Worldwide Genetic Diversity for Mineral Element Concentrations in Rice Grain
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Published December 5, 2014 RESEARCH Worldwide Genetic Diversity for Mineral Element Concentrations in Rice Grain Shannon R. M Pinson,* Lee Tarpley, Wengui Yan, Kathleen Yeater, Brett Lahner, Elena Yakubova, Xin-Yuan Huang, Min Zhang, Mary Lou Guerinot, and David E. Salt S.R.M. Pinson, USDA–ARS Rice Research Unit, 1509 Aggie Drive, ABSTRACT Beaumont, TX 77713; S.R.M. Pinson, present address, USDA–ARS With the aim of identifying rice (Oryza spp.) germ- Dale Bumpers National Rice Research Center, 2890 Highway 130 plasm having enhanced grain nutritional value, East, Stuttgart, AR 72160; L. Tarpley, Texas A&M Univ. System, Texas the mineral nutrient and trace element concen- A&M AgriLife Research, 1509 Aggie Dr., Beaumont, TX 77713; W. trations (or ionome) of whole (unmilled) grains Yan, USDA–ARS Dale Bumpers National Rice Research Center, 2890 from a set of 1763 rice accessions of diverse geo- Highway 130 East, Stuttgart, AR 72160; K. Yeater, USDA–ARS–SPA, graphic and genetic origin were evaluated. Seed 1001 Holleman Drive East, College Station, TX 77840; K. Yeater, cur- for analysis of P, Mg, K, S, Ca, As, Cd, Co, Cu, rent address, USDA-ARS-PA, 2150 Centre Ave., Building D, Suite 300, Fe, Mn, Mo, Ni, Rb, Sr, and Zn concentrations by Fort Collins, CO 80526; B. Lahner, Purdue Univ., Dep. of Horticulture inductively coupled plasma mass spectrometry and Landscape Architecture, 625 Agriculture Mall Dr., West Lafayette, was produced over 2 yr in Beaumont, TX, under IN 47907; E. Yakubova, Purdue Univ., Dep. of Horticulture and Land- both flooded and unflooded watering regimes. scape Architecture, West Lafayette, IN 47907; X.-Y. Huang and D.E. The distributions of all element concentrations Salt, Univ. of Aberdeen, Institute of Biological and Environmental Sci- analyzed were skewed toward higher concentra- ences, Cruickshank Building, St. Machar Drive, Aberdeen, AB24 3UU, tion. A significant portion of this ionomic varia- UK; M. Zhang, Purdue Univ., Dep. of Statistics, 150 N. Univ. Street, tion has a genetic basis (broad sense heritabili- West Lafayette, IN 47907; M.L. Guerinot, Dartmouth College, Dep. of ties 0.14–0.75), indicating an ability to breed for Biological Sciences, Hanover, NH 03755. Mention of a trademark or improved grain concentration of all elements proprietary product does not constitute a guarantee or warranty of the except possibly Ni. Variation in grain elemental product by the U.S. Department of Agriculture or Texas A&M AgriLife concentrations was not strongly associated with Research and does not imply its approval to the exclusion of other prod- plant height, heading time, or grain shape, sug- ucts that also can be suitable. USDA is an equal opportunity provider gesting these physiological factors are not of and employer. All experiments complied with the current laws of the primary importance in controlling ionomic varia- United States or the country in which they were performed. Received 1 tion in rice grain. Accessions high in specific Oct. 2013. *Corresponding author ([email protected]). elements were sometimes found to have similar Abbreviations: ARO, aromatic subgroup; AUS, aus subgroup; DHD, genetic or geographic origins, suggesting they days from planting to heading (also known as flowering); GL, grain share a heritable mechanism underlying their length; GW, grain width; H2, broad sense heritability; ICP–MS, induc- enhanced ionomes. For example, accessions tively coupled plasma mass spectrometry; IND, indica subgroup; LS with high Ca, Mg, or K were more common in Mean, least squares mean; PCA, principal component analysis; QTL, the indica than in the japonica subgroup; low As quantitative trait locus (QTLs, quantitative trait loci); TEJ, temperate was most common among temperate japonica japonica subgroup; TRJ, tropical japonica subgroup. accessions; and several lines high in Mo origi- nated in Malaysia or adjacent Brunei. Published in Crop Sci. 55:1–18 (2015). doi: 10.2135/cropsci2013.10.0656 Freely available online through the author-supported open-access option. © Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher. CROP SCIENCE, VOL. 55, JANUARY–FEBRUARY 2015 WWW.CROPS.ORG 1 ith about half the world’s human population White and Veneklaas, 2012), though the association may Wdependent on rice (Oryza spp.) as a staple food, the not be obligatory (Rose et al., 2013a). The first step toward grain provides the majority of dietary nutrients to bil- breeding rice cultivars with an enhanced elemental com- lions of people. Unfortunately, rice grains are not dense in position (or ionome) is to understand the genetic diversity mineral nutrients, making nutrient deficiencies common in germplasm collections available to breeders. among those