Skip to main content

All Roads Leading to: Iron Phytofortification

  • Chapter
  • First Online:
Nutritional Quality Improvement in Plants

Abstract

Enhancing the nutritional quality of food crops is an arena of research that is receiving much footfall among the scientific fraternity, owing to the heavy dependence of humans on plant-based diets. These diets often lack essential micronutrients like iron, thus compromising health and productivity, especially among women and children from impoverished countries. Additionally, although iron is abundant in soil, the calcareous nature of soil renders it unavailable to the plant. This has aggravated the problem, as the bioavailability of iron from staple plant foods is already low in humans. Thus, increasing iron content in the edible portions of the plant may help ameliorate this deficit. Toward this, the past decade has witnessed extensive focus on understanding the mechanisms of iron uptake and redistribution in plants. This understanding has afforded greater insight into altering the existing strategies to achieve this goal. Approaches such as crop and mutation breeding, as well as transgenic technologies, have been used for the introduction of useful traits via genome manipulation. Also, a newly emergent area of study concerns the interaction of rhizosphere microbiota with plant roots and their effects on iron acquisition by plants. In this chapter, we have attempted to summarize the impact of associated microbiota in iron acquisition in addition to the conventional and transgenic efforts toward phytofortification for the alleviation of iron deficiency anemia in the global populace, particularly the affected strata.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aciksoz SB, Yazici A, Ozturk L, Cakmak I (2011) Biofortification of wheat with iron through soil and foliar application of nitrogen and iron fertilizers. Plant Soil 349(1–2):215–225

    Article  CAS  Google Scholar 

  • Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163(2):173–181

    CAS  PubMed  Google Scholar 

  • Ali B, Sabri AN, Ljung K, Hasnain S (2009) Auxin production by plant associated bacteria: impact on endogenous IAA content and growth of Triticum aestivum L. Lett Appl Microbiol 48(5):542–547

    Google Scholar 

  • Allen LH (2000) Anemia and iron deficiency: effects on pregnancy outcome. Am J Clin Nutr 71(5):1280S–1284S

    Article  CAS  PubMed  Google Scholar 

  • Altomare C, Norvell WA, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295-22. Appl Environ Microbiol 65(7):2926–2933

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aluru MR, Rodermel SR, Reddy MB (2011) Genetic modification of low phytic acid 1-1 maize to enhance iron content and bioavailability. J Agri Food Chem 59(24):12954–12962

    Article  CAS  Google Scholar 

  • Andersson M, Thankachan P, Muthayya S, Goud RB, Kurpad AV, Hurrell RF, Zimmermann MB (2008) Dual fortification of salt with iodine and iron: a randomized, double-blind, controlled trial of micronized ferric pyrophosphate and encapsulated ferrous fumarate in southern India. Am J Clin Nutr 88(5):1378–1387

    CAS  PubMed  Google Scholar 

  • Aoyama T, Kobayashi T, Takahashi M, Nagasaka S, Usuda K, Kakei Y, Ishimaru Y, Nakanishi H, Mori S, Nishizawa NK (2009) OsYSL18 is a rice iron (III)–deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Mol Biol 70(6):681–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baltussen R, Knai C, Sharan M (2004) Iron fortification and iron supplementation are cost-effective interventions to reduce iron deficiency in four sub regions of the world. J Nutr 134(10):2678–2684

    Article  CAS  PubMed  Google Scholar 

  • Banfield JF, Barker WW, Welch SA, Taunton A (1999) Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. Proc Natl Acad Sci USA 96(7):3404–3411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bar-Ness E, Hadar Y, Chen Y, Römheld V, Marschner H (1992a) Short-term effects of rhizosphere microorganisms on Fe uptake from microbial siderophores by maize and oat. Plant Physiol 100(1):451–456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bar-Ness E, Hadar Y, Chen Y, Shanzer A, Libman J (1992b) Iron uptake by plants from microbial siderophores: a study with 7-nitrobenz-2 oxa-1, 3-diazole-desferrioxamine as fluorescent ferrioxamine B analog. Plant Physiol 99(4):1329–1335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barona-Gómez F, Wong U, Giannakopulos AE, Derrick PJ, Challis GL (2004) Identification of a cluster of genes that directs desferrioxamine biosynthesis in Streptomyces coelicolor M145. J Am Chem Soc 126(50):16282–16283

    Article  CAS  PubMed  Google Scholar 

  • Bashir K, Ishimaru Y, Shimo H, Kakei Y, Senoura T, Takahashi R, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011a) Rice phenolics efflux transporter 2 (PEZ2) plays an important role in solubilizing apoplasmic iron. Soil Sci Plant Nutri 57(6):803–812

    Article  CAS  Google Scholar 

  • Bashir K, Ishimaru Y, Shimo H, Nagasaka S, Fujimoto M, Takanashi H, Tsutsumi N, An G, Nakanishi H, Nishizawa NK (2011b) The rice mitochondrial iron transporter is essential for plant growth. Nat Commun 2:322

    Article  CAS  PubMed  Google Scholar 

  • Beard J (2003) Iron deficiency alters brain development and functioning. J Nutr 133(5):1468S–1472S

    Article  CAS  PubMed  Google Scholar 

  • Beer HS, Luna L, Pompano, Przybyszewski E, Udipi S, Ghugre P, Haas J (2014) Consuming iron-biofortified pearl millet increased hemoglobin concentrations and prevented a decline in energy efficiency in Indian girls. FASEB J 28(Suppl 1):646-7

    Google Scholar 

  • Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84(1):11–18

    Article  CAS  PubMed  Google Scholar 

  • Boiero L, Perrig D, Masciarelli O, Penna C, Cassán F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74(4):874–880

    Article  CAS  PubMed  Google Scholar 

  • Boonyaves K, Gruissem W, Bhullar NK (2016) NOD promoter-controlled AtIRT1 expression functions synergistically with NAS and FERRITIN genes to increase iron in rice grains. Plant Mol Biol 90(3):207–215

    Article  CAS  PubMed  Google Scholar 

  • Bruner AB, Joffe A, Duggan AK, Casella JF, Brandt J (1996) Randomised study of cognitive effects of iron supplementation in non-anaemic iron-deficient adolescent girls. Lancet 348(9033):992–996

    Article  CAS  PubMed  Google Scholar 

  • Busi MV, Zabaleta EJ, Araya A, Gomez-Casati DF (2004) Functional and molecular characterization of the frataxin homolog from Arabidopsis thaliana. FEBS Lett 576(1–2):141–144

