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      Rice Genotype Differences in Tolerance of Zinc-Deficient Soils: Evidence for the Importance of Root-Induced Changes in the Rhizosphere

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          Abstract

          Zinc (Zn) deficiency is a major constraint to rice production and Zn is also often deficient in humans with rice-based diets. Efforts to breed more Zn-efficient rice are constrained by poor understanding of the mechanisms of tolerance to deficiency. Here we assess the contributions of root growth and root Zn uptake efficiency, and we seek to explain the results in terms of specific mechanisms. We made a field experiment in a highly Zn-deficient rice soil in the Philippines with deficiency-tolerant and -sensitive genotypes, and measured growth, Zn uptake and root development. We also measured the effect of planting density. Tolerant genotypes produced more crown roots per plant and had greater uptake rates per unit root surface area; the latter was at least as important as root number to overall tolerance. Tolerant and sensitive genotypes took up more Zn per plant at greater planting densities. The greater uptake per unit root surface area, and the planting density effect can only be explained by root-induced changes in the rhizosphere, either solubilizing Zn, or neutralizing a toxin that impedes Zn uptake (possibly HCO 3 or Fe 2+), or both. Traits for these and crown root number are potential breeding targets.

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          Most cited references 24

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          Zinc in plants.

          Zinc (Zn) is an essential component of thousands of proteins in plants, although it is toxic in excess. In this review, the dominant fluxes of Zn in the soil-root-shoot continuum are described, including Zn inputs to soils, the plant availability of soluble Zn(2+) at the root surface, and plant uptake and accumulation of Zn. Knowledge of these fluxes can inform agronomic and genetic strategies to address the widespread problem of Zn-limited crop growth. Substantial within-species genetic variation in Zn composition is being used to alleviate human dietary Zn deficiencies through biofortification. Intriguingly, a meta-analysis of data from an extensive literature survey indicates that a small proportion of the genetic variation in shoot Zn concentration can be attributed to evolutionary processes whose effects manifest above the family level. Remarkable insights into the evolutionary potential of plants to respond to elevated soil Zn have recently been made through detailed anatomical, physiological, chemical, genetic and molecular characterizations of the brassicaceous Zn hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri.
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            Zinc: the missing link in combating micronutrient malnutrition in developing countries.

            The first cases of human Zn deficiency were described in the 1960s in the Middle East. Nevertheless, it was not until 2002 that Zn deficiency was included as a major risk factor in the global burden of disease, and only in 2004 did WHO/UNICEF include Zn supplements in the treatment of acute diarrhoea. Despite this recognition Zn is still not included in the UN micronutrient priority list, an omission that will continue to hinder efforts to reduce child and maternal mortality, combat HIV/AIDS, malaria and other diseases and achieve the UN Millennium Development Goals for improved nutrition in developing countries. Reasons for this omission include a lack of awareness of the importance of Zn in human nutrition, paucity of Zn and phytate food composition values and difficulties in identifying Zn deficiency. Major factors associated with the aetiology of Zn deficiency include dietary inadequacies, disease states inducing excessive losses or impairing utilization and physiological states increasing Zn requirements. To categorize countries according to likely risk of Zn deficiency the International Zinc Nutrition Consultative Group has developed indirect indicators based on the adequacy of Zn in the national food supplies and/or prevalence of childhood growth stunting. For countries identified as at risk confirmation is required through direct measurements of dietary Zn intake and/or serum Zn in a representative sample. Finally, in at risk countries either national or targeted Zn interventions such as supplementation, fortification, dietary diversification or modification, or biofortification should be implemented, where appropriate, by incorporating them into pre-existing micronutrient intervention programmes.
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              How do plants achieve tolerance to phosphorus deficiency? Small causes with big effects.

              Genotypic differences in phosphorus (P) uptake from P-deficient soils may be due to higher root growth or higher external root efficiency (micrograms of P taken up per square centimeter of root surface area). Both factors are highly interrelated because any additional P provided by externally efficient roots will also stimulate root growth. It will be necessary to separate both factors to identify a primary mechanism to formulate hypotheses on pathways and genes causing genotypic differences in P uptake. For this purpose, a plant growth model was developed for rice (Oryza sativa) grown under highly P-deficient conditions. Model simulations showed that small changes in root growth-related parameters had big effects on P uptake. Increasing root fineness or the internal efficiency for root dry matter production (dry matter accumulated per unit P distributed to roots) by 22% was sufficient to increase P uptake by a factor of three. That same effect could be achieved by a 33% increase in external root efficiency. However, the direct effect of increasing external root efficiency accounted for little over 10% of the 3-fold increase in P uptake. The remaining 90% was due to enhanced root growth as a result of higher P uptake per unit root size. These results demonstrate that large genotypic differences in P uptake from a P-deficient soil can be caused by rather small changes in tolerance mechanisms. Such changes will be particularly difficult to detect for external efficiency because they are likely overshadowed by secondary root growth effects.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                11 January 2016
                2015
                : 6
                Affiliations
                [1] 1Crop Production and Environment Division, Japan International Research Center for Agricultural Sciences Tsukuba, Japan
                [2] 2Cranfield Soil and Agrifood Institute, School of Energy, Environment and Agrifood, Cranfield University Cranfield, UK
                [3] 3Crop and Environmental Sciences Division, International Rice Research Institute Metro Manila, Philippines
                Author notes

                Edited by: Manuel González-Guerrero, Universidad Politécnica de Madrid, Spain

                Reviewed by: Hannetz Roschzttardtz, Pontificia Universidad Católica de Chile, Chile; Soumitra Paul, Krishnagar Government College, India

                *Correspondence: Matthias Wissuwa wissuwa@ 123456affrc.go.jp

                This article was submitted to Plant Nutrition, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2015.01160
                4707259
                b5c3389c-d290-41fe-8a32-59e430f9fee8
                Copyright © 2016 Mori, Kirk, Lee, Morete, Nanda, Johnson-Beebout and Wissuwa.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 6, Tables: 3, Equations: 8, References: 31, Pages: 10, Words: 7368
                Funding
                Funded by: BBSRC 10.13039/501100000268
                Award ID: BB/J011584/1
                Funded by: Japan Society for the Promotion of Science 10.13039/501100001691
                Categories
                Plant Science
                Original Research

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