The Plant Stress group is based in the School of Natural Sciences at the University of Manchester. In trying to understand how stress impacts on plants, we use a range of techniques from molecular to ecological. Current projects focus on the short term regulation of electron transport in response to stress and the longer term ability of plants to change their photosynthetic capacity in response to changing environmental conditions.

In recent years concern has been growing about the consequences of global climate change caused by human emissions of CO₂. This is predicted, in addition to causing a general warming of the planet, to cause an increase in the occurrence of extreme weather events (IPCC). Periods of drought and extreme temperature (high and low) and incidents of flooding are all liable to increase. This is of particular concern because of the likely impact on food production. Even if average conditions are favourable for plant growth, even short periods of extreme conditions at crucial times on the growing season can stress plants, lowering crop yields. The aim of our research is to understand how plants are damaged when exposed to changing conditions and how stress tolerant plants are able to avoid that damage. The particular focus of our research is to understand the impact of stress on the process of photosynthesis. the photosynthetic apparatus is especially sensitive to environmental stress and is the source of most of the damage that can occur.

We are interested in the regulation of higher plant photosynthesis under conditions of environmental stress. In particular we are trying to understand the mechanisms that allow certain plants to tolerate stress and avoid the production of Reactive Oxygen Species (ROS) when exposed to stress. We use a range of techniqes, including spectroscopic analyses of in vivo photosynthetic performance, biochemical approaches, including quantitative proteomics, and molecular approaches.

For our purposes, we define environmental (or abiotic) stress as being any conditions that give rise to imbalances in the ability of a plant to perform normal metabolic processes. This might include extremes of temperature, light, water availability etc. We are primarily interested in conditions that are liable to result in an imbalance between the absorption of light by chlorophyll and the use of the absorbed energy in photosynthetically driven metabolic processes. When such an imbalance occurs, any excess absorbed energy is liable to give rise to ROS production.

Absorption of excess energy is liable to result in the production of ROS. These are highly reactive derivatives of oxygen that are capable of reacting with and destroying a wide range of biomolecules including DNA, proteins and lipids. The chloroplast is the major source of ROS in plant leaves, with these being mainly formed via one of two routes: 1) photoreduction of molecular oxygen gives rise to superoxide (O₂^-) in the so-called Mehler reaction. This in turn can undergo dismutation to produce hydrogen peroxide (H₂O₂) which can in turn form hydroxyl radicals. 2) Singlet excited oxygen can be formed by the interaction of molecular oxygen with triplet excited chlorophyll. The latter is formed either via intersystem crossing from singlet excited chlorophyll or through charge recombination reactions taking place primarily in the photosystem II reaction centre.

When the absorption of light exceeds the capacity for photosynthetic metabolism, ROS are liable to be formed. To avoid this, the plant must ensure that the excess energy is dissipated harmlessly. Avoidance of the Mehler reaction can be achieved through controlling the flow of electrons through the electron transport chain. This is achieved by down regulating the cytochrome b6f complex, between photosystems II and I. The mechanism of this regulation is uncertain, however we have evidence that this is achieved via a redox feedback mechanism, probbaly from NADPH (Johnson 2003 ; Hald et al. 2008). Avoidance of singlet oxygen formation is achieved by activating processes that dissipate excess light energy as heat - in particular high energy state quenching. This is triggered by the presence of a pH gradient across the thylakoid membrane. The control of this gradient is not fully understood, however there is growing evidence that this requires cyclic electron transport to occur, involving only the Photosystem I reaction centre (see Johnson 2005 ; Johnson et al. 2015). We are seeking to understand the mechanism and regulation of cyclic electron transport.

Currently we are actively researching the role of a thylakoid protein complex called the Plastid Terminal Oxidase (PTOX) in protecting plants from excess light (Johnson and Stepien, 2017 ; Stepien and Johnson 2018). PTOX is a plastoquinone oxygen oxidoreductase, which we have shown acts as a significant sink for electron transport in the model salt tolerant plant Eutrema salsugineum. The activation of this protein requires a translocation in the thylakoid membrane, from the stromal lamellae to the grana stacks. We are working to establish how this process is controlled.