    Article  CAS  PubMed  Google Scholar 

  • Busi MV, Maliandi MV, Valdez H, Clemente M, Zabaleta EJ, Araya A, Gomez-Casati DF (2006) Deficiency of Arabidopsis thaliana frataxin alters activity of mitochondrial Fe–S proteins and induces oxidative stress. Plant J48(6):873–882

    Google Scholar 

  • Calvaruso C, Turpault MP, Frey-Klett P (2006) Root-associated bacteria contribute to mineral weathering and to mineral nutrition in trees: a budgeting analysis. Appl Environ Microbiol 72(2):1258–1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carrillo-Castañeda G, Muñoz JJ, Peralta-Videa JR, Gomez E, Gardea-Torresdey JL (2005) Modulation of uptake and translocation of iron and copper from root to shoot in common bean by siderophore-producing microorganisms. J Plant Nutr 28(10):1853–1865

    Article  CAS  Google Scholar 

  • Cassan F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45(1):28–35

    Google Scholar 

  • Chakraborty U, Chakraborty B, Basnet M (2006) Plant growth promotion and induction of resistance in Camellia sinensis by Bacillus megaterium. J Basic Microbiol 46(3):186–195

    Article  CAS  PubMed  Google Scholar 

  • Chakraborty AP, Chakraborty BN, Chakraborty U (2015) Bacillus megaterium from tea rhizosphere promotes growth and induces systemic resistance in tea against Sclerotium rolfsii. Indian Phytopathol 68(3):237–247

    Google Scholar 

  • Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis thaliana. Plant Physiol 110

    Google Scholar 

  • Chu HH, Chiecko J, Punshon T, Lanzirotti A, Lahner B, Salt DE, Walker EL (2010) Successful reproduction requires the function of Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 metal-nicotianamine transporters in both vegetative and reproductive structures. Plant Physiol 154(1):197–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe (III) uptake. Nature 409(6818):346

    Article  CAS  PubMed  Google Scholar 

  • Dellagi A, Rigault M, Segond D, Roux C, Kraepiel Y, Cellier F, Briat JF, Gaymard F, Expert D (2005) Siderophore-mediated upregulation of arabidopsis ferritin expression in response to Erwinia chrysanthemi infection. Plant J 43(2):262–272

    Article  CAS  PubMed  Google Scholar 

  • Douchkov D, Gryczka C, Stephan UW, Hell R, Bäumlein H (2005) Ectopic expression of nicotianamine synthase genes results in improved iron accumulation and increased nickel tolerance in transgenic tobacco. Plant Cell Environ 28(3):365–374

    Article  CAS  Google Scholar 

  • Drakakaki G, Christou P, Stöger E (2000) Constitutive expression of soybean ferritin cDNA intransgenic wheat and rice results in increased iron levels in vegetative tissues but not in seeds. Transgenic Res 9(6):445–452

    Article  CAS  PubMed  Google Scholar 

  • Drakakaki G, Marcel S, Glahn RP, Lund EK, Pariagh S, Fischer R, Christou P, Stoger E (2005) Endosperm-specific co-expression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron. Plant Mol Biol 59(6):869–880

    Article  CAS  PubMed  Google Scholar 

  • Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144(1):197–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duy D, Wanner G, Meda AR, von Wirén N, Soll J, Philippar K (2007) PIC1, an ancient permease in arabidopsis chloroplasts, mediates iron transport. Plant Cell 19(3):986–1006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Failla ML, Chitchumroonchokchai C, Siritunga D, De Moura FF, Fregene M, Manary MJ, Sayre RT (2012) Retention during processing and bio-accessibility of β-carotene in high β-carotene transgenic cassava root. J Agric Food Chem 60(15):3861–3866

    Article  CAS  PubMed  Google Scholar 

  • Fan SK, Fang XZ, Guan MY, Ye YQ, Lin XY, Du ST, Jin CW (2014) Exogenous abscisic acid application decreases cadmium accumulation in Arabidopsis plants, which is associated with the inhibition of IRT1-mediated cadmium uptake. Front Plant Sci 5:721

    Article  PubMed  PubMed Central  Google Scholar 

  • Farag MA, Ryu CM, Sumner LW, Paré PW (2006) GC–MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67(20):2262–2268

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein JL, Mehta S, Udipi SA, Ghugre PS, Luna SV, Wenger MJ, Murray-Kolb LE, Przybyszewski EM, Haas JD (2015) A randomized trial of iron-biofortified pearl millet in school children in India. J Nutr 145(7):1576–1581

    Article  CAS  PubMed  Google Scholar 

  • Flythe M, Kagan I (2010) Antimicrobial effect of red clover (Trifolium pratense) phenolic extract on the ruminal hyper ammonia-producing bacterium, Clostridium sticklandii. Curr Microbiol 61(2):125–131

    Article  CAS  PubMed  Google Scholar 

  • Fourcroy P, Sisó-Terraza P, Sudre D, Savirón M, Reyt G, Gaymard F, Abadía A, Abadia J, Álvarez‐Fernández A, Briat JF (2014) Involvement of the ABCG 37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol 201(1):155–167

    Google Scholar 

  • Galloway R, McGuire J (1994) Determinants of compliance with iron supplementation: supplies, side effects, or psychology? Soc Sci Med 39(3):381–390

    Article  CAS  PubMed  Google Scholar 

  • Garg M, Sharma N, Sharma S, Kapoor P, Kumar A, Chunduri V, Arora P (2018) Biofortified crops generated by breeding, agronomy, and transgenic approaches are improving lives of millions of people around the world. Front Nutr 5:12

    Article  PubMed  PubMed Central  Google Scholar 

  • Gegios A, Amthor R, Maziya-Dixon B, Egesi C, Mallowa S, Nungo R, Gichuki S, Mbanaso A, Manary MJ (2010) Children consuming cassava as a staple food are at risk for inadequate zinc, iron, and vitamin A intake. Plant Foods Hum Nutr 65(1):64–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giehl RF, Lima JE, von Wirén N (2012) Localized iron supply triggers lateral root elongation in arabidopsis by altering the AUX1-mediated auxin distribution. Plant Cell 24(1):33–49

