Phenological and Physiological responses of plants to heat stress

3. Phenological changes

The developmental stage at which the plant is exposed to the stress may determine the severity of possible damages experienced by the crop.

Vulnerability of species and cultivars to high temperatures may vary with the stage of plant development, but all vegetative and reproductive stages are affected by heat stress to some extent.

During vegetative stage, for example, high day temperature can damage leaf gas exchange properties.

During reproduction, a short period of heat stress can cause significant increases in floral buds and opened flowers abortion; however, there are great variations in sensitivity within and among plant specie.

Different phenological stages differ in their sensitivity to high temperature, however, this depends on species and genotype

Impairment of pollen and anther development by elevated temperatures is another important factor contributing to decreased fruit set in many crops at moderate to- high temperatures.

The staple cereal crops can tolerate only narrow temperature ranges, which if exceeded during the flowering phase can damage fertilization and seed production, resulting in reduced yield. Grain filling duration can also be decreased due to high temperature.

4. Physiological responses

Water relations

Plants tend to maintain stable tissue water status regardless of temperature when moisture is ample; however, high temperatures severely impair this tendency when water is limiting.

Under field conditions, high temperature stress is frequently associated with reduced water availability.

In general, during daytime enhanced transpiration induces water deficiency in plants, causing a decrease in water potential and leading to perturbation of many physiological processes.

High temperatures seem to cause water loss in plants more during day time than night time.

Accumulation of compatible osmolytes

}Sugars, Alcohols, Proline (Amino Acid).

4-aminobutyric acid (GABA), a non-protein amino acid

Glycinebetaine (GB); quaternary amine.

Capacity to synthesize GB under stress conditions differs from species to species

For example, high level of GB accumulation was reported in maize and sugarcane due to desiccating conditions of water deficit or high temperature.

In contrast, plant species such as rice, mustard, Arabidopsis and tobacco naturally do not produce GB under stress conditions.

However, genetic engineering has allowed the introduction of GB-biosynthetic pathways into GB-deficit species

c. Photosynthesis

• Alterations in various photosynthetic attributes under heat stress are good indicators of thermotolerance of the plant as they show correlations with growth.
• Any constraint in photosynthesis can limit plant growth at high temperatures.
• Photochemical reactions in thylakoid lamellae and carbon metabolism in the stroma of chloroplast have been suggested as the primary sites of injury at high temperatures
• In tomato genotypes differing in their capacity for thermotolerance as well as in sugarcane, an increased chlorophyll a:b ratio and a decreased chlorophyll:carotenoids ratio were observed in the tolerant genotypes under high temperatures, indicating that these changes were related to thermotolerance of tomato.
• Furthermore, under high temperatures, degradation of chlorophyll a and b was more pronounced in developed compared to developing leaves.
• Such effects on chlorophyll or photosynthetic apparatus were suggested to be associated with the production of reactive oxygen species (ROS).
• High temperature influences the photosynthetic capacity of C3 plants more strongly than in C4 plants.
• It alters the energy distribution and changes the activities of carbon metabolism enzymes, particularly the rubisco, thereby altering the rate of RuBP regeneration by the disruption of electron transport and inactivation of the oxygen evolving enzymes of PSII.
• PSII is highly thermolabile, and its activity is greatly reduced or even partially stopped under high temperatures which may be due to the properties of thylakoid membranes where PSII is located.
• Heat stress may lead to the dissociation of oxygen evolving complex (OEC).
• Heat shock reduces the amount of photosynthetic pigments, soluble proteins, rubisco binding proteins (RBP) and large- (LS) and small subunits (SS) of rubisco in darkness but increases them in light, indicating their roles as chaperones and HSPs.

Figure. Heat induced inhibition of oxygen evolution and PSII activity. Heat stress leads to either (1) dissociation or (2) inhibition of the oxygen evolving complexes (OEC).

This enables an alternative internal e−-donor such as proline instead of H2O to donate electrons to PSII (De Ronde et al. ,2004).

Cell membrane thermostability

• Heat stress accelerates the kinetic energy and movement of molecules across membranes thereby loosening chemical bonds within molecules of biological membranes.
• This makes the lipid bilayer of biological membranes more fluid by either denaturation of proteins or an increase in unsaturated fatty acids.
• Such alterations enhance the permeability of membranes, as evident from increased loss of electrolytes.
• The increased solute leakage, as an indication of decreased cell membrane thermostability (CMT), has long been used as an indirect measure of heat-stress tolerance in diverse plant species.