The term acclimation refers to a change in the phenotype of a plant in response to its environment. This is distinguished from adaptation, which describes a different in the genotype of plants which are native to different habitats. When plants are grown in particular conditions, they can adjust the composition of their photosynthetic apparatus to suit those conditions. For example, plants growing in low light will typically have a high content of chlorophyll binding proteins, increasing their light capture, relative to the enzymes which assimilate that light energy (e.g. Rubisco, which fixes carbon dioxide). This is a form of acclimation which is seen during the development of the plant. Plants grown in shade will often have thinner leaves and a lower capacity for photosynthesis than those grown in full sun

If plants are transferred from one set of environmental conditions to another (e.g. low to high light; high to low temperature), we commonly observe that they are able to change their photosynthetic capacity. This is an example of dynamic acclimation. We have seen that developmental and dynamic acclimation are, at least to some extent, distinct processes.

We are studying the mechanisms controlling dynamic acclimation to light and temperature. We have used transciptomics and metabolomics to show that the signals involved in regulation of the acclimation responses arise from metabolism, probably the relative concentrations of or fluxes to particular metabolites. We are using semi-quantitative proteomics to fully identify the molecular changes involved and are using metabolic modelling to try and better understand the responses of metabolism to the environment.

Current group members are:

• Megan Barker - senior technician
• Norazreen Binti Abd Rahman - PhD student
• Emma Blackledge - MSci student
• Pablo Calzadilla - Honorary research fellow
• Prof. Giles Johnson - group leader
• Nabila Juhi - PhD student
• Aashna Khan - PhD student
• Paula Munoz - Post doctoral research associate
• Josef Oliver - PhD student
• Shukanta Saha - PhD student
• Junliang Song - PhD student

Links are to publishers websites. If you are unable to access these please email us for a reprint