    Google Scholar 

  • Goto F, Yoshihara T, Shigemoto N, Toki S, Takaiwa F (1999) Iron fortification of rice seed by the soybean ferritin gene. Nat Biotechnol 17(3):282

    Article  CAS  PubMed  Google Scholar 

  • Gregorio GB, Senadhira D, Htut H, Graham RD (2000) Breeding for trace mineral density in rice. Food Nutr Bull 21(4):382–386

    Article  Google Scholar 

  • Guerinot ML, Yi Y (1994) Iron: nutritious, noxious, and not readily available. Plant Physiol 104(3):815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo HC, Wang WB, Luo XH, Wu XP (2015) Characteristics of rhizosphere and bulk soil microbial communities in rubber plantations in Hainan island, China. J Trop For Sci 27(2):202–212

    Google Scholar 

  • Gutiérrez-Luna FM, López-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, de la Cruz HR, Macías-Rodríguez L (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51(1):75–83

    Article  CAS  Google Scholar 

  • Haas JD, Beard JL, Murray-Kolb LE, Del Mundo AM, Felix A, Gregorio GB (2005) Iron-biofortified rice improves the iron stores of non anemic Filipino women. J Nutr 135(12):2823–2830

    Article  CAS  PubMed  Google Scholar 

  • Haas JD, Luna SV, Lung’aho MG, Wenger MJ, Murray-Kolb LE, Beebe S, Gahutu JB, Egli IM (2016) Consuming iron biofortified beans increases iron status in Rwandan women after 128 days in a randomized controlled feeding trial. J Nutr 146(8):1586–1592

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Wang S, Zhao N, Deng S, Zhao C, Li N, Sun J, Zhao R, Yi H, Shen X, Chen S (2016) Exogenous abscisic acid alleviates cadmium toxicity by restricting Cd+2 influx in Populus euphratica cells. J Plant Growth Regul 35(3):827–837

    Article  CAS  Google Scholar 

  • Han D, Hou Y, Liu W, Zhang Z, Ding H, Li H, Yang G (2018) Isolation and functional analysis of MdNAS1, with functions in improved iron stress tolerance and abnormal flower in transgenic tobacco. J Plant Interact 13(1):213–220

    Article  CAS  Google Scholar 

  • HarvestPlus (2014) Biofortification Progress Briefs. http://www.harvestplus.org/sites/default/files/Biofortification_Progress_Briefs_August2014_WEB_2.pdf. Accessed 27 July 2018

  • Hayashi A, Kimoto K (2007) Nicotianamine preferentially inhibits angiotensin I-converting enzyme. J Nutr Sci Vitaminol 53(4):331–336

    Article  CAS  PubMed  Google Scholar 

  • Hess SY, Zimmermann MB, Arnold M, Langhans W, Hurrell RF (2002) Iron deficiency anemia reduces thyroid peroxidase activity in rats. J Nutr 132(7):1951–1955

    Article  CAS  PubMed  Google Scholar 

  • Hindu V, Palacios-Rojas N, Babu R, Suwarno WB, Rashid Z, Usha R, Saykhedkar GR, Nair SK (2018) Identification and validation of genomic regions influencing kernel zinc and iron in maize. Theor Appl Genet 1–5

    Google Scholar 

  • Hoppe M, Hulthén L, Hallberg L (2006) The relative bio- availability in humans of elemental iron powders for use in food fortification. Eur J Nutr 45(1):37–44

    Article  CAS  PubMed  Google Scholar 

  • Hördt W, Römheld V, Winkelmann G (2000) Fusarinines and dimerum acid, mono-and dihydroxamatesiderophores from Penicillium chrysogenum, improve iron utilization by strategy I and strategy II plants. Biometals 13(1):37–46

    Article  PubMed  Google Scholar 

  • Hurrell R (2002) How to ensure adequate iron absorption from iron-fortified food. Nutr Rev 60:S7–S15

    Article  PubMed  Google Scholar 

  • Hurrell R, Egli I (2010) Iron bioavailability and dietary reference values. Am J Clin Nutr 91(5):1461S–1467S

    Article  CAS  PubMed  Google Scholar 

  • Iannotti LL, Tielsch JM, Black MM, Black RE (2006) Iron supplementation in early childhood: health benefits and risks. Am J ClinNutr 84(6):1261–1276

    CAS  Google Scholar 

  • ICRISAT (2016) Biofortified pearl millet varieties to fight iron and zinc deficiencies. http://www.icrisat.org/biofortified-pearl-millet-varieties-to-fight-iron-and-zinc-deficiencies-in-india/ Accessed 27 July 2018

  • Ihemere U, Narayanan N, Sayre R (2012) Iron biofortification and homeostasis in transgenic cassava roots expressing an algal iron assimilatory protein, FEA1. Front Plant Sci 3:171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (2009) Rice OsYSL15 is an iron-regulated iron (III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem 284(6):3470–3479

    Google Scholar 

  • Ishimaru Y, Kakei Y, Shimo H, Bashir K, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. J Biol Chem 286(28):24649–24655

    Google Scholar 

  • Jean ML, Schikora A, Mari S, Briat JF, Curie C (2005) A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading. Plant J 44(5):769–782

    Article  CAS  PubMed  Google Scholar 

  • Jeong J, Connolly EL (2009) Iron uptake mechanisms in plants: functions of the FRO family of ferric reductases. Plant Sci 176(6):709–714

    Article  CAS  Google Scholar 

  • Jeong J, Cohu C, Kerkeb L, Pilon M, Connolly EL, Guerinot ML (2008) Chloroplast Fe (III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc Natl Acad Sci 105(30):10619–10624

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin CW, He YF, Tang CX, Wu P, Zheng SJ (2006) Mechanisms of microbially enhanced Fe acquisition in red clover (Trifolium pratense L.). Plant Cell Environ 29(5):888–897

    Google Scholar 

  • Jin CW, You GY, He YF, Tang C, Wu P, Zheng SJ (2007) Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover. Plant Physiol 144(1):278–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin CW, Li GX, Yu XH, Zheng SJ (2010) Plant Fe status affects the composition of siderophore-secreting microbes in the rhizosphere. Ann Bot 105(5):835–841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson AA, Kyriacou B, Callahan DL, Carruthers L, Stangoulis J, Lombi E, Tester M (2011) Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron-and zinc-biofortification of rice endosperm. PLoS ONE 6(9):e24476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanobe MN, Rodermel SR, Bailey T, Scott P (2013) Changes in endogenous gene transcript and protein levels in maize plants expressing the soybean ferritin transgene. Front Plant Sci 4:196

