Plant Metallomics

David E. Salt

Professor David E. Salt's research interest is to understand the function of the genes and gene networks that regulate the plant ionome (elemental composition), along with the evolutionary forces that shape this regulation. To achieve this he couples high-throughput elemental profiling with bioinformatics, genomics and genetics, biochemistry, physiology and field work. Professor Salt has held faculty positions at Rutgers University (1993–1997), Northern Arizona University (1998–2001), and Purdue University (2001–2011), and currently holds a Sixth Century Chair at the University of Aberdeen, where he has been since 2011. Professor Salt has published over 115 papers since 1989 with over 7800 citations.

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Since their birth in the early 2000's the ionome¹ and the metallome^2,3 have evolved independently, with ionomics becoming associated with the plant functional genomics community whereas metallomics is used more by the bioinorganic chemistry community. In essence, both terms speak to the same biological concept, that the inorganic constituents of an organism (all the essential mineral nutrients and trace elements) represent the ‘fourth pillar’ of functional genomics, taking its place with the transcriptome, the proteome and the metabolome as part of the machinery that translates the information encoded in the genome into a living system. Such a view highlights the need to remain aware that a systems-level understanding of cellular and organismal biology will require systems-level approaches to understand how each of these critical ‘omes’ is regulated, and further, how they interact with the genome and the environment. New insights in biology are generally preceded by new developments in analytical chemistry. For example, advances in DNA sequencing, array technologies, microscopy and mass spectrometry are leading to major new insights in biology, including in the ‘fourth pillar’ of functional genomics described variously as the ionome or the metallome. Over the last decade the plant research community has embraced the concept of applying new genomics approaches to the study of mineral nutrient and trace element homeostasis, and the themed issue of Plant Metallomics aims to reflect this growing body of new work. The themed issue contains eight reviews and 12 research papers from authors in 16 different countries, providing a good cross section of work on genes, small metabolites, and proteins involved in the mineral nutrient and trace element homeostasis in plants. Papers are also included that highlight some of the analytical techniques used to make such discoveries.

The research paper by Gayomba et al. (DOI: 10.1039/c3mt00111c) provides a nice example of the importance of investigating the cross-talk between micronutrients and trace elements. In this paper the molecular mechanisms of the interactions between cadmium (Cd) and copper (Cu) are probed, revealing an elegant molecular network between Cd resistance, and Cu sensing and uptake. Andrés-Colás et al. (DOI: 10.1039/c3mt00025g) also investigate Cu homeostasis, but rather than focusing on specific genes they take a systems-level view of the response of the transcriptome to Cu deficiency and slight excess. By applying bioinformatic tools, genes and gene networks involved in Cu homeostasis are revealed. By focusing on mineral nutrient and trace element regulation in specific tissues (seeds or nitrogen fixing nodules) Eggert and von Wirén (DOI: 10.1039/c3mt00109a), Rodrígues-Haas et al. (DOI: 10.1039/c3mt00060e) and Wu et al. (DOI: 10.1039/c3mt00071k) are able to provide an integrated view of how mineral nutrients and trace elements are distributed in relation to the function and development of the organ. These three studies also highlight the use of different analytical approaches to address similar questions, demonstrating the capabilities of ICP-MS, ICP-MS coupled to laser ablation and synchrotron-based X-ray fluorescence. At the opposite end of the size scale, Peroza et al. (DOI: 10.1039/c3mt00079f) focus on the metal-binding properties of the thiol rich metallothionein family of proteins. Clearly, the mineral nutrient and trace elements in plants must interact with the metabolome, and these interactions are nicely explored by Anan et al. (DOI: 10.1039/c3mt00108c), Gómez Ojeda et al. (DOI: 10.1039/c3mt00058c), Grevenstuk et al. (DOI: 10.1039/c3mt00101f) and Ouerdane et al. (DOI: 10.1039/c3mt00113j). These papers highlight the distinction and different analytical tools required to study metabolites that contain trace elements such as selenium (Se) and tellurium (Te) as part of their covalent molecular structure, and trace elements such as aluminium (Al) which are coordinated by small metabolites such as citrate. Mineral nutrient and trace element homeostasis also plays a critical role in the interaction of organisms at an ecological scale, and this is nicely highlighted by the study of Ruytinx et al. (DOI: 10.1039/c3mt00061c) looking at the regulation of zinc (Zn) transport in the plant associated fungus Suillus bovines. At high levels in the soil, trace elements such as mercury (Hg) can be toxic to plants, and the paper of Lopes et al. (DOI: 10.1039/c3mt00084b) details the plants' genome-wide transcriptional and physiological responses to this toxicity.

In this Plant Metallomics themed issue, reviews are also presented that provide a broader overview of the topics and techniques highlighted in the research papers. The toxicity of heavy metals to plants is reviewed by Dal Corso et al. (DOI: 10.1039/c3mt00038a), and this work is complemented by that of Yang and Chen (DOI: 10.1039/c3mt00022b) in which the roles of microRNAs in these toxicity responses are reviewed. In contrast, reviews by Hermans et al. (DOI: 10.1039/c3mt20223b), Assunção et al. (DOI: 10.1039/c3mt00070b) and Tejada-Jiménez et al. (DOI: 10.1039/c3mt00078h) focus on homeostasis and metabolism of the essential mineral nutrients magnesium (Mg), zinc (Zn) and molybdenum (Mo). Reviews by Yruela (DOI: 10.1039/c3mt00086a) and Leszczyszyn et al. (DOI: 10.1039/c3mt00072a) contract the diversity of metals and metal-binding proteins in the complex biological process of photosynthesis with a single family of metallothionein proteins. As a capstone, Punshon et al. (DOI: 10.1039/c3mt00120b) provide a nice review of the use of synchrotron X-ray fluorescence (SXRF) imaging, which uses the electronic structure of atoms to allow their localization at the cellular resolution with very limited sample preparation, providing a new window to describe and understand the processes that control the mineral nutrient and trace element composition of an organism.

References

1. D. E. Salt, I. Baxter and B. Lahner, Ionomics and the study of the plant ionome, Annu. Rev. Plant Biol., 2008, 59, 709–733.
2. R. J. P. Williams, Chemical selection of elements by cells, Coord. Chem. Rev., 2001, 216–217, 583–595.
3. C. E. Outten and T. V. O'Halloran, Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis, Science, 2001, 292, 2488–2492.

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