• Calzadilla P.I. Song J. Gallois P. and Johnson G.N. (2024) "Proximity to Photosystem II is necessary for activation of Plastid Terminal Oxidase (PTOX) for photoprotection". Nature Communications 15 287
• Gjindali A. and Johnson G.N. (2023) "Photosynthetic acclimation to changing environments". Biochemical Society Transactions 51 473-486
• Saunders H.A., Calzadilla P.I., Schwartz J.M. and Johnson G.N.(2022) "Cytosolic fumarase acts as a metabolic fail-safe for both high and low temperature acclimation of Arabidopsis thaliana". Journal of Experimental Botany 73 2112-2124
• Kennedy J.P., Johnson G.N., Preziosi R.F. and Rowntree J.K. (2022) "Genetically based adaptive trait shifts at an expanding mangrove range margin". Hydrobiologia 849 1777-1794
• Ajith A., Milnes P.J., Johnson G.N. and Lockyer N.P. (2022)  "Mass Spectrometry Imaging for Spatial Chemical Profiling of Vegetative Parts of Plants". Plants 11 1234
• Karim M.F. and Johnson G.N. (2021)  "Acclimation of Photosynthesis to Changes in the Environment Results in Decreases of Oxidative Stress in Arabidopsis thaliana". Frontiers in Plant Science doi: 10.3389/fpls.2021.683986
• Gjindali A., Hermann H.A., Schwartz J.M., Johnson G.N. and Calzadilla P.I. (2021)  "A Holistic Approach to Study Photosynthetic Acclimation Responses of Plants to Fluctuating Light". Frontiers in Plant Science doi: 10.3389/fpls.2021.668512
• Ahmad N., Khan M.O., Silam E., Wei Z., McAusland L., Lawson T., Johnson G.N. and Nixon P.J.. (2020) "Contrasting responses to stress displayed by tobacco overexpressing algal plastid terminal oxidase in the chloroplast". Frontiers in Plant Science doi: 10.3389/fpls.2020.00501
• Hermann H.A. Schwartz J.-M. and Johnson G.N. (2019) "From Empirical to Theoretical Models of Light Response Curves:Linking photosynthetic and metabolic acclimation". Photosynthesis Research doi: 10.1007/s11120-019-00681-2
• Herrmann H.A., Dyson B.C., Vass L., Johnson G.N. and Schwartz J.M. (2019) "Flux sampling as a powerful tool to study metabolism under changing environmental conditions" NPJ Systems Biology and Applications, 5, 32
• Johnson, G. (2019) "Plant physiology: a primer" [Video file]. In The Biomedical& Life Sciences Collection, Henry Stewart Talks.
• Herrmann H.A., Schwartz J.-M. and Johnson G.N. (2019) "Metabolic acclimation—a key to enhancing photosynthesis in changing environments? " Journal of Experimental Botany 70, 3043-3056
• Stepien P. and Johnson G.N. (2018) "Plastid terminal oxidase requires translocation to the grana stacks to act as a sink for electron transport" Proceedings of the National Academy of Sciences USA 115 9634-9639
• Fry EL, Johnson GN, Hall AL, Pritchard WJ, Bullock JM, Bardgett RD (2018) "Drought neutralises plant–soil feedback of two mesic grassland forbs."  Oecologia, 186, 1113–1125
• Casella S., Huang F., Mason D.,  Zhao G.Y., Johnson G.N., Mullineaux C.W., and Liu L-N. (2017) "Dissecting the native architecture and dynamics of cyanobacterial photosynthetic machinery"  Molecular Plant, Volume 10, 1434–1448
• Chapman S.P.,  Trindade dos Santos, M., Johnson,G.N.,  Vieira Kritz, M. and Schwartz J.M. (2017) Cyclic decomposition explains a photosynthetic down regulation for Chlamydomonas reinhardtii Biosystems 162, 119–127
• Miller M.A.E., O'Cualain R., Selley J., Karim M.F., Knight D., Hubbard S. and Johnson G.N. (2017) "Dynamic Acclimation to High Light in Arabidopsis thaliana Involves Widespread Reengineering of the Leaf Proteome".  Frontiers in Plant Science doi:10.3389/fpls.2017.01239
• Dyson B.C., Miller M.A.E., Feil R., Rattray N., Bowsher C.G., Goodacre R., Lunn J.E. and Johnson G.N. (2016) "FUM2, a cytosolic fumarase, is essential for acclimation to low temperature in Arabidopsis thaliana".  Plant Physiology 172,  1818-127
• Johnson G.N. and Stepien P. (2016)  "Plastid Terminal Oxidase as a Route to Improving Plant Stress Tolerance: Known Knowns and Known Unknowns" Plant and Cell Physiology, 57 1387-1396. .
• Finazzi, G., Minigawa J., Johnson G.N. (2016) The Cytochrome b6f Complex: A Regulatory Hub Controlling Electron Flow and the Dynamics of Photosynthesis?  in W.A. Cramer and T. Kallas (eds.), Cytochrome Complexes: Evolution, Structures,
  Energy Transduction, and Signaling, Advances in Photosynthesis and Respiration 41, pp. 437–452, DOI 10.1007/978-94-017-7481-9_22,Springer, Dordrecht
• Finazzi, G. and Johnson G.N. (2017) "Cyclic electron flow: facts and hypotheses"  Photosynthesis Research 129, 227-230 
  
• Ogbaga C.C., Stepien P., Dyson B.C., Rattray N.J.W., Ellis D.I. Goodacre R. and Johnson G.N. (2016) "Biochemical analyses of sorghum varieties reveal differential responses to drought". Plos One 11(5): e0154423. doi:10.1371/journal.pone.0154423.
• Chapman S.P., Paget C.M., Johnson G.N. and Schwartz J.-M. (2015) "Flux balance analysis reveals acetate metabolism modulates cyclic electron flow and alternative glycolytic pathways in Chlamydomonas reinhardtii".  Front. Plant Sci. 6, 474 doi:10.3389/fpls.2015.00474.
• Retuke R., Smith-Unna S.E., Smith R.W., Burgess A.J., Jensen O.E., Johnson G.N. and Murchie E.H. (2015) "Exploiting heterogeneous environments:  does photosynthetic acclimation optimise carbon gain in fluctuating light?" Journal of Experimental Botany, 66, 2437-2447.
• Dyson B.C., Allwood J.W., Feil R., Yun X., Miller M., Bowsher C.G., Goodacre R., Lunn J.E. and Johnson G.N. (2015) "Acclimation of metabolism to light in Arabidopsis thaliana - the glucose-6-phosphate/phosphate translocator GPT2 directs metabolic acclimation".  Plant Cell and Environment 38, 1404-1417.
• Johnson G.N., Cardol P., Minigawa J. and Finazzi G. (2014) "Regulation of Electron Transport in Photosynthesis" in Plastid Biology, Theg S. and Wollman F.A. eds, Springer.
  