    Article  PubMed  PubMed Central  Google Scholar 

  • Khalid S, Asghar HN, Akhtar MJ, Aslam A, Zahir ZA (2015) Biofortification of iron in chickpea by plant growth promoting rhizobacteria. Pak J Bot 47(3):1191–1194

    CAS  Google Scholar 

  • Kim SA, Punshon T, Lanzirotti A, Li L, Alonso JM, Ecker JR, Kaplan J, Guerinot ML (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314(5803):1295–1298

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita E, Yamakoshi J, Kikuchi M (1993) Purification and identification of an angiotensin I-converting enzyme inhibitor from soy sauce. Biosci Biotechnol Biochem 57(7):1107–1110

    Article  CAS  PubMed  Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286(5776):885

    Article  CAS  Google Scholar 

  • Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Suzuki M, Inoue H, Itai RN, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) Expression of iron-acquisition-related genes in iron-deficient rice is co-ordinately induced by partially conserved iron-deficiency-responsive elements. J Exp Bot 56(415):1305–1316

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Ogo Y, Itai RN, Nakanishi H, Takahashi M, Mori S, Nishizawa NK (2007) The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants. Proc Natl Acad Sci USA 104(48):19150–19155

    Article  PubMed  PubMed Central  Google Scholar 

  • Kobayashi T, Itai RN, Ogo Y, Kakei Y, Nakanishi H, Takahashi M, Nishizawa NK (2009) The rice transcription factor IDEF1 is essential for the early response to iron deficiency, and induces vegetative expression of late embryogenesis abundant genes. Plant J 60(6):948–961

    Article  PubMed  Google Scholar 

  • Kobayashi T, Itai RN, Aung MS, Senoura T, Nakanishi H, Nishizawa NK (2012) The rice transcription factor IDEF1 directly binds to iron and other divalent metals for sensing cellular iron status. Plant J 69(1):81–91

    Article  CAS  PubMed  Google Scholar 

  • Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2004) OsYSL2 is a rice metal‐nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J 39(3):415–424

    Google Scholar 

  • Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40(1):37–44

    Article  CAS  PubMed  Google Scholar 

  • La Frano MR, Woodhouse LR, Burnett DJ, Burri BJ (2013) Biofortified cassava increases β-carotene and vitamin A concentrations in the TAG-rich plasma layer of American women. Br J Nutr 110(2):310–320

    Article  CAS  PubMed  Google Scholar 

  • Lanquar V, Lelièvre F, Bolte S, Hamès C, Alcon C, Neumann D, Vansuyt G, Curie C, Schröder A, Krämer U, Barbier-Brygoo H (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24(23):4041–4051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Layrisse M, Cook JD, Martinez C, Roche M, Kuhn IN, Walker RB, Finch CA (1969) Food iron absorption: a comparison of vegetable and animal foods. Blood 33(3):430–443

    Article  CAS  PubMed  Google Scholar 

  • Lee S, An G (2009) Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ 32(4):408–416

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Jeon US, Lee SJ, Kim YK, Persson DP, Husted S, Schjørring JK, Kakei Y, Masuda H, Nishizawa NK, An G (2009) Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc Natl Acad Sci USA 106(51):22014–22019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S, Kim YS, Jeon US, Kim YK, Schjoerring JK, An G (2012) Activation of rice nicotianamine synthase 2 (OsNAS2) enhances iron availability for biofortification. Mol Cells 33(3):269–275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemanceau P, Bauer P, Kraemer S, Briat JF (2009) Iron dynamics in the rhizosphere as a case study for analyzing interactions between soils, plants and microbes. Plant Soil 321(1–2):513–535

    Article  CAS  Google Scholar 

  • Li KT, Moulin M, Mangel N, Albersen M, Verhoeven-Duif NM, Ma Q, Zhang P, Fitzpatrick TB, Gruissem W, Vanderschuren H (2015) Increased bioavailable vitamin B 6 in field-grown transgenic cassava for dietary sufficiency. Nat Biotechnol 33(10):1029

    PubMed  Google Scholar 

  • Li Z, Zu C, Wang C, Yang J, Yu H, Wu H (2016a) Different responses of rhizosphere and non-rhizosphere soil microbial communities to consecutive Piper nigrum L. monoculture. Sci Rep 6:35825

    Google Scholar 

  • Li X, Zhang H, Ai Q, Liang G, Yu D (2016b) Two bHLH transcription factors, bHLH34 and bHLH104, regulate iron homeostasis in Arabidopsis thaliana. Plant Physiol 170(4):2478–2493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang G, Zhang H, Li X, Ai Q, Yu D (2017) bHLH transcription factor bHLH115 regulates iron homeostasis in Arabidopsis thaliana. J Exp Bot 68(7):1743–1755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin XY, Ye YQ, Fan SK, Jin CW, Zheng SJ (2016) Increased sucrose accumulation regulates iron-deficiency responses by promoting auxin signaling in Arabidopsis plants. Plant Physiol 170(2):907–920

    Article  CAS  PubMed  Google Scholar 

  • Lindsay WL, Schwab AP (1982) The chemistry of iron in soils and its availability to plants. J Plant Nutr 5(4–7):821–840

    Article  CAS  Google Scholar 

  • Ling HQ, Bauer P, Bereczky Z, Keller B, Ganal M (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci USA 99(21):13938–13943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lingam S, Mohrbacher J, Brumbarova T, Potuschak T, Fink-Straube C, Blondet E, Genschik P, Bauer P (2011) Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell 23(5):1815–1829

    Google Scholar 

  • Liu G, Greenshields DL, Sammynaiken R, Hirji RN, Selvaraj G, Wei Y (2007) Targeted alterations in iron homeostasis under lie plant defense responses. J Cell Sci 120(4):596–605

    Article  CAS  PubMed  Google Scholar 

  • Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22(7):2219–2236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lucca P, Hurrell R, Potrykus I (2001) Genetic engineering approaches to improve the bioavailability and the level of iron in rice grains. Theor Appl Genet 102(2–3):392–397

    Article  CAS  Google Scholar 

  • Marschner P, Crowley DE (1998) Phytosiderophores decrease iron stress and pyoverdine production of Pseudomonas fluorescens Pf-5 (pvd-inaZ). Soil Biol Biochem 30(10–11):1275–1280

