, L., HOLDSWORTH, M. J., BASSEL, G. and ONATE-SANCHEZ, L., 2018. A Regulatory Module Controlling GA-Mediated Endosperm Cell Expansion Is Critical for Seed Germination in Arabidopsis. Molecular Plant.
• 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. and HOLDSWORTH, M. J., 2018. Oxygen-dependent proteolysis regulates the stability of angiosperm polycomb repressive complex 2 subunit VERNALIZATION 2 NATURE COMMUNICATIONS. 9,
• SASIDHARAN R, BAILEY-SERRES J, ASHIKARI M, ATWELL BJ, COLMER TD, FAGERSTEDT K, FUKAO T, GEIGENBERGER P, HEBELSTRUP KH, HILL RD, HOLDSWORTH MJ, ISMAIL AM, LICAUSI F, MUSTROPH A, NAKAZONO M, PEDERSEN O, PERATA P, SAUTER M, SHIH MC, SORRELL BK, STRIKER GG, VAN DONGEN JT, WHELAN J, XIAO S, VISSER EJW and VOESENEK LACJ, 2017. Community recommendations on terminology and procedures used in flooding and low oxygen stress research. New Phytologist. 214(4), 1403-1407
• VICENTE J, MENDIONDO GM, MOVAHEDI M, PEIRATS-LLOBET M, JUAN YT, SHEN YY, DAMBIRE C, SMART K, RODRIGUEZ PL, CHARNG YY, GRAY JE and HOLDSWORTH MJ, 2017. The Cys-Arg/N-End Rule Pathway Is a General Sensor of Abiotic Stress in Flowering Plants. Current Biology. 27, 3183-3190
• HOLDSWORTH MJ, 2017. First hints of new sensors. Nature Plants. 3(10), 767-768
• DISSMEYER N, GRACIET E, HOLDSWORTH MJ and GIBBS DJ, 2017. N-term 2017: Proteostasis via the N-terminus. Trends in biochemical sciences. (In Press.)
• ZHANG H, GANNON L, HASSALL KL, DEERY MJ, GIBBS DJ, HOLDSWORTH MJ, VAN DER HOORN RAL, LILLEY KS and THEODOULOU FL, 2017. N-terminomics reveals control of Arabidopsis seed storage proteins and proteases by the Arg/N-end rule pathway. The New phytologist. (In Press.)
• 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, 2016. Enhanced waterlogging tolerance in barley by manipulation of expression of the N-end rule pathway E3 ligase PROTEOLYSIS6. Plant Biotechnology Journal. 40(1), 40-50
• GRAVOT A, RICHARD G, LIME T, LEMARIÉ S, JUBAULT M, LARIAGON C, LEMOINE J, VICENTE J, ROBERT-SEILANIANTZ A, HOLDSWORTH MJ and MANZANARES-DAULEUX MJ, 2016. Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot. BMC plant biology. 16(1), 251
• DEKKERS BJ, PEARCE SP, VAN BOLDEREN-VELDKAMP RP, HOLDSWORTH MJ and BENTSINK L, 2016. Dormant and after-Ripened Arabidopsis thaliana Seeds are Distinguished by Early Transcriptional Differences in the Imbibed State. Frontiers in plant science. 7, 1323
• GIBBS DJ, BAILEY M, TEDDS HM and HOLDSWORTH MJ, 2016. From start to finish: amino-terminal protein modifications as degradation signals in plants. The New phytologist. 211(4), 1188-94
• SHORINOLA O, BIRD N, SIMMONDS J, BERRY S, HENRIKSSON T, JACK P, WERNER P, GERJETS T, SCHOLEFIELD D, BALCÁRKOVÁ B, VALÁRIK M, HOLDSWORTH MJ, FLINTHAM J and 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), 4169-78
• WILSON, MICHAEL H, HOLMAN, TARA J, SORENSEN, IBEN, CANCHO-SANCHEZ, ESTER, WELLS, DARREN M, SWARUP, RANJAN, KNOX, J PAUL, WILLATS, WILLIAM G T, UBEDA-TOMAS, SUSANA, HOLDSWORTH, MICHAEL, BENNETT, MALCOLM J, VISSENBERG, KRIS and HODGMAN, T CHARLIE, 2015. Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone. Frontiers in cell and developmental biology. 3, 10