• Dyson B. and Johnson G.N. (2014) "Photosynthesis: Ecology" Encyclopedia of Life Sciences DOI: 10.1002/9780470015902.a0003198.pub2
• Ogbaga C., Stepien, P. and Johnson G.N. (2014) Sorghum (Sorghum bicolor L.) varieties adopt strongly contrasting strategies in response to drought.  Physiologia Plantarum, 152, 389-401.
  
• Dyson B., Webster R.E. and Johnson G.N. (2014) GPT2: a glucose 6-phosphate/phosphate transporter translocator with a novel role in the regulation of sugar signalling during seedling development.  Annals of Botany, 113 (4): 643-652
• Johnson G. and Murchie E. (2011) Gas Exchange Measurements for the Determination of Photosynthetic Efficiency in Arabidopsis Leaves. in Jarvis R.P. ed. Chloroplast Research in Arabidopsis pp 311-326. Humana Press, New York
  
• Joliot P. and Johnson G.N. (2011) Regulation of Cyclic and Linear Electron Flow in Higher Plants.  Proc. Nat. Acad. Sci 108, 13317-13322.
  
• Johnson G.N. (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim. Biophys. Acta - Bioenergetics 1807, 384-389.
  
• Athanasiou K., Dyson B., Webster R.E. and Johnson G.N. (2010). Dynamic acclimation of photosynthesis increases plant fitness in changing environments. Plant Physiology, 152(1), 366-373.
• Bondarava N., Gross C.M., Mubarakshina M., Golecki J.R., Johnson G.N. and Krieger-Liszkay A.. (2010). Putative function of cytochrome b559 as a plastoquinol oxidase. Physiologia Plantarum, 138(4), 463-473
• Stepien P, Johnson GN. (2009). Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis thaliana and the halophyte Thellungiella halophila. Role of the plastid terminal oxidase as an alternative electron sink. Plant Physiology, 149, 1154-1165.
• Hunt J.W., Dean A.P., Webster R.E. Johnson G.N. and Ennos A.R. (2008) A novel mechanism by which silica defends grasses against herbivory. Annals of Botany 102, 653-656.
• Hald S., Pribil M., Leister D., Gallois P. and Johnson G.N. (2008) Competition between linear and cyclic electron flow in plants deficient in Photosystem I. Biochimica et Biophysica Acta 1777, 1173-1183
• Hald S., Nandha B., Gallois P. and Johnson G.N. (2008) Feedback regulation of photosynthetic electron transport by NADP(H) redox poise. Biochimica et Biophysica Acta 1777 433-440.
• Nandha B., Finazzi G., Joliot P., Hald S. and Johnson G.N. (2007) The role of PGR5 in the redox poising of photosynthetic electron transport. Biochimica et Biophysica Acta 1767, 1252-1259
• Perez-Torres E., Bravo L.A., Corcuera L.J. and Johnson G.N. (2007) Is electron transport to oxygen an important mechanism in photoprotection? Contrasting responses from Antarctic vascular plants Physiologia Plantarum 130, 185–194
• Breyton C., Nandha B., Johnson G.N., Joliot P. and Finazzi G. (2006) Redox modulation of cyclic electron flow around Photosystem I in C3 plants. Biochemistry, 45, 13465-13475
• Finazzi G., Johnson G.N., Dall’Osto L. Zito F. Bonente F., Bassi R. and Wollman F.-A. (2006)  Non-photochemical quenching of chlorophyll fluorescence and light adaptation in Chlamydomonas reinhardtii.  Biochemistry, 45, 490-498
• Joliot P., Joliot A. and Johnson G.N. (2006) "Cyclic electron transfer around Photosystem I" in "Photosystem I: The Light-Driven Plastocyanin:Ferredoxin Oxidoreductase" pp 639-656 J. Goldbeck ed. Springer, Netherlands.
• Johnson G.N. (2005) “Cyclic electron transport in C3 plants: fact or artefact?  J. Exp. Bot. 56, 407-416
• Golding A.J. Joliot P. and Johnson G.N. (2005) “Equilibration between cytochrome f and P700 in intact leaves” Biochimica et Biophysica Acta-Bioenergetics, 1706, 105-109
• Johnson G.N. (2004) “Controversy remains: regulation of pH gradient across the thylakoid membrane” Trends in Plant Science, 9, 570-571.
• Golding A.J., Finazzi, G. and Johnson G.N. (2004) “Reduction of the thylakoid electron transport chain by stromal reductants – evidence for activation of cyclic electron transport upon dark adaptation or under drought”.  Planta, 220, 356-363