    Article  CAS  Google Scholar 

  • Marschner H, Römheld V, Kissel M (1986) Different strategies in higher plants in mobilization and uptake of iron. J Plant Nutr 9(3–7):695–713

    Article  CAS  Google Scholar 

  • Marschner P, Crowley D, Rengel Z (2011) Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis–model and research methods. Soil Biol Biochem 43(5):883–894

    Article  CAS  Google Scholar 

  • Martínez-Medina A, Van Wees SC, Pieterse CM (2017) Airborne signals from Trichoderma fungi stimulate iron uptake responses in roots resulting in priming of jasmonic acid-dependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum. Plant Cell Environ 40(11):2691–2705

    Article  CAS  PubMed  Google Scholar 

  • Masalha J, Kosegarten H, Elmaci Ö, Mengel K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biol Fertil Soil 30(5–6):433–439

    Article  CAS  Google Scholar 

  • Masuda H, Usuda K, Kobayashi T, Ishimaru Y, Kakei Y, Takahashi M, Higuchi K, Nakanishi H, Mori S, Nishizawa NK (2009) Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice 2(4):155–166

    Article  Google Scholar 

  • Masuda H, Ishimaru Y, Aung MS, Kobayashi T, Kakei Y, Takahashi M, Higuchi K, Nakanishi H, Nishizawa NK (2012) Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Sci Rep 30(2):543

    Article  CAS  Google Scholar 

  • Masuda H, Kobayashi T, Ishimaru Y, Takahashi M, Aung MS, Nakanishi H, Mori S, Nishizawa NK (2013) Iron-biofortification in rice by the introduction of three barley genes participated in mugineic acid biosynthesis with soybean ferritin gene. Front Plant Sci 4:132

    Article  PubMed  PubMed Central  Google Scholar 

  • Maurer F, Müller S, Bauer P (2011) Suppression of Fe deficiency gene expression by jasmonate. Plant Physiol Biochem 49(5):530–536

    Article  CAS  PubMed  Google Scholar 

  • Mendoza-Cózatl DG, Xie Q, Akmakjian GZ, Jobe TO, Patel A, Stacey MG, Song L, Demoin DW, Jurisson SS, Stacey G, Schroeder JI (2014) OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds. Mol Plant 7(9):1455–1469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer JA, Abdallah MA (1978) The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. Microbiology 107(2):319–328

    CAS  Google Scholar 

  • Mohammad MJ, Malkawi HI, Shibli R (2003) Effects of arbuscularmycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts. J Plant Nutr 26(1):125–137

    Article  CAS  Google Scholar 

  • Morrissey J, Baxter IR, Lee J, Li L, Lahner B, Grotz N, Kaplan J, Salt DE, Guerinot ML (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in arabidopsis. Plant Cell 21(10):3326–3338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakanishi H, Yamaguchi H, Sasakuma T, Nishizawa NK, Mori S (2000) Two dioxygenase genes, Ids3 and Ids2, from Hordeum vulgare are involved in the biosynthesis of mugineic acid family phytosiderophores. Plant Mol Biol 44(2):199–207

    Article  CAS  PubMed  Google Scholar 

  • Nantongo A (2016) Legumes News

    Google Scholar 

  • Narayanan NN, Ihemere U, Ellery C, Sayre RT (2011) Overexpression of hydroxylnitrilelyase in cassava roots elevates protein and free amino acids while reducing residual cyanogen levels. PLoS ONE 6(7):e21996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narayanan N, Beyene G, Chauhan RD, Gaitán-Solis E, Grusak MA, Taylor N, Anderson P (2015) Overexpression of arabidopsis VIT1 increases accumulation of iron in cassava roots and stems. Plant Sci 240:170–181

    Article  CAS  PubMed  Google Scholar 

  • Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y et al (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286(7):5446–5454

    Article  CAS  PubMed  Google Scholar 

  • Ogo Y, Nakanishi Itai R, Nakanishi H, Kobayashi T, Takahashi M, Mori S, Nishizawa NK (2007) The rice bHLH protein OsIRO2 is an essential regulator of the genes involved in Fe uptake under Fe-deficient conditions. Plant J 51(3):366–377

    Article  CAS  PubMed  Google Scholar 

  • Ogo Y, Kobayashi T, Itai RN, Nakanishi H, Kakei Y, Takahashi M, Toki S, Mori S, Nishizawa NK (2008) A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. J Biol Chem 283(19):13407–13417

    Article  CAS  PubMed  Google Scholar 

  • Omidvari M, Sharifi RA, Ahmadzadeh M, Dahaji PA (2010) Role of fluorescent pseudomonads siderophore to increase bean growth factors. J Agric Sci 2(3):242

    Google Scholar 

  • Palmer CM, Hindt MN, Schmidt H, Clemens S, Guerinot ML (2013) MYB10 and MYB72 are required for growth under iron-limiting conditions. PLoS Genet 9(11):e1003953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel P, Yadav K, Ganapathi TR (2016) Biofortification for alleviating iron deficiency anemia. In: Mohandas S, Ravishankar KV (eds) Banana: genomics and transgenic approaches for genetic improvement. Springer, Singapore, pp 301–337

    Google Scholar 

  • Paul S, Ali N, Gayen D, Datta SK, Datta K (2012) Molecular breeding of Osfer2 gene to increase iron nutrition in rice grain. GM Crops Food 3(4):310–316

    Article  PubMed  Google Scholar 

  • Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassán FD, Luna MV (2007) Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl Microbiol Biotechnol 75(5):1143–1150

    Article  CAS  PubMed  Google Scholar 

  • Perry RD, San Clemente CL (1979) Siderophore synthesis in Klebsiella pneumoniae and Shigellasonnei during iron deficiency. J Bacteriol 140(3):1129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petit JM, Briat JF, Lobréaux S (2001) Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family. Biochem J 359(3):575–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeiffer WH, McClafferty B (2007) HarvestPlus: breeding crops for better nutrition. Crop Sci 47(Supplement_3):S-88

    Google Scholar 

  • Pompano LM, Przybyszewski EM, Udipi SA, Ghugre P, Haas JD (2013) VO2 max improves in Indian school children after a feeding trail with iron biofortified pearl millet. FASEB J 845-28

    Google Scholar 

  • Press CM, Loper JE, Kloepper JW (2001) Role of iron in rhizobacteria-mediated induced systemic resistance of cucumber. Phytopathology 91(6):593–598

