(Advances in agronomy 115) donald l sparks (eds ) advances in agronomy 115 academic press, elsevier (2012)

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ADVANCES IN AGRONOMY Advisory Board PAUL M BERTSCH RONALD L PHILLIPS University of Kentucky University of Minnesota KATE M SCOW LARRY P WILDING University of California, Davis Texas A&M University Emeritus Advisory Board Members JOHN S BOYER KENNETH J FREY University of Delaware Iowa State University EUGENE J KAMPRATH MARTIN ALEXANDER North Carolina State University Cornell University Prepared in cooperation with the American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America Book and Multimedia Publishing Committee DAVID D BALTENSPERGER, CHAIR LISA K AL-AMOODI CRAIG A ROBERTS WARREN A DICK MARY C SAVIN HARI B KRISHNAN APRIL L ULERY SALLY D LOGSDON Academic Press is an imprint of Elsevier 525 B Street, Suite 1900, San Diego, CA 92101-4495, USA 225 Wyman Street, Waltham, MA 02451, USA 32 Jamestown Road, London, NW1 7BY, UK Radarweg 29, PO Box 211, 1000 AE Amsterdam, The Netherlands First edition 2012 Copyright # 2012 Elsevier Inc All rights reserved No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone (+44) (0) 1865 843830; fax (+44) (0) 1865 853333; email: permissions@elsevier.com Alternatively you can submit your request online by visiting the Elsevier web site at http://elsevier.com/locate/permissions, and selecting Obtaining permission to use Elsevier material Notice No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made ISBN: 978-0-12-394276-0 ISSN: 0065-2113 (series) For information on all Academic Press publications visit our website at elsevierdirect.com Printed and bound in USA 12 13 14 15 10 CONTRIBUTORS Numbers in Parentheses indicate the pages on which the authors’ contributions begin Nanthi S Bolan (215) Centre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, Australia; Cooperative Research Centre for Contamination Assessment and Remediation of the Environment, Adelaide, Australia P Dhakal (181) University of Kentucky, Lexington, Kentucky, USA Alison J Eagle1 (79) Institute for Land Use Innovation, University of Alberta, Edmonton, Alberta, Canada R Evans (41) Anglia Ruskin University, Cambridge, Cambridgeshire, United Kingdom P D Falloon (41) Met Office Hadley Centre, Exeter, Devon, United Kingdom Robin D Graham (1) School of Biology, Flinders University of South Australia, Adelaide, Australia P M Haygarth (41) Centre for Sustainable Water Management, Lancaster Environment Centre, Lancaster University, Lancaster, Lancashire, United Kingdom A M Ismail (299) International Rice Research Institute (IRRI), Metro Manila, Philippines Won-Il Kim (215) Chemical Safety Division, Department of Agro-Food Safety, National Academy of Agricultural Science, Suwon-si, Gyeonggi-do, Republic of Korea Marija Knez (1) School of Biology, Flinders University of South Australia, Adelaide, Australia Formerly with the Nicholas Institute for Environmental Policy Solutions, Duke University, Durham, North Carolina, USA ix x Contributors Anitha Kunhikrishnan (215) Centre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, Australia; Cooperative Research Centre for Contamination Assessment and Remediation of the Environment, Adelaide, Australia; Chemical Safety Division, Department of Agro-Food Safety, National Academy of Agricultural Science, Suwon-si, Gyeonggi-do, Republic of Korea R V Labios (299) College of Agriculture, University of the Philippines, Los Ban˜os, Philippines Seth Laurenson (215) Land and Environment, AgResearch Ltd, Invermay, New Zealand ăller (215) Karin Mu Systems Modelling, The NZ Institute for Plant and Food Research Ltd., Hamilton, New Zealand D J Mackill (299) International Rice Research Institute (IRRI), Metro Manila, Philippines; Mars, Inc.; Department of Plant Sciences, University of California, Davis, USA C J A Macleod (41) The James Hutton Institute, Craigiebuckler, Aberdeen, United Kingdom C J Matocha (181) University of Kentucky, Lexington, Kentucky, USA Ravi Naidu (215) Centre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, Australia; Cooperative Research Centre for Contamination Assessment and Remediation of the Environment, Adelaide, Australia Lydia P Olander (79) Nicholas Institute for Environmental Policy Solutions, Duke University, Durham, North Carolina, USA T R Paris (301) International Rice Research Institute (IRRI), Metro Manila, Philippines S M Pyzola (181) University of Kentucky, Lexington, Kentucky, USA U S Singh (299) International Rice Research Institute (IRRI), New Delhi, India Ross