A Test of the Inadvertent Uptake Hypothesis Using Plant Species Adapted to Serpentine Soil

Abstract

Serpentine soils are a stressful growing environment for plants, largely due to nutrient deficiencies and high concentrations of toxic heavy metals (e.g., Ni). Plants have evolved various adaptations for tolerating these extreme environments, including metal hyperaccumulation into above-ground tissues. However, the adaptive significance of metal hyperaccumulation is a topic of debate, with several non-mutually-exclusive hypotheses under study. For example, the inadvertent uptake hypothesis (IUH) states that heavy metal accumulation is a consequence of an efficient nutrient-scavenging mechanism for plants growing in nutrient-deficient soils. Thus, it is possible that metal hyperaccumulation is simply a byproduct of non-specific ion transport mechanisms allowing plants to grow in nutrient-deficient soils, such as serpentine soils, while simultaneously tolerating other potentially toxic heavy metals. Furthermore, some nutrient needs are tissue-specific, and heavy metal toxicity can be more pronounced in reproductive tissues; thus, studies are needed that document nutrient and metal uptake into vegetative and reproductive plant tissues across species of plants that vary in the degree to which they accumulate soil metals. To test these ideas, we grew nine plant species that are variously adapted to serpentine soils (i.e., Ni-hyperaccumulating endemic, non-hyperaccumulating endemic, indicator, or indifferent) in a common garden greenhouse experiment. All species were grown in control soils, as well as those that were amended with the heavy metal Ni, and then analyzed for macronutrient (Ca, Mg, K, and P), micronutrient (Cu, Fe, Zn, Mn, and Mo), and heavy metal (Cr and Co) concentrations in their vegetative and reproductive organs (leaves, anthers, and pistils). In accordance with the IUH, we found that hyperaccumulators often accumulated higher concentrations of nutrients and metals compared to non-hyperaccumulating species, although these differences were often organ-specific. Specifically, while hyperaccumulators accumulated significantly more K and Co across all organs, Cu was higher in leaves only, while Mn and Zn were higher in anthers only. Furthermore, hyperaccumulators accumulated significantly more Co and Mo across all organs when Ni was added to the soil environment. Our work provides additional evidence in support of the IUH, and contributes to our understanding of serpentine adaptation in plants.