Elemental Profiles Reflect Plant Adaptations to the Environment

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Science  29 Jun 2012:
Vol. 336, Issue 6089, pp. 1661-1663
DOI: 10.1126/science.1219992


Most mineral elements found in plant tissues come exclusively from the soil, necessitating that plants adapt to highly variable soil compositions to survive and thrive. Profiling element concentrations in genetically diverse plant populations is providing insights into the plant-environment interactions that control elemental accumulation, as well as identifying the underlying genes. The resulting molecular understanding of plant adaptation to the environment both demonstrates how soils can shape genetic diversity and provides solutions to important agricultural challenges.

The majority of the elements that make up a plant, with the exception of carbon and oxygen, are obtained from soil through the roots. These soil-derived elements are required for plant structure, metabolism, protein function, signaling, and proper osmotic and electrochemical potential. Elemental accumulation requires the integration of processes across biological scales, including interactions with the soil matrix and biota, subcellular localization, metabolism, and gas exchange. Thus, the elemental composition of tissues [the “ionome” (1)] is a consequence of complex plant processes and plant-environment interactions.

“Soil” is not a homogeneous entity at any scale. To adapt to element availability differences, which can vary across distances as small as a few meters (see Fig. 1), plants must alter their uptake and storage of both nutrients and toxic elements. Ionomic phenotyping of genetically distinct plants can identify alleles that alter element concentrations in tissues (2). The distribution of these alleles in plant populations can be related back to the soil characteristics of each plant’s position on the landscape. This ecological genomics approach, comparing the spatial distribution of genetic polymorphisms affecting the ionome to soil composition, has begun to identify the genetic determinants of plant adaptation to the soils in which they grow (3, 4).

The concentrations of distinct elements are interdependent and covary between genetic backgrounds and environmental conditions. Elemental species and compounds that are sufficiently similar in size and charge can be bound, metabolized, and transported by some of the same proteins, chelators, and pathways. This results in the coordinated accumulation of these chemically similar elemental species when the shared membrane transport proteins or chelating metabolites are up- or down-regulated. Examples include transport of both Fe2+ and Zn2+ by an iron transporter (5), AsO43– and PO43– by phosphate transporters (6), and arsenite and silicic acid by silicic acid transporters (7). Similarly, the nonspecific chelator nicotianamine affects both iron and zinc accumulation in shoot vacuoles (8), and iron limitation increases leaf concentrations of zinc in Arabidopsis thaliana (9). Iron limitation also alters levels of molybdenum, which indicates that this covariation can include chemically dissimilar elements. Analyzing the ionome of recombinant inbred populations in several species (1013) revealed multielement covariation networks that include many nonsimilar element pairs. The connections between elements in the covariation networks differed between genotypes, species, and environments. Plant responses to element limitation can affect nonintuitive sets of elements, which indicates that we have much to learn about how element accumulation is regulated. A future goal of ionomics research is to identify the molecular causes of this variation and to use genome sequences to identify orthologous processes across species.

Fig. 1

Local soil variation can determine plant communities and performance. (Left) Soils surrounding serpentine outcrops have highly varied soil chemistries and plant species distinct from the surrounding environment inhabit them. (Right) Spatial variation in wheat plant performance due to saline soil. [Photos: (left) Nishanta Rajakaruna, (right) International Maize and Wheat Improvement Center (CIMMYT)]

Ionomic profiling of mutant populations is also identifying genes responsible for plant processes beyond membrane transport. In A. thaliana, the loss of either the Enhanced Suberin 1 gene (ESB1) or the sphingolipid biosynthetic gene TSC10A increases suberin in the endodermis in roots (14, 15). Both mutants accumulate more potassium, calcium, and iron in shoots. These multielement phenotypes were only observable by using the ionomics approach and provide genetic confirmation that the Casparian strip forms a barrier to transport for some elements, as hypothesized from histological evidence 147 years ago (16).

For traits that are responsive to the environment, extrapolating findings from a few environments or a few alleles will not be sufficient to explain the distribution of extant wild individuals or to predict the effects of changes in climate or land use. Multivariate differences in genotypes, soil types, climatic factors, and nutrients prohibit testing every combination. Alternatively, association mapping and population genetics use genetic markers and recombinant genotypes in extant populations to detect alleles of phenotypic consequence. The gene-level resolution of these approaches is an ideal complement to ionomics and other high-throughput phenotyping data. If the collection sites (wild) or preferred growth sites (domesticated) of the members of the population are known, environmental descriptors can be estimated for each accession. These environmental variables can be tested for correlation with allelic data to identify candidate genes as the molecular determinants of adaptation. For example, when 200,000 single-nucleotide polymorphisms (SNPs) were used to scan for signs of past selection in 1307 A. thaliana accessions, SNPs associated with laboratory-generated ionomic phenotypes (in 93 accessions) were overrepresented in regions that had undergone complete or nearly complete selective sweeps (4). This suggests that soil-driven selection plays a substantial role in patterns of diversity in A. thaliana and that ionomic profiling detects alleles with adaptive consequences across a wide range of environments.

