Heat stress and recovery of photosystem II efficiency in wheat (Triticum aestivum L.) cultivars acclimated to different growth temperatures

https://doi.org/10.1016/j.envexpbot.2013.10.017Get rights and content

Highlights

  • Heat stress effect on photosystem II efficiency in four wheat cultivars were studied.

  • The cultivars C518 and KK3 showed heat tolerance performing better PSII efficiency.

  • The cultivars PWS7 and KKM1353 belonged to the heat susceptible group.

  • The cultivars varied for their rapid recovery capability after heat stress.

  • Heat stress significantly decreased relative chlorophyll content in all cultivars.

Abstract

The effect of heat stress on photosystem II (PS II) efficiency and post-stress recovery was studied in four wheat cultivars using chlorophyll fluorescence. The main aim was to examine the cultivar differences in relation to inhibition and recovery of PSII functionality after heat stress at different growth stages. The secondary aim was to investigate whether a pre-acclimation of plants to elevated temperature during the growth period induces a better tolerance to heat stress than for plants grown in ambient temperature or not. The plants were grown in two growth temperature conditions (15 °C and 25 °C) and subjected to heat stress (40 °C) for two days at early tillering and three days at anthesis and early grain development stages. The plants were returned to their original growth conditions after heat stress and recovery was observed for three days. The maximum photochemical efficiency (Fv/Fm) and the quantum yield of PSII (Fq/Fm) were measured before, during and after the heat stress. The heat stress significantly inhibited the Fv/Fm and Fq/Fm in all wheat cultivars at all growth stages. There were significant differences in Fv/Fm among the cultivars at anthesis and at early grain development but not at early tillering stage. However, the cultivars differed significantly in Fq/Fm at all growth stages. At anthesis and early grain development, the cultivar C518 had the lowest reduction in Fv/Fm and Fq/Fm after heat stress and recovered fully after 72 h in both growth conditions illustrating higher heat tolerance characteristics as compared to the other three cultivars. The largest decrease in Fv/Fm and Fq/Fm after heat stress occurred in the cultivar PWS7, which did not recover completely after 72 h. All cultivars grown at 25 °C had a slightly increased heat tolerance and better recovery compared to plants grown at 15 °C. The relative leaf chlorophyll content decreased significantly after heat stress in all cultivars at all growth stages. The elevated growth temperature (25 °C) accelerated plant growth resulting in early heading and reduced grain yield in comparison to ambient temperature (15 °C).

Introduction

Wheat (Triticum aestivum L.) is the most important crop in the temperate zone and the crop is often grown in areas where high temperatures limit productivity (Paulsen, 1994). The increased temperature and incidences of drought associated with global warming poses potential threats to wheat yield loses in Europe. Heat stress is often defined as the rise in temperature beyond a threshold level for a period of time sufficient to cause irreversible damage to plant growth and development (Hall, 2001). In general, a transient elevation in temperature, usually 10–15 °C above ambient, is considered heat shock or heat stress (Wahid et al., 2007). Photosynthesis is one of the most heat sensitive processes in plants and thermo sensitive components are found in both light- (PSII) (Heckathorn et al., 2002) and dark- (Rubisco activase) dependent reactions (Crafts-Brandner and Salvucci, 2002). PSII has been shown to be the most thermally labile component of the electron transport chain and the critical site of damage by high temperature (Allakhverdiev et al., 2008). Temperatures above 45 °C damage PSII (Sharkey, 2005, Yamane et al., 1998), while moderate heat stress normally encountered by most plants does not damage PSII (Sharkey, 2005), but has been reported to increase PSI cyclic electron flow (Zhang and Sharkey, 2009), thereby reducing the photosynthetic rate (Feller et al., 1998).

During the vegetative stage, efficient photosynthesis and assimilate partitioning play a decisive role in the formation of generative organs and thus directly affects the final yield (Asseng et al., 2002, Wollenweber et al., 2003). The cereal crops, however, has a narrow temperature tolerance range in the flowering phase and if exceeded it can damage pollination and subsequent seed production (Porter, 2005).

Studies have revealed genetic variability in the photosynthetic rate among different wheat cultivars when exposed to high temperatures associated with loss of chlorophyll and a change in the chlorophyll a:b ratio (Al-Khatib and Paulsen, 1984, Blum, 1986, Harding et al., 1990, Shanmugam et al., 2013). The stay-green trait has been associated with heat tolerance within fixed lines and similarly high chlorophyll contents have been associated with heat tolerance of sister lines in some wheat crosses (Reynolds et al., 1997). Elevated CO2 can reduce the stress effects at most growth stages except from the anthesis stage (Shanmugam et al., 2013).

Chlorophyll fluorescence has been used to detect genotypic differences in response to heat stress (Araus et al., 1998, Brestic et al., 2012, Sharma et al., 2012). The ratio Fv/Fm provides an estimate of the maximum photochemical efficiency of PSII and has been widely used to detect stress induced perturbations in the photosynthetic apparatus (Baker and Rosenqvist, 2004). Other parameters commonly used are quantum yield of PSII, non-photochemical quenching, NPQ and the redox state of PSII, qL (Kramer et al., 2004). The quantum yield of PSII (also known as PSII operating efficiency), Fq/Fm, measures the proportion of light absorbed by chlorophyll associated with PSII that is used in photochemistry (Baker and Rosenqvist, 2004). The NPQ (heat dissipation) compares the light-induced Fm level to the dark-adapted Fm and monitors the apparent rate constant for non-radiative decay (heat loss) from PSII and its antennae (Baker and Rosenqvist, 2004). The qL is a parameter estimating the fraction of PSII centres in open states with a high connectivity of PSII units (Kramer et al., 2004).