M Welch (1) Department of Crop and Soil Sciences, Cornell University, Ithaca, New York, USA PREFACE Volume 115 contains six excellent reviews covering important global topics including human health, climate change, nutrient and trace metal mobility and bioavailability, and food production Chapter is a comprehensive review on the role of zinc deficiency on nutritional iron deficiency in humans Chapter deals with an assessment of climate impacts on hydrological mobilization of diffuse substances from agriculture Chapter provides an overview of greenhouse gas mitigation with agricultural land management in the United States Chapter covers the role of abiotic and coupled biotic/abiotic mineral controlled redox processes in nitrate reduction Chapter provides a critical review of the role of wastewater irrigation on the transformation and bioavailability of heavy metal(loids) in soil Chapter addresses the development and adoption of submergencetolerant rice varieties I appreciate the fine reviews of the authors DONALD L SPARKS Newark, Delaware, USA xi C H A P T E R O N E How Much Nutritional Iron Deficiency in Humans Globally Is due to an Underlying Zinc Deficiency? Robin D Graham,* Marija Knez,* and Ross M Welch† Contents Introduction Agronomy of Micronutrients in Respect to the Green Revolution 1960–1980 2.1 Seed nutrient content 2.2 Iron deficiency in humans 2.3 Zinc deficiency and its impact on iron nutrition 2.4 Vitamin A deficiency and its significance 2.5 Food systems strategies Iron and Zinc Interactions in Human Nutrition 3.1 Synergy or antagonism 3.2 Supplementation studies 3.3 Fortification studies show no antagonism 3.4 Zinc and anemia 3.5 The regulation of hemoglobin levels 3.6 Micronutrient deficiencies are occurring together 3.7 Iron and zinc transporters in enterocytes of the small intestine 3.8 Positive role of zinc in oxidative damage and protein synthesis Whole Body Regulation of Iron and Zinc in Humans 4.1 Iron homeostasis 4.2 Hepcidin, an iron store regulator 4.3 Hepcidin regulates DMT1 and/or FPN expression and function 4.4 Zinc, an important regulator of iron absorption 4.5 The role of zinc in decreasing systemic intestinal inflammation and iron deficiency 4.6 Anticipated mechanism of zinc action on iron deficiency 10 12 12 14 14 15 16 16 17 18 18 21 22 22 24 25 26 27 28 * School of Biology, Flinders University of South Australia, Adelaide, Australia Department of Crop and Soil Sciences, Cornell University, Ithaca, New York, USA { Advances in Agronomy, Volume 115 ISSN 0065-2113, DOI: 10.1016/B978-0-12-394276-0.00001-9 # 2012 Elsevier Inc All rights reserved Robin D Graham et al Healthy Food Systems Conclusion Acknowledgment References 30 32 33 33 Abstract This chapter recounts the impact of the green revolution (1960–1980) on subsequent world food supplies and its consequences in terms of human nutrition and health via its impact on the micronutrient status of staple foods and of diets generally Micronutrient deficiency disorders now occur in over half of the total human population This chapter then reviews the recent medical literature on the molecular physiology of the human gut in relation to micronutrient absorption from food and the regulation of nutrient balance from diets heavily based on cereals that are relatively poor in micronutrients Weaving these two literatures together leads to the conclusion that basing the green revolution on low micronutrient-dense cereals to replace the lower yielding but more nutrient-dense pulses and other dicotyledonous food crops is the probable cause of the epidemics of micronutrient deficiencies in the burgeoning human population in the years since 1980 There are lessons in this for the implementation of new efforts to increase food production in the face of even further increases in population forecast to 2050, especially the new effort starting in Africa, and for improving primary health care generally in resourcerich as well as resource-poor countries We conclude that while complete nutrient balance in our diets is the only satisfactory aim of a sustainable food strategy, we focus attention on zinc deficiency and its alleviation as the most extensive and urgent problem among several that arose as an unforeseen side effect of the first green revolution Introduction The first green revolution (begun in 1960) more than doubled cereal production worldwide (Fig 1), an achievement that, in the face of a rapidly rising human population, turned aside the threat of mass starvation in 1960 and of continuing food shortages during the 1960s and 1970s to