A convergence of global factors is adding to the difficulties of securing a sustainable supply of food and feed to support the increasing global population. The positive impact of the rise in atmospheric CO2 on photosynthesis is more than offset by the increase in average global temperatures accompanying the change in atmospheric composition. This article provides a brief overview of how these adverse events affect some of the critical molecular processes of the chloroplast and by extension how this impacts the yields of the major crops. Although the tools are available to introduce genetic elements in most crops that will mitigate these adverse factors, the time needed to validate and optimize these traits can be extensive. There is a major concern that at the current rate of change to atmospheric composition and the accompanying rise in temperature the benefits of these traits may be rendered less effective soon after their introduction.

Supply and demand constraints

Demand side

There is an increasing concern amongst the plant science community that the accelerating changes to the atmosphere will soon overwhelm the adaptive processes that plants can deploy in the face of extreme environmental stress, endangering reliable supplies of food from the major crops. Optimistically, changes to the climate will offer a longer growing season at higher latitudes and future yields of the these crops; wheat, corn, rice, soy will follow what on average has been a 1–2% annual rise achieved broadly over the last 50 years since the introduction of new higher yielding varieties. Combining this with a super-efficient food production chain coupled with minimal waste, output might just double in approximately 40–60 years, probably enough to satisfy a world population that will grow from the 7.3 billion figure of today to at least 9.7 billion expected by 2050 [1]. However, more likely is a worst case scenario where yields have peaked, cannot be sustained at current levels as it seems they have done over the recent 20 years, deteriorating from now into the future [2], while population numbers climb above 10 billion. A population that is desirous of the same energy intensive meat-centric diet that is standard in all developed countries.

These population numbers are huge and almost incomprehensible, their enormity only better appreciated if they are expressed in ‘per day’ units. Assuming population numbers stay on the current trajectory, the increase in souls per day is approximately 500000 or equivalent to a city the size of Atlanta that would need to materialize daily if all the new residents were to live in the same location. This is the extent of the challenge the agriculture industry faces in simply dealing with just the demand component, a demand that must be satisfied in the face of what could be substantial loss of agricultural land in providing the space and infrastructure to accommodate and support these new inhabitants. Should population growth rate slow or hold steady, there is no guarantee that beyond 2050 much more can be wrought from the current major sources of food to sustain those that will be in need.

There are more factors at play than just population growth and loss of land, that will have a greater deleterious impact on the global food supply. Those other factors involve accelerating changes to the atmosphere intruding on the seasonal nature of our current agricultural system. Although there seems to now be wide consensus about the import of these atmospheric changes, there seems little evidence that this global consensus is being acted on with much urgency in a concerted way. It is therefore reasonable to anticipate that the worst case situation just defined will unfold and should be the one projection that warrants immediate attention and drives future action. If overly pessimistic, at least then there will be some chance that for a few years beyond 2050 agriculture might provide an overabundance of produce offering some short-term respite, as the precariousness of food security globally becomes more broadly appreciated.

One might argue that an explanation for the increasing number of migrants moving across borders is symptomatic of their inability to find sustainable living standards including adequate diet and nutrition within a local area. Although the events behind the reasons for mass migration might be numerous and obscure, escaping armed conflict and maintaining physical well-being are clearly immediate imperatives, ones that are often exacerbated by food insecurity [3]. After all, these peoples are not moving to regions with worse agricultural practices, rather to countries where proportionately less time is required to acquire food relative to that needed to find employment and establish improved living standards.

The question arises whether there are any factors that might mitigate the worst case projections just outlined. It is sobering to step back and realize that it is the prodigious output of the chloroplast which is the reason a large proportion of the world’s population is facing such stark immediate and ultimately difficult long-term socio- and geopolitical choices. Due to the remarkable productivity of this small endosymbiotic organelle generating an abundance of fossil and natural vegetative mass, humans have reaped the benefits. The energy released from fossil fuel combustion alone drove first an agrarian, then industrial revolution followed by various technological revolutions that have had such a huge influence on both modern day industry and subsequent green revolutions in agriculture, providing the wealth to sustain all the developed nations. It is the ‘waste emissions’ from these endeavors that has accumulated slowly but steadily in increasing amounts that are testing the limits of sustainability of this tenuous supply and demand dynamic. Ironic then that it is the exploitation and manipulation of this same organelle, especially testing the limits of its plasticity, that will be necessary to find solutions to the impending demands. Although there is general agreement that these problems must be addressed strategically, few outside the plant science community appreciate what is entailed in delivering those solutions that will ultimately satisfy future demand.