Genetic diversity of heat tolerance has been shown to exist both in conventional wheat cultivars and in wild Triticum and Aegilops species (Edhaie and Waines, 1992, Reynolds et al., 1994). Balouchi (2010) evaluated the genotypic variation of eight Australian wheat genotypes affected by heat and drought at the vegetative stage and found significant decreases in the quantum yield of PSII when the temperature increased from 28 °C to 36 °C. Furthermore, bread wheat was comparatively more tolerant to heat stress than durum wheat during grain filling (Dias et al., 2011). Recently, genotypic variability of 1274 wheat cultivars from different regions of the world was assessed based on their ability to maintain high Fv/Fm under heat stress conditions (Sharma et al., 2012), which led to the identification of cultivars contrasting for the trait. Further, better understanding of such physiological trait and the cultivar differences at genetic levels by QTL analysis is in progress (Sharma et al., unpublished). Such studies may facilitate better utilisation of existing genetic variability for improving stress tolerance.

Marked alterations in the chlorophyll a fluorescence, chlorophyll accumulation and photosynthesis in the primary leaves of the wheat cultivars have been reported at 37 °C and 45 °C for 8 h (Efeoglu and Terzioglu, 2009). On the other hand, no changes in the maximal efficiency of PSII were observed at moderately elevated temperatures (30–37.5 °C), while the decrease in PSII efficiency was irreversible at temperatures higher than 37.5 °C (Lu and Zhang, 2000), particularly at 45 °C in wheat leaves (Mathur et al., 2011). This indicates that the effect of heat stress on the photosynthetic apparatus of wheat leaves is reversible at temperatures below 45 °C.

Despite this, only few studies have been undertaken to characterize the nature of recovery of photosynthesis and photosynthetic electron transport after heat treatments (Kreslavskii and Khristin, 2003, Kreslavski et al., 2008, Yucel et al., 1992, Zhang et al., 2011). A 37 °C heat stress treatment for 30 min decreased the fluorescence parameter Fv/Fo by 40–50% in two wheat cultivars, but the values completely recovered after returning the heat treated seedlings to 22 °C for 24 h (Yucel et al., 1992). The after-effect of heat stress in wheat seedlings was examined after exposure to temperatures of 40 °C and 42 °C for 20 min and to temperature 42 °C for 40 min in the dark by monitoring the growing heat-treated plants in low/moderate/high light at 20 °C for 72 h (Kreslavski et al., 2008). The Fv/Fm fell during the heat stress treatment, but completely or partly recovered after 72 h of heat stress in different growth light conditions.

Heat tolerance is an important trait in plant breeding. Information concerning the ability of wheat to acclimate to elevated temperature and the mechanism of heat stability as well as recovery after heat stress, however, is scanty. The main aim of this paper was to examine inhibition and recovery of maximum photochemical efficiency of PSII (Fv/Fm) and quantum yield of PSII (Fq/Fm) in four wheat cultivars after a short term heat stress of 40 °C. The secondary aim was to investigate if pre-acclimation of plants in a slightly elevated temperature regime during the growth period improve heat stress tolerance.

Section snippets

Plant materials and growth conditions

The four spring wheat cultivars (T. aestivum L.) used in this study were Postelberger Wechsel St. 7 (PWS7), Kloka KM 1353 (KKM1353), C518 and Kamysinskaja 3 (KK3) received from the Institute of Plant Genetics and Crop Research (IPK, Gatersleben, Germany). The origin of the first two cultivars is Germany and the latter two are from Pakistan and Soviet Union, respectively. The cultivars were selected on the basis of the effect on Fv/Fm after 2 h of 38 °C heat stress on young plants, in a

Maximum photochemical efficiency of PSII (Fv/Fm)

The maximum photochemical efficiency of PSII, Fv/Fm, declined gradually with the duration of heat stress in all wheat cultivars and increased steadily during the recovery periods. At early tillering stage, all cultivars responded similarly in terms of Fv/Fm, and there were no significant differences (Table 1, Fig. 1,). In both 15 °C and 25 °C, Fv/Fm of all the cultivars in non-stressed plants ranged between 0.80 and 0.83. The reduction in Fv/Fm during the heat stress was more extensive in plants

Discussion

The Fv/Fm parameter has been established as a quantitative measurement of maximal photochemical efficiency of the PSII complex and the photon yield of oxygen evolution under different environmental stresses (Adams et al., 1990, Janka et al., 2013, Yan et al., 2010). In the present study, Fv/Fm was highly influenced by a heat stress treatment of 40 °C, and the decrease in Fv/Fm values ranged from 5–36% in comparison to the Fv/Fm values measured before the stress, depending on cultivars, growth

Conclusion

Heat stress significantly decreased the maximum photochemical efficiency (5–36%) and quantum yield of PSII (14–63%) in four wheat cultivars grown in two temperature conditions and different growth stages. The results confirm the reproducibility of the performance of these four cultivars namely, C518 and KK3 (heat tolerant) and PWS7 and KKM1353 (heat susceptible) according to their performance during selection based on Fv/Fm under heat stress in climate chambers (Sharma et al., 2012). The

Acknowledgments

The research project HEATWHEAT was kindly sponsored by a grant from the Ministry of Food, Agriculture and Fisheries. We would like to thank Ruth Nielsen, Kaj Ole Dideriksen and Helle K. Sørensen for an invaluable assistance during the experiments.

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