• SCHELER C, WEITBRECHT K, PEARCE SP, HAMPSTEAD A, BÜTTNER-MAINIK A, LEE KJD, VOEGELE A, ORACZ K, DEKKERS BJW, WANG X, WOOD ATA, BENTSINK L, KING JR, KNOX JP, HOLDSWORTH MJ, MÜLLER K and LEUBNER-METZGER G, 2015. Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases. Plant Physiology. 167(1), 200-215
• 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. 25(11), 1483-8
• GIBBS D, VICENTE CONDE J, BERCKHAN S, MENDIONDO GM, PRASAD G and HOLDSWORTH MJ, 2015. Group VII Ethylene Response Factors co-ordinate oxygen and nitric oxide signal transduction and stress responses in plants. Plant Physiology. 169, 23-31
• GIBBS DJ, MD ISA N, MOVAHEDI M, LOZANO-JUSTE J, MENDIONDO GM, BERCKHAN S, MARÍN-DE LA ROSA N, VICENTE CONDE J, SOUSA CORREIA C, PEARCE SP, BASSEL GW, HAMALI B, TALLOJI P, TOMÉ DFA, COEGO A, BEYNON J, ALABADÍ D, BACHMAIR A, LEÓN J, GRAY JE, THEODOULOU FL and HOLDSWORTH MJ, 2014. Nitric Oxide Sensing in Plants Is Mediated by Proteolytic Control of Group VII ERF Transcription Factors. Molecular Cell. 53(3), 369-379
• MARIN-DE LA ROSA N, SOTILLO B, MISKOLCZI P, GIBBS DJ, VICENTE J, CARBONERO P, ONATE-SANCHEZ L, HOLDSWORTH MJ, BHALERAO R, ALABADI D and BLAZQUEZ MA, 2014. Large-scale identification of gibberellin-related transcription factors defines Group VII ERFs as functional DELLA partners. Plant Physiology. 166, 1022-1032
• MENDIONDO GM, MEDHURST A, VAN ROERMUND CW, ZHANG X, DEVONSHIRE J, SCHOLEFIELD D, FERNÁNDEZ J, AXCELL B, RAMSAY L, WATERHAM HR, WAUGH R, THEODOULOU FL and HOLDSWORTH MJ, 2014. Barley has two peroxisomal ABC transporters with multiple functions in β-oxidation. Journal of Experimental Botany. 65(17), 4833-4847
• BASSEL GW, STAMM P, MOSCA G, BARBIER DE REUILLE P, GIBBS DJ, WINTER R, JANKA A, HOLDSWORTH MJ and SMITH RS, 2014. Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo. Proceedings of the National Academy of Sciences of the United States of America. 111(23), 8685-90
• GIBBS DJ, BACARDIT J, BACHMAIR A and HOLDSWORTH MJ, 2014. The eukaryotic N-end rule pathway: conserved mechanisms and diverse functions. Trends in Cell Biology. 24, 603–611
• DEKKERS B.J.W., PEARCE S., VAN BOLDEREN-VELDKAMP R.P., MARSHALL A., WIDERA P., GILBERT J., DROST H., BASSEL G.W., MÜLLER K., KING J.R., WOOD A.T.A., GROSSE I., QUINT M., KRASNOGOR N., LEUBNER-METZGER G., HOLDSWORTH M.J. and BENTSINK L., 2013. Transcriptional dynamics of two seed compartments with opposing roles in Arabidopsis seed germination. Plant physiology. 163(1), 205-15
• BAILEY-SERRES J., FUKAO T., GIBBS D.J., HOLDSWORTH M.J., LEE S.C., LICAUSI F., PERATA P., VOESENEK L.A.C.J. and VAN DONGEN J.T., 2012. Making Sense Of Low Oxygen Sensing. Trends In Plant Science. 17, 129-138
• MIDDLETON A.M., UBEDA-TOMÁS S., GRIFFITHS J., HOLMAN T., HEDDEN P., THOMAS S.G., PHILLIPS A.L., HOLDSWORTH M.J., BENNETT M.J., KING J.R. and OWEN M.R., 2012. Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signaling Proceedings of the National Academy of Sciences of the United States of America. 109(19), 7571-7576
