Photosynthesis for a changing world

29 April 2017 - By: Caroline Wood

Photosynthesis for a changing world

Chlorophyl flurometer sweet potato
Chlorophyl flurometer sweet potato. Photo: Michael Martin, University of Glasgow.

By Caroline Wood

In one way or another, most of our energy comes from the sun, captured by plants at the bottom of the chain. But as our populations rise, this puts increasing pressure on the photosynthetic capacity of our food and fuel crops. Researchers face the dual challenge of optimising photosynthesis to boost yields, whilst also equipping crops to cope with our changing climate.

During our Annual Meeting in Gothenburg in July 2017, strategies to achieve this will come under the spotlight in the session ‘Photosynthetic response to a changing environment – Towards sustainable energy production.’ Meanwhile, here is a taste of the exciting ideas that could revolutionise this most fundamental of processes for all life on earth.

Turning off the dimmer switch

Whilst light is essential to drive photosynthesis, too much of a good thing can also be a problem. Excess energy that can’t be used by the photosystems is transferred instead to other molecules – including oxygen – resulting in damaging high-energy oxygen radicals. To counter this, plants have developed a form of ‘reactive sunscreen’ known as nonphotochemical quenching (NPQ). This involves both the activity of the PSII subunit S (PsbS) protein and the interconversion of three carotenoid pigments in a process known as the xanthophyll cycle. When plants are exposed to sudden sunlight, this system is rapidly induced, damping down photosynthetic efficiency. But it takes much longer to reset the system – similar to how it takes our eyes time to adjust to the dimness of a dark room. This is a problem for crop plants that naturally experience fluctuating light levels, e.g. from passing clouds or shade from other leaves. “During this time the leaf is converting light that could be used in photosynthesis into heat, and as a result, this slow recovery could cost between 8 and 40% of potential carbon gain,” says Professor Steve Long (University of Illinois, USA and Lancaster University, UK). In a seminal paper1, published with colleagues at the University of California, Berkeley, Steve has shown that targeting NPQ could be an effective strategy to boost stagnant crop yields. “We hypothesised that by accelerating the xanthophyll cycle and increasing PsbS, NPQ relaxation would be more rapid when leaves were transferred from high light to shade,” says Steve. “This was done by overexpressing three genes in transgenic tobacco plants and the results were startling. The transgenic plants were 14%–20% more productive in replicated field trials in terms of mbiomass accumulation than the control plants, with taller stalks and bigger, broader leaves. Because the NPQ process is the same in all crops, we see no reason why it should not produce similar increases in the major food crops.” 

However, other mechanisms may also exist to dissipate excess light energy. Freezing conditions make plants particularly vulnerable to photo-damage – a problem deciduous trees avoid by simply shedding their leaves in autumn. But what about conifers that retain their needles throughout winter? “Conifers have clearly evolved efficient light-dissipation systems to survive boreal winters without irreversible damage – a trait we take for granted in our Christmas trees,” says Professor Stefan Jansson (Umeå University, Sweden), whose research so far suggests that spruce trees do not use the PsbS system to dissipate light energy. “The PsbS system is very dynamic and requires a low lumenal pH, but in conifers, quenching is more static and the trees would have a problem to keep the lumenal pH low during the winter,” he says. So how do they manage it? At the Gothenburg meeting, Stefan hopes to shed some light on this in his talk ‘How can spruce needles be green in the winter?’ Stefan plans to present his first biochemical and ultrastructural studies, besides transcript profiling of overwintering spruce trees. “Ultimately, once we can suggest some mechanisms, we hope to confirm these by generating spruce trees with reduced capacity for these then seeing if they can survive the winter.” Potentially, understanding these mechanisms could suggest novel ways to protect photosynthesis in crops.

