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

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.

Broomrape Species Parasitizing Odontarrhena lesbiaca (Brassicaceae) Individuals Act as Nickel Hyperaccumulators

The elemental defense hypothesis supports that metal hyperaccumulation in plant tissues serves as a mechanism underpinning plant resistance to herbivores and pathogens. In this study, we investigate the interaction between Odontarrhena lesbiaca and broomrape parasitic species, in the light of the defense hypothesis of metal hyperaccumulation. Plant and soil samples collected from three serpentine sites in Lesbos, Greece were analyzed for Ni concentrations. Phelipanche nowackiana and Phelipanche nana were found to infect O. lesbiaca. In both species, Ni concentration decreased gradually from tubercles to shoots and flowers. Specimens of both species with shoot nickel concentrations above 1000 mg.kg−1 were found, showing that they act as nickel hyperaccumulators. Low values of parasite to O. lesbiaca leaf or soil nickel quotients were observed. Orobanche pubescens growing on a serpentine habitat but not in association with O. lesbiaca had very low Ni concentrations in its tissues analogous to excluder plants growing on serpentine soils. Infected O. lesbiaca individuals showed lower leaf nickel concentrations relative to the non-infected ones. Elevated leaf nickel concentration of O. lesbiaca individuals did not prevent parasitic plants to attack them and to hyperaccumulate metals to their tissues, contrary to predictions of the elemental defense hypothesis.

Incidence of hyperaccumulation and tissue-level distribution of manganese, cobalt, and zinc in the genusGossia(Myrtaceae)

The rare phenomenon of plant manganese (Mn) hyperaccumulation within the Australian flora has previously been detected in the field, which suggested that the tree genus Gossia (Myrtaceae) might contain new Mn hyperaccumulators. We conducted the first growth experiment on Gossia using a multi-factorial dosing trial to assess Mn, cobalt (Co), and zinc (Zn) (hyper)accumulation patterns in selected Gossia species (G. fragrantissima and G. punctata) after a systematic assessment of elemental profiles on all holdings of the genus Gossia at the Queensland Herbarium using handheld X-ray fluorescence spectroscopy. We then conducted detailed in situ analyses of the elemental distribution of Mn, Co, Zn and other elements at the macro (organ) and micro (cellular) levels with laboratory- and synchrotron-based X-ray fluorescence microscopy (XFM). Gossia pubiflora and Gossia hillii were newly discovered to be Mn hyperaccumulator plants. In the dosing trial, G. fragrantissima accumulated 17 400 µg g−1 Mn, 545 µg g−1 Co, and 13 000 µg g−1 Zn, without signs of toxicity. The laboratory-based XFM revealed distinct patterns of accumulation of Co, Mn, and Zn in G. fragrantissima, while the synchrotron XFM showed their localization in foliar epidermal cells, and in the cortex and phloem cells of roots. This study combined novel analytical approaches with controlled experimentation to examine metal hyperaccumulation in slow-growing tropical woody species, thereby enabling insight into the phenomenon not possible through field studies.

Visualizing Hotspots and Future Trends in Phytomining Research Through Scientometrics

Phytomining has attracted widespread attention as a technique for harvesting “bio-ore.” This technology has potential applications in the metal and minerals industry for low-grade metal and mineral mining as well as metal recycling from polluted soil. The hotspots and future trends of this technology deserve in-depth exploration. This paper presents a systematic review of the phytomining research area through the scientometrics method based on the citation data collected from the Web of Science Core Collection (WoSCC). The results show that the earliest phytomining-related research was published in 1997. Between 1997 and 2019, 232 publications were published in 109 journals. Plant and Soil, the International Journal of Phytoremediation, and the Journal of Geochemical Exploration were the top three most prolific journals and accounted for 18.1% of these publications. Guillaume Echevarria, J.L. Morel, and Antony Van der Ent were the top three most prolific authors, and their work accounted for 40.1% of these publications. The cluster results of document co-citation analysis revealed that the hotspots in phytomining research area mainly includes “nickel accumulation,” “heavy metal uptake,” “mining site,” “heavy metal,” “hyperaccumulation yield,” “growth effect,” and “alternative method.” Keyword burst detection results find that the hot topics have changed over time from “phytomining” to “agromining”; from “contaminated soil” to “serpentine soil”; and from “mechanism” to “phytomining process” and “commercial phytoextraction.” This study describes the intellectual landscape of research and provides future research directions for phytomining research so that researchers can identify future research topics and partners.