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Thakur, M.; Raza, A.; , .; Prakash, C.S.; Anand, A. Respiratory Control of Crop Yield under High Temperature. Encyclopedia. Available online: https://encyclopedia.pub/entry/21872 (accessed on 22 July 2024).
Thakur M, Raza A,  , Prakash CS, Anand A. Respiratory Control of Crop Yield under High Temperature. Encyclopedia. Available at: https://encyclopedia.pub/entry/21872. Accessed July 22, 2024.
Thakur, Meenakshi, Ali Raza,  , Channapatna S. Prakash, Anjali Anand. "Respiratory Control of Crop Yield under High Temperature" Encyclopedia, https://encyclopedia.pub/entry/21872 (accessed July 22, 2024).
Thakur, M., Raza, A., , ., Prakash, C.S., & Anand, A. (2022, April 18). Respiratory Control of Crop Yield under High Temperature. In Encyclopedia. https://encyclopedia.pub/entry/21872
Thakur, Meenakshi, et al. "Respiratory Control of Crop Yield under High Temperature." Encyclopedia. Web. 18 April, 2022.
Respiratory Control of Crop Yield under High Temperature
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This entry is adapted from the peer-reviewed paper 10.3390/agronomy12040806

Respiration and photosynthesis are indispensable plant metabolic processes that are affected by elevated temperatures leading to disruption of the carbon economy of the plants. Increasing global temperatures impose yield penalties in major staple crops that are attributed to increased respiratory carbon loss, through higher maintenance respiration resulting in a shortage of non-structural carbohydrates and an increase in metabolic processes like protein turnover and maintenance of ion concentration gradients.

acclimation alternative oxidase heat stress mitochondria

1. Introduction

The rising temperature is an intrinsic component of global climate change that controls the carbon fluxes in all the crops. High temperature affects the major plant physiological processes, such as photosynthesis and respiration; therefore, it becomes important to estimate the plant carbon dioxide (CO2) balance that finally decides the crop productivity [1][2][3].Through these two pathways, the terrestrial ecosystems exchange about 120 Gt of carbon per year with the atmosphere [4]. A rough estimate states that half of the CO2 assimilated annually through photosynthesis is released back to the atmosphere by plant respiration [5][6][7], and merely 15–25% of the fixed carbon finally translates into yield [8][9]. The projected elevation in temperature beyond 2.0 °C by the end of the decade [10] may increase the magnitude of carbon loss exponentially in the physiological temperature range of 0 to 38 °C [11], which will further exacerbate in a species-and environment-dependent manner at higher temperatures between 48 and 60 °C [12][13][14][15].
The carbon lost through the ‘breathing out’ processes in plants can occur via two mechanisms, namely photorespiration and dark/mitochondrial respiration. These processes release CO2, but dark respiration occurs regardless of light in the plant cells [16][17]. Biochemically, dark respiration is an enzymatically regulated, multistep, amphibolic process that produces ATP by the oxidation of glucose formed during photosynthesis. Glucose is initially broken into pyruvate during glycolysis, which is oxidized to form acetyl-CoA, releasing a molecule of CO2. The acetyl-CoA then enters the tricarboxylic acid (TCA) cycle, where it is oxidized to CO2 and also produces reductants (nicotinamide adenine dinucleotide: NADH; dihydroflavine-adenine dinucleotide: FADH2) that pass through the mitochondrial electron transport chain (ETC). The oxidation of the reductants produces a proton gradient across the inner membrane of the mitochondria that drives the synthesis of ATP. High temperatures impact dark respiration in plants with an exponential increase [18], which can become detrimental due to irreversible damage to the enzymatic machinery [15]. Climate change prediction models have speculated a 3–20% decline in the yield of major crops like wheat, rice, maize, and soybean with every 1 °C increase in the global mean temperatures [19][20], which makes it pertinent to relate this loss to the waste of carbon due to respiration.

2. Respiratory Carbon Loss-A Constraint to Crop Yield

Respiration, rather than photosynthesis, may be the primary contributor to yield losses in a high temperature climate [11]. Low respiration rates are generally correlated with high crop yields [21][22]. Walker et al. [23] reported that photorespiration decreased soybean and wheat yields by 36% and 20%, respectively, in the United States. In another study, a 10–12% and 17–35% decrease in the yields of wheat and rice, respectively, was reported due to high temperatures [24]. The yield loss in wheat and rice due to high night temperature (HNT) is mainly ascribed to higher dark respiration, which increases the consumption of photoassimilates, thereby resulting in the reduction of non-structural carbohydrates (NSCs) in stem tissues [25][26]. Glaubitz et al. [27] reported that increasing night temperature from 25 °C to 35 °C resulted in increased leaf respiratory carbon losses in grapevines, as reflected by the decrease in NSCs of 0.025 and 0.041 mg g−1dry weight, respectively. Such losses are consistent with metabolite profiling studies in wheat and rice, which revealed an increase in TCA cycle intermediates in leaves exposed to HNT, supporting increased respiration in the photosynthesizing tissue [25][28]. Xu et al. [29] suggest that increased dark respiration restrains source availability under the combined stress of high day and night temperatures, leading to a considerably more severe yield penalty due to carbon loss.