Lessons from the past

With pressure increasing on our dwindling fossil fuels, there is considerable interest in developing fuels that sustainably harness the power of photosynthesis. But conventional biofuel crops can divert land away from food production, and hence the ‘next generation’ of  biofuels are focusing on engineering algae or cyanobacteria using synthetic biology approaches. Professor Eva-Mari Aro (University of Turku, Finland) explains her research on cyanobacteria: “Our goal is the economically viable conversion of solar energy to chemicals and fuels using inexhaustible raw materials: sunlight, water and CO2, rather than biomass which has a limited supply,” she says. Cyanobacteria are particularly suitable for a production chassis: their light harvesting and electron transfer processes are well known, they are genetically tractable and they have already been engineered to produce a number of useful fuels and chemicals2. Less is known, however, about the mechanisms they use for regulating photosynthesis as these appear to differ considerably from those in vascular plants. As Eva-Mari explains: “To dissipate excess electrons, algae, mosses, conifers and higher plants protect their photosystems using sophisticated regulatory mechanisms, including strict control of electron flow. But these systems are absent in cyanobacteria.” Instead, cyanobacteria rely on flavodiiron proteins that act as ‘electron valves’3. These function by using excess electrons to catalyse the photoreduction of oxygen to water. Indeed, so effective are flavodiiron proteins as electron scavengers that it is currently a mystery why they became lost in ‘higher plants’. At the Gothenburg meeting, Eva-Mari will be exploring this mystery during her talk ‘Maintenance of the photosynthetic apparatus in changing environments.’ “We believe that the evolution of photo-protective mechanisms was necessary for the transition of photosynthetic organisms from aquatic to terrestrial environments,” she says. But understanding the ancient flavodiiron pathway will be vital in order to optimize photosynthesis for the future. In artificially engineered cyanobacteria, strong electron sinks will be necessary to allow the ‘living factories’ to run at full capacity, as this avoids having to impose strict regulatory mechanisms to protect the photosystems.

Flavodiiron proteins could also help boost photosynthesis in terrestrial crops, as demonstrated by a study led by Kyoto University. Here, the flavodiiron genes FlvA and FlvB from the moss Physcomitrella patens were introduced into wild type Arabidopsis. It was found that the flavodiiron proteins still acted as a strong electron sink and did not compete with normal cyclic electron flow. As such, the photosystems of the transgenic plants were more robust against fluctuating periods of high light intensity4. This suggests that despite flavodiiron proteins being lost in plant evolution, reintroducing them into crops could be a mechanism to protect them against photo-damage. It just goes to show that looking to the past can sometimes help to plan for the future...

Ramping up repairs

Another strategy to optimise photosynthesis is to enhance the repair processes that renew components damaged by abiotic stresses such as cold, drought and heat. This is particularly relevant for the light harvesting complexes, which are responsible for the first stage of photosynthesis: harvesting energy from sunlight and transmitting this to the reaction centres. To prevent irreversible damage from over-excitation, these complexes have to be tightly regulated, being degraded in strong sunlight and assembled anew under low light conditions. “Despite the pigmentbinding proteins in light-harvesting complexes being among the most abundant membrane proteins on earth, their degrading protease remains unknown,” says biochemist Professor Christiane Funk (Umeå University, Sweden). At Gothenburg, Christiane will be presenting results from her studies on a promising protease family during her talk ‘Deg proteases – survival at abiotic stress’.” The Deg proteases (from Degradation of periplasmic proteins) are found in organisms from all kingdoms of life and in humans their roles include removing damaged cell components, tumour suppression and combating toxic protein aggregates that can cause neurodegeneration. Plants also possess Deg proteases; 16 Deg genes have been identified so far in Arabidopsis, with at least five located specifically in the chloroplast, making them prime candidates for photosynthetic repair. To investigate this, Christiane has been examining how deleting one or multiple Deg proteases affects growth under various abiotic stress conditions in Arabidopsis and the cyanobacterium Synechocystis. “We compare the physiological phenotype, when they are grown under various abiotic stress conditions,” she says. Her results have already shown that Deg proteases can function in very specific ways: “We found that one of the three Deg proteases of Synechocystis 6803 is expressed in high amounts and is very active, while another one is activated only during abiotic stress like heat or high light,” says Christiane. Potentially, over-expressing stress-related Deg proteases could be a strategy to protect the photosynthetic machinery of crops from adverse conditions. But Christiane warns it might not be so straightforward: “Over-expression would remove malfunctioning proteins faster, but cells usually keep the number of proteases at exactly the right amount needed,” she says. “Overexpressing proteases might even cause additional stress as functional proteins may be attacked.” Her current work is investigating whether this would be the case by overexpressing Deg proteases in Synechocystis. Although under-explored until now, it seems likely that we will be hearing about the Deg proteases a lot more in the future…

Matching the environment to the planet

To meet the demand for colourful fruit and vegetables all year round, much of the photosynthesis that produces our food takes place in controlled environments such as greenhouses and dedicated indoor ‘plant factories’. Whilst these minimize the impact of external stresses, they typically require supplemental light to achieve year-round crop production – which comes at a cost. “Lighting accounts for about 30% of the production cost in greenhouses and 50–60% of the costs in plant factories,” says Professor Marc van Iersel (University of Georgia). “To make this industry profitable and sustainable we need to look at how efficiently plants use the light they receive.” 

