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Title: Xylem exudate composition and root-to-shoot nickel translocation in Alyssum species

Author
item CENTOFANTI, T - University Of Maryland
item SAYERS, Z - Sabanci University
item CABELLO-CONEJO, M - Consejo Superior De Investigaciones Cientificas (CSIC)
item KIDD, P - Consejo Superior De Investigaciones Cientificas (CSIC)
item NISHIZAWA, N - University Of Tokyo
item KAKEI, Y - University Of Tokyo
item DAVIS, A - University Of Maryland
item Sicher Jr, Richard
item Chaney, Rufus

Submitted to: Plant and Soil
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/15/2013
Publication Date: 6/4/2013
Citation: Centofanti, T., Sayers, Z., Cabello-Conejo, M.I., Kidd, P., Nishizawa, N.K., Kakei, Y., Davis, A.P., Sicher, Jr., R.C., Chaney, R.L. 2013. Xylem exudate composition and root-to-shoot nickel translocation in Alyssum species. Plant and Soil. DOI 10:1007/s11104-013-1782-1.

Interpretive Summary: Improved understanding of the physiology of nickel hyperaccumulator plants is expected to improve the development of phytoextraction/phytomining technology for nickel. The chemicals involved in nickel translocation remains one of the unsettled questions about how Alyssum species achieve such extreme nickel accumulation in their shoots which is required for commercial phytoextraction of nickel. Early studies suggested nickel was chelated to malate, a common organic acid in plants. But the weak chelation of nickel by malate indicated that citrate was more likely chelating xylem nickel. Subsequently, a report indicated that histidine was greatly increased in xylem exudate of Alyssum hyperaccumulating nickel. But additional studies suggested that this outcome may have been an artifact of the experimental method. To clarify nickel translocation chemistry in Alyssum, we grew several hyperaccumulator and non-accumulator species in nutrient solutions with varied nickel levels, or in naturally Ni rich serpentine soils, and used modern methods of analysis of trace levels of organic compounds suspected to be involved. Further, we grew the plants for months with the high nickel solutions or soils to attain a steady-state in nickel translocation. Xylem exudate from these plants commonly contained 3000 micromolar nickel, but only less than 100-300 micromolar citrate, malate or histidine. Another suspected nickel chelator, nicotianamine, was also not high enough to chelate much of the exudate nickel. We conclude that most of the nickel in stem exudate of nickel hyperaccumulating Alyssum species is the free cation rather than chelated forms.

Technical Abstract: An improved understanding of Ni root-to-shoot translocation mechanism in hyperaccumulators is necessary to increase Ni uptake efficiency for phytoextraction technologies. It is presumed that an important aspect of Ni translocation and storage involves chelation with organic ligands. It has been reported that exposing several Ni hyperaccumulator species of Alyssum to Ni elicited a large increase in the histidine level of the xylem sap. However, only 19% of Ni present in the xylem sap was chelated with histidine. In later studies it was shown that as time progressed the histidine: Ni:histidine ratio dropped considerably. Moreover, previous studies analyzed the relationship between Ni and ligands in plants that were exposed to Ni only for a few hours and therefore obtained results that are unlikely to represent field soils where plants are at steady-state Ni uptake. The aim of this study was to understand the relationship between Ni and organic ligands in the xylem sap of various Alyssum genotypes or species that reached steady-state Ni uptake after being exposed to Ni in either hydroponic solution or serpentine soil for up to 6 weeks. Total Ni concentration, 17 amino acids, 9 organic acids, and nicotianamine were measured in xylem sap of 100-day old plants of Alyssum. Results showed that the concentration of Ni in xylem sap of various Alyssum genotypes was 10-1000 fold higher than the concentration of histidine, malate, citrate, and nicotianamine, which were the predominant ligands measured in the sap. When the physiology of the whole plant is taken into account, our results indicate that the concentration of organic chelators is too low to account for the complexation of all the Ni present in the xylem sap of Alyssum, and suggest that most of the Ni in xylem sap of this species is likely present as a hydrated cation.