reach a global surplus again by 1980 The emphasis by the international consortium of agricultural scientists was naturally on increasing yield, both by plant breeding and use of NPK fertilizers, and as it was known that across varieties an inverse relation existed between yield of grain and protein concentration in grain, the latter and other issues of nutritional quality were largely set aside No attention whatever was paid to micronutrient density of the green revolution cereal varieties, a quality issue that was a low priority among nutritionists at that time Cereal production Pulse production Population 200 200 Developing nations World Developing nations Bangladesh 50 Pakistan 50 India 100 Developing nations 100 Bangladesh 150 Pakistan 150 % Increase in population (from 1965 to 1999) 250 250 India % Increase in production (from 1965 to 1999) Iron and Zinc Deficiencies in Crops and Humans Figure Percent changes in cereal and pulse (grain legume) production and in population, 1965–1999 (Welch, 2002a,b) Figure shows the percentage increases of cereal and of pulse (grain legume) production in developing countries between 1965 and 1999 Developing country population doubled during this period (represented by the “100%” line) It is the great achievement of the green revolution that cereal production much more than doubled due to rapid technological change However, pulse production per capita declined markedly; owing to the urgency to produce more, the new technology was not applied to these low-yielding secondary staples or to vegetables These changes in production altered the relative prices of these commodities—lower prices of cereals and higher noncereal food prices—so it became even more difficult for the poor to achieve mineral and vitamin adequacy in their diets In the absence of adequate knowledge among resource-poor populations of the importance for health of micronutrient and vitamin intakes, diets have shifted toward increasing reliance on cereal staples (Graham et al., 2007), leading to micronutrient malnutrition, poorer health, and much misery During the 1980s, a steady rise was noted in the extent of iron-deficiency anemia in humans, especially among the resource-poor populations that benefited most from the greater productivity of the green revolution (Graham, 2008; Graham et al., 2007); however, a putative cause-and-effect association between the rising extent of nutritional iron deficiency and the low micronutrient density of the expanding green revolution cereal varieties, vis-a`-vis the lower-yielding crops they displaced, was not canvassed until much later The anemia was treated by the medical community using diet Robin D Graham et al supplementation and food fortification strategies, with a major program called for by the end of the 1980s decade These programs were facilitated by the ease of diagnosis of iron deficiency in a small sample of peripheral blood During this decade, three other micronutrient deficiencies affecting large numbers of people, those of iodine, vitamin A, and selenium, were promoted and treatments developed (Ren et al., 2008) Deficiencies of iodine and selenium were regional, associated with extreme low levels of the nutrients in the soil, and as neither of them was known to affect crop production, these were treated medically, as with anemia, by food fortification and supplementation in the deficient regions Vitamin A, however, was more generally associated with population density, insufficiency of the food supply, and again like anemia, associated with the production of the green revolution varieties of cereals; again no attribution of cause and effect was made and health authorities deployed supplementation and food fortification strategies The new green revolution varieties of wheat and rice were uniformly white-floured, containing very low concentrations of yellow provitamin A carotenoids; however, yellow endosperm varieties were known and held in the germplasm banks of both crops A clinical deficiency of zinc in a human was reported in a remarkably prescient paper in the 1960s (Prasad et al., 1963) and Prasad later published results of a clinical trial in the 1980s (Prasad, 1991), but both efforts were largely ignored Only in the 1990s was a body of evidence accumulated that attracted some recognition (Prasad, 2003), but as there was, unlike anemia, no quick and simple diagnostic for zinc deficiency in humans, the problem continued to be largely ignored Not until Hotz and Brown (2004) edited an important paper on the extent of zinc-deficient diets of the