• Hermans C., Johnson G.N., Strasser R.J., Verbruggen N. (2004) “Physiological characterisation of magnesium deficiency in sugar beet: acclimation to low magnesium differentially affects photosystems I and II” Planta 220, 344-355.
• Finazzi G., Johnson G.N., Dallosto L., Joliot P., Wollman F.A., Bassi  R (2004) “A zeaxanthin-independent non-photochemical quenching mechanism localized in the Photosystem II core complex.”.  Proc. Nat. Acad. Sci. 101 12375-12380
• Kramer, D.M., Johnson, G., Kiirats, O. and Edwards, G.E. (2004) “New fluorescence parameters for the determination of QA redox state and excitation energy fluxes”.  Photosynthesis Research, 79, 209-218
• Johnson, G.N. (2003) “Thiol regulation of the thylakoid electron transport chain – a missing link in the regulation of photosynthesis? Biochemistry, 42, 3040-3044
• Semerdjieva, S.I., Sheffield, E., Phoenix, G.K., Gwynn-Jones, D., Callaghan, T.V. and Johnson, G.N. (2003) "Contrasting strategies for UV-B screening in sub-Arctic dwarf shrubs".  Plant Cell and Environment, 26, 957-964
• Golding, A.J. and Johnson, G.N. (2003) "Down regulation of linear and activation of cyclic electron transort during drought".  Planta, 218, 107-114 + erratum
• Clarke, J. and Johnson, G.N. (2001) "Temperature dependence of cyclic and pseudocyclic electron transport in barley leaves" Planta 212, 808-816
• Rosevear, M. Young, A.J. and Johnson, G.N. (2001) "Growth conditions are more important than species origin in determining leaf pigment content of British plant species" Functional Ecology 15, 474-480
• Yin, Z.-H. and Johnson, G.N. (2000) "Acclimation of photosynthesis to growth in flecked light regimes" Photosynthesis Research 63, 97-107
• Maxwell, K. and Johnson, G.N. (2000) "Chlorophyll fluorescence: a beginners guide." Journal of Experimental Botany 51, 659-668.
• Johnson, G.N., Rumsey, F.J, .Headley, A.D. and Sheffield, E. (2000) "Adaptations to extreme low light in the fern Trichomanes speciosum" New Phytologist 148, 423-431
• Krieger, A. Kienzler, K. and Johnson, G.N.  (2000) "Inhibition of the electron transport chain protects against photoinibition of photosystem II" FEBS Letters 486, 191-194
• Ott, T., Clarke, J., Birks, K. and Johnson, G.N. (1999) "Regulation of higher plant photosynthetic electron transport" Planta, 209, 250-258.
• Walters, R.G. and Johnson, G.N. (1997) "The effects of elevated light on photosystem II function: A thermoluminescence study" Photosynthesis Research 54, 169-183
• Johnson, G.N., Rutherford, A.W. and Krieger, A. (1995) "A change in the mid-point potential of the quinone QA in Photosystem II associated with photoactivation of oxygen evolution" Biochim. Biophys. Acta, 1229, 202-207.
• Krieger, A. Rutherford, A.W. and Johnson G.N. (1995) "On the determination of the redox mid-point potential of the primary quinone electron acceptor QA, in Photosystem II"  Biochim Biophys Acta 1229, 193-201
• Johnson, G.N., Boussac, A. and Rutherford, A.W. (1994) "The origin of the 40-50°C thermoluminescence bands in Photosystem II"  Biochim. Biophys. Acta, 1184, 85-92.
• Johnson, G.N. and Krieger, A.W. (1994) "Thermoluminescence as a probe of Photosystem II in intact leaves: Non-photochemical fluorescence quenching in peas grown in an intermittent light regime" Photosynth. Res. 41, 371-380. 
• Johnson, G.N. Young, A. and Horton, P.  (1994) "Activation of non-photochemical quenching in thylakoids and leaves" Planta 194, 550-556.
• Johnson, G.N., Scholes, J.D., Horton, P. and Young, A. (1993) "Relationships between carotenoid composition and growth habitat in British plant species" Plant Cell Envir. 16, 681-686.
• Johnson, G.N., Scholes, J.D., Young, A.J. and Horton, P. (1993) "The dissipation of excess excitation energy in British plant species" Plant Cell Envir. 16, 673-680.

