Changes in chloroplast ultrastructure, fatty acid components of thylakoid membrane and chlorophyll a fluorescence transient in flag leaves of a super-high-yield hybrid rice and its parents during the reproductive stage
Introduction
Leaf senescence has been a major topic in plant research. It is characterized by a programmed degradation of constituents such as chlorophyll (Chl), proteins, nucleic acids and lipids, together with structure of leaf cell and organelles, resulting in significant photosynthetic decline and a resultant decrease in yield. However, the complex nature of this process is not been well understood.
Chloroplasts are one of the first organelles to be targeted for breakdown (Quirino et al., 2000). Chloroplasts are the sites of photosynthesis, and the decline in photosynthesis is expected to correspond with ultrastructural alterations in the chloroplast as the leaf progresses towards senescence (Bondada and Oosterhuis, 1998). One of the major events in leaf senescence is the decomposition of biomembranes, including degradation of membrane lipids (McRae et al., 1985). The fatty acids liberated during this degradation process constitute suitable substrates for enzymatic and non-enzymatic lipid peroxidation (Berger et al., 2001). The damage of thylakoid membranes may inevitably lead to a significant decrease in photosynthesis and decreased biomass production, mainly in grain yield for crop plants. Chloroplasts are also the organelles most exposed to oxygen toxicity because they function at conditions of high oxygen concentration and high intensity (Halliwell and Gutteridge, 1989). In chloroplasts, the primary source of H2O2 is thought to be the Mehler reaction. Lipid peroxidation is caused by active oxygen species (AOS) (Thompson et al., 1987). AOS are generated from the plasma-membrane NADPH oxidase, which transfers electrons from cytoplasmic NADPH to O2 to form O2−•, followed by dismutation of O2−• to H2O2 (Kuo Tung Hung and Ching Huei Kao, 2004). Quantities of lipid peroxidation products in leaves of different developmental stages, including natural senescence, show a strong increase in the level of oxygenated polyenoic fatty acids (PUFAs) during the late stages of leaf senescence.
Selection of new varieties of cereal plants with a high crop yield is one of the biggest challenges to plant breeders (Vivekanandan and Saralabai, 1997). Yuan Longping, director of China’s National Hybrid Rice Research and Development Center in Changsha, Hunan Province, has spent 2 decades working on breeding a male sterility trait into the indica rice varieties grown in China (Normile, 2000). He first succeeded in developing two-line inter-sub-specific techniques. Hybrid rice now covers about 50% of China’s rice acreage and accounts for 60% of production (Normile, 2000). LiangYouPeiJiu (LYPJ) is a newly developed two-line inter-sub-specific hybrid rice that is a combination of WuMang9311 (WM9311, a restoration line) as the paternal line and PeiAi64S (PA64S, a sterile line) as the maternal line (Lu and Zou, 2000). Its yield can reach 9750–10,500 kg hm−2, 1200–1800 kg hm−2 higher than that of the traditional cultivar ShanYou63 presently cultivated most of the area in China (Lu and Zou, 2000).
Although many authors have reported that there are close relationships among chloroplast ultrastructure, composition of fatty acids of the thylakoid membrane, lipid peroxidation and Chl a fluorescence transient in different species (Heinz and Roughan, 1983; Lichtenthaler et al., 2007), little work has been performed with rice. Chonan et al. (1977) examined changes in chloroplast ultrastructure during leaf senescence in rice plants, but no data are available, to our knowledge, about the chloroplast ultrastucture of new rice cultivars, although many high-yield cultivars have been developed in last 30 years. Some work in our laboratory has examined the high-yield cultivar in terms of photosynthesis, resistance to various stresses (Chen et al., 2004) and morphology showing that its type is similar to its paternal line 9311, an ideal plant type. Our previous data indicated that LYPJ shows greater resistance to stressors than do other rice cultivars. When detached rice leaves are used to study senescence, wounding is always a problem (Kuo Tung Hung and Ching Huei Kao, 2004) and, accordingly, findings may be not entirely responsible for the nature of leaf senescence. Therefore, a study of leaf senescence under natural conditions may well elucidate leaf senescence. In this study, we applied natural conditions of leaf senescence to identify changes in the ultrastructure of chloroplasts during flag leaf senescence in this newly developed super-high-yield hybrid rice and the relationship between it and its parents, as well as the association with fatty acid compositions. It is necessary for plant biologists to comprehensively understand changes in ultrastructure of chloroplasts during the entire process of leaf development in different species, since photosynthesis is central to plant productivity and chloroplasts are the sole organelles to photosynthesize. We also believe that comparison of these properties between a high-yield rice cultivar and its parents could be helpful to crop breeders in further breeding new rice cultivars with even higher yield through selection of ideal rice parents.
Section snippets
Materials and methods
Field experiments were carried out at the experimental fields of the Institute of Agricultural Sciences of Jiangsu Nanjing, China (32°03′N, 118°47′E). Nanjing is located in the monsoon climate area of the north subtropical zone, with four distinctive seasons. Its average annual temperature is 15±2.7° and the annual precipitation 989.3±156 mm (Fan and Chen, 1997). The soil types are clay loam with 1.25 g cm−1 bulk density. During the period from 1 August (22 d before the first sampling) to 8 October
Results
At the stage of full expansion of flag leaves, chloroplasts exhibited the normal ultrastructural level of their organization; most were lens-like oblong shapes, with a typical arrangement of grana and stroma thylakoids.
Chloroplasts appeared densely occupied by thylakoids arranged in grana and in grana-interconnecting membranes, and the chloroplasts were lined close to the cell periphery. A typical membrane structure was also recognized, such as a double membrane in the chloroplast envelope.
Discussion
In 1977, Sitte (1977) first put forward the concept of gerontoplast, describing changes in the senescing chloroplasts (in review of Shen, 2001). One of the most obvious events occurring during early senescence at the cellular level is the transformation of chloroplasts into gerontoplasts (Noodén et al., 1997). With leaf aging, chloroplasts undergo significant alterations in their structure and their inclusions as well as in their biochemical properties.
Transmission electron microscopy in this
Acknowledgements
Financial support was provided by the National Natural Sciences Foundation of China (30771299), by the Specialized Research Fund for the Doctoral Program of Higher Education (20060319005), by grants from the National Basic Research Program of China (2009CB118500) and by the ShanXi Province Natural Sciences Foundation (2009021030-2). We also want to thank Prof. Tang RuHang for his help, Mr. Du KaiHe for his help with electron microscopy, and Lv ChuanGen provided material.
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