Ionomics reveals as role for dirigent proteins in lignin deposition

New research into the function of ESB1 (Enhanced Suberin 1) has revealed that this dirigent protein plays an essential role in building lignin-based Casparian strips in cell walls of endodermal cells. These discoveries recently published in PNAS start to dissect the molecular mechanisms involved in endodermal control of solute entry into plants. Further, they provide in vivo evidence for proteins in the dirigent family functioning as part of the machinery that builds extracellular lignin-based structures, opening a new avenue to determine the elusive role of this protein family in planta.

Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Guerinot ML, Salt DE. Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. Proc Natl Acad Sci U S A. 2013 Aug 27;110(35):14498-503. doi: 10.1073/pnas.1308412110. Epub 2013 Aug 12. PubMed PMID: 23940370.

Abstract: The endodermis acts as a “second skin” in plant roots by providing the cellular control necessary for the selective entry of water and solutes into the vascular system. To enable such control, Casparian
strips span the cell wall of adjacent endodermal cells to form a tight junction that blocks extracellular diffusion across the endodermis. This junction is composed of lignin that is polymerized by oxidative coupling of monolignols through the action of a NADPH oxidase and peroxidases. Casparian strip domain proteins
(CASPs) correctly position this biosynthetic machinery by forming a protein scaffold in the plasma membrane at the site where the Casparian strip forms. Here, we show that the dirigent-domain containing protein, enhanced suberin1 (ESB1), is part of thismachinery, playing an essential role in the correct formation of Casparian strips. ESB1 is localized to Casparian strips in a CASP-dependent manner, and in the absence of ESB1, disordered and defective Casparian strips are formed. In addition, loss of ESB1 disrupts the localization of the CASP1 protein at the casparian strip domain, suggesting a reciprocal requirement for both ESB1 and CASPs in forming the Casparian Strip Domain.

Ionomics sheds new light on evolution

A new paper in Science from the Salt lab describes how polyploidy enhances leaf concentration of potassium and fitness in saline soils, supporting the notion that genome duplication is important in the evolutionary history of plants.

Chao DY, Dilkes B, Luo H, Douglas A, Yakubova E, Lahner B, Salt DE. Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science. 2013 Aug 9;341(6146):658-9. doi: 10.1126/science.1240561. Epub 2013 Jul 25.
PubMed PMID: 23887874.

Abstract: Genome duplication (or polyploidization) has occurred throughout plant evolutionary history, and is thought to have driven the adaptive radiation of plants. We found that the cytotype of the root, and not the genotype, determined the majority of heritable natural variation in the concentration of leaf potassium (K) in Arabidopsis thaliana. Autopolyploidy also provided resistance to salinity and may represent an adaptive outcome of the enhanced K accumulation of plants with higher ploidy.

GWAS paper on Cd accumulation

The Salt lab recently published a paper in PLoS Genetics in which we describe the use of GWA mapping to identify HMA3 as the primary locus controlling natural variation in foliar accumulation of Cd in Arabidopsis thaliana. The paper can be read at http://www.plosgenetics.org/article/info%3Adoi%2F10.1371%2Fjournal.pgen.1002923 and the abstract can be seen below.

Abstract: Understanding the mechanism of cadmium (Cd) accumulation in plants is important to help reduce its potential toxicity to both plants and humans through dietary and environmental exposure. Here, we report on a study to uncover the genetic basis underlying natural variation in Cd accumulation in a world-wide collection of 349 wild collected Arabidopsis thaliana accessions. We identified a 4-fold variation (0.5-2 µg Cd g(-1) dry weight) in leaf Cd accumulation when these accessions were grown in a controlled common garden. By combining genome-wide association mapping, linkage mapping in an experimental F2 population, and transgenic complementation, we reveal that HMA3 is the sole major locus responsible for the variation in leaf Cd accumulation we observe in this diverse population of A. thaliana accessions. Analysis of the predicted amino acid sequence of HMA3 from 149 A. thaliana accessions reveals the existence of 10 major natural protein haplotypes. Association of these haplotypes with leaf Cd accumulation and genetics complementation experiments indicate that 5 of these haplotypes are active and 5 are inactive, and that elevated leaf Cd accumulation is associated with the reduced function of HMA3 caused by a nonsense mutation and polymorphisms that change two specific amino acids.