Chlorophyll fluorescence analysis is very widely used in plant physiology as it provides the ability to monitor with great precision processes occurring in the chloroplast in a completely non-invasive manner. Simply applying a flash of light to a leaf is enough to rapidly assess the efficiency with which the leaf is performing photosynthesis. Fluorescence arises primarily from Photosystem II and by examining changes in fluoresence yield over time we can both follow changes in photosynthesis, in the ability of the plant to dissipate light energy as heat and in the extent of damage to Photosystem II (photoinhibition). To measure chlorophyll fluorescence in the lab we use Walz fluorimeters. These are incorportated into data acquisition systems using National Instruments data acquisition cards combined with laboratory written software

A detailed discussion of this analysis can be found in Maxwell and Johnson (2000)

Many of the components of the photosynthetic apparatus undergo optical changes depending on their redox state. This allows us to follow electron flow through multiple components of the electron transport chain, including cytochrome f, cytochrome b, P700 and plastocyanin. The absorbtion changes occurring are however very small and occur in a background that is both highly absorbing and highly scattering, therfore specialised, purpose built spectrophotometers. We have a system that is specially designed for leaf measurements and which was developed for us by Daniel Beal and Pierre Joliot . A commercial version of this system is available from Biologic. For routine measurements of Photosystem I turnover, we use a Walz spectrophotometer with a NIR detector. We also work with a portable PhotosynQ system, developed by Prof David Kramer and colleagues

Positions for post-docs, when available, are advertised in jobs.ac.uk. Scientists nearing the end or having completed their PhD's who are interested in coming to join us are welcome to enquire, however, about the possibilities of applying for fellowships. We are able to offer help to any suitably qualified individuals wishing to apply for a postdoctoral fellowship. Funds for non-UK residents in particular are available e.g. through the European Union, FEBS, EMBO, Royal Society and through national funding councils.

Positions for PhD studies are available annually, usually starting in September. Funding may be available through BBSRC, Presidents Award or Deans Award. Applicants with their own sources of funding are also encouraged to apply and we can, if appropriate, provide support for such applications. Informal enquiries to Giles Johnson, formal applications must be made via the University web site.

Prof Giles Johnson
Department of Earth and Environmental Sciences
University of Manchester
Michael Smith Building
Oxford Road
Manchester
M13 9PT

Email: giles.johnson@manchester.ac.uk

Tel: +44 161 275 5750
Lab: +44 161 275 3916
Fax: +44 161 275 5082