Assimilate partitioning

• Under low to moderate heat stress, a reduction in source and sink activities may occur leading to severe reductions in growth, economic yield and harvest index.
• However, considerable genotypic variation exists in crop plants for assimilate partitioning, as for example among wheat genotypes .
• To elucidate causal agents of reduced grain filling in wheat under high temperatures, main components of the plant system including
• ¨Source (flag leaf blade)
• ¨Sink (ear)
• ¨ Transport pathway (peduncle)
• photosynthesis had a broad temperature optimum from 20 to 30◦C, however it declined rapidly at temperatures above 30◦C.
• The rate of C assimilate movement out of the flag leaf (phloem loading), was optimum around 30◦C, however, the rate of movement through the stem was independent of temperature from 1 to 50◦C.
• It was concluded that, at least in wheat, temperature effects on translocation result indirectly from temperature effects on source and sink activities.
• From such results, increased mobilization efficiency of reserves from leaves, stem or other plant parts has been suggested as a potential strategy to improve grain filling and yield in wheat under heat stress.

f. Hormonal changes

Abscisic acid

• ABA mediates acclimation/adaptation of plants to desiccation by modulating the up- or down-regulation of numerous genes.
• Under field conditions, where heat and drought stresses usually coincide, ABA induction is an important component of thermotolerance, suggesting its involvement in biochemical pathways essential for survival under heat-induced desiccation stress.
• Other studies also suggest that induction of several HSPs (e.g., HSP70) by ABA may be one mechanism whereby it confers thermotolerance.

2. Ethylene…..

• A gaseous hormone, ethylene regulates almost all growth and developmental processes in plants, ranging from seed germination to flowering and fruiting as well as tolerance to environmental stresses.
• Heat stress changes ethylene production differently in different plant species.
• For example, while ethylene production in wheat leaves was inhibited slightly at 35◦C and severely at 40◦C, in soybean ethylene production in hypocotyls increased by increasing temperature up to 40◦C and it showed inhibition at 45◦C.
• Despite the fact that ACC (1-amino-cyclopropane-1-carboxylic acid) accumulated in both species at 40◦C, its conversion into ethylene occurred only in soybean hypocotyls but not in wheat.

3. Salicylic acid (SA)

• Among other hormones, salicylic acid (SA) has been suggested to be involved in heat-stress responses elicited by plants.
• SA is an important component of signaling pathways in response to systemic acquired resistance (SAR) and the hypersensitive response (HR)
• SA stabilizes the trimers of heat shock transcription factors and aids them bind heat shock elements to the promoter of heat shock related genes.
• Long term thermotolerance can be induced by SA, in which both Ca2+ homeostasis and antioxidant systems are thought to be involved.

4. Gibberellins and Cytokinins

• The effects of gibberellins and cytokinins on high temperature tolerance are opposite to that of ABA.
• An inherently heat-tolerant dwarf mutant of barley impaired in the synthesis of gibberellins was repaired by application of gibberellic acid, whereas application of triazole paclobutrazol,  gibberellin antagonist, conferred heat tolerance.
• In a dwarf wheat variety, high temperature- induced decrease in cytokinin content was found to be responsible for reduced kernel filling and its dry weight.

5. Brassinosteroids

Another class of hormones, brassinosteroids have recently been shown to confer thermotolerance to tomato and oilseed rape (Brassica napus), but not to cereals.

g. Secondary metabolites

• High-temperature stress induces production of phenolic compounds such as flavonoids and phenylpropanoids.
• Phenylalanine ammonia-lyase (PAL) is considered to be the principal enzyme of the phenylpropanoid pathway.
• Increased activity of PAL in response to thermal stress is considered as the main acclimatory response of cells to heat stress.
• Thermal stress induces the biosynthesis of phenolics and suppresses their oxidation, which is considered to trigger the acclimation to heat stress.
• Carotenoids are widely known to protect cellular structures in various plant species irrespective of the stress type.
• it functions to prevent peroxidative damage to the membrane lipids triggered by ROS.
• Recent studies have revealed that carotenoids of the xanthophyll family and some other terpenoids, such as isoprene or –tocopherol, stabilize and photoprotect the lipid phase of the thylakoid membranes.
• Phenolics, including flavonoids, anthocyanins, lignins, etc., are the most important class of secondary metabolites in plants and play a variety of roles including tolerance to abiotic stresses
• Isoprenoids, another class of plant secondary products, are synthesized via mevalonate pathway
• Being of low molecular weight and volatile in nature, their emission from leaves has been reported to confer heat-stress tolerance to photosynthesis apparatus in different plants.
• In summary, like other stresses, heat stress causes accumulation of secondary metabolites of multifarious nature in plants.