Drought, heat, and their combined effect on the photosynthetic performance of Psidium myrtoides O. Berg (Myrtaceae)¹

ABSTRACT

Popularly known as araçá-una, Psidium myrtoides is an endemic tree species in Brazil, with fruits much appreciated by the fauna. It is indicated for the composition of reforestation and for enriching the vegetation of degraded areas. This work aimed to evaluate the effects of drought, heat, and the interaction of both in the physiological attributes of Psidium myrtoides plants. Monitored fluorescence, gas exchange, and chlorophyll index in araçá-una plants induced by drought, heat, and the combination of both during 1, 3, and 7 days after treatment induction (DAT). After, the plants were returned to their initial condition, and their recovery was evaluated at 15 DAT. The results indicate that Psidium myrtoides plants reduce photosynthetic activity in the absence of water, contrary to what has been shown in other studies; in addition, they are not potentiated by the combination with heat. Therefore, we conclude that this species has a potential tolerance to heat (T_mean 30.3 °C). However, if water is available in the soil, it maintains photosynthetic activity at normal levels.

Keywords
drought stress; heat stress; JIP-test; photosynthesis

INTRODUCTION

Global warming, intensified in the last 35 years, is a well-established fact worldwide. The latest climate change models predict the rise in global temperature and changes in patterns of weather events, such as precipitation. As these events intensify, it becomes necessary to understand how they will affect plant physiological processes (Teskey et al., 2015; Bindoff et al., 2019) and, consequently, their effects on the structures and compositions of natural ecosystems (Malhi et al., 2020).

Environmental adversities such as drought and heat negatively affect plant growth and development. However, the exposure of plants to these conditions provides a range of responses and physiological adaptations that aim to reduce the damage caused by the stress condition (Zandalinas et al., 2016; 2018). For example, drought is one of the factors responsible for inducing stomatal closure, limiting the performance of the photosynthetic apparatus and, consequently, the increase in biomass. Heat, on the other hand, impairs plant metabolism, causing destabilization of proteins and enzymes, disturbing the flow of electrons and energy reactions, and impairing carbon assimilation. Together, these two stresses have positive interactions that intensify their effects (Teskey et al., 2015; Singh & Thakur, 2018).

Of all plant metabolism, photosynthesis is one of the most fundamental components of plant growth and development (Singh & Thakur, 2018). Given this, variables related to photosynthesis, such as chlorophyll a fluorescence, and gas exchange, have been widely used to identify the occurrence of physiological changes in plants under both greenhouse (Goltsev et al., 2016; Zhao et al., 2017b) and field conditions (Faria-Silva et al., 2017; Faria-Silva et al., 2019).

Although the effects of drought (Faria-Silva et al., 2017), heat (Faria-Silva et al., 2017) and their interaction (Urban et al., 2018; Haworth et al., 2018) have been studied in cultivated species, relatively few studies have evaluated these effects in native tree species in Brazil. Given this, studying plants’ behavior under stress conditions is essential to understanding natural vegetation’s fate (Chaves et al., 2003).

Psidium myrtoides O. Berg (Myrtaceae), popularly known as araçá-una, is a tree species endemic to Brazil with wide distribution, occurring from the Caatinga, Cerrado to the Atlantic Forest (Psidium Flora do Brasil, 2020). It has a height of 4-8 m elongated and a semi-deciduous crown. Its fruits are berries type, sweet pulp, and much appreciated by the fauna. In addition, it is indicated for the reforestation composition and for enriching the vegetation of degraded areas (Lorenzi, 1998).

Despite the importance of Psidium myrtoides plants in the ecosystems in which they are inserted (Lorenzi, 1998), in natural medicine (Dias et al., 2018), and also the potential of their fruits for the agroindustry (Franzon et al., 2009), it is virtually non-existent studies on the physiology, as well as the effects of abiotic stresses of this species. With this, we hypothesize that the combined effects of drought and heat lead to quantitatively more significant damage to the photosynthetic performance of Psidium myrtoides plants than they alternately remained.

This study aimed to evaluate the effects of drought, heat, and their interaction on the chlorophyll a fluorescence, gas exchange, and photosynthetic pigment content of Psidium myrtoides plants.