    Article  CAS  PubMed  Google Scholar 

  • Qu LQ, Yoshihara T, Ooyama A, Goto F, Takaiwa F (2005) Iron accumulation does not parallel the high expression level of ferritin in transgenic rice seeds. Planta 222(2):225–233

    Article  CAS  Google Scholar 

  • Rampey RA, Woodward AW, Hobbs BN, Tierney MP, Lahner B, Salt DE, Bartel B (2006) An arabidopsis basic helix-loop-helix leucine zipper protein modulates metal homeostasis and auxin conjugate responsiveness. Genetics

    Google Scholar 

  • Ramzani PM, Khalid M, Naveed M, Ahmad R, Shahid M (2016) Iron biofortification of wheat grains through integrated use of organic and chemical fertilizers in pH affected calcareous soil. Plant Physiol Biochem 104:284–293

    Article  CAS  PubMed  Google Scholar 

  • Ravet K, Touraine B, Boucherez J, Briat JF, Gaymard F, Cellier F (2009) Ferritins control interaction between iron homeostasis and oxidative stress in arabidopsis. Plant J 57(3):400–412

    Article  CAS  PubMed  Google Scholar 

  • Reyes I, Valery A, Valduz Z (2007) Phosphate-solubilizing microorganisms isolated from rhizospheric and bulk soils of colonizer plants at an abandoned rock phosphate mine. In: First international meeting on microbial phosphate solubilization. Springer, Dordrecht, pp 69–75

    Google Scholar 

  • Robin A, Mougel C, Siblot S, Vansuyt G, Mazurier S, Lemanceau P (2006a) Effect of ferritin overexpression in tobacco on the structure of bacterial and pseudomonad communities associated with the roots. FEMS Microbiol Ecol 58(3):492–502

    Article  CAS  PubMed  Google Scholar 

  • Robin A, Vansuyt G, Corberand T, Briat JF, Lemanceau P (2006b) The soil type affects both the differential accumulation of iron between wild-type and ferritin over-expressor tobacco plants and the sensitivity of their rhizosphere bacterioflora to iron stress. Plant Soil 283(1–2):73–81

    Article  CAS  Google Scholar 

  • Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397(6721):694

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez H, Gonzalez T, Goire I, Bashan Y (2004) Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften 91(11):552–555

    Article  CAS  PubMed  Google Scholar 

  • Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80(1):175–180

    Article  PubMed  PubMed Central  Google Scholar 

  • Roschzttardtz H, Séguéla-Arnaud M, Briat JF, Vert G, Curie C (2011) The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout arabidopsis development. Plant Cell 23(7):2725–2737

    Google Scholar 

  • Rroço E, Kosegarten H, Harizaj F, Imani J, Mengel K (2003) The importance of soil microbial activity for the supply of iron to sorghum and rape. Eur J Agron 19(4):487–493

    Article  CAS  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in arabidopsis. Plant Physiol 134(3):1017–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in arabidopsis roots. New Phytol 183(4):1072–1084

    Article  CAS  PubMed  Google Scholar 

  • Sarria R, Torres E, Angel F, Chavarriaga P, Roca WM (2000) Transgenic plants of cassava (Manihot esculenta) with resistance to Basta obtained by Agrobacterium-mediated transformation. Plant Cell Rep 19(4):339–344

    Article  CAS  PubMed  Google Scholar 

  • Segarra G, Van der Ent S, Trillas I, Pieterse CM (2009) MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol 11(1):90–96

    Article  CAS  PubMed  Google Scholar 

  • Segarra G, Casanova E, Avilés M, Trillas I (2010) Trichoderma asperellum strain T34 controls Fusarium wilt disease in tomato plants in soilless culture through competition for iron. Microbe Ecol 59(1):141–149

    Article  Google Scholar 

  • Séguéla M, Briat JF, Vert G, Curie C (2008) Cytokinins negatively regulate the root iron uptake machinery in arabidopsis through a growth-dependent pathway. Plant J55(2):289–300

    Google Scholar 

  • Selote D, Samira R, Matthiadis A, Gillikin JW, Long TA (2015) Iron-binding E3 ligase mediates iron response in plants by targeting basic helix-loop-helix transcription factors. Plant Physiol 167(1):273–286

    Article  CAS  PubMed  Google Scholar 

  • Shenker M, Oliver I, Helmann M, Hadar Y, Chen Y (1992) Utilization by tomatoes of iron mediated by a siderophore produced by Rhizopus arrhizus. J Plant Nutr 15(10):2173–2182

    Article  CAS  Google Scholar 

  • Shi JY, Yuan XF, Lin HR, Yang YQ, Li ZY (2011) Differences in soil properties and bacterial communities between the rhizosphere and bulk soil and among different production areas of the medicinal plant Fritillaria thunbergii. Int J Mol Sci 12(6):3770–3785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sivitz AB, Hermand V, Curie C, Vert G (2012) Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. PLoS ONE 7(9):e44843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sperotto RA, Ricachenevsky FK, de Abreu Waldow V, Fett JP (2012) Iron biofortification in rice: it’s a long way to the top. Plant Sci 190:24–39

    Article  CAS  PubMed  Google Scholar 

  • Sradnick A, Oltmanns M, Raupp J, Joergensen RG (2018) Microbial biomass and activity down the soil profile after long-term addition of farmyard manure to a sandy soil. Org Agric 8(1):29–38

    Article  Google Scholar 

  • Stacey MG, Koh S, Becker J, Stacey G (2002) AtOPT3, a member of the oligopeptide transporter family, is essential for embryo development in arabidopsis. Plant Cell 14(11):2799–2811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stacey MG, Patel A, McClain WE, Mathieu M, Remley M, Rogers EE, Gassmann W, Blevins DG, Stacey G (2008) The arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol 146(2):589–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stringlis IA, Yu K, Feussner K, de Jonge R, Van Bentum S, Van Verk MC, Berendsen RL, Bakker PA, Feussner I, Pieterse CM (2018) MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci USA 115(22):E5213–E5222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Z, Liu K, Zhang J, Zhang Y, Xu K, Yu D, Wang J, Hu L, Chen L, Li C (2017) IAA producing Bacillus altitudinis alleviates iron stress in Triticum aestivum L. seedling by both bioleaching of iron and up-regulation of genes encoding ferritins. Plant Soil 419(1–2):1–11

