Volume 3 Issue 3 - January 25, 2008
How do Plants Sense Heavy Metal Pollutants?
Hao-Jen Huang*, Chuan-Ming Yeh, and Pei-Shan Chien

Department of Life Sciences

Chuan-Ming Yeh, Pei-Shan Chien and Hao-Jen Huang (2007)
Journal of Experimental Botany. 58(3):659-671

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One challenge in modern life sciences is to understand how cells respond to and distinguishes between different environmental stressing stimuli.

Environmental stresses, including biotic and abiotic stresses, are important factors that affect growth and development of land plants. Heavy metal toxicity is one of the major environmental health problems in modern society, with potentially dangerous bioaccumulation through the food chain. The ions of both essential and non-essential metals such as copper, cadmium, chromium, and nickel, respectively, can be toxic to plants. However, the molecular mechanistic basis of toxicity is not well understood in detail. Cadmium (Cd2+) is a toxic metal with a long biological half-life and represents a serious environmental pollutant for both animals and plants. In plants, Cd2+ is known to inhibit seed germination and root growth, induce chromosomal aberrations and micronucleus formation, and cause faster wilting and a grey-green leaf color. Although copper (Cu2+) is essential for normal plant growth and development, elevated concentrations of Cu2+ in the soil can also lead to toxicity symptoms and stunted growth in most plants. Although heavy metals are associated with a number of physiological disorders in plants, the molecular mechanisms of heavy metal signal transductions are not well understood.

One intriguing challenge in modern life sciences is to understand how cells respond to and distinguishes between different metal stressing stimuli. Plants have developed systems that quickly and accurately transmit stimuli from the external environment and adjust metabolic pathways by modulating the expression of genes. Mitogen-activated protein kinase (MAP Kinase) pathways are modules involved in the transduction of extracellular signals to intracellular targets in all eukaryotes. Distinct MAP Kinase pathways are regulated by different extracellular stimuli and are implicated in a wide variety of biological processes. In plants, there is evidence for MAP Kinases playing a role in the signaling of abiotic stresses, pathogens, and plant hormones. In our previous paper, we have first isolated a MAP Kinase from rice (Oryza sativa) termed OsMAPK2. In addition, our previous results indicate that abiotic stress regulates transcription of OsMAPK2, OsMAPK3 and OsMAPK4 mRNA. This is the first demonstration of a MAP Kinase-related kinase in monocotyledonous species that is induced by abiotic stress.

Samet et al. reported that As3+, V4+, Cr3+, Cu6+, and Zn2+ activate the MAP kinases in mammalian cells. The MAP kinases were also activated by Cd2+ in human T cells. Studies of growth inhibition and apoptosis in a human non-small cell lung carcinoma cell line (CL3) show that JNK and p38 co-operatively participate in apoptosis induced by Cd2+, and the decreased ERK signal induced by low Cd2+ doses contributes to growth inhibition or apoptosis. Recently, MAP kinase pathways involved in heavy metal stresses have also been demonstrated in rice by my laboratory. However, the relationship between plant MAP kinase pathways and heavy metal stress has not been well examined.
Fig. 1A, B. (A) ROS production and (B) Ca2+ accumulation in rice roots during heavy metal stress. Green fluorescence indicates the presence of ROS (A) and Ca2+ (B). Ten control and 10 treated roots showed similar results. The magnification for all images was x100.

The aim of this study was to search for MAP kinases regulated at the translational and post-translational levels during heavy metal-induced stress responses and to investigate the molecular mechanisms of signalling networks underlying heavy metal stress in the model plant, rice. In this study, the roles of second messengers, ROS and calcium, in Cd2+- and Cu2+-induced signal transduction pathways were examined (Fig. 1A, B). Using pharmacological inhibitors, it is demonstrated that Cd2+ and Cu2+ induce MAP kinase activation via distinct ROS-generating systems. The Cd2+- and Cu2+-induced MAP kinase activation required the involvement of Ca2+-dependent protein kinase (CDPK) and phosphatidylinositol 3-kinase (PI3 kinase) as shown by the inhibitory effect of a CDPK antagonist, W7, and a PI3 kinase inhibitor, wortmannin, respectively. Furthermore, bongkrekic acid (BK), a mitochondrial permeability transition pore opening blocker, suppressed Cd2+-, but not Cu2+-, induced MAP kinase activation, indicating that Cd2+-induced MAP kinase activities are dependent on the functional state of mitochondria. Collectively, these findings imply that Cd2+ and Cu2+ may induce MAP kinase activation through distinct signalling pathways (Fig. 2). Moreover, it was found that the 42 kDa MAP kinase activities are higher in Cd-tolerant cultivars (TNG67) than in Cd-sensitive cultivars (TN1) (Fig. 3). Therefore, the Cd-induced 42 kDa MAP kinase activation may confer Cd tolerance in rice plants.
Fig. 2. Schematic representation of heavy metal-induced signal transduction in rice.
Fig.3. Activation of MAP kinase in Cd2+-tolerant and Cd2+-sensitive cultivars. Rice seedlings of the Cd2+-tolerant cultivar Tainung 67 (TNG67) and Cd2+-sensitive cultivar Taichung Native 1 (TN1) were treated with different concentrations of CdCl2 for 1 h. Arrows indicate the MAP kinase-active bands.

Understanding how plants perceive and respond to metal stresses is of fundamental interest to biology. Current knowledge of the plant MAP kinase genes indicates that they are excellent markers to study the molecular basis of responses of plants towards environmental factors like metal stress, pathogens, nutrients and hormone. From a biotechnological point of view, the identification of heavy metal-induced signallings could lead to new strategies for the creation of transgenic metal-tolerant plants. We believe that accumulation of information about plant defense mechanism will facilitate engineering of genes conferring durable resistance to a broad spectrum of heavy metal stresses.
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