MATERIALS AND METHODS

Plant material and growth conditions

The experiment was conducted in the experimental area of the Department of Botany at the Federal University of Espírito Santo (20°27′49″ S e 40°33′44″ W, alt. 6m) in February 2018. Psidium myrtoides seedlings, 36 months old, from seeds grown in 32-liter pots filled with soil and sand substrate, were used (2:1; v/v). First, 50 ml of the nutrient solution was added to each pot with ½ force (Hoagland & Arnon, 1950). Then, before starting the experiment, the plants were kept in ambient conditions (T_mean 26.8 °C) for 30 days. Still in this period, irrigation occurred periodically, aiming to keep the soil moisture close to the field capacity. Then, the plants were subjected to drought, heat, and a combination of both. Subsequently, after the stress-inducing period, the plants were returned to their initial condition, and their recovery was evaluated for seven days (Figure 1).

Figure 1
Scheme of treatments in Psidium myrtoides plants. Where: T1 = drought stress, T2 = heat stress and T3 = drought + heat stress.

Chl a fluorescence measurements

The chlorophyll a fluorescence transient (OJIP) was quantified with the Handy-PEA fluorometer (Hansatech Instruments, Norfolk, UK). Evaluations took place between 7:00 am and 8:00 am on fully expanded young leaves (i.e., fourth or fifth leaf from the apex), previously adapted to the dark for 40 minutes. Subsequently, with the collected data, the biophysical parameters were calculated using the JIP test proposed by Strasser et al. (1995; 2000), using the PEA-Plus software version 1.11. Table 1 shows the parameters and equations of the JIP test used in this study (Goltsev et al., 2016).

Table 1
Summary of parameters and formulas used to evaluate the chlorophyll a fluorescence transient (Goltsev et al. 2016)

Abbreviations	Formulas	Definition
φP0	Fv/Fm = 1 - F0/FM	Maximum quantum yield of primary Photosystem II (PSII) photochemistry
ψE0	1 - VJ = ET0/TR0	Efficiency with which a PSII trapped electron is transferred from Quinone A (QA) to Quinone B (QB)
φE0	1 - FJ/FM = ET0/ABS	Quantum yield for electron transport
δR0	1 - FI/FM = RE0/ET0	Quantum yield of the electron transport flux until the Photosystem I (PSI) electron acceptors
PIabs	(RC/ABS) · (φP0/(1 – φP0)) (ψE0/(1 – ψE0))	Potential performance index of PSII
PItotal	PIABS · (δR0/(1 – δR0))	Total photochemical performance index

Gas exchange measurements

The net CO₂ uptake rate was determined with a portable gas exchange system (LCi-Pro model, ADC BioScientific Ltd., Hoddesdon, UK). The evaluations took place between 7:00 am and 8:00 am in young leaves completely expanded (i.e., fourth or fifth leaf from the apex), using ambient CO₂ (≈ 380 Pa), under saturating light conditions of 1300 μmol m^-2 s^-1 (determined from the previously performed light curve) and controlled temperature of 25 °C in the leaf chamber.

The variables evaluated were: net photosynthesis rate (A; μmol m^-2 s^-1), transpiration rate (E; μmol H₂O m^-2 s^-1), and stomatal conductance (gs; μmol H₂O m^-2 s^-1).

Photosynthetic pigment measurements

The chlorophyll index was determined whit a SPAD chlorophyll meter (Konica Minolta SPAD-502, Osaka, Japan). Each leaf was measured five times in different parts, avoiding the ribs. The leaves selected for this measurement were the fully expanded young leaves (i.e., the fourth or fifth leaf from the apex).

Statistics analysis

Statistical analyzes were performed using InfoStat software version 2017d in a randomized experimental design (n = 5). The data were subjected to analysis of variance and, when significant, were compared by the Scott-Knott test of means at a 5% probability of error.

RESULTS

Chlorophyll a fluorescence parameters analyses

In 1DAT, no changes were observed between treatments and control for chlorophyll a fluorescence parameters (Table 2). However, in 4DAT, all of them showed a significant increase of ≈ 3% in φP₀ about the control (Table 2). In the following measurement, T₁ and T₃ plants significantly reduced 30% in φP₀.