• GONZALEZ-GUZMAN M, PIZZIO GA, ANTONI R, VERA-SIRERA F, MERILO E, BASSEL GW, FERNÁNDEZ MA, HOLDSWORTH MJ, PEREZ-AMADOR MA, KOLLIST H and RODRIGUEZ PL, 2012. Arabidopsis pyr/pyl/rcar receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. The Plant Cell. 24(6), 2483-96
• LUCAS, M., SWARUP, R., PAPONOV, I.A., SWARUP, K., CASIMIRO, I., LAKE, D., PERET, B., ZAPPALA, S., MAIRHOFER, S., WHITWORTH, M., WANG, J., LJUNG, K. and ET AL, 2011. Short-Root regulates primary, lateral, and adventitious root development in Arabidopsis. Plant Physiology. 155(1), 384-98
• BASSEL, G.W., LAN, H., GLAAB, E., GIBBS, D.J., GERJETS, T., KRASNOGOR, N., BONNER, A.J., HOLDSWORTH, M.J. and PROVART, N.J., 2011. Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions Proceedings of the National Academy of Sciences of the United States of America: PNAS. 108(23), 9709-9714
• BASSEL, G. W, HOLDSWORTH, M.J and PROVART, N.J., 2011. Seed bioinformatics. Methods in molecular biology (Clifton, N.J.). 773, 403-19
• BASSEL, G.W., GLAAB, E., MARQUEZ, J., HOLDSWORTH, M.J. and BACARDIT, J., 2011. Functional network construction in Arabidopsis using rule-based machine learning on large-scale data sets The Plant Cell. 23(9), 3101-3116
• GIBBS, D.J., LEE, S.C., ISA, N.M., GRAMUGLIA, .S, FUKAO, T., BASSEL, G.W., CORREIA, C.S., CORBINEAU, F., THEODOULOU, F.L., BAILEY-SERRES, J. and HOLDSWORTH, M.J., 2011. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature. 479(7373), 415-418
• PEARCE, SP, KING, JR and HOLDSWORTH, MJ, 2011. Axisymmetric Indentation Of Curved Elastic Membranes By A Convex Rigid Indenter International Journal Of Non-Linear Mechanics. 46(9), 1128-1138
• DUPEUX, F., SANTIAGO, J., BETZ, K., TWYCROSS, J., PARK, S-Y., RODRIGUEZ, L., GONZALEZ-GUZMAN, M., JENSEN, M.R., KRASNOGOR, N., BLACKLEDGE, M., HOLDSWORTH, M., CUTLER, S.R., RODRIGUEZ, P.L. and MÁRQUEZ, J.A., 2011. A thermodynamic switch modulates abscisic acid receptor sensitivity EMBO Journal. 30(20), 4171-4184
• GERJETS, T., SCHOLEFIELD, D., FOULKES, M.J., LENTON, J.R. and 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
• HOLMAN, T J, WILSON, M H, KENOBI, K, DRYDEN, I L, HODGMAN, T C, WOOD, A T and 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
• DIETRICH, D, SCHMUTHS, H, DE MARCOS LOUSA, C, BALDWIN, J M, BALDWIN, S A, BAKER, A, THEODOULOU, F L and HOLDSWORTH, M J, 2009. Mutations in the Arabidopsis peroxisomal ABC transporter COMATOSE allow differentiation between multiple functions in planta: insights from an allelic series. Molecular Biology of the Cell. 20(1), 530-43
• HOLMAN, T.J., JONES, P.D., RUSSELL, L., MEDHURST, A., TOMÁS, S.U., TALLOJI, P., MARQUEZ, J., SCHMUTHS, H., TUNG, S-A., TAYLOR, I., FOOTITT, S., BACHMAIR, A., THEODOULOU, F.L. and HOLDWORTH, M.J., 2009. The N-end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis Proceedings of the National Academy of Sciences of the United States of America: PNAS. 106(11), 4549-4554
• HOLDSWORTH, M J, BENTSINK, L and SOPPE, W J J, 2008. Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytologist. 179(1), 33-54
• HOLDSWORTH, M J, FINCH-SAVAGE, W E, GRAPPIN, P and JOB, D, 2008. Post-genomics dissection of seed dormancy and germination. Trends in Plant Science. 13(1), 7-13
