Effect of heat stress on the photosynthetic apparatus in maize (Zea mays L.) grown at control or high temperature

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Abstract

The effects of short exposure to heat stress in the dark on maize seedlings grown at 25 °C or 41 °C were investigated by means of chlorophyll fluorescence and oxygen evolution. Exposure of plants grown at 25 °C to 35 °C for 20 min in the dark led to a transient inhibition (by about 50%) of the rate of photosynthesis, which recovered within 4 h. Treatments at temperatures above 45 °C led to permanent damage; the plants did not recover within 96 h. In contrast, no damage occurred to plants grown at 41 °C after exposure to temperatures up to 50 °C. Improved thermo-tolerance as a result of high growth temperature was not related to the presence of zeaxanthin, since it did not accumulate in heat-stressed leaves in the dark. In plants grown at 25 °C, measurements of the quantum yield of electron transport at PSII in leaves infiltrated with methylviologen (MV) indicated the presence of a heat-sensitive component of the photosynthetic apparatus, located downstream of photosystem II (PSII) and before the carbon cycle.

Introduction

The photosynthetic apparatus has long been recognized as one of the plant components most sensitive to high temperature stress (Berry and Björkman, 1980). Inhibition of photosynthesis has been observed after short exposure (15–60 min) to moderately high temperature (35–40 °C) in various plant species (Havaux, 1993a, Law and Crafts-Brandner, 1999, Crafts-Brandner and Salvucci, 2000) including maize (Crafts-Brandner and Salvucci, 2002). Following heat stress, the loss of photosynthetic electron transport in potato leaves was attributed to the thermolability of photosystem II (PSII) and water-splitting was the most heat-sensitive component (Havaux, 1993a). More recently, inhibition of the activation of ribulose-1,5-biphosphate carboxylase/oxygenase has been identified as one of the most heat-sensitive components of the photosynthetic apparatus (Law and Crafts-Brandner, 1999, Crafts-Brandner and Salvucci, 2000, Crafts-Brandner and Salvucci, 2002).

Although the photosynthetic apparatus is relatively heat-sensitive, improved thermo-tolerance can be achieved by exposure to moderately high temperature. The exposure of potato plants to 35 °C for 20 min significantly increased the stability of PSII to heat stress (Havaux, 1993b). This rapid acclimation was attributed to the accumulation of the xanthophyll zeaxanthin in the leaves (Havaux and Tardy, 1996), which stabilizes the lipid phase of the thylakoid membrane (Havaux, 1998). Additionally, unsaturation of membrane lipids, as shown in the cyanobacterium Synechocystis (Gombos et al., 1994), and the accumulation of heat-shock proteins, which was observed in Chenopodium album and Lycopersicum esculentum (Downs et al., 1999), are thought to play a role in protecting the photosynthetic apparatus from heat damage. Information concerning the ability of maize to acclimate to high temperature, however, is scanty. It was demonstrated that further heat tolerance of maize plants was induced by moderate heat shock (Gong et al., 2001) or gradually increased temperature. The latter was associated with the appearance of a new activase polypeptide (Crafts-Brandner and Salvucci, 2002).

To get new insights into the mode of acclimation to heat stress, we addressed the question whether the primary target of heat-induced perturbation of photosynthesis is identical in heat-acclimated and non-acclimated maize plants. To elucidate this, the effect of high growth temperature on the heat tolerance of the photosynthetic apparatus in maize leaves was investigated by means of chlorophyll fluorescence measurements and photosynthetic oxygen evolution. Heat stress treatment was conducted in the dark to prevent heat-induced photoinhibition as well as leaf cooling due to transpiration.

Section snippets

Plant material and growth conditions

All the experiments were performed with the tropical maize (Zea mays L.) inbred line Penjalinan. Seeds were sown in pots containing 1 l of a mixture of soil:peat (5:1 (v/v)) in a growth chamber (PGV36, Conviron, Winnipeg, Canada) until emergence. Seedlings were then thinned to two per pot. At the first leaf stage, half the pots were transferred from the control-temperature regime (25 °C/22 °C, day/night) to the high-temperature regime (41 °C/30 °C, day/night). The seedlings were irrigated daily with

Results

The effects of a short exposure (20 min) to high temperature in the dark on the functioning of the photosynthetic apparatus were studied in maize plants grown at 25 and 41 °C (Fig. 1). Heat treatments similarly affected photosynthetic O2 evolution and ΦPSII in leaves developed at 25 and 41 °C. A regression analysis of the pooled data of both leaf types (Fig. 1) revealed an r2 of 0.963 for the linear relationship between the rate of photosynthesis and ΦPSII. The photosynthesis of leaves grown at

Discussion

The linear relationship between the rate of photosynthesis and ΦPSII suggests that the proportion of electron transport used for photosynthesis remained constant, regardless of growth temperature and heat treatments. A similar relationship was found for maize grown under cold conditions in the field (Leipner et al., 1999).

According to Genty et al. (1989), the quantum yield of electron transfer at PSII (ΦPSII) is the product of the efficiency of the open PSII reaction centers (Fv′/Fm′) and the

Acknowledgements

This work was supported in part by the Swiss Federal Commission for Scholarship for Foreign Students.

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Present address: Ubonratchathani Field Crops Research Center, P.O. Box 69, Ubonratchathani 34000, Thailand.

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