Supply side

There is incontrovertible evidence that the atmospheric composition of the planet is changing and that the rate of change is becoming more rapid. One component of the atmosphere that has been monitored closely since the 1950s is CO2 [4] because it was known to be the major product from burning fossil fuels and that more consumption would be necessary to power the growth and progress of the developed and developing worlds.

One huge consequence of the increase in atmospheric CO2 [5] is warming of the air through absorbance of sunlight, converting the energy into IR wavelengths that do not escape the earth. Through much of history including the prior two centuries the concentration of CO2 was less than 300 ppm, but since then the amount has climbed above 400 ppm and, without intervention is projected to reach 700 ppm or above by 2100 [6]. Many have argued that there are advantages to these changes, after all plants can benefit from both increases in temperature and CO2. In 1973, Kimball [7] reviewed the positive effects of CO2 enrichment on vegetative growth and harvested yields of numerous plants including crops. Subsequent studies have confirmed these beneficial effects in all the major crops, soybean, wheat, and rice that operate C3 type C-fixation, although from large-scale free air CO2 enrichment (FACE) experiments, grain crop yields were far less than those found from studies involving more confined conditions [8]. However, temperature increase, that other component influenced by CO2, has a more broad and profound impact on plant responses [9], one which limits C-fixation severely.

Although the stated desire is to restrict average temperature increase to less than 2°C globally, those studying climate change with a view to understand the impact of a warming world are realizing that atmospheric composition is changing more rapidly than first projected. In addition to CO2, increased emissions of methane are becoming a significant factor for warming, one that could exceed the contribution from CO2. The desired case of an approach trajectory to only an average 2°C rise globally by the end of the century is now being rapidly exceeded. A warming atmosphere induces positive feedback effects on microbial emissions of both CO2 and methane, which with added livestock methane emissions means a 2°C rise will be easily surpassed by 2050 and higher average temperatures, potentially as high as 5°C or more, are projected by end of the century [10].

Based on what we know and are learning about the response of plant and particularly chloroplasts to changing CO2 and temperature impinging on the productivity of CO2 fixation and the photochemical reactions of photosynthesis, it appears that the overall positive yield response to CO2 will be seriously offset by the negative effects of higher temperatures, especially when changes to weather patterns are also anticipated.

Effects on molecular events of a changing atmosphere

CO2 emissions

Increasing CO2 in the atmosphere has positive effects on photosynthetic C-assimilation in three of the major row crops; wheat, soy, and rice; namely those operating C3 photosynthesis. The most impact is through suppression of the oxygenase reaction of ribulose bisphosphate carboxylase/oxygenase (Rubisco) due to direct competition between CO2 and molecular O2 for the bisphosphate reaction intermediate of ribulose 1,5-bisphosphate (rubp) generated by the enzyme following the initial deprotonation step of catalysis. Increased CO2 ensures more of the bisphosphate substrate is partitioned through carboxylation to form phosphoglycerate and less rubp is lost through oxidative conversion into phosphoglycolate. At high enough concentrations of CO2, overall C-assimilation is no longer limited by the activity of Rubisco but shifts to production of the rubp substrate [11].

In C3 crops, there is a wealth of evidence that a reduction in photorespiration results in productive benefits such as vegetative growth improvement, which ultimately translates into increased harvested yields (for review, see [7]). Beneficial secondary effects are also observed. Due to the slow rate of Rubisco catalysis, the amount of enzyme in the stroma of C3 chloroplasts is high at millimolar concentrations, accounting for at least 25% of the nitrogen in the plant. More CO2 and thus more flow of rubp into C-fixation means there is less requirement to invest as much nitrogen in protein and thus overall plant nitrogen-use efficiency improves. Furthermore, higher CO2 concentrations in the plant also mean stomatal aperture movements are such that less water is lost from intercellular spaces, which translates into improved water use efficiency. So simply enhancing partitioning of rubp into carboxylation compared with oxygenation induces these other positive responses that, compounded over a growing season, combine to give enhanced vegetative and reproductive growth.

