The xanthophyll cycle and antioxidative defense system are enhanced in the wheat hybrid subjected to high light stress
Introduction
Normally, leaves cannot utilize all of the light absorbed during exposure to full sunlight for photosynthesis (Björkman and Demmig-Adams, 1994, Demmig-Adams et al., 1996). Thus, under natural conditions, plants are often exposed to high light conditions, in particular during a sunny day. The absorption of excess light can be deleterious because it can potentially lead to the production of reactive oxygen species (ROS), such as singlet oxygen, superoxide and H2O2. Xanthophyll cycle-dependent energy dissipation in the light-harvesting antennae and the detoxification of reduced ROS by chloroplast's antioxidant systems play a photoprotective role in leaves by mitigating oxidative damage to cellular macromolecules under high light conditions.
It is widely accepted that excess excitation energy is harmlessly dissipated in the antennae complexes of photosystem II (PSII) as heat through a process which involves the xanthophyll cycle and a low thylakoid pH. The xanthophyll cycle pigments zeaxanthin (Z) and antherxanthin (A) are formed from violaxanthin (V) under conditions of excess excitation energy and are both thought to be involved in the photoprotective dissipation process (Demmig-Adams and Adams, 1992, Gilmore, 1997, Niyogi, 1999). In this cycle, excess excitation energy can be harmlessly dissipated in the antennae complexes of PSII as heat through the formation of Z by de-epoxidation of V, via the intermediate A. Z plays an important role in the photoprotective dissipation of surplus excitation energy in the antennae complexes of PSII as heat (Demmig-Adams and Adams, 1992, Gilmore, 1997). Z is believed to interact in a pH-dependent manner with CP22 protein encoded by the psbS gene to facilitate energy dissipation (Li et al., 2000, Li et al., 2002). In addition, A is also directly involved in the photoprotective dissipation process and is able to trap surplus excitation energy in the antennae complexes of PSII and to dissipate it harmlessly as heat (Gilmore et al., 1998, Gilmore and Yamamoto, 2001, Gilmore, 2001).
The antioxidative defense system includes enzymatic and non-enzymatic constituents that detoxify reduced ROS. Superoxide dismutase (SOD), which is located in chloroplasts, mitochondria and other cellular compartments, catalyzes the dismutation of superoxide to H2O2 and O2 (Van Camp et al., 1994). Catalase (CAT) catalyzes the dismutation of H2O2 to O2 and is present predominantly in mitochondria and peroxisomes (Scandalios, 1994). The superoxide generated by the direct reduction of O2 in the vicinity of photosystem I (PSI) is rapidly converted to H2O2 by SOD, whereas H2O2 is detoxified by CAT in mitochondria and peroxisomes and by ascorbate peroxidase (APX), an enzyme for which over 90% of leaf activity is localized in chloroplasts (Gillham and Dodge, 1986). Additionally, the redox reagents ascorbate and glutathione are re-reduced, during which several enzymes dehydroascorbate reductase (DHAR), monodehydroascorbate reductase (MDHAR), and glutathione reductase (GR) are involved (Asada, 1999).
Wheat is one of the most important agricultural crops in China. However, a continental hot, dry wind occurs during the period of wheat grain-filling from late May to June in northern China. This hot, dry wind, combined with full sunlight during a sunny day, often leads to photo-oxidative damage to photosynthetic apparatus, resulting in a decrease in wheat yield. Therefore, a cultivar with superior photosynthetic traits and high resistance to photo-oxidative stress is important to wheat production in northern China. For this purpose, we have successfully selected a hybrid (1–12) from the progeny (F3) by crossing Xiaoyan 54 (maternal parent) and Jing 411 (paternal parent), since Jing 411 is a cultivar with high yield and superior photosynthetic traits but not with high resistance to photo-oxidative stress and Xiaoyan 54 is a cultivar with high photo-oxidative resistance but a normal yield (Wang et al., 2000). Plot experiments under field conditions have shown that this hybrid is a potential wheat variety, since it has higher yield than its parents when grown in northern China. We have previously observed that photosynthetic capacity was higher in the hybrid than in its parents during later grain-filling process under field conditions, and this higher photosynthetic capacity in the hybrid was associated with its higher CO2 assimilation rate, PSII efficiency, and Rubisco activity (Yang et al., 2007a). In addition, the higher photosynthetic capacity in the hybrid may be associated with its higher resistance to photoinhibition (Yang et al., 2006). However, the physiological mechanisms responsible for this higher resistance of photoinhibition in the hybrid remain unknown. The objective of this study was to investigate why the hybrid shows higher resistance to photoinhibition than its parents. We investigated the responses of PSII photochemistry, the xanthophyll cycle, and antioxidative defense system in the hybrid and its parents during exposure to high light stress. Our results suggest that the higher resistance to photoinhibition in the hybrid than in its parents was associated with its higher capacity for antioxidative defense and xanthophyll cycle-dependent energy dissipation. Our results also suggest that the xanthophyll cycle and antioxidative defense can be used as indicators for wheat breeding.
Section snippets
Plant material and growth conditions
The winter wheat (Triticum aestivum L.) hybridization line 1–12 was selected from the F3 progeny of crossing between Xiaoyan 54 (maternal parent) and Jing 411 (paternal parent). The line 1–12 is genetically stable and shows no separation phenomenon after six generations. The lines 1–12, Jing 411, and Xiaoyan 54 were grown in a field at the farm of Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing from September 2003 to June 2004 and from September 2004 to
Characterization of PSII during high light treatments
To investigate the possible mechanisms of higher tolerance to photoinhibition in the hybrid, we examined the responses of PSII photochemistry to high light stress, the leaves in the hybrid and its parents at the flowering stage were exposed to high light (1500 μmol m−2 s−1) for up to 3 h. Fig. 1 shows the changes in Fv/Fm, ΦPSII, qP, and NPQ in the hybrid and its parents during exposure to high light. There was a significant decrease in Fv/Fm, ΦPSII, and qP in the hybrid and its parents, but the
Discussion
The wheat hybrids have often shown higher grain yields, which is of vital agronomic importance. However, the genetic and physiological basis of the higher yields remains unknown. Recent studies have suggested that the differentially expressed genes and proteins between the wheat hybrids and their parents involved in diverse physiological process pathways, including metabolism, materials transport, photosynthesis, and signal transduction, could play important roles for hybrids (Yao et al., 2005,
Acknowledgements
We are grateful to the financial support by the National Natural Sciences Foundation of China (30725024), the State Key Basic Research and Development Plan of China (2009CB118503), and the Frontier Project of the Knowledge Innovation Engineering of Chinese Academy of Sciences (KSCX2-EW-J-1).
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