Boron deficiency decreases growth and photosynthesis, and increases starch and hexoses in leaves of citrus seedlings
Introduction
Boron (B) is an essential element required for the normal growth of higher plants. Boron deficiency is a widespread problem in many agricultural crops, including citrus (Shorrocks, 1997). The role of B in plant nutrition is little understood, which is surprising, since on a molar basis the requirement for B is, at least for dicotyledons, higher than that of any other micronutrient (Marschner, 1995; Alves et al., 2006).
Previous studies have shown that B deficiency decreases plant photosynthetic capacity (Kastori et al., 1995; Zhao and Oosterhuis, 2002, Zhao and Oosterhuis, 2003). In mustard (Brassica campestris), decreased rate of CO2 assimilation appears to result from both decreased Hill reaction activity and low intercellular CO2 concentration (Sharma and Ramchandra, 1990). Plesničar et al. (1997) suggested that the decreased rate of photosynthetic O2 evolution in B-deficient sunflower (Helianthus annuus) leaves could be correlated with reduced chlorophyll (Chl) content, photosynthetic electron transport rate and photophosphorylation. El-Shintinawy (1999) investigated the structural and functional damage caused by B deficiency in sunflower leaves and suggested that B deficiency affected photosynthesis directly or indirectly. Accumulation of starch and hexoses occurs despite decreased photosynthesis (Kastori et al., 1995; Zhao and Oosterhuis, 2002; Camacho-Cristóbal et al., 2004) because growth is more affected than photosynthesis, and they are not used. This leads us to hypothesize that CO2 assimilation is feedback-regulated by excessive accumulation of starch and hexoses in B-deficient leaves via direct interference with chloroplast function and/or indirect repression of photosynthetic enzymes.
A consequence of the imbalance between photosynthetic production of carbohydrates and their use in growth is that less of the absorbed photon-energy captured by the light harvesting system is used in CO2 assimilation, so the photosystem electron transport chain becomes over-reduced. This leads to accelerated production of reactive oxygen species (ROS) such as single oxygen (1O2), superoxide anion (O2−), hydrogen peroxide (H2O2) and hydroxyl radicals (OH). To minimize cellular damage caused by ROS, plants have evolved a scavenging system composed of antioxidants such as ascorbate (AsA) and reduced glutathione (GSH) and antioxidant enzymes such as superoxide dismutase (SOD, EC 1.15.1.1), ascorbate peroxidase (APX, EC 1.11.1.11), glutathione reductase (GR, EC 1.6.4.2), monodehydroascorbate reductase (MDAR, EC 1.6.5.4), and dehydroascorbate reductase (DHAR, EC 1.8.5.1) involved in the water–water cycle, as well as catalase (CAT, EC 1.11.1.16) involved in scavenging the bulk H2O2 generated by photorespiration (Chen et al., 2005). Although there have been several reports investigating the antioxidant responses in leaves of plants treated with excess B (Keles et al., 2004; Molassiotis et al., 2006), data are limited on the effects of B deficiency. Liu and Yang (2000) reported that low B decreased SOD, APX, and CAT activities, and AsA content of soybean (Glycine max) leaves. In sunflower leaves, B deficiency increased APX activity, decreased GR and CAT activities, decreased AsA and non-protein SH-compound contents, but did not affect SOD activity (Cakmak and Römheld, 1997; Dube et al., 2000). Thus, it is not well known how B deficiency affects antioxidant system in plants.
In China, B deficiency is frequently observed in citrus orchards, and is responsible for considerable loss of productivity and poor fruit quality. To our knowledge, there is hardly any information on gas exchange, photosynthetic enzymes, carbohydrates, and antioxidant system of citrus leaves in response to B deficiency. The objectives of this study were to test the hypothesis that CO2 assimilation is feedback-regulated by excessive accumulation of starch and hexoses in B-deficient leaves, and to determine how B deficiency affects antioxidant system in B-deficient leaves.
Section snippets
Plant culture and B treatments
This study was conducted outdoors from March to November 2005 at Fujian Agriculture and Forestry University, Fuzhou. Seeds of citrus (Citrus sinensis (L.) Osbeck cv. Xuegan) were germinated in plastic trays containing sand, and fertilized when necessary with 1/4 strength nutrient solution until dripping. Full-strength nutrient solution contained 6 mM KNO3, 4 mM Ca(NO3)2, 2 mM NH4H2PO4, 1 mM MgSO4, 50 μM KCl, 10 μM H3BO3, 2 μM MnSO4, 2 μM ZnSO4, 0.5 μM CuSO4, 0.065 μM (NH4)6Mo7O24, and 40 μM Fe-EDTA (
Plant growth
Plants grown in the absence of B firstly developed B-deficient symptoms at the apex and in the actively growing leaves. In the young leaves B-deficient symptoms included dieback of terminal growth, yellow, water-soaked spots in the lamina, and general deformation. Symptoms in the mature leaves were characterized by yellowing, enlargement, splitting, and corking of leaf veins. No symptoms were observed in plants supplied with 2.5 or 10 μM B, and foliar B concentration was in the normal range for
Discussion
Our finding that B-deficient symptoms started at the apex and in the actively growing leaves is consistent with the result that B is phloem immobile in lime (Citrus aurantifolia) (Konsaeng et al., 2005). Evidence suggests that the predominant role of B is in the formation of primary cell walls, where it cross-links the pectic polysaccharide rhamnogalacturonan II (RG-II) (Brown and Hu, 1997; O’Neill et al., 2004). The borate cross-linked RG-II has been shown to be essential for normal plant
Acknowledgments
This work was supported by the Agricultural Commonweal Industrial Special Fund Program of Department of Agriculture, China (nyhyzx07-023). The authors wish to thank Dr. David W. Lawor, Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Herts. AL5 2JQ, UK, for language correction and constructive comments on this manuscript.
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