• CARRERA, E, HOLMAN, T, MEDHURST, A, DIETRICH, D, FOOTITT, S, THEODOULOU, F L and HOLDSWORTH, M J, 2008. Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant Journal. 53(2), 214-24
• CARRERA, E., HOLMAN, T., MEDHURST, A., PEER, W., SCHMUTHS, H., FOOTITT, S., THEODOULOU, F.L. and HOLDSWORTH, M.J., 2007. Gene expression profiling reveals defined functions of the ATP-binding cassette transporter COMATOSE late in phase II of germination Plant Physiology. 143(4), 1669-79
• FOOTITT, S, DIETRICH, D, FAIT, A, FERNIE, A R, HOLDSWORTH, M J, BAKER, A and THEODOULOU, F L, 2007. The COMATOSE ATP-Binding Cassette Transporter Is Required for Full Fertility in Arabidopsis. Plant Physiology. 144(3), 1467-80
• HUNT, L, HOLDSWORTH, M J and GRAY, J E, 2007. Nicotinamidase activity is important for germination. Plant Journal. 51(3), 341-51
• BAUDO, M. M., LYONS, R., POWERS, S., PASTORI, G. M., EDWARDS, K. J., HOLDSWORTH, M. J. and SHEWRY, P. R., 2006. Transgenesis has less impact on the transcriptome of wheat grain than conventional breeding Plant Biotechnology Journal. VOL 4(NUMBER 4), 369-380
• FOOTITT, S, MARQUEZ, J, SCHMUTHS, H, BAKER, A, THEODOULOU, F L and HOLDSWORTH, M, 2006. Analysis of the role of COMATOSE and peroxisomal beta-oxidation in the determination of germination potential in Arabidopsis. Journal of Experimental Botany. 57(11), 2805-14
• MAYES, S., HOLDSWORTH, M.J., PELLEGRINESCHI, A. and REYNOLDS, M., 2005. Allying genetic and physiological innovations to improve productivity of wheat and other crops. In: Yields of farmed species - Constraints and Opportunities in the 21st century Nottingham University Press, Nottingham. 89 - 122
• EDWARDS, D., STEVENSON, D., FORSYTH, A., HEGARTY, M., BATLEY, J., HOLDSWORTH, M.J. and EDWARDS, K.J., 2004. Identification of transposon-tagged maize genes displaying homology to arrayed cDNA clones with the use of Mutator insertion display Genome. 1, 48-55
• FOOTITT, S., SLOCOMBE, S.P., LARNER, V., KURUP, S., WU, Y., LARSON, T., GRAHAM, I., BAKER, A. and HOLDSWORTH, M., 2002. Control of germination and lipid mobilisation by COMATOSE, the Arabidopsis homologue of human ALDP EMBO Journal. 21(12), 2912-2922
• MCKIBBIN, R.S., WILKINSON, M.D., BAILEY, P.C., FLINTHAM, J.E., ANDREW, L.M., LAZZERI, P.A., GALE, M.D., LENTON, J.R. and HOLDSWORTH, M.J., 2002. Transcripts of Vp-1 homeologues are misspliced in modern wheat and ancestral species Proceedings of the National Academy of Sciences of the United States of America. 99(15), 10203-8
• WILKINSON, M. D., MCKIBBIN, R. S., BAILEY, P. C., FLINTHAM, J. E., GALE, M. D., LENTON, J. R. and HOLDSWORTH, M. J., 2002. Use of comparative molecular genetics to study pre harvest sprouting in wheat Euphytica. VOL 126(1), 27 - 33
• PAZ-ARES, JAVIER and THE REGIA CONSORTIUM,, 2002. REGIA, An EU Project on Functional Genomics of Transcription Factors From Arabidopsis Thaliana. Comparative and functional genomics. 3(2), 102-8
• HEDDEN, P, HOLDSWORTH, M J, SIMPSON, G G, EDWARDS, K J and LENTON, J R, 2002. New frontiers in plant development: from genes to phenotype. Trends in Plant Science. 7(9), 381-3