3. Heat-Induced Changes in the Proportion of Maintenance Respiration

Dark respiration (Rd) is typically partitioned into two functional components, i.e., growth respiration (Rg) and maintenance respiration (Rm), which are impacted upon by environmental stresses [9][30][31]. Figure 1 illustrates the differences in these components under elevated temperatures. Growth respiration is a dominant component of respiration in younger tissues, while the latter contributes majorly to the older tissues [32]. Growth respiration is defined as the amount of photoassimilates respired to provide energy for the synthesis of additional biomass [33]. It also provides a carbon skeleton and reductants to facilitate nutrient uptake/assimilation followed by biosynthesis of cellular components to drive the growth of tissues. Thus, the relationship between the growth rates of a species and temperature is actually a measure of the rate of the growth respiration component [34]. A recent analysis of 101 evergreen species growing in different biomes (boreal to tropical) showed that respiration increased with an increase in growth temperatures in accordance with previous studies [35][36]. Leaf form accounted for the response ratio of Rg to warming, as species with needle-like leaves had a significantly higher response (25 ± 9%) than broad-leaved ones [36].
Agronomy 12 00806 g001
Figure 1. Growth respiration and maintenance respiration under elevated environmental temperature. HSPs: heat shock proteins; NSCs: non-structural carbohydrates; Rg: growth respiration; Rm: maintenance respiration; Rt: total respiration.
On the other hand, maintenance respiration comprises the respiratory processes that help in supporting the already established biomass of the plant [33]. It depends upon the amount and composition of the biomass, as both these factors undergo change depending on the environment and developmental stage of the plant. Although the role of both the components is integral to the life cycle of the plants, their estimation can only be done by employing physiological models [32][37][38][39]. The higher temperature responsiveness of Rm over Rg in mature tissues was concluded from various studies, e.g., Marigolds when exposed to a 10 °C increase in temperature resulted in a 43% to 55% increase in the proportion of maintenance respiration to total respiration (Rt) [40]. Additionally, a significant reduction in ATP content and total biomass was observed in rice plants subjected to 10 °C higher temperature at the reproductive stage than the ambient temperature (28 °C), thereby suggesting that energy produced by respiration under high temperature conditions was mainly attributed to maintenance respiration rather than growth respiration [32]. Mathematically, maintenance respiration is expressed as the product of maintenance respiration coefficient and plant size. The Q10 value (proportional increase in rate of respiration with a 10 °C rise in temperature) of the maintenance respiration coefficient varies between 1.35 and 3.0 depending upon the species, developmental stage, and environmental conditions as shown in the data compiled from various studies (Table 1). The sensitivity of Q10 to temperature indicates that the response of respiration to temperature cannot be represented by one value.
Table 1. Q10 values for maintenance respiration coefficient in various crops.
Crop Experimental Temperature Q10 Value Reference
Marigold (Tagetes patula) 20 °C (Control)
30 °C (Elevated)		 1.35–1.55 [40]
Barley (Hordeum vulgare) 15 °C (Control)
28 °C (Elevated)		 3.00 [41]
Subterranean clover (Trifolium subterraneum) 10 °C (Control)
35 °C (Elevated)		 1.85 [42]
Japanese knotweed
(Reynoutria japonica)		 15 °C (Control)
25 °C (Elevated)		 1.90 [43]
Wheat (Triticum aestivum) 15 °C (Control)
20 °C (Elevated)		 1.80 [44]
10 °C (Control-Night temperature)
21 °C (Elevated-Night temperature)		 1.97 [45]

4. Substrate Availability for Respiration under High Temperature

The considerable variation observed in the Q10–temperature relationship is influenced by the supply of the respiratory substrate and the respiration capacity [4][46]. Environmental variables that affect the biosynthesis of the substrates [18][46] or increase the metabolism of energy consuming processes like turnover of proteins and maintenance of ion gradients [47], make Q10 values highly dynamic in response to temperature. Additional energy costs are incurred by mechanisms imparting heat tolerance in the crops, e.g., upregulation of the antioxidant defense system to counteract the upsurge in the level of reactive oxygen species (ROS), synthesis of osmoprotectants, and accretion of heat shock proteins (HSPs). The need for respiratory substrate in the plants is mainly met from the non-structural carbohydrates [25][26][27][48] and the protein turnover [11][32]. Studies on the effect of elevated night temperatures have shown that the high rate of nighttime respiration exerted pressure on the supply of NSCs, which subsequently reduced the biomass and yield of rice [25][26]. The concentration of sugars has been positively correlated with the rate of dark respiration in Pinus [49], Quercus rubra [50], and Spinacia oleracea [51]. The light control of carbohydrate synthesis affected the rate of dark respiration in Geum urbanum plants grown under 75% shade as it declined due to limited photosynthate supply, but Q10 declined only when the leaves experienced near darkness for long periods. It was concluded that intense shade for a prolonged period would cause a reduction in both respiration and Q10 due to adenylate restriction on respiration in addition to the substrate availability [4].