    Google Scholar 

  • Tan S, Han R, Li P, Yang G, Li S, Zhang P, Wang WB, Zhao WZ, Yin LP (2015) Over-expression of the MxIRT1 gene increases iron and zinc content in rice seeds. Transgenic Res 24(1):109–122

    Article  CAS  PubMed  Google Scholar 

  • Teintze M, Leong J (1981) Structure of pseudobactin A, a second siderophore from plant growth promoting Pseudomonas B10. Biochemistry 20(22):6457–6462

    Article  CAS  PubMed  Google Scholar 

  • Tilman D (1999) Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. Proc Natl Acad Sci USA 96(11):5995–6000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trijatmiko KR, Dueñas C, Tsakirpaloglou N, Torrizo L, Arines FM, Adeva C, Balindong J, Oliva N, Sapasap MV, Borrero J, Rey J (2016) Biofortified indica rice attains iron and zinc nutrition dietary targets in the field. Sci Rep 6:19792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Usuda K, Wada Y, Ishimaru Y, Kobayashi T, Takahashi M, Nakanishi H, Nagato Y, Mori S, Nishizawa NK (2009) Genetically engineered rice containing larger amounts of nicotianamine to enhance the antihypertensive effect. Plant Biotechnol J 7(1):87–95

    Article  CAS  PubMed  Google Scholar 

  • Van der Ent S, Verhagen BW, Van Doorn R, Bakker D, Verlaan MG, Pel MJ, Joosten RG, Proveniers MC, Van Loon LC, Ton J, Pieterse CM (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in arabidopsis. Plant Physiol 146(3):1293–1304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Wuytswinkel O, Vansuyt G, Grignon N, Fourcroy P, Briat JF (1999) Iron homeostasis alteration in transgenic tobacco overexpressing ferritin. Plant J 17(1):93–97

    Article  PubMed  Google Scholar 

  • Vansuyt G, Mench M, Briat JF (2000) Soil-dependent variability of leaf iron accumulation in transgenic tobacco overexpressing ferritin. Plant Physiol Biochem 38(6):499–506

    Article  CAS  Google Scholar 

  • Vansuyt G, Souche G, Straczek A, Briat JF, Jaillard B (2003) Flux of protons released by wild type and ferritin over-expressor tobacco plants: effect of phosphorus and iron nutrition. Plant Physiol Biochem 41(1):27–33

    Article  CAS  Google Scholar 

  • Vansuyt G, Robin A, Briat JF, Curie C, Lemanceau P (2007) Iron acquisition from Fe-pyoverdine by Arabidopsis thaliana. Mol Plant Microbe Interact 20(4):441–447

    Article  CAS  PubMed  Google Scholar 

  • Vasconcelos M, Datta K, Oliva N, Khalekuzzaman M, Torrizo L, Krishnan S, Oliveira M, Goto F, Datta SK (2003) Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Sci 164(3):371–378

    Article  CAS  Google Scholar 

  • Velu G, Ortiz-Monasterio I, Cakmak I, Hao Y, Singh RP (2014) Biofortification strategies to increase grain zinc and iron concentrations in wheat. J Cereal Sci 59(3):365–372

    Article  CAS  Google Scholar 

  • Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14(6):1223–1233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Wirén N, Klair S, Bansal S, Briat JF, Khodr H, Shioiri T, Leigh RA, Hider RC (1999) Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiol 119(3):1107–1114

    Google Scholar 

  • Walter T, De Andraca I, Chadud P, Perales CG (1989) Iron deficiency anemia: adverse effects on infant psychomotor development. Pediatrics 84(1):7–17

    CAS  PubMed  Google Scholar 

  • Wang Y, Brown HN, Crowley DE, Szaniszlo PJ (1993) Evidence for direct utilization of a siderophore, ferrioxamine B, in axenically grown cucumber. Plant Cell Environ 16(5):579–585

    Article  CAS  Google Scholar 

  • Wang HY, Klatte M, Jakoby M, Bäumlein H, Weisshaar B, Bauer P (2007) Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana. Planta 226(4):897–908

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Christie P, Xiao Z, Qin C, Wang P, Liu J, Xie Y, Xia R (2008) Arbuscular mycorrhizal enhancement of iron concentration by Poncirustrifoliata L. Raf and Citrus reticulata Blanco grown on sand medium under different pH. Biol Fertil Soil 45(1):65–72

    Google Scholar 

  • Wang N, Cuia Y, Liua Y, Fana H, Dua J, Huangd Z, Yuana Y, Wua H, Linga HQ (2013) Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol Plant 6(2):503–513

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Zhou C, Xiao X, Xie Y, Zhu L, Ma Z (2017) Enhanced iron and selenium uptake in plants by volatile emissions of Bacillus amyloliquefaciens (BF06). Appl Sci 7(1):85

    Article  CAS  Google Scholar 

  • Waters BM, Sankaran RP (2011) Moving micronutrients from the soil to the seeds: genes and physiological processes from a biofortification perspective. Plant Sci 180(4):562–574

    Article  CAS  PubMed  Google Scholar 

  • Waters BM, Chu HH, DiDonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL (2006) Mutations in arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141(4):1446–1458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welsch R, Arango J, Bär C, Salazar B, Al-Babili S, Beltrán J, Chavarriaga P, Ceballos H, Tohme J, Beyer P (2010) Provitamin A accumulation in cassava (Manihot esculenta) roots driven by a single nucleotide polymorphism in a phytoene synthase gene. Plant Cell 22(10):3348–3356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets–iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182(1):49–84

    Article  CAS  PubMed  Google Scholar 

  • Wirth J, Poletti S, Aeschlimann B, Yakandawala N, Drosse B, Osorio S, Tohge T, Fernie AR, Günther D, Gruissem W, Sautter C (2009) Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotechnol J 7(7):631–644

    Article  CAS  PubMed  Google Scholar 

  • Wu TY, Gruissem W, Bhullar NK (2019) Targeting intracellular transport combined with efficient uptake and storage significantly increases grain iron and zinc levels in rice. Plant Biotechnol J 17(1):9–20