dependent on rice as a dietary staple (Grusak Rice is grown under a wide range of environmen- and Della Penna, 1999). In addition to dietary supplemen- tal conditions around the world. It is produced below sea tation and industrial food fortification, biofortification level as well as in mountainside terraces as much as 1800 m via the development of new crop cultivars with increased above sea level, in tropical equatorial countries as well in concentration of nutrients in their edible portions has been the more temperate areas of Eastern and Western Europe. proposed as a possible solution to alleviate global malnu- Although rice is most commonly produced under a shal- trition (e.g., Graham et al., 1999, 2001; Gregorio et al., low flood (8 to 20 cm water) in the United States, on 2000; White and Broadley, 2005; Bouis and Welch, 2010; a global view it is also commonly grown under upland Masuda et al., 2013; Rawat et al., 2013; Murgia et al., (aerated rainfed) conditions and even under deep-water 2013). In fact, studies have documented improved health flood (more than 50 cm) in tropical areas that experience indicators from human consumption of crops biofortified a monsoon season. Grassi et al. (2009) showed that a cul- for iron and β-carotene (Haas et al., 2005; van Jaarsveld tivar developed for upland production yielded more when et al., 2005; Low et al., 2007; Cercamondi et al., 2013). grown flooded, indicating that an aerobic or unflooded While most white (milled) rice in U.S. grocery stores is production system limits rice yields even in the absence of fortified by adding nutrients to the external surface of the water stress or drought. It has been shown that the con- milled rice grains (Flour Fortification Initiative, 2012), centrations of various elements in rice grain are so affected enhancement of the rice grain’s nutritional value through by the soil and other aspects of the environment under genetic improvements could include both increasing con- which a rice grain is produced that grain ionome profiles centrations of desirable elements (e.g., Fe, Zn, or Ca) and can be used to distinguish among rices produced in differ- decreasing concentrations of undesirable elements (e.g., ent countries and geographical regions of the world (Kelly As or Cd) and could create new marketing strategies for et al., 2002; Gonzálvez et al., 2011; Li et al., 2012). This nutritionally enhanced, value-added products. If the bio- suggests that rice cultivars adapted to geographic regions fortification is accomplished through traditional breeding where a particular element is especially lacking, or pres- and selection, rather than through genetic engineering, ent in excess, may express genes for enhanced ability to then the nutritionally enhanced crops would not require mine those elements out of the soil and/or partition them special regulation or documentation and could thus be to other organs once taken up by the plant’s roots or com- deployed more rapidly. Cultivars biofortified through partmentalized in leaves. While Zn deficiency is wide- traditional breeding methods would be able to acquire spread throughout the rice-growing regions of the world, organic certification if grown under organic field con- deficiencies and toxicities of other elements (e.g., As, Ca, ditions, and use of alleles conferring intermediate rather Fe, K, and Mo) are more specific to certain soil types or than extreme phenotypes found naturally functional irrigation conditions. It is likely that landraces and culti- among diverse rice accessions could be used to fine-tune vars adapted to these particular geographic regions may grain element concentrations. contain enhanced ability to absorb, exclude, or detoxify The most prevalent nutrient deficiencies worldwide specific elements. One goal of the present study was to are Fe and Zn, with estimates that more than 25% of the compare the grain ionome of 1763 diverse rice accessions world’s population are at risk of mild to severe deficiency to determine if rice accessions adapted to a particular in one or both elements and with each element attributable region of the world or if those from a particular ances- for the deaths of 0.8 million persons per year (World Health tral lineage were more likely to produce rice grains with Organization [WHO], 2002, 2009; Maret and Sandstead, reduced or elevated concentrations of one or more of the 2006). Because of significant interest in biofortifying 16 elements (P, Mg, K, S, Ca, As, Cd, Co, Cu, Fe, Mn, grains for Fe and Zn, numerous studies have focused on Mo, Ni, Rb, Sr, Zn) we analyzed. the routes and mechanisms governing accumulation of Fe A second goal of the study was to evaluate correlations and Zn in crop grains (for reviews, see Stangoulis, 2010; between the elements and plant traits, as these can impli- Masuda et al., 2013).