world, affecting nearly half the global population, was zinc deficiency taken as a potentially serious public health problem Still little has been done about it even to the present day, although two developments must be acknowledged: first, the appearance of zinc deficiency as a priority in public health on the WHO website in 2001, and second, zinc deficiency diagnosis in blood serum by ICP atomic emission spectrometry is now deemed a valid diagnostic at a population level but not for the individual; moreover, this analysis is still far from as easy and inexpensive as is the simple test for anemia (de Benoist et al., 2007) At the same time, soil scientists and agronomists were well aware that zinc-deficient soils are widespread on Earth, about half of the major agriculturally productive soil types (Sillanpaa, 1982, 1990) In contrast, crops were iron deficient on only 3% of soils (Table 1) Moreover, zinc is low in cereal grains, now the basis of diets for the majority of people everywhere More zinc can be incorporated into cereal grains both by zinc fertilization of the crop and by breeding new cereal varieties inherently richer in zinc (Graham et al., 1992; Yilmaz et al., 1998), so the tools to solve zinc deficiency globally have been available, but motivation is still lacking for an integrated “Food Systems” approach that will provide a sustainable solution on a global scale This chapter reviews the medical literature on zinc deficiency, iron deficiency, and their interactions in the human gut, and presents a physiologically Iron and Zinc Deficiencies in Crops and Humans Table Percentage of nutrient-deficient soils among 190 major soils worldwide (Sillanpaa, 1982) and in parts of Bangladesh for comparison (Morris et al., 1997) Macronutrients Deficiency World Acute Latent Total Bangladesh Total Micronutrients N P K B Cu Fe Mn Mo Zn 71 14 85 55 18 73 36 19 55 10 21 31 10 14 3 10 12 15 25 24 49 100 22 69 24 15 85 A latent deficiency is one masked by an even more severe deficiency of another nutrient, often N or P, such that the latent deficiency becomes limiting after the other, more acute deficiency is corrected based case that, potentially, a significant proportion of the iron-deficiency anemia in humans is due to zinc deficiency This is intended to strengthen the case for a greater effort to eliminate zinc deficiency worldwide (and with it some of the anemia) through an integrated Food Systems-based new green revolution (Graham, 2008) Because of the complex of homeostatic mechanisms in the body for preventing excess iron accumulation that in turn prevents peroxidative cellular damage (Edison et al., 2008), this chapter also questions the wisdom of some of the supplementation, biofortification, and process fortification of iron, that is current practice, based on blood tests for hemoglobin and ferritin alone, without showing improvements in health and physical and mental work capacity We therefore raise the question whether relatively more of the global effort to relieve iron deficiency should be spent on eliminating zinc deficiency and other overt, interacting micronutrient deficiencies, sustainably through an agriculturally based Food Systems strategy In this review, we deal first with the agronomy of the green revolution effort and then we present a summary of a recent, extensive medical literature on the molecular physiology of the human intestine and on its implications for human nutrition Finally, we bring these two facets together to develop recommendations for radical change in the current strategy to eliminate anemia and to propose a new Food Systems strategy Agronomy of Micronutrients in Respect to the Green Revolution 1960–1980 In the time man has practised agriculture, crops produced on our soils have become widely deficient in nitrogen and phosphorus and to a lesser extent, in potassium and sulfur, nutrients that, until the turn of the twentieth ... socially acceptable Integrating all this requires successful deployment of expertise in several disciplines and includes agronomic, fertilizer, plant breeding, sociological, and nutritional expertise... Zealand ăller (21 5) Karin Mu Systems Modelling, The NZ Institute for Plant and Food Research Ltd., Hamilton, New Zealand D J Mackill (29 9) International Rice Research Institute (IRRI), Metro Manila,... maintaining intracellular iron status (Lichten and Cousins, 200 9) In an experiment with Caco-2 cell lines, Iyengar et al (200 9) examined the mechanism of interaction of iron and zinc using kinetic
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