• HOLDSWORTH, M.J., LENTON, J.R., FLINTHAM, J.E., GALE, M.D., KURUP, S., MCKIBBIN, R.S., BAILEY, P.C., LARNER, V. and RUSSELL, L., 2001. Genetic control mechanisms regulating the initiation of germination Journal of Plant Physiology. 158(4), 439
• RUSSELL, L, LARNER, V, KURUP, S, BOUGOURD, S and HOLDSWORTH, M, 2000. The Arabidopsis COMATOSE locus regulates germination potential. Development (Cambridge). 127(17), 3759-67
• KURUP, S, JONES, H D and HOLDSWORTH, M J, 2000. Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds. Plant Journal. 21(2), 143-55
• JONES, H D, KURUP, S, PETERS, N C and HOLDSWORTH, M J, 2000. Identification and analysis of proteins that interact with the Avena fatua homologue of the maize transcription factor VIVIPAROUS 1. Plant Journal. 21(2), 133-42
• BAILEY, P. C., MCKIBBIN, R. S., LENTON, J. R., HOLDSWORTH, M. J., FLINTHAM, J. E. and GALE, M. D., 1999. Genetic map locations for orthologous Vp1 genes in wheat and rice Theoretical and Applied Genetics. VOL 98(NUMBER 2), 281-284
• ALBANI, D, HAMMOND-KOSACK, M C, SMITH, C, CONLAN, S, COLOT, V, HOLDSWORTH, M and BEVAN, M W, 1997. The wheat transcriptional activator SPA: a seed-specific bZIP protein that recognizes the GCN4-like motif in the bifactorial endosperm box of prolamin genes. Plant Cell. 9(2), 171-84
• HOLDSWORTH, M J, MUñOZ-BLANCO, J, HAMMOND-KOSACK, M, COLOT, V, SCHUCH, W and BEVAN, M W, 1995. The maize transcription factor Opaque-2 activates a wheat glutenin promoter in plant and yeast cells. Plant Molecular Biology. 29(4), 711-20
• GRIERSON, C, DU, J S, DE TORRES ZABALA, M, BEGGS, K, SMITH, C, HOLDSWORTH, M and BEVAN, M, 1994. Separate cis sequences and trans factors direct metabolic and developmental regulation of a potato tuber storage protein gene. Plant Journal. 5(6), 815-26
• BEVAN, M, COLOT, V, HAMMOND-KOSACK, M, HOLDSWORTH, M, TORRES DE ZABALA, M, SMITH, C, GRIERSON, C and BEGGS, K, 1993. Transcriptional control of plant storage protein genes. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences. 342(1301), 209-15
• HAMMOND-KOSACK, M C, HOLDSWORTH, M J and BEVAN, M W, 1993. In vivo footprinting of a low molecular weight glutenin gene (LMWG-1D1) in wheat endosperm. EMBO Journal. 12(2), 545-54
• HOLDSWORTH, M J, GRIERSON, C, SCHUCH, W and BEVAN, M, 1992. DNA-binding properties of cloned TATA-binding protein from potato tubers. Plant Molecular Biology. 19(3), 455-64
• HOLDSWORTH, M.J and G.G. LATIES, 1989. Site-specific binding of a nuclear factor to the carrot extensin gene is influenced by ethylene and wounding Planta. 179, 17-23
• HOLDSWORTH, M.J and G.G. LATIES, 1989. Identification of a wound-induced inhibitor of a nuclear factor that binds the carrot extensin gene Planta. 180, 74-81
• HOLDSWORTH, M J, SCHUCH, W and GRIERSON, D, 1987. Nucleotide sequence of an ethylene-related gene from tomato. Nucleic Acids Research. 15(24), 10600
• HOLDSWORTH, M J, BIRD, C R, RAY, J, SCHUCH, W and GRIERSON, D, 1987. Structure and expression of an ethylene-related mRNA from tomato. Nucleic Acids Research. 15(2), 731-9