Exposure to cadmium causes declines in growth and photosynthesis in the endangered aquatic fern (Ceratopteris pteridoides)

Highlights

• Cd induced ecophysiological responses of Ceratopteris pteridoides were studied.

• Photosynthesis of C. pteridoides was greatly affected by Cd treatment.

• Cd modified reactive oxygen species-related responses in C. pteridoides.

• Cd influenced nitrogen metabolism in C. pteridoides.

Abstract

With rapid development of agriculture and urbanization, aquatic systems and aquatic plants in China face a great threat of heavy metal pollution where toxic contaminant cadmium (Cd) concentrations were reported up to 4500 μg l⁻¹ in some heavy metal polluted waters. Our objectives were to assess the biological causes of heavy metal Cd in aquatic systems associated with the population decline of an endangered aquatic species Ceratopteris pteridoides. The effects of cadmium (Cd) toxicity on the photosynthetic performance, leaf chlorophyll content, antioxidant enzyme activities and nitrogen metabolism in C. pteridoides were investigated under greenhouse conditions. Seedlings were exposed to various Cd concentrations (0, 5, 10, 20, and 40 μM) for 7 days. The accumulation of Cd ions in plant tissues inhibited the relative growth rate of C. pteridoides through net assimilation rate retardation and leaf area ratio reduction. A significant reduction in biomass was observed in C. pteridoides at 20 and 40 μM Cd concentrations. Exposure to Cd severely restricted plant net photosynthetic rates. Factors limiting photosynthesis in Cd-treated plants were more related to non-stomatal constraints than to stomatal limitation. Cd reduced chlorophyll content of the treated plants and affected also plant ribulose-1,5-bisphosphate (RuBP) activity and regeneration capacity. Decreased leaf photosynthesis showed that a significant amount of Rubisco was not active in photosynthesis under Cd stress. The Cd treatments reduced significantly the relative quantum efficiency of PSII, electron transport rate and photochemical efficiency of PSII reaction centers, which corresponded to the reduction in Rubisco activity. Increased Cd concentrations showed similar effects on the superoxide dismutase, catalase, and peroxidase activities in the leaves and roots. Also, Cd retention caused cell membrane damage shown by increased malondialdehyde content. Cd toxicity may have interfered with plant nutritional assimilation because there was a deficiency in nitrogen uptake and translocation, shown by the reduced nitrate reductase and glutamine synthetase activities. We conclude that physiological disturbances in Cd-stressed plants are congruent with the observed plant growth inhibition. Plant Cd stress inhibited both nitrogen absorption and photosynthesis in C. pteridoides, thus enhancing its mortality risk. An efficient strategy to restore environmental quality for this endangered fern implies the reduction of Cd pollution in the environment.

Introduction

Aquatic systems are highly valued because of their biodiversity and ecological functions such as flood prevention, water use, recreation and tourism. At present, heavy metal contamination in soil and water is a growing problem in many areas around the world (Fritioff and Greger, 2006). Aquatic systems and their plants face a great threat of heavy metal and metalloid (i.e. Cd, As, Pb) pollution emanating from agriculture and other human activities. Heavy metals occur naturally in soils and in source materials used to manufacture fertilizers (Hu et al., 2006). Cd can also be found in fertilizers blended with recycled industrial waste, i.e. mine tailings (ICdA, 2012). The presence of heavy metals in inorganic fertilizers is well established, and a wide range of fertilizer products contain elevated levels of cadmium, arsenic and lead (Cook and Morrow, 1995, Ran et al., 2005, Feng et al., 2010). Runoff from agricultural land into aquatic systems is one of the major sources of heavy metal pollution, which is the largest source of water quality and aquatic system health problems in the world (Li et al., 2008, Li et al., 2009, ICdA, 2012).