Higher leaves
Higher leaves on a cassava plant inadvertently rob lower leaves of their productivity due to photo protection, a process that protects leaves in full sun but inhibits photosynthesis in the shade. Photo: Amanda De Souza and Justin McGrath/ University of Illinois

 To do this, Marc helped to develop a ‘biofeedback mechanism’, where the level of supplementary light is adjusted depending on how efficiently photosynthesis is operating in the plant. When a leaf absorbs a photon, the energy is either used in electron transport for photosynthesis, dissipated as heat or emitted as a lower energy photon (chlorophyll fluorescence). These three pathways are in competition, so that increased efficiency in one will cause a decreased yield for the other two. In the biofeedback system, a chlorophyll fluorometer attached to one of the plant’s leaves is connected to a central datalogger, which is also linked to the LED lights of the growth chamber. The datalogger uses readings from the fluorometer to calculate the quantum yield of photosystem II to derive a measure of photosynthetic efficiency. This is combined with the measured light level to give an estimate of the electron transport rate through photosystem II, which is compared to a pre-programmed target rate for optimal yield. “If the measured rate is lower than the target, the datalogger increases power to the lights, which increases the electron transport rate, and vice versa,” says Marc. Crucially, the system was tested successfully in three crops with very different light requirements: sweet potato (which requires high light), lettuce (which prefers moderate light) and pothos (an understory plant which needs deep shade). This demonstrates that the system could be used in the production of a wide range of food crops. 

However, it may be a while before biofeedback systems can be applied on a commercial scale. “We would first have to develop an affordable chlorophyll fluorometer that can scan entire canopies, rather than a small spot on a single leaf,” explains Marc. In the meantime, he has already developed another lighting system for greenhouses, using a controller that automatically adjusts the intensity of supplemental light depending on the amount of natural sunlight, ensuring that the crop always receives the right amount of light but no more. “So far, our findings suggest this can result in energy savings of up to 60%,” Marc concludes.

Waste of space

Most approaches to improving photosynthesis focus on the cells, but Professor Andrew Fleming (University of Sheffield, UK) believes that the spaces in between are just as important. Plant leaves show a distinct structure: the upper palisade layer is tightly packed with cells to facilitate light capture whilst the lower spongy mesophyll layer has a network of large air spaces to allow CO2 diffusion. “Essentially, we have no idea how these layers develop,” says Andrew. “But we have found that by manipulating cell division and cell wall separation genes, we can indirectly alter the pattern of air spaces in the mesophyll.” Working with colleagues at the University of Nottingham, Andrew has been using micro-CT imaging (a 3D X-Ray technique) to quantify the distribution of air spaces in such Arabidopsis mutants. The plants are then tested with gas exchange analysis to determine how well photosynthesis is working. “We have found that, under controlled conditions, at least, there is a lot of flexibility in the system,” says Andrew. “You can replace a surprising amount of air space with solid tissue, and so achieve more photosynthesis.” So why haven’t plants evolved to naturally ‘fill in the gaps’ to boost photosynthesis? Andrew believes that one of the main factors is the additional cost in nitrogen and phosphorous that making additional cells would require.

More extreme mutations can even invert the actual patterning of air spaces between the layers. Normally, the density of air channels decreases from the mesophyll to the palisade layer, but one cell-cycle gene mutant showed a distinct peak of air channels in the palisade layer. Essentially, this allows more CO2 gas to reach the plastids where light capture takes place. “Compared to the wildtype, this mutant seems to photosynthesise particularly well indeed,” says Andrew. “This suggests that in the top palisade layer, the cells aren’t limited by rubisco or the amount of light but the concentration of CO2.” In his latest projects, Andrew hopes to explore whether similarly manipulating mesophyll architecture in rice and wheat also affects photosynthetic efficiency. “We are now working with engineers using gas and liquid diffusion modelling to investigate whether altering the pattern of air spaces changes the flux of gas within the leaf,” he says. “So far, altering mesophyll architecture has been an under-explored approach, but if it does prove to play a significant role in photosynthetic efficiency then, in theory, it could be improved.”


1. Kromdijk J, Głowacka K, Leonelli L, et al. (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354, 857–861.
2. Aro EM (2016) From first generation biofuels to advanced solar biofuels. Ambio 45 Suppl 1, S24–S31.
3. A Allahverdiyeva Y, Mustila H, Ermakova M, et al. (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proceedings of the National Academy of Sciences, USA 110, 4111–4116.
4. Yamamoto H, Takahashi S, Badger MR et al. (2016) Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nature Plants 2, 16012.



Category: Cell Biology
Caroline Wood

Caroline Wood

Caroline Wood was the SEB’s 2014 science communication intern. Since then, Caroline has been a regular contributor the SEB, reporting on events and writing insightful features for our members. Caroline has an undergraduate degree from Durham University in Cell Biology and is currently a PHD student at Sheffield University studying parasitic Striga weeds that infect food crops. You can read her blog here.