One might speculate what would be the maximum yield increases should photorespiration be totally suppressed in a C3 plant. In current atmosphere at 25°C, the relative specificities of Rubisco of C3 plants in terms of the partitioning of the bisphosphate substrate between fixation compared with oxygenation is approximately 4:1. At concentrations of CO2 that saturate the enzyme and suppress photorespiration the expectation would be at least a 20% increase in productive photosynthetic assimilation with essentially all rubp substrates committed to carboxylation and negligible amounts lost by photorespiratory processes. Indeed, models suggest a 12–55% improvement in gross photosynthesis where photorespiration is to be suppressed by rising CO [12]. In studies where CO2 amounts were doubled relative to atmospheric concentrations, actual yields were enhanced by at least 33% [7].

In comparative terms, corn, a crop that operates a C4 type of C-fixation, Rubisco is at saturation in terms of CO2 concentrations at the site of carboxylation. With minimal exposure to oxygen from photochemical reactions due to the particular cellular architecture of C plants, photorespiratory losses are negligible. Advantages are thus secondary, for example superior water use in drought conditions due to less stomatal dynamics [13] and less nitrogen invested in Rubisco than in C3 plants. Corn yield estimates across various models indicate that doubling of CO2 would on average produce a 7.5% increase in yield [14].

Temperature and moisture

In a broad sense then, it seems to be a generally positive development when rising CO2 is considered in isolation and purely in terms of effects on plant responses. However, these positive aspects diminish significantly, indeed are completely negated, when temperature rise that accompanies increasing CO2 is taken into account [9]. With higher temperatures comes a variety of significant and complex shifts in equilibria that result in changes in plastid morphology and dynamics which in the extremes are irreversible and detrimental to plant productivity if not survivability.

The current variety of crop species are maximally productive over approximately a 10°C range of temperature, i.e. corn 26–36°C compared with wheat at 12–22°C [15]. More importantly, even an average temperature change of 2°C on either side of these ranges can impart huge negative consequences to yield especially if (i) they occur at certain critical points in development and (ii) the changes are prolonged for hours or days [15]. The negative impact of warmer temperatures on yield are even more severe when coincident with drought conditions.

Over short exposure to above than 10°C the optimum for about 1-h periods, the vegetative tissues of plants are robust and adaptive, the underlying biochemical processes are reversible and the system largely recovers [16]. Over longer periods, especially days, physiologically higher temperatures affect the various stages of the growth cycle such that each defined stage is accelerated to the point where not only is vegetative growth compromised but especially reproductive phases such as pollen germination, grain fill, and fruit development may suffer premature arrest, i.e. those yield factors that farmers are particularly interested in (for review, see [17]). There are well documented and recent examples of wheat harvest failure in more than one country due to adverse temperature events causing severe dry periods at sowing or during flowering that impact production significantly [18].

As might be expected, it is C3 crops of temperate zones like cereals and rice that are more susceptible to heat extremes than are the C4 varieties that originate from tropical climates, most likely due to the added decline in water use efficiency that often accompanies higher temperatures, especially in dry conditions [18]. Even modest increase in temperatures, e.g. 3.5°C during the early stages of development favors vegetative growth over later seed production phases [19]. In vegetative phases, heat stress may compromise photoassimilation movement to developing roots due to less transpiration, which in turn limits water uptake.