As an environmental hazard, Cd enters the aquatic environment primarily from natural and anthropogenic sources, not only agricultural runoff but also industrial effluents, fossil fuel combustion, cement and steel production, and municipal solid waste incineration (Li et al., 2008, Sun et al., 2008). Cd concentrations have been reported as 100–500 μg l⁻¹ in the earth's crust, 100–900 μg l⁻¹ in lake waters, 900–1100 μg l⁻¹ in marine sediments (ICdA, 2012), and up to 200 mg l⁻¹ in phosphorus fertilizers (Cook and Morrow, 1995). Cd concentrations reach up to 4500 μg l⁻¹ in some heavy metal polluted waters in China, while the Cd safety regulation standard is 30 μg l⁻¹ in China (Yu, 1999, Ran et al., 2005, Feng et al., 2010). Cd is a highly toxic contaminant that affects many plant metabolic processes. Cd ions can inhibit photosynthesis by impairing chlorophyll synthesis (Li et al., 2008, Sun et al., 2008), chloroplast organization (Vecchia et al., 2005), and other photosynthetic processes (Li et al., 2008). Moreover, Cd can affect cell metabolism by changing the behavior of enzymes crucial in various metabolic pathways and the composition and function of cell membrane (Vecchia et al., 2005) through enhanced production of reactive oxygen species (ROS) that damage cellular components (Singh et al., 2006). Furthermore, Cd can disturb plant water status (Perfus-Barbeoch et al., 2002) and interfere with mineral nutrition by hampering the uptake and translocation of essential elements (Hassan et al., 2008), resulting in growth reduction. Decreased transpiration rate due to stomatal closure in Cd-treated plants may impair nutrient uptake and transport, and Cd stress can also impair plasma membrane integrity by increasing lipid peroxidation (Singh et al., 2006, Tian et al., 2011).

Ceratopteris pteridoides (Hook.) Hieron. (Parkeriaceae) is an aquatic isosporous floating fern, classified as an endangered aquatic species in China, but known widely because of its distribution via aquarium trade (Dong et al., 2010, Li et al., 2008). C. pteridoides is mainly distributed in ponds, lakes, rivers, and ditches in central and southern China (Sun et al., 2008). Recently, only five populations of C. pteridoides have been found in China. The species is now considered to be endangered in China, and is listed in the second category of protected wild plants (Yu, 1999). The decline in C. pteridoides populations has been attributed to several factors including habitat loss, over-harvesting, exotic invasive species, and exposure to environmental pollution (Dong et al., 2007).

As Cd concentrations were high in aquatic systems and Cd toxicity could affect many plant processes including impairment of photosynthesis (Li et al., 2008), we hypothesized that the declined population of this floating fern was related to Cd toxicity in waters. However, relationships between C. pteridoides species survival and Cd toxicity are currently not known. It is reported that anatomical alterations occurring during plant Cd uptake could have an effect on the accumulation processes and vegetative growth (Lux et al., 2011). The accumulation of Cd ions could imply root toxicity, causing root growth reduction and root morphological changes (Wang et al., 2008, Li et al., 2009, Djebali et al., 2010). Cd toxicity might reduce significantly plant leaf number, leaf area (LA), leaf area ratio (LAR) and index of leafiness of aquatic plants in a concentration-dependent manner (Dhir et al., 2004). Decrease in LA and leafiness in Cd-treated plants could be partly attributed to reduce in leaf mass per unit area (LMA), an important variable that relates plant dry matter production to leaf area expansion (Dhir et al., 2004). Also, decreased turgor potential and cell wall elasticity could result in smaller leaf cells formed with smaller intercellular space area (Vassilev and Yordanov, 1997).

The effects of Cd ions on photosynthetic performance varied with different plant species and Cd concentrations (Mobin and Khan, 2007). In this work, the effects of Cd on different morphological, physiological and nutritional variables as well as antioxidant enzymes in C. pteridoides were studied. The objectives of the study were to assess the biological causes of heavy metal Cd in aquatic systems associated with the population decline of the C. pteridoides, examine the chemical stress and sensitivity of this endangered species to Cd toxicity, and to determine the mechanisms involved in the sensitivity of aquatic plants to this environmental hazard metal.