New Perspective in Science

Brian Dilkes and I have a perspective in the new issue of Science titled "Elemental Profiles Reflect Plant Adaptations to the Environment". The abstract is below. Science puts a very (and I mean VERY) tight word limit on the manuscript and so one of the things that we needed to cut was the acknowledgements. So we would like to take the time here to give huge thanks to all the great people who took the time to read drafts and give us (lots of) feedback. 

Jim Fleet,David Salt, Kirsten Bomblies, Elizabeth Haswell, Elizabeth Buescher, Nancy Emery, Clint Chapple, Jody Banks, Joanna Dinsmore, Luca Comai, Aimee Terauchi, Greg Ziegler and five anonymous reviewers for comments on the perspective. 

Pamela Hines, our editor at Science, contributed lots of wisdom, insight and most of all patience, for which we are ever grateful. 

THANKS!

Ivan

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.                      

 

New Paper in PLoS ONE

Our most recent paper was just published in PLoS ONE. "Biodiversity of Mineral Nutrient and Trace Element Accumulation in Arabidopsis thaliana" is our first installment of all the association panel data that we have generated.  It looks at the corrections between elements within and between tissues in the initial 96 accession 'Nordborg' panel.  It includes some very nice data on hydroponics grown plants from samples generated by Christian Hermans and Nathalie Verbruggen from Université Libre de Bruxelles in Belgium.  Special thanks are due to Jennie Hard for all the help with figure preparation. There will be several more papers analyzing this and similar data submitted in the (hopefully) near future.  

 

Here is the abstract:

In order to grow on soils that vary widely in chemical composition, plants have evolved mechanisms for regulating the elemental composition of their tissues to balance the mineral nutrient and trace element bioavailability in the soil with the requirements of the plant for growth and development. The biodiversity that exists within a species can be utilized to investigate how regulatory mechanisms of individual elements interact and to identify genes important for these processes. We analyzed the elemental composition (ionome) of a set of 96 wild accessions of the genetic model plant Arabidopsis thaliana grown in hydroponic culture and soil using inductively coupled plasma mass spectrometry (ICP-MS). The concentrations of 17–19 elements were analyzed in roots and leaves from plants grown hydroponically, and leaves and seeds from plants grown in artificial soil. Significant genetic effects were detected for almost every element analyzed. We observed very few correlations between the elemental composition of the leaves and either the roots or seeds. There were many pairs of elements that were significantly correlated with each other within a tissue, but almost none of these pairs were consistently correlated across tissues and growth conditions, a phenomenon observed in several previous studies. These results suggest that the ionome of a plant tissue is variable, yet tightly controlled by genes and gene×environment interactions. The dataset provides a valuable resource for mapping studies to identify genes regulating elemental accumulation. All of the ionomic data is available at www.ionomicshub.org.

 

and here is the non-technical summary:

Understanding how plants regulate element composition of tissues is critical for agriculture, the environment, and human health. Sustainably meeting the increasing food and biofuel demands of the planet will require growing crops with fewer inputs such as the primary macronutrients phosphorus (P) and potassium (K). Ionomics is the study of elemental accumulation in living systems using high-throughput elemental profiling. With this technique, we can rapidly generate large quantities of data on thousands of samples, allowing for the profiling of large genetic mapping populations and the discovery of hundreds of loci important for elemental accumulation. We have used this approach to sample the natural diversity present in collections of a model plant, the wild mustard Arabidopsis. We find that the elemental composition of a plant is tightly controlled by its genes. We also find that elements will have different relationships between them depending on the environment and the tissues (root, seed or leaf) under study. This suggests that crop varieties developed for improved elemental uptake and accumulation will be highly environment specific.

First iHUB workshop

The first NSF sponsored iHUB workshop held 26 & 27 April, 2012 in St Louis, US was a success. New tools and features discussed at the workshop should be appearing on the iHUB soon.

Aberdeen Ionomics Facility running

The ICP-MS instruments in David Salt's Ionomics Facility at the University of Aberdeen are now up and running.