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14.7.3 - Heat injury and inhibition

Heat stress affects plants through three principle mechanisms: excessive membrane fluidity; disruption of protein function and turnover; and metabolic imbalances. Metabolic imbalances can be due to differences in the activation energy of the component reactions, or to the effect of the other two mechanisms on the thermal response of each reaction.  The inhibition of metabolism from these three mechanisms also results in the accumulation of toxic compounds and reactive oxygen species (ROS), the removal of which is also inhibited by heat stress.

(a) Whole plant effects

Generally, inhibition of photosynthesis is seen as a critical factor in heat stress. Net photosynthesis is typically the first process to be inhibited at high temperatures (Berry and Bjorkman 1980; Allakhverdiev et al. 2008). As temperature rises above optimum, gross photosynthesis is inhibited while respiration and photorespiration increase. The combined effect of these three processes is a marked reduction in net photosynthesis during moderate heat stress (Figure 14.12).

C4 plants do not suffer from the increase in photorespiration and so can maintain a higher photosynthetic optimum; however, the maximum temperature does not vary to the same extent. The imbalance between photosynthesis and respiration is itself damaging, as carbohydrate reserves can become depleted. As temperature rises further, membrane transport and respiration become inhibited, eventually leading to cell death. Both the light reactions and the Calvin cycle are highly sensitive to moderate heat stress. Injury following severe heat stress is perhaps most acute for the light reactions, with even brief exposure resulting in long-term inhibition of photosystem II (PSII). As the activity of PSII is highly temperature sensitive it can be used as an indicator of heat stress and heat injury; measurements of chlorophyll fluorescence have been widely used for this purpose (

For many years, the inhibition of gross photosynthesis was thought to occur at temperatures too low to be explained by the thermal deactivation of photosynthetic enzymes. Experiments comparing the thermal response of many steps in the photosynthetic apparatus, suggested the initial inhibition was due to the sensitivity of the thylakoid membrane to high temperatures (Berry and Bjorkman 1980). However, this view has been questioned recently with the observation that at moderately high temperatures photosynthetic inhibition coincides with a reversible reduction in the activity of certain Calvin cycle enzymes (Sharkey 2005). Severe heat stress is still thought to be due to injury of PSII, through direct cleavage of the D1 protein and a range of other mechanisms. Although the thermal sensitivity of PSII is not solely due to the thermal sensitivity of cell membranes, membrane properties are a major regulator of both inhibition and injury of PSII (Sharkey 2005; Allakhverdiev et al. 2008).

The thermal sensitivity of reproductive processes can be a limiting factor for plant productivity and it is often the critical factor for crop production in areas prone to heat stress (Table 14.3; Heat stress can reduce the duration of reproductive development and severely inhibits floral development, fertilization and post fertilization processes in many species. Pollen viability is particularly vulnerable to heat damage. Severe heat stress inhibits both the photosynthetic source and the reproductive sink, resulting in a significant reduction in the number and size of seeds and/or fruit. This is a particular problem in fruit and grain crops such as tomato, cowpea, wheat, and maize (

At high temperatures dry matter production is often more limited by photosynthesis than by cell expansion (while at low temperatures dry matter production is more limited by cell expansion than by photosynthesis). Generally, the inhibition of photosynthesis and other growth maintaining processes during moderate or short-term heat stress results in a comparatively small reduction in the rate of dry matter production (relative growth rate) (Chapter 6.2.2; As temperature increases within a plant’s thermal range, the duration of growth decreases but the rate of growth increases, as shown earlier in this chapter. As a consequence, organ size at maturity may change very little in response to temperature, despite variation in growth rate. As temperatures are raised further, an increased rate of growth is no longer able to compensate for a reduction in the duration of development, and the final mass of any given organ at maturity is reduced. This response can be seen in a range of tissues including leaves, stems and fruit. A smaller organ size at maturity due to high temperature is associated with smaller cells rather than a change in cell number. This implies that cell enlargement is more sensitive to temperature than is cell division. The reduced duration of development can also limit the number of organs that are produced, e.g. grain number in wheat is reduced when plants are grown at moderately high temperatures (Stone and Nicolas 1994). Under certain conditions plants grown under moderate heat stress accumulate sugars in their leaves, indicating that translocation can be more limiting than photosynthesis, but this is not thought to be a general limitation.