The explanatory power of combining ionomics, association mapping, and environmental data is illustrated by studies of polymorphism in the Na+ transporter HKT1. In A. thaliana, HKT1 knockouts exhibit altered sodium accumulation and sensitivity to salinity stress (17). Quantitative trait loci (QTLs) for sodium accumulation mapped to HKT1, and association mapping of sodium levels identified alleles of HKT1 that modulate leaf sodium accumulation (3, 18). Colocalization of accessions with these alleles and high predicted soil sodium concentration implicate HKT1 in adaptation to sodic soils (3). The strength of this correlation is partly derived from the proximity of collection sites to the ocean, not exclusively from observed soil profiles. The resolution of current soil maps (at best ~10,000 m2) and collection location metadata are likely insufficient to support most tests of soil-mediated selection; additional joint soil and accession collections may be required to obtain growth location environmental data.

Many questions regarding plant interactions with soil are best addressed in nonmodel plant species. For example, ionomic profiling of locally adapted plant species could help explain how certain species thrive on soils with radically different chemistries, such as serpentines (low calcium/magnesium ratio; low nitrogen, phosphorus, and potassium; and high heavy metals) (19). Such extreme conditions impose selective pressures on plants that result in fitness trade-offs such that sister taxa [e.g., Lasthenia (20)] can be found growing on either side of serpentine soil borders (Fig. 1) and even restricted to ionically distinct regions within a serpentine outcrop. Ionomic study of these forms of adaptation has the potential to uncover molecular mechanisms of adaptation and speciation. Identification of the genes responsible for adaptation to the environment, the role of soil-driven selection in patterns of genetic diversity, and the consequences and constraints imposed by plant physiology is now within our reach and could yield the necessary knowledge to make agriculture resilient to abiotic stress.

Production on most agricultural land is limited by soil elemental content (21). Adapting crops to overcome this constraint through improved genetics is an essential component of the effort to improve the human condition. Deficiencies of essential nutrients such as nitrogen, phosphorus, and potassium and excesses of toxic elements such as sodium and aluminum limit production in large parts of the developed and developing world. In addition to limiting yield, poor food quality—such as deficiencies in the essential nutrients iron, zinc, and calcium or excesses of the toxic elements arsenic and cadmium—can negatively impact human health. It is predicted that human population growth, soil nutrient depletion, and salinization by irrigation of fields will increase agricultural utilization of compromised soils. Fertilizer costs, already prohibitive for most farmers, will rise as the cost of producing nitrogen fertilizer rises and known reserves of phosphorus and potassium are depleted (22). However, substantial progress has been made in both ameliorating important elemental limits to crop production and improving food safety by utilizing a molecular understanding of elemental accumulation (23, 24).

As an example of the former, analysis of wheat lines with an introgressed QTL for sodium tolerance identified an HKT1 allele that can extract Na+ from xylem sap and thereby prevent sodium translocation to the shoots (25). Although a difference in leaf sodium was evident in all environments tested, yield gains were only evident where concentrations of sodium in the soil were highest. This confirms that, in the absence of meter-scale environmental information, heritable ionomic phenotypes are more informative for the adaptation of crop genotypes to high-sodium environment than yield and other complex traits that integrate many biological processes.

The shared transport of compounds containing arsenic and chemically similar molecules containing the nutrients silicon and phosphorus underlies both a global food safety crisis and its solution. In rice, silicic acid and phosphate transporters can also move arsenite and AsO43–, respectively. Particularly in regions of Southeast Asia with high arsenic concentrations in groundwater, the promiscuity of these transporters is responsible for acute toxicity, disease, and shortened life spans because of dietary intake of arsenic via consumption of rice. Even in the United States, arsenic intake from rice increases breast cancer risk (26). Because we have a molecular understanding of arsenic uptake, breeding (27) and transgenic modification of crops with a transporter that sequesters arsenic in the root (28) have the potential to improve food safety and the health of hundreds of millions of people.

The prediction of tolerance to sodium stress by element accumulation measurements demonstrates that ionomics can accelerate crop improvement. This is complicated by the many agroecological challenges that limit yield and our insufficient understanding of the trade-offs that result from adaptation to particular soil conditions. Fortunately, the problem of local adaptation has been solved by evolution many times over. Ionomics and genetic association studies in model organisms and crops will directly identify alleles that promote element uptake or exclusion by plants. Using precise quantitative phenotyping of the ionome to characterize variation in plant-soil interactions, we are on the cusp of adding a new dimension to our understanding of why and how particular plants occupy their positions in the landscape and adapting agriculture to marginal soils.

References and Notes

  1. Acknowledgments: The authors acknowledge NSF (IOS-1126950), U.S. Department of Energy (DE-EE0003046) and USDA-ARS intramural funds.
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