Those biochemical processes of the plastid impacting photosynthetic yield directly most susceptible to temperature changes have focussed on Rubisco and the reactions associated with CO2 fixation. The preamble to the mechanism of fixation involves activation by CO2 through formation of a carbamate at an active site lysine residue. The site is then receptive to co-ordinating essential Mg2+ cations. During normal turnover, both carboxylase and oxygenase reactions of the enzyme are characterized by a progressive loss of activity. This inactivation is due to formation of catalytically unproductive complexes between the bisphosphate substrate or one of numerous misprotonated forms of the enediol intermediate and the non-carbamylated enzyme. The off-rates of these various isomeric forms are slow, essentially trapping the enzyme in dead-end states [20]. Fortunately, under normal conditions these dead-end complexes are reversed by the action of Rubisco activase that consumes ATP in releasing the inactive complexes [21], and C-fixation proceeds unabated. However, at elevated temperatures this reactivation is seriously compromised due to both the heat sensitivity of activase [22] and because the rate of inactivation is faster than the activase catalyzed reactivation of Rubisco.

Another temperature sensitive factor limiting C-fixation involving Rubisco directly is the relative specificities of the carboxylase and oxygenase reactions. As temperatures increase, a higher proportion of rubp is partitioned through oxygenase than carboxylase because of the difference in the temperature dependencies of the solubilities of the two gases that favors O2 at higher temperatures. Thus less rubp is partitioned into C-fixation and more energy wasted recapturing the carbon diverted into the increased production of phosphoglycolate.

In C4 plants where the influence of higher atmospheric CO2 concentrations on yield is much less than C3 plants due to negligible photorespiration, most impact of higher temperature is on activase [23] limiting assimilation through slower Rubisco reactivation. When the intact plant is considered, there is an influence on the distribution of photosynthate such that more is allocated to above ground vegetative biomass at the expense of accumulation in yield-bearing reproductive structures [18].

Photosynthetic light reactions

The photochemical events that drive the production of ATP and reducing equivalents in the form of NADPH, essential for supporting C-fixation, is an electron transport chain that in oxygenic photosynthesis derives reducing power from water. The photosynthetic electron transport chain is oriented within the thylakoid membrane, such that electron transfer produces a transmembrane proton and electrical potential that drives ATP synthesis by the integral membrane enzyme ATP synthase. Excited states of photoreactive chlorophylls of PSI reaction centers are sufficiently reducing to enable the indirect reduction of NADP. Together, NADPH and ATP support the regeneration of rubp and in C3 plants drive the recovery of carbon lost through photorespiration. Molecular oxygen evolved from water can, under conditions of high light intensity when C-fixation is limiting, form reactive oxygen species (ROS). These include singlet oxygen and reduced oxygen species (e.g. O2 and H2O2) which have the potential to cause significant damage to photochemical centers and internal chloroplast membranes.

The chloroplast wages a constant battle to minimize ROS production that through regulatory mechanisms and the production of a cocktail of metabolites such as carotenoids, act to impede the formation of and quench these highly reactive species [24]. PSII is particularly susceptible to damage from ROS production having a half-life of hours in normal conditions, a rate of degradation which is much enhanced in high light and especially at high temperatures. The most sensitive component is the D1 polypeptide and the oxygen evolving complex (OEC) of the PSII complex that must be replaced by newly synthesized protein. It is regeneration of D1 and other susceptible proteins of the photosystem that is most sensitive to temperature [25]. The membrane where the photochemical centers reside in extreme thermal conditions rearrange, forming fewer appressed regions also accompanied by alteration of the composition of the thylakoid membrane. PSI is less susceptible to ROS damage allowing cyclic electron flow to accelerate dramatically as part of an adaptive response to temperature stress that is mirrored by a reduction in linear flow through PSII [26]. Recently, better understanding of the regulation of cyclic processes has emerged, revealing details of the interplay with linear flow and the role in generating proton gradients protecting chloroplasts against excess light as well as the effect of different stress conditions, including heat [27,28].

The combination of these adjustments offers two advantages: (i) PSII complexes recover through protein turnover and replacement of damaged subunits and (ii) a rebalancing of the reductive pool of acceptor components occurs in response to the fall in C-fixation caused by inactivation of Rubisco. Again, short-term exposure to moderate warming and subsequent inhibition of overall photosynthetic C-assimilation in many plants is readily reversible. With prolonged exposure at more elevated temperatures however, the composition of the reaction center components changes dramatically such as chlorophyll content declines as tocopherols, plastoquinone, and related metabolic protectants increase, to quench the rise in ROS. There are two distinct pools of plastoquinones in chloroplasts, one associated with the photochemical processes of the thylakoid and PSII-mediated linear electron flow, the other is a pool that is localized to plastoglobules associated with non-photosynthetic processes. Plastoglobules are lipoprotein-rich enzyme-containing subcompartments of the chloroplast coupled to thylakoid membranes [29]. In particular stress conditions like heat, the dynamic physical relationship and contacts with thylakoids become quite pronounced and the numbers of plastoglobules increase. In thermal stress conditions and a slowing of linear flow, there is a shift in the amount of plastoquinone in the form of large quantities of PQH-9 accumulating in the plastoglobuli localized reductive pool that acts as a membrane protectant.