Table 2
Photosynthetic parameters deduced by the JIP test analysis of fluorescence transients in Psidium myrtoides of control plants and of plants under drought (T₁), heat (T₂), and drought + heat (T₃) stress at 1, 4 and 7 days after treatments (DAT), and at 7 days of restoration of the initial conditions of irrigation and temperature (recovery)

		φP0	ψE0	φE0	PIABS	δR0	PITOTAL
1DAT	Control	0.75 a	0.53 a	0.40 a	1.59 a	0.48 a	1.40 a
	T1	0.74 a	0.51 a	0.38 a	1.27 a	0.51 a	1.30 a
	T2	0.76 a	0.51 a	0.39 a	1.35 a	0.48 a	1.21 a
	T3	0.75 a	0.49 a	0.37 a	1.15 a	0.50 a	1.14 a
4DAT	Control	0.76 a	0.52 a	0.40 a	1.42 a	0.48 a	1.27 a
	T1	0.78 b	0.55 a	0.43 b	1.76 a	0.41 a	1.24 a
	T2	0.79 b	0.57 a	0.45 b	2.27 a	0.45 a	1.89 b
	T3	0.78 b	0.56 a	0.44 b	1.88 a	0.44 a	1.49 a
7DAT	Control	0.75 b	0.49 b	0.36 b	1.15 b	0.53 b	1.26 b
	T1	0.51 a	0.43 a	0.22 a	0.23 a	0.38 a	0.14 a
	T2	0.77 b	0.55 c	0.42 b	1.73 b	0.51 b	1.81 c
	T3	0.55 a	0.44 a	0.24 a	0.33 a	0.36 a	0.18 a
Recovery	Control	0.76 a	0.55 b	0.42 b	1.61 a	0.44 a	1.27 a
	T1	0.73 a	0.47 a	0.34 a	0.98 a	0.57 b	1.19 a
	T2	0.77 a	0.55 b	0.42 b	1.72 a	0.50 b	1.73 a
	T3	0.76 a	0.53 b	0.40 b	1.49 a	0.51 b	1.50 a

• Different letters in columns of the same treatment day indicate statistically significant (p < 0.05) differences among treatments by the Scott-Knott test.

In this scenario, ψE₀ presented the first changes at 7DAT. T₂ plants showed a significant increase of 12%, about control plants. In the other treatments, a reduction of ≈ 11% was observed in ψE₀. As with φP₀, φE₀ of all treatments showed a significant increase of 10%, about the control plants in 4DAT.

Regarding the potential performance index of the PSII (PI_ABS), changes were only observed at 7DAT. In this scenario, there was a significant reduction of ≈ 90% in PI_ABS of T₁ and T₃ plants compared to control plants. The efficiency with which electrons moved from the intersystem receptors to the final PSI receptors (δR₀) occurred according to what was observed in PI_ABS. Regarding the total photochemical index (PI_TOTAL), T2 plants showed a significant increase of ≈ 44%, about control plants in the period of maximum stress. On the other hand, plants under the treatments (T₁ and T₃) showed a reduction of 88 and 85% in PI_TOTAL, respectively.

After restoring the initial conditions of irrigation and temperature for seven days (recovery), the plants recovered and showed PI_ABS and PI_TOTAL similar to the control plants.

Gas exchange analyses

In 1DAT, there were no significant differences in gas exchanges between the control plants and those under treatment (Figure 2). In this scenario, the values of net photosynthesis rate (A), transpiration rate (E), and stomatal conductance (gs) were, respectively, 4.85 (± 1.96), 0.037 (± 0.08) and 0.643 (± 1.86). On the other hand, in 4DAT, the T₂ plants had a 67% increase in net photosynthesis rate compared to the control plants. Concomitantly, the T₁ and T₃ plants showed a reduction of 77 and 51%, respectively. Finally, in 7DAT, the control and T₂ plants maintained A at around 5.97 (± 1.3), while the two treatments with water restriction (T₁ and T₃) had A equal to zero.

Regarding the transpiration rate (E), in 4DAT, plants under all treatments showed values ≈ 48% lower than the control plants’ rates (4.15 ± 1.1). During the subsequent measurement, on 7DAT, T₂ plants showed a significant increase for E of 73% compared to the control. In turn, the T₁ and T₃ plants showed values close to zero. Stomatal conductance (gs) exhibited behavior similar to the sweating rate (E), mainly in the recovery phase.

With the restoration of the initial conditions of irrigation and temperature for seven days (recovery), the rates of net photosynthesis (A), stomatal conductance (gs), and transpiration (E) of all treatments regained values similar to the control, noteworthy is the rapid recovery of T₁ and T₃ plants.

Chlorophyll index (u.r. SPAD)

In 1DAT and 4DAT, no significant differences were observed between the chlorophyll index of plants submitted to all treatments. In 7DAT, the T₁ plants showed, in isolation, a 5% reduction in the chlorophyll index in comparison to the control and the other treatments (T₂ and T₃). However, after the recovery phase, the T₂ and T₃ plants showed an increase of 8 and 5% in the chlorophyll index, respectively, differing statistically from the control (Figure 2).