    Article  CAS  PubMed  Google Scholar 

  • Xie X, Zhang H, Pare P (2009) Sustained growth promotion in Arabidopsis with long-term exposure to the beneficial soil bacterium Bacillus subtilis (GB03). Plant Signal Behav 4(10):948–953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong H, Kakei Y, Kobayashi T, Guo X, Nakazono M, Takahashi H, Nakanishi H, Shen H, Zhang F, Nishizawa NK, Zuo Y (2013) Molecular evidence for phytosiderophore-induced improvement of iron nutrition of peanut intercropped with maize in calcareous soil. Plant Cell Environ 36(10):1888–1902

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Pan W, Zhang R, Lu Q, Xue W, Wu C, Song B, Du S (2018) Inoculation with Bacillus subtilis and Azospirillum brasilense produces abscisic acid that reduces IRT1-mediated cadmium uptake of roots. J Agric Food Chem 66(20):5229–5236

    Article  CAS  PubMed  Google Scholar 

  • Yadav K, Patel P, Srivastava AK, Ganapathi TR (2017) Overexpression of native ferritin gene MusaFer1 enhances iron content and oxidative stress tolerance in transgenic banana plants. PLoS ONE 12(11):e0188933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang CH, Crowley DE (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl Environ Microbiol 66(1):345–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4

    Article  CAS  PubMed  Google Scholar 

  • Yokosho K, Yamaji N, Ueno D, Mitani N, Ma JF (2009) OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol 149(1):297–305

    Google Scholar 

  • Yuan YX, Zhang J, Wang DW, Ling HQ (2005) AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants. Cell Res 15(8):613

    Article  CAS  PubMed  Google Scholar 

  • Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, Wang D, Ling HQ (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18(3):385

    Article  CAS  PubMed  Google Scholar 

  • Zamioudis C, Hanson J, Pieterse CM (2014) β-Glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in arabidopsis roots. New Phytol 204(2):368–379

    Article  CAS  PubMed  Google Scholar 

  • Zamioudis C, Korteland J, Van Pelt JA, van Hamersveld M, Dombrowski N, Bai Y, Hanson J, Van Verk MC, Ling HQ, Schulze-Lefert P, Pieterse CM (2015) Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB 72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses. Plant J 84(2):309–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zancani M, Peresson C, Biroccio A, Federici G, Urbani A, Murgia I, Soave C, Micali F, Vianello A, Macrì F (2004) Evidence for the presence of ferritin in plant mitochondria. Eur J Biochem 271(18):3657–3664

    Article  CAS  PubMed  Google Scholar 

  • Zandavalli RB, Dillenburg LR, de Souza PV (2004) Growth responses of Araucaria angustifolia (Araucariaceae) to inoculation with the mycorrhizal fungus Glomusclarum. Appl Soil Ecol 25(3):245–255

    Article  Google Scholar 

  • Zhai Z, Gayomba SR, Jung HI, Vimalakumari NK, Piñeros M, Craft E, Rutzke MA, Danku J, Lahner B, Punshon T, Guerinot ML (2014) OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis. Plant Cell 26(5):2249–2264

    Google Scholar 

  • Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Paré PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in arabidopsis. Planta 226(4):839

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008) Soil bacteria augment arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56(2):264–273

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58(4):568–577

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Liu B, Li M, Feng D, Jin H, Wang P, Liu J, Xiong F, Wang J, Wang HB (2015) The bHLH transcription factor bHLH104 interacts with IAA-LEUCINE RESISTANT3 and modulates iron homeostasis in arabidopsis. Plant Cell 27(3):787–805

    Google Scholar 

  • Zheng SJ, Arakawa Y, Kurata H, Yamamoto Y, Matsumoto H, Masaoka Y (2000) The resistant mechanism to iron deficiency in red clover. II. The characteristics and functions of root exudates. In: Abstracts of the annual meetings, Japanese Society of soil science and plant nutrition 46 2000 Mar 25, Japanese Society of Soil Science and Plant Nutrition, p 72

    Google Scholar 

  • Zheng L, Cheng Z, Ai C, Jiang X, Bei X, Zheng Y, Glahn RP, Welch RM, Miller DD, Lei XG, Shou H (2010a) Nicotianamine, a novel enhancer of rice iron bioavailability to humans. PLoS ONE 5(4):e10190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng L, Ying Y, Wang L, Wang F, Whelan J, Shou H (2010b) Identification of a novel iron regulated basic helix-loop-helix protein involved in Fe homeostasis in Oryza sativa. BMC Plant Biol 10(1):166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou C, Zhu L, Ma Z, Wang J (2018) Improved iron acquisition of Astragalus sinicus under low iron-availability conditions by soil-borne bacteria Burkholderia cepacia. J Plant Interact 13(1):9–20

    Article  CAS  Google Scholar 

  • Zielińska-Dawidziak M (2015) Plant ferritin-a source of iron to prevent its deficiency. Nutrients 7(2):1184–1201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmermann MB, Hurrell RF (2007) Nutritional iron deficiency. Lancet 370(9586):511–520

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann M, Adou P, Torresani T, Zeder C, Hurrell R (2000) Persistence of goiter despite oral iodine supplementation in goitrous children with iron deficiency anemia in Cote d’Ivoire. Am J ClinNutr 71(1):88–93

    CAS  Google Scholar 

  • Zimmermann MB, Zeder C, Chaouki N, Saad A, Torresani T, Hurrell RF (2003) Dual fortification of salt with iodine and microencapsulated iron: a randomized, double-blind, controlled trial in Moroccan schoolchildren. Am J Clin Nutr 77(2):425–432

    Article  CAS  PubMed  Google Scholar 

  • Zlotkin S, Arthur P, Schauer C, Antwi KY, Yeung G, Piekarz A (2003) Home-fortification with iron and zinc sprinkles or iron sprinkles alone successfully treats anemia in infants and young children. J Nutr 133(4):1075–1080

    Article  CAS  PubMed  Google Scholar 

  • Zuo J, Wu Z, Li Y, Shen Z, Feng X, Zhang M, Ye H (2017) Mitochondrial ABC transporter ATM3 is essential for cytosolic iron-sulfur cluster assembly. Plant Physiol 173(4):2096–2109

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. R. Ganapathi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Yadav, K., Patel, P., Ganapathi, T.R. (2019). All Roads Leading to: Iron Phytofortification. In: Jaiwal, P., Chhillar, A., Chaudhary, D., Jaiwal, R. (eds) Nutritional Quality Improvement in Plants. Concepts and Strategies in Plant Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-95354-0_2

Download citation

Publish with us

Policies and ethics