5. Regulation of Respiratory Flux at High Temperature

Adenylates (in particular the ratio of ATP to ADP and the concentration of ADP per se), are likely the most important in regulating respiratory flux at warm temperatures [52]. Adenylate control would indicate that the respiratory capacity at warmer temperatures exceeded the level required for cell processes to proceed [18], which in turn would lead to elevated ATP:ADP ratios or low ADP concentration, causing downregulation of respiration [53]. The increased leakiness of membranes at high temperatures could further contribute to substrate limitation because concentration gradients of TCA cycle intermediates are more difficult to maintain when mitochondrial membranes are excessively fluid [18].

6. Positive Correlation between Protein Turnover Cost and Respiratory Cost at High Temperature

Nitrogen (N) utilization processes, including nitrate reduction and ammonium assimilation, are thought to have high respiratory costs [54]. In fact, the estimates of construction respiration are greatly influenced by the form of N source, e.g., nitrate or ammonium [55]. The protein turnover rate increases with temperature, suggesting that the protein turnover cost is a major component of the N-utilization cost and dominates during maintenance respiration. Hachiya et al. [56] studied the protein turnover cost in Petunia x hybrida petals grown at three different temperatures (20, 25,and 35 °C) during the development of the petals. Most petals are non-photosynthetic; therefore, ATP and reducing equivalents are supplied mainly from the respiratory pathway. The integrated protein turnover cost on dry weight basis was similar between 20 and 25 °C but increased by more than four times at 35 °C, suggesting that the high temperature enhanced the cost of protein turnover, thereby increasing the total cost of N-utilization along with respiration in the petals.

7. Diurnal Dynamics of Respiration

The diurnal or diel cycle of plant growth interacts with the respiratory metabolism, which can be directly linked with the availability of respiratory metabolites regulating the process at different times of the day [57]. The photosynthate synthesized during the day supports carbon supply for the entire plant during the day, which is reduced to critical levels by the end of the night [58]. The strong coupling between carbon fixation through photosynthesis and loss due to respiration [59] indicates the diurnal fluctuation in rates of dark respiration as a result of changes in the concentration of various metabolites supporting the respiratory process [60]. In this case, the supply of sugars is stabilized over the day–night cycle, and the diel variation in respiration may be explained by changes in the availability of amino acids, proteins, organic acids, and/or lipids. These metabolites may drive respiration by supplying intermediates to the TCA cycle, reductants for ATP synthesis via oxidative phosphorylation, and carbon skeletons required for biosynthesis or nitrogen assimilation into amino acids [61].
Metabolomic studies have shown that warmer day (30 °C) and night (28 °C) temperatures lead to the accumulation of amino acids derived from shikimate pathways, such as phenylalanine, tyrosine, tryptophan, aspartic acid, lysine, proline, and ɣ-amino butyrate (GABA), in thermo-sensitive rice cultivars (DR2 and M202) but not in intermediate (IR64 and IRRI123) and temperature-tolerant cultivars (IR72 and Taipei 309) [28]. Similarly, in wheat, high night temperatures showed a prevalence of fumarate and alanine without any significant change in the level of glutamine, glutamate, and GABA [25]. The accumulation of TCA intermediates like malate and fumarate during the day, and citrate, aconitate, and succinate during the night [62][63], reiterates the circadian control of the TCA pathway, which is a hub for the process of respiration and can be markedly influenced by an increase in temperature [64]. Rashid et al. [64] assessed the influence of growth temperature and the diel cycle on the concentrations of metabolites involved in the respiratory network of rice. They raised the plants under 25 °C:20 °C, 30 °C:25 °C, and 40 °C:35 °C day:night cycles and measured the dark respiration and changes in metabolites at five time points spanning a single 24 h period and observed that shikimate pathway-derived aromatic amino acids were the only metabolites to interact in response to both the growth temperature and the day:night cycle. Cook et al. [65] reported increased concentrations of α-ketoglutarate, fumarate, malate, and citrate in Arabidopsis leaves when cooled from 20 °C to 4 °C. All these studies suggest that there are distinct respiratory metabolite adjustments to temperature and the diel cycle.Further, detailed experiments on the interaction of the diel cycle and temperature will generate a better understanding of the metabolites controlling dark respiration in plants. Therefore, the instantaneous measurement of respiration rates at a single point during the day can overlook the differential response prevalent during an extended period.

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Anjali Anand
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Entry Collection: Environmental Sciences
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Update Date: 18 Apr 2022
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