(b) Membrane properties

The structure and fluidity of lipid membranes is dependent on their composition and on temperature. An increase in temperature will result in an increase in the fluidity of lipid membranes as the hydrogen bonding between adjacent fatty acids become weak. This increase in fluidity is associated with an uncontrolled increase in membrane permeability as the activity of membrane bound proteins is disrupted. Indeed, this uncontrolled membrane permeability is used as an assay to test for damage due to heat stress (

Membrane-associated processes, such as photosynthesis and membrane transport, are typically the first to be inhibited during exposure to high temperature (Berry and Bjorkman 1980; Allakhverdiev et al. 2008). The high temperature sensitivity of PSII is thought to be due, at least in part, to its close association with the thylakoid membrane. In addition to these direct effects on metabolic function the changes in membrane fluidity during heat stress act as a signal to initiate other stress responses in the cell (Mittler et al. 2012).

(c) Protein function and turnover

For most metabolic reactions, the optimum and maximum temperatures are determined by the thermal response of key enzymes. Enzymes act to lower the activation energy and increase the rate of reactions at any given temperature. However, as temperature increases the catalytic properties of most enzymes are lost and they begin to denature (i.e. enzymes are thermolabile). The synthesis of replacement enzymes and other cell proteins is also impaired, resulting in an overall limitation due to reduced protein turnover. Under prolonged severe heat stress many enzymes will become denatured. This, combined with the loss of membrane function will result in cell death.

For some reactions, the thermal response of a particular enzyme can be rate limiting. The inhibition of photosynthesis during moderate heat stress has been associated with a reduction in the catalytic activity of Rubisco (Ribulose 1:5 bisphosphate carboxylase/oxygenase), due in part to the thermal sensitivity of Rubisco activase. In some species, production of heat stable forms of Rubisco activase has been shown to play role in acclimation to high temperature (Yamori et al. 2013). There have been attempts to engineer less temperature sensitive forms of Rubisco activase in order to increase the thermal range of crop species, but it remains to be seen if altering a single component of the photosynthetic system will improve overall heat tolerance (Sharkey 2005; Allakhverdiev et al. 2008).

(d) Metabolic imbalances

When a plant is grown outside of its optimum thermal range, metabolic imbalances occur. Imbalances may result in a short-fall of essential metabolites or intermediaries, or in a build-up of substances that becomes toxic (e.g. aggregated proteins). Such imbalances cause further inhibition of processes such as photosynthesis and respiration. The imbalances can be due to differences in the thermal response of particular reactions. For instance, the enzymes used in photosynthesis are deactivated at a lower temperature than those used in respiration. This has the result that as temperatures increase, the rate of carbon fixation falls while the rate of carbon use may rise. The point at which the plant is using more carbon than it is assimilating is termed the ‘temperature compensation point’. Beyond the temperature compensation point, the plant begins to use up carbohydrate reserves, e.g. in many legumes the net uptake of CO2 by the green pod is low due to the high rate of pod and seed respiration, at high temperatures net uptake can become negative. As plants acclimate to high temperatures the rate of respiration falls lessening the impact on net photosynthesis.

Imbalances can also occur due to the effect of temperature on physical processes, e.g. as temperature rises, the solubility of oxygen increases more than that of carbon dioxide, so oxygen becomes more concentrated in the cell solution compared to carbon dioxide. This imbalance contributes to the increase in the oxygenation of RuBP at high temperatures (i.e. an increased rate of photorespiration).

The high temperature sensitivity of reproductive development can be viewed as an imbalance. Detailed studies have found that the yield of certain cowpea varieties was limited at high temperatures due to reduced seed set. This limitation was mitigated by increasing sink demand through breeding with more heat tolerant varieties. The fact that seed set can be limited by the demand for assimilates at high temperature shows that the thermal sensitivity of the reproductive sink can be out of balance with than that of the photosynthetic source ( A similar sink restriction is found in cereals grown at high temperatures, where grain development is restricted by its ability to convert the available assimilates into starch (Stone and Nicolas 1994).