Figure 2
(a) Net photosynthesis rate (A; μmol m^-2 s^-1), (b) stomatal conductance (gs; μmol H₂O m^-2 s^-1), (c) transpiration rate (E; μmol H₂O m^-2 s^-1) and (d) SPAD chlorophyll index in Psidium myrtoides of control plants and plants under drought (T₁), heat (T₂) and drought + heat (T₃) stress at 1, 4 and 7 days after treatments (DAT), and at 7 days of restoration of the initial conditions of irrigation and temperature (recovery). *p < 0.05 and **p < 0.01 compared to the control by the Scott-Knott test. Error bars indicate SD.

DISCUSSION

In this study, the induction of plants to drought (T₁) combined drought and heat stress (T₃) stress reduced the photochemical (φP₀, ψE_0, φE₀, δR₀, PI_abs e PI_total) and photosynthetic (A, E e g_s) performance of Psidium myrtoides plants. The significant 30% reduction in φP0 suggests that dehydration possibly reduced the oxide-reduction reactions of the PSII. Furthermore, after watering for seven days (recovery), the plants of all treatments were similar to the control condition. The significant increase of 12% in ψE₀, for T₂ plants, about control plants, suggests that: in a situation of adequate irrigation, the temperature can increase electron transport by ETC after a Q_A in Psidium myrtoides plants.

Photosynthesis limitations caused by drought occur due to stoma closure (Flexas et al., 1999). In drought stress, plants regulate stomatal closure to prevent dehydration. As a result, the entry of CO₂ into the leaf mesophile is impaired, directly impacting its assimilation and reducing photosynthesis rates and photochemical performance rates (Yan et al., 2017). According to Martin-StPaul et al. (2017), this mechanism is a process to prevent dehydration and ensure that the plant aerial parts demand for water does not exceed the supply capacity of the root system. However, in severe drought conditions, the PSII can suffer damage of different intensities (Lang et al., 2018), reducing the photosynthetic activity, the electron transport rate (ETR), and the photochemical (qP) and non-photochemical (qN) quenching coefficients (Li et al., 2017). In general, photosynthetic activity is reduced when plants are subjected to stresses due to the destabilization of RuBisCO and damage to PSII caused by reactive oxygen species (ROS) produced in chloroplasts (Dietz et al., 2016; Nishiyama & Murata, 2014). On the other hand, the heat increased the transpiration rate to decrease leaf temperature (Zandalinas et al., 2016) and increased ψE₀ and PI_TOTAL.

Several studies have pointed out that the combined drought and heat stress had a worse potential effect than drought or heat stress alone (Mittler & Blumwald, 2010; Zhao et al., 2017a). This stress is because the stomatal responses to drought, heat, and the combination of both represent a challenging condition for plants. Therefore, it is necessary to establish a balance to prevent water loss and provide leaf cooling (Zandalinas et al., 2018). That is, while high temperatures induce the plant to increase stomatal conductance to cool the leaves, drought is one of the factors responsible for inducing stomatal closure to reduce water loss (Mittler 2002; 2006). According to Tardieu et al. (2018), plants have evolved and developed a regeneration cycle in which increased transpiration promotes the stomata closure, reducing the transpiration rate. However, this study did not observe these responses for Psidium myrtoides plants since the drought (T₁), and the drought + heat (T₃) treatments demonstrated similar behaviors.

On the other hand, plants subjected only to heat stress (T2) proved similar to control plants. It is known that in C3 plants, high temperatures limit the rate of photosynthetic CO₂ assimilation due to the increase in RuBisCO oxygenase capacity (Yan et al., 2017). However, recent studies indicate that this mechanism, known as photorespiration, can act in the photoprotection of the photosynthetic apparatus using the excess energy in the ETR and dissipating it through the C2 cycle (Teskey et al., 2015; Haworth et al., 2018). The results show that the plants of Psidium myrtoides submitted to heat (T2) have manifested mechanisms of photoprotection because the parameters of fluorescence and gas exchange were similar to the control and, in some cases, as for ψE₀ and PI_TOTAL, were even higher. It is likely to assume that, given the conditions imposed by the treatments, the limiting factor in the photosynthesis of Psidium myrtoides plants was drought and not heat. The photosynthetic apparatus is more tolerant to heat than drought (Urban et al., 2018).

