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Soybean: A new frontier in understanding the iron deficiency tolerance mechanisms in plants

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Abstract

Background

Soybean (Glycine max L.) is an agronomic crop belonging to the legume family, and is the top second plant species with the highest iron (Fe) content. When exposed to Fe-deficiency during growth in the field, soybean yields are negatively affected from impaired chlorophyll biosynthesis, which is called as Fe-deficiency chlorosis (IDC). Although IDC in soybeans has been observed for years, the molecular studies to develop IDC-tolerant soybean cultivars were slower compared to the studies of other plant species.

Scope

Recently, there are efforts to understand the molecular mechanisms behind IDC tolerance and use them to develop IDC-tolerant soybeans via molecular breeding and transgenic approaches. Genetic transformation of soybean is relatively easy, and loss-of-function mutant collections are readily available. There is a divergence in IDC tolerance among soybean cultivars, suggesting a potential improvement of soybean tolerance to IDC via molecular breeding. This mini review covers the latest developments in the field of soybean research to elucidate the molecular mechanisms of IDC tolerance.

Conclusion

Soybean should be used a new model plant in understanding the Fe-deficiency tolerance mechanisms especially because of its high potential to be used as a bio-fortified crop to treat the iron deficiency in humans in the future.

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References

  • Aksoy E, Jeong IS, Koiwa H (2013) Loss of function of arabidopsis c-terminal domain phosphatase-like1 activates iron deficiency responses at the transcriptional level. Plant Physiol 161:330–345

    Article  CAS  PubMed  Google Scholar 

  • Atwood SE, O’ROURKE JA, Peiffer GA, Yin T, Majumder M, Zhang C, Cianzio SR, Hill JH, Cook D, Whitham SA (2014) Replication protein a subunit 3 and the iron efficiency response in soybean. Plant Cell Environ 37:213–234

    Article  CAS  PubMed  Google Scholar 

  • Barberon M, Zelazny E, Robert S, Conejero G, Curie C, Friml J, Vert G (2011) Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (irt1) transporter controls iron uptake in plants. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1100659108

    PubMed  PubMed Central  Google Scholar 

  • Bernard R (1975) Genetic stocks available. Soybean genetic. Newsletter 2:57–74

    Google Scholar 

  • Bolon Y-T, Haun WJ, Xu WW, Grant D, Stacey MG, Nelson RT, Gerhardt DJ, Jeddeloh JA, Stacey G, Muehlbauer GJ (2011) Phenotypic and genomic analyses of a fast neutron mutant population resource in soybean. Plant Physiol 156:240–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brumbarova T, Bauer P, Ivanov R (2015) Molecular mechanisms governing arabidopsis iron uptake. Trends Plant Sci 20:124–133

    Article  CAS  PubMed  Google Scholar 

  • Butenhoff K J (2015) Qtl mapping and gwas identify sources of iron deficiency chlorosis and canopy wilt tolerance in the fiskeby iii x mandarin (ottawa) soybean population. Dissertation, UNIVERSITY OF MINNESOTA

  • Charlson DV, Cianzio SR, Shoemaker RC (2003) Associating ssr markers with soybean resistance to iron deficiency chlorosis. J Plant Nutr 26:2267–2276

    Article  CAS  Google Scholar 

  • Charlson DV, Bailey TB, Cianzio SR, Shoemaker RC (2005) Molecular marker satt481 is associated with iron-deficiency chlorosis resistance in a soybean breeding population. Crop Sci 45:2394–2399

    Article  CAS  Google Scholar 

  • Clemens S, Aarts MG, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99

    Article  CAS  PubMed  Google Scholar 

  • Connolly EL, Fett JP, Guerinot ML (2002) Expression of the irt1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14:1347–1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connolly EL, Campbell NH, Grotz N, Prichard CL, Guerinot ML (2003) Overexpression of the fro2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol 133:1102–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in arabidopsis halleri colocalizes with hma4, a gene encoding a heavy metal atpase. Plant Physiol 144:1052–1065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diers B, Cianzio S, Shoemaker R (1992) Possible identification of quantitative trait loci affecting iron efficiency in soybean. J Plant Nutr 15:2127–2136

    Article  CAS  Google Scholar 

  • Dong J, Feng Y, Kumar D, Zhang W, Zhu T, Luo M-C and Messing J (2016) Analysis of tandem gene copies in maize chromosomal regions reconstructed from long sequence reads. Proceedings of the National Academy of Sciences, 201608775

  • Duc C, Cellier F, Lobreaux S, Briat JF, Gaymard F (2009) Regulation of iron homeostasis in Arabidopsis thaliana by the clock regulator time for coffee. J