There is thus a relatively clear order of events associated with limiting photosynthetic yield and temperature increase. At moderate changes, 10°C above optimum temperatures, CO2 fixation is most likely the cause of decreasing assimilation, but above those temperatures, compromised photochemical processes make a larger contribution to the decline. Even at moderately higher temperatures, alterations to thylakoid composition, particularly the membrane and thus the charge potential, affect the redox balance of photosynthetic electron transport. With prolonged exposure to thermal extremes more dramatic changes have been reported, such as altered localization of light harvesting chlorophyll harvesting protein (LHCP) [30] from appressed regions of the thylakoid to unappressed regions and more energetically coupled to PSI than PSII. Efficient operation of photosynthesis especially electron flow between the photochemical centers and the ΔpH generated by PSII requires the phosphorylation and dephosphorylation of attendant proteins like LHCP. The phosphorylation status of LHCP is important for the excitation energy status of the two photochemical reaction centers of PSII. Increased temperature results in LHCP becoming dephosphorylated which is accompanied by perturbation of the distribution of light energy between the two photosystems, alteration of the thylakoid structure, composition and granal stacking. Interestingly, other proteins of the photochemical centers in these same conditions increase their phosphorylation status, although the importance of this to adaptive processes is yet to be fully understood.

When accompanied by high light, a redistribution of chloroplasts along the walls of the cells occurs furthest from the source of irradiance to minimize light capture and thus photochemical damage [31]. Accompanying these movements are morphological changes to chloroplasts, particularly thylakoids which swell along with grana destacking, which results in a reduction in the absorbance of light [32]. Since lipids of the thylakoid membrane are in dynamic equilibrium with lipids of the plastoglobules, it is feasible that heat-induced changes to thylakoids are directly associated with the increase in plastoglobule formation [2].

In direct sunlight at the intensities of a typical growing season, local heating may exceed average shade temperatures especially in conditions where water is limiting. It is considered that temperatures above 40°C for C3 plants over prolonged periods severely compromises the photosynthetic machinery beyond the adaptive capabilities of the plant, resulting in irreversible and broad plastid and cellular damage. It would be expected that, even at intermediate temperatures above optimum, much energy is expended in adaptive processes such that overall growth and development are compromised with a concomitant detrimental impact on yield. Depending on the species and origins of plants, extent of exposure to moderate compared with high temperatures, there is a difference in the ability of the plant to recover from the exposure. For example, tomato plants that are of tropical origin seem capable of withstanding longer exposure [33] than temperate zone plants.

Import events

Some 80% of the proteins required by the chloroplast are nuclear encoded, translated in the cytosol as N-terminally extended precursors and imported into the plastid by an ATP-dependent process [34]. As part of the translocation process, the transit peptide extension is removed by proteolysis. These stages of importation and translocation and the components that compose the underlying machinery that results in protein maturation have low thermal stability [35]. The nuclear-encoded events that are so critical for replenishing many of the proteins of the plastid that are damaged in heat-stress conditions accumulate in the cytosol and do not reach the stroma. The rates of protein degradation are enhanced relative to the rates of synthesis and thus photosynthetic function suffers because those proteins that are degraded are not replaced in sufficient amounts to support normal photosynthetic rates. Additionally, due to down-regulation of transcription of those proteins specific to the import process, the translocation process itself is severely curtailed.