After the recovery, the plants submitted to heat (T₂), and dry + heat (T₃) stress showed both the parameters of the JIP test and those of gas exchange similar to the control plants. However, a difference remained in the SPAD index. The mentioned treatments showed an increase in leaf chlorophyll production, contrary to the studies of Bahrami et al. (2019), who reported that leaf chlorophyll is negatively influenced by heat, and a drought condition can lead to its degradation. Given the above, it is suggested that the increase in temperature imposed on T₂ and T₃ increased chlorophyll production, raising the value detected by a higher SPAD index.

In ‘Ubá’ mango tree under combined light and temperature stress (Faria-Silva et al., 2017), and under nonirrigated conditions (Faria-Silva et al., 2019) the chlorophyll content also showed higher values, in addition to a high positive correlation with the number of active reaction centers, suggesting that these has adaptation strategies of PSII and PSI to light and thermal stress.

According to Ahmad & Prasada (2012), the recovering capacity of plants to abiotic stresses is associated with the intensity and time of exposure. Therefore, further studies are needed to establish the limits of the recovering capacity of Psidium myrtoides plants subjected to drought, heat, and a combination of these stresses.

CONCLUSIONS

The plants of Psidium myrtoides showed a reduction in photochemical and leaf gas exchange when subjected to drought and drought + heat, recovering after seven days of restoration of normal conditions of irrigation and temperature. These same treatments showed an increase in the SPAD index at the end of the recovery period.

• 1
  This study is part of independent work developed by Photosynthesis Research Center students during their postgraduate course. The financial incentive came through scholarships in force at the time, granted by CAPES.

