Impact of toxic metals on agriculture and crop yields

Study evaluated effects of aluminum and cadmium on tomato plants and used grafting to investigate how one part of a plant signals stress caused by heavy metals to the other.

By José Tadeu Arantes  |  Agência FAPESP – Contamination of soil and water with toxic metals is a major problem for agriculture. It is harmful to farmers because it impairs crop yields, and it is a health hazard for consumers.

The various facets of this problem were studied in depth by the Thematic Project “Oxidative stress induced by metals: new approaches”, developed over a five-year period from 2010 to 2015 with support from FAPESP.

“The metals we studied most were aluminum and cadmium, and the crop we focused on was tomatoes,” said Ricardo Antunes de Azevedo, Full Professor at the University of São Paulo’s Luiz de Queiroz College of Agriculture (ESALQ-USP) in Brazil and principal investigator for the project.

“Unlike zinc, nickel and other metals, aluminum and cadmium aren’t used by living beings as nutrients,” Azevedo told Agência FAPESP. “However, their toxicity damages plants in several ways. For example, they inhibit radicular development and the absorption of water and nutrients by roots. The consequences may range from a reduction in crop yield to plant death.”

Soil naturally contains large amounts of aluminum, which in fact is the most abundant element in the Earth’s crust. Because hydrolysis of aluminum produces hydrogen ions, the abundance of this metal is one of the main causes of soil acidification. “In soils with neutral pH, aluminum is generally inoffensive, but in acidic soils it can have a very negative effect on plant development,” Azevedo said.

Cadmium naturally occurs in far smaller amounts. Its presence in soil is due mainly to environmental pollution caused by anthropogenic factors such as cadmium mining and the manufacturing and disposal of nickel-cadmium batteries and cadmium-based pigments.

“The biggest problem with cadmium is that it’s easily absorbed by plants and accumulates in their metabolism even when it’s only present in small concentrations in the soil or water used for irrigation,” Azevedo said. “And this toxic metal may affect the consumer's organs if the plant is used by animals or humans.”

An aspect of the problem that is often overlooked, he added, is that cadmium contamination can occur even when a plant containing it is not directly ingested. Tobacco is an example. The leaves of the tobacco plant accumulate cadmium, which may be taken in by the smoker’s respiratory system as the leaves burn. Research has shown that cadmium concentrations tend to be higher in smokers than non-smokers.

Crop yields

In addition to potential harm to consumers, cadmium can also impair crop yields, owing mainly to plant stress. “Plants suffer two kinds of stress: abiotic stress caused by metals, lack of water and excessive temperature and biotic stress due to pathogens. The metabolism of normal cells produces reactive oxygen species (ROS), but there’s a self-regulation mechanism that keeps ROS below a critical level. In situations of stress, an imbalance occurs, and the production of ROS reaches much higher levels, potentially causing plant death,” Azevedo explained.

The research addressed the question from various angles. A particularly interesting study involved the technique of grafting. “This technique is ancient and highly disseminated in agriculture,” Azevedo said. “We used grafting to understand how part of a plant contaminated by cadmium sends signals to an uncontaminated part that it’s under stress.“

In grafting, a shoot or bud of one plant, called the scion, is inserted into or joined to the stem, branch or root of another plant, called the rootstock, so that the two grow together as a single plant.

The procedure used in the experiment consisted of cultivating plants with and without the presence of cadmium and then performing reciprocal grafting.

“In other words, we swapped the plants’ upper parts, joining an uncontaminated scion to a contaminated rootstock and joining a contaminated scion to an uncontaminated rootstock. It’s a simple idea, but in practice it required a large number of controls because the grafting process itself puts the plant under stress, albeit temporarily,” Azevedo said.

The findings are described in the article “Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants” published by the journal Biometals.

The conclusion was that two-way stress signaling occurred: not only was metal in the roots transported to the aerial part (scion), as expected, albeit in varying amounts, but metal in the scion was also transported to the roots – not an intuitive result.

Genotoxicity was another important issue the researchers investigated. They wanted to observe the effects of cadmium on the structures of nucleic acids in the plant, i.e., whether the toxic metal bonded with the plant’s DNA and if so what happened as a result.

“We found that cadmium did indeed have adverse genetic effects,” Azevedo said. “It altered the cell division rate quite significantly and caused a series of chromosomal aberrations. These included chromosomal breaks and bridges during mitosis, the process of cell division. This occurred even with very low concentrations of cadmium. They don’t cause visible manifestations of plant stress, but there are major intracellular alterations.”

The effects of cadmium contamination depend on a number of variables. One of these is the type of plant variety exposed to the metal. Some varieties are more tolerant than others. Several mechanisms are involved, and these may modify the rate at which the plant absorbs cadmium or reduce its effects once absorbed. For this reason, the project also included mutagenesis and the selection of more tolerant mutants.

When farmers understand these mechanisms, they can leverage them in breeding programs to obtain more resistant varieties. For consumers, however, a more resistant plant may mean absorbing even more of the toxic metal.

“For completely safe consumption, you’d have to know whether the soil and water used in growing the crop were contaminated, and if so which part of the plant accumulated the metal. It could be the part that’s consumed or parts that are thrown away. A great many factors are involved, so it’s a highly complex type of study,” Azevedo said.

Another line of research in the Thematic Project therefore entailed studying phytoremediation, the rehabilitation of contaminated soil by planting highly resistant varieties capable of absorbing heavy metals and hence removing them from the natural environment. Plants such as hyacinth bean (Dolichos lablab) can absorb large amounts of cadmium without becoming stunted and can be used as phytostabilizers.

An article about the study (“Physiological and biochemical responses of Dolichos lablab L. to cadmium support its potential as a cadmium phytoremediator”) has been submitted for publication in the Journal of Soils and Sediments and is currently in press.

The Thematic Project has so far led to the publication of more than 50 articles in scientific journals, and several others are currently being written up. The experiments were performed in greenhouses or using soil-grown or hydroponic plants. The tomato was chosen for several reasons. It is a model plant species for genetic studies, with a large number of varieties and mutants. Moreover, the world’s smallest tomato, the Micro-Tom, is a small plant with small fruit and has a very short lifecycle that lasts approximately 90 days, making it ideal for experiments. Finally, tomatoes are economically important and widely consumed all over the world, both fresh and in processed form.