In a detailed study of 40°C temperature stressed whole pea plants, excised leaf, and isolated chloroplasts [35], insight into which step of protein import was impaired and by how much was revealed. Exposure of leaves to these temperatures for as little as 40 min reduces binding of the precursor of Rubisco small subunit (rbSS) to plastid envelope membrane by 80% and import into isolated chloroplasts by 90%. Treatment of isolated chloroplasts to these same temperatures showed impaired import within 10 min. Gene expression of Tic, Toc components of the translocation complex was reduced by varying amounts, but in all cases by at least 50%. Western analysis indicated that the changes in expression were partially reflected in the loss of these protein components and presumably with longer exposure would ultimately decline by similar amounts. Toc159 is susceptible, which compromises particularly optimal import of rbSS precursor and thus the integrity of the Rubisco L8S8 functional aggregate. Cytosolic heat shock proteins (HSPs) provide some protection for a short period but beyond 30 min this limited amount of stabilization is lost and immature HSPs also accumulate in the cytosol. Thus, under high temperature stress, the net loss in photosynthetic function is due to degradation of chloroplast proteins coupled with impaired post-translational targetting of their precursor proteins into the chloroplast. Non-replenishment of degraded proteins combined with energy costs of rbSS degradation, exceeds the ability of the system to resynthesize essential proteins and thus impairment becomes irreversible and recovery to full functionality impossible.

Impact on yield

Although not all details of the negative effects of higher temperature on molecular events of photosynthesis and chloroplast output have been delineated, particularly the response of the most sensitive control points, heat exposure regimes are not necessarily equivalent, i.e. multiple short periods of heating and cooling are unlikely to render the same effects as fewer more prolonged periods. Nor is it likely that the initial response to stress will be the same for subsequent repeat events. Nevertheless, no matter the subtleties of these different conditions it is clear the thermal effects on plastid localized molecular processes ultimately manifest themselves at a whole plant level by changes in physiology that are detrimental to yield. Initially, the response of the plant is adaptive, which offers short-term compensation that is reversible with a minimum of loss in photosynthetic output. However, where heat stress is more chronic and extends into the reproductive phases of development, yield losses become less to do with photosynthetic limitations and more associated with the heat sensitivity of developing reproductive tissues. It is estimated from heat effect studies that for every 1°C rise in temperature there will be an accompanying drop in yield of 17% [36], which may translate to losses of approximately 35% if average global temperatures are kept to 2°C. If in fact conditions approach more extreme warming of 5°cC, crop losses could be so huge that farming as a business in its current form will be unsustainable.

What is the likelihood that average temperatures will exceed 2°C by a significant margin and crop yields decline even further? There are two other components of the atmosphere that are increasing in concentration and will prove detrimental to plant health further negating the apparent positive productive effect of rising CO2. Methane is significantly more consequential than CO2 to atmospheric temperature change by a factor of 25-fold and has contributed 20% to the average increase. Over the long-term methane, unlike CO2 is lost from the atmosphere and so one might consider that its impact will be of limited long-term consequence. However, for purposes of defining remediating conditions over the short term to ensure the average rise is limited to only 2°C within the next few decades, the heat factor of methane emissions is more realistically closer to 70-fold over CO2 [37]. Warming of the atmosphere in the higher latitudes is reawakening the biome trapped in the permafrost that will be the major source of methane in the near term [38,39], but what is exacerbating the impact of this component is the conversion of forested and other agricultural land into more livestock farming [40]. Natural processes of CO2 sequestration are further compromised and more livestock means more methane emissions. With further intensification of these detrimental positive feedback loops, thawing of the permafrost, livestock production means in actuality the 2°C ‘red line’ might be breached by 2030, with methane becoming even more consequential to warming on a percent basis than CO2.

The other component of the atmosphere rising in concentration that will impact yield is ozone [41]. Ozone is formed as a result of sunlight initiating photochemical reactions with byproducts of burning fossil fuels, organic hydrocarbons, oxides of nitrogen etc. One of the organic hydrocarbons at significant atmospheric concentration is isoprene that originates from the chloroplast isoprenoid pathway and emitted by plants in response to heat stress. Isoprene generates hydroxyl radicals as a result of photo-oxidative degradation that in turn leads to ozone production [42] over and above that originating from fuel combustion. On calm, cloudless days in spring and summer ozone concentrations rise dramatically which, combined with weather inversions, remain trapped at surface elevations and can persist for days. Ozone enters the leaf through stomata as a part of the normal process of gas exchange. Constant exposure results in chlorosis and ultimately necrosis of photosynthetic leaf tissue. Both monocots and dicots are susceptible to damage [43] and yield loss of soybean, the most sensitive of C3 crops, was found to decline 20% at ozone concentrations of 65 ppb over a growing season [44].