REFERENCES

• Ahmad P & Prasad MNV (2012) Abiotic Stress Responses in Plants: Metabolism, Productivity and Sustainability. Springer, 978:01-19.
• Bahrami F, Arzani A & Rahimmalek M (2019) Photosynthetic and yield performance of wild barley (Hordeum vulgare ssp. spontaneum) under terminal heat stress. Photosynthetica, 57:09-17.
• Bindoff NL, Cheung WWL, Kairo JG, Arístegui J, Guinder VA, Hallberg R, Hilmi N, Jiao N, Karim MS, Levin L, O’donoghue S, Cuicapusa SRP, Rinkevich B, Suga T, Tagliabue A & Williamson P (2019) Changing Ocean, Marine Ecosystems, and Dependent Communities. In: Pörtner HO, Roberts DC, Masson-Delmotte V, Zhai P, Tignor M, Poloczanska E, Mintenbeck K, Alegría A, Nicolai M, Okem A, Petzold J, Rama B & Weyer NM (Eds.) IPCC Special Report on the Ocean and Cryosphere in a Changing Climate. Cambridge, Cambridge University Press. p.447-588.
• Chaves MM, Maroco JP & Pereira JS (2003) Understanding plant responses to drought from genes to the whole plant. Functional Plant Biology, 30:239.
• Dias ALB, Batista HRF, Estevam EBB, Alves CCF, Forim MR, Nicolella HD, Furtado RA, Tavares DC, Silva TS, Martins CHG & Miranda MLD (2018) Chemical composition and in vitro antibacterial and antiproliferative activities of the essential oil from the leaves of Psidium myrtoides O. Berg (Myrtaceae). Natural Product Research, 33:2566-2570.
• Dietz KJ, Turkan I & Krieger-Liszkay A (2016) Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosyxnthesizing Chloroplast. Plant Physiology, 171:1541-1550.
• Faria-Silva L, Gallon CZ, Purgatto E & Silva DM (2017) Photochemical metabolism and fruit quality of Ubá mango tree exposed to combined light and heat stress in the field. Acta Physiologiae Plantarum, 39:238.
• Faria-Silva L, Gallon CZ, Filgueiras PR & Silva DM (2019) Irrigation improves plant vitality in specific stages of mango tree development according to photosynthetic efficiency. Photosynthetica, 57:820-829.
• Franzon RC, Campos LZO, Proença CEB & Sousa-Silva JC (2009) Araçás do gênero Psidium: principais espécies, ocorrência, descrição e usos. Embrapa Cerrados, 1:01-47.
• Flexas J, Escalona JM & Medrano H (1999) Water Stress Induces Different Levels of Photosynthesis and Electron Transport Rate Regulation in Grapevines. Plant, Cell & Environment, 22:39-48.
• Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H & Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russian Journal of Plant Physiology, 63:869-893.
• Haworth M, Marino G, Brunetti C, Killi D, de Carlo A & Centritto M (2018) The Impact of Heat Stress and Water Deficit on the Photosynthetic and Stomatal Physiology of Olive (Olea europaea L.) — A Case Study of the 2017 Heat Wave. Plants, 7:76.
• Hoagland DR & Arnon DI (1950) The water-culture method for growing plants without soil. Berkeley, California Agricultural Experiment Station. 32p. (Circular, 347).
• Lang Y, Wang M, Xia J & Zhao Q (2018) Effects of soil drought stress on photosynthetic gas exchange traits and chlorophyll fluorescence in Forsythia suspensa. Journal of Forestry Research, 29:45-53.
• Li J, Cang Z, Jiao F, Bai X, Zhang D & Zhai R (2017) Influence of drought stress on photosynthetic characteristics and protective enzymes of potato at seedling stage. Journal of the Saudi Society of Agricultural Sciences, 16:82-88.
• Lorenzi H (1998) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas do brasil. 2ª ed. Nova Odessa, Instituto Plantarum de Estudos da Flora. 351p.
• Malhi Y, Franklin J, Seddon N, Solan M, Turner MG, Field CB & Knowlton N (2020) Climate change and ecosystems: threats, opportunities and solutions. Royal Society, 375:01-08.
• Martin-StPaul N, Delzon S & Cochard H (2017) Plant resistance to drought depends on timely stomatal closure. Ecology Letters, 20:1437-1447.
• Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends in Plant Science, 11:15-19.
• Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7:405-410.
• Mittler R & Blumwald E (2010) Genetic Engineering for Modern Agriculture: Challenges and Perspectives. Annual Review of Plant Biology, 61:443-462.
• Nishiyama Y & Murata N (2014) Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Applied Microbiology and Biotechnology, 98:8777-8796.
• Psidium Flora do Brasil (2020) Jardim Botânico do Rio de Janeiro. Available at: <http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB10874>. Accessed on: July 23^rd, 2023.
  » http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB10874
• Singh J & Thakur JK (2018) Photosynthesis and Abiotic Stress in Plants. In: Vats S (Ed.) Biotic and Abiotic Stress Tolerance in Plants. Springer, Singapore. p.27-46.
• Strasser RJ, Srivastava A & Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochemistry and Photobiology, 61:3242.
• Strasser RJ, Srivastava A & Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M & Pathre U (Eds.) Probing Photosynthesis: Mechanism, Regulation & Adaptation. London, Taylor & Francis. p.445-483.
• Tardieu F, Simonneau T & Muller B (2018) The Physiological Basis of Drought Tolerance in Crop Plants: A Scenario-Dependent Probabilistic Approach. Annual Review of Plant Biology, 69:733-759.
• Teskey R, Wertin T, Bauweraerts I, Ameye M, Mcguire MA & Steppe K (2015) Responses of tree species to heat waves and extreme heat events. Plant, Cell & Environment, 38:1699-1712.
• Urban O, Hlaváčová M, Klem K, Novotná K, Rapantová B, Smutná P, Horáková V, Hlavinka P, Škarpa P & Trnka M (2018) Combined effects of drought and high temperature on photosynthetic characteristics in four winter wheat genotypes. Field Crops Research, 223:137-149.
• Yan W, Zheng S, Zhong Y & Shangguan Z (2017) Contrasting dynamics of leaf potential and gas exchange during progressive drought cycles and recovery in Amorpha fruticosa and Robinia pseudoacacia. Scientific Reports, 7:01-12.
• Zandalinas SI, Mittler R, Balfagón D, Arbona V & Gómez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiologia Plantarum, 162:02-12.
• Zandalinas SI, Rivero RM, Martínez V, Gómez-Cadenas A & Arbona V (2016) Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biology, 16:105.
• Zhao G, Xu H, Zhang P, Su X & Zhao H (2017a) Effects of 2,4-epibrassinolide on photosynthesis and Rubisco activase gene expression in Triticum aestivum L. seedlings under a combination of drought and heat stress. Plant Growth Regulation, 81:377-384.
• Zhao P, Jackson PA, Basnayake J, Liu J, Chen X, Zhao J, Zhao X, Bai Y, Yang L, Zan F, Yang K, Xia H, Qin W, Zhao L, Yao L, Lakshmanan P & Fan Y (2017b) Genetic variation in sugarcane for leaf functional traits and relationships with cane yield, in environments with varying water stress. Field Crop Research, 213:143-153.

Publication Dates

• Publication in this collection
  09 Oct 2023
• Date of issue
  2023

History

• Received
  02 June 2022
• Accepted
  28 Mar 2023