Mitigation of the effects of atmospheric changes

The evidence is compelling that a worse case scenario will be the most likely trajectory climatically and atmospherically over the next half century and thus should direct decisions about what factors might be selected to mitigate these conditions most effectively. The question arises whether appropriate mitigating factors be identified that might accelerate another green revolution and provide some hope of securing future food production enough to satisfy projected demand. The last revolution of the mid-20th century generated a doubling of production over 50 years, achieved by a combination of improved breeding and agronomic practices, protected by a range of new active pesticidal products. In the face of changes to the atmosphere and by extension weather patterns, as well as a more constraining regulatory environment, new traits yet to be identified will have to satisfy the demand for not only food, but feed and fiber in addition to other applications for which plants may be advantageous commercially [45,46].

The most effective way of mitigating increase in temperature resulting from atmospheric changes and drive sustainable yields will require extensive engineering of chloroplast output. Studies of photosynthesis, both light and dark reactions across a wide range of plant species, offer potential solutions for driving improved efficiency of C-fixation and photochemical processes. With respect to the energetics and output of the chloroplast, much is known about the molecular events of CO2 fixation and the photochemical reactions to identify how they might be improved [47]. It is generally accepted that the reactions of Rubisco are not optimal and that increasing the concentration of CO2 at the substrate site relative to O2 will make a significant positive boost to productivity. The article by Andralojc et al. in this issue of Essays in Biochemistry [48], provides details of the challenges involved in engineering plants to achieve full carbon assimilating potential at the site of carboxylation. If these are achieved when coupled with accelerating specific rate limiting steps of the C-fixation cycle [49] then a significant boost in productivity of 60% or more might be forthcoming. This improvement is partially achieved through the suppression of photorespiration, but some recent work suggests that the rate of CO2 uptake might be increased by exploiting photorespiratory nitrogen assimilation [50]. In either case it should be recognized that to deal with the thermal sensitivity of Rubisco and its activation, the components engineered into the plant will need to be thermotolerant otherwise improved potential will be compromised. Even more challenging is finding ways to adjust the photochemical events necessary to support any improvement in C-fixation. In this issue, Cardona et al. [51] describe how components of the photosystem complexes might be engineered to enhance photosynthetic potential which would need to be accompanied with improved forms of photoprotection [24]. Assuming both driving power and assimilatory output of the organelle can be translated into a step change in yield, there are other indirect factors available that might mitigate rising temperatures (see also Long et al. [52]).

Although the innate adaptive responses of plants will be inadequate to provide much protection above a moderate elevation in temperature, nevertheless products of these processes are indicative of what metabolites might act as natural protectants. For example, isoprene is now well established to impart thermotolerance in plants, although the basis is still unclear [53]. Inhibition of isoprenoid formation in chloroplast using fosmidomycin treatment of plants increases the sensitivity of photosynthesis to increased temperatures, which can be reversed by isoprene fumigation. Other examples of natural metabolites that might be overproduced to mitigate abiotic stress particularly thermotolerance and protection from ROS are captured in [54]. The question remains will their enhancement in major crop plants be accompanied by the desired production boost or, as found when isoprene was increased in tobacco, provided protection but at the expense of yield [55].

There are numerous examples like these that impart some level of relief to abiotic stress and likewise traits that have potential to provide resistance to new and adverse biotic assaults that will emerge with a changing climate. The chloroplast plays an essential role in activating plant immunity to stress conditions [56]. The major challenge is first, identifying which traits will be most effective and then second, introducing and optimizing these traits in crops. Even as singular events it takes at least 10 years from discovery through development to fully assess the performance of any one trait and then make it available generally. One might anticipate then that for crops to withstand these multitude of adverse conditions, both abiotic and biotic, will require stacking multiple traits together and thus take longer to integrate into crop lines. Arguably, a major tipping point has already come and gone, namely the ability to engineer crop varieties to maintain even current yields, let alone approach the desired doubling of production. The question arises is there enough time to do the research necessary to first, assess the compatibility of matching new production related traits with modern crop varieties [57] then, optimize them and alter metabolism to overproduce natural stress mitigators, without causing a severe drag on overall yield. Given the current investment in plant-related research, these development horizons are much longer than the rate at which adverse environmental factors are accumulating. A serious constraint is the time required to complete studies to confirm there is minimal yield drag from stacking and then navigate the regulatory process before commercialization. Time is becoming another commodity very much in short supply.

This article has not addressed all the constraints that are converging to adversely impact crop yields e.g., the effect of water, especially shortages when coincident with heat, causes even more severe yield losses. Clearly these stress factors are changing at a rate faster than research has the ability to respond with solutions. By the time a new suite of traits is ready for launch, average temperature might already be above 2°C [58], tropical regions may no longer support agriculture in its traditional form and desertification will have extended far beyond the current boundaries. Alarmingly, just over the past 2 years the rate of CO2 emissions has gone up by 50% [59].

Acute food shortages are certain to become chronic, which does not bode well for a global population whose numbers become limiting because of lack of basic nutrition. Rather like plants and other living systems, there are limits to human adaptation, which in turn will manifest itself in the form of larger mass migrations to areas perceived to be more fertile. Rather than deal with population migrations, surely it is better to acknowledge that broad agricultural practices, especially in the less developed countries, are poor where crops substantially underperform and could be managed more effectively. During a period of new trait discovery and optimization of novel technologies for pest and weed control to protect these high value crop varieties, better land and crop management practices that limit agriculture’s contribution to greenhouse gas emissions should be adopted more broadly so that much more can be wrought from the most tolerant varieties of current crop species. Further research should also be done to identify new traits [60] from those plants and photosynthetic microorganisms that naturally withstand extreme conditions that might be introduced to enhance performance of crops. Enough is known now about how to integrate these traits into the genomes of elite germplasms to minimize yield drag, and so the discovery phase on new trait performance might be accelerated significantly.

Over the longer term, research will be necessary to elevate less well known but more resilient crops like sorghum and develop specific extremophile species into new crops. When it comes to C-fixation, those plants operating C4 photosynthesis are more productive than C3 species and withstand higher temperatures. One example of a C4 plant that might be promoted to crop status is Amaranthus [61], currently classified as a weed, considered a difficult to control noxious invader of the corn acreage of the U.S.A. midwest, but a crop in its own right in other cultures. Whatever combination of approaches will ultimately be adopted, in all events that modest but complex plant endosymbiont, the chloroplast, will be at the center of any long-term solution to improve the performance and output of photosynthesis to satisfy the needed production.

Summary

  • Increasing atmospheric CO2 enhances the yields of the major crops.

  • These positive effects on outputs are more than offset by the rise in global temperatures.

  • Additional adverse factors, including depleting water tables, soil degradation, and poor agronomic practices, constrain achieving food and feed security.

  • The molecular processes of photosynthesis that limit crop output are well defined and might be altered genetically to support the growing global population.

I thank the authors and co-authors who agreed to contribute their time and expertise to composing a collection of superb and readable articles. I am aware that quite a few, myself included, ventured beyond their comfort zone to explore the various topics. I would like to thank the many reviewers who ensured our speculations were not too fanciful. I would especially like to thank Bruce Diner, who contributed to the photochemical section of the article and also cast a critical eye over the other sections.

Competing interests

The author declares that there are no competing interests associated with the manuscript.

Abbreviations

     
  • HSP

    heat shock protein

  •  
  • LHCP

    light harvesting chlorophyll harvesting protein

  •  
  • rbSS

    rubisco small subunit

  •  
  • ROS

    reactive oxygen species

  •  
  • Rubisco

    ribulose bisphosphate carboxylase/oxygenase

  •  
  • rubp

    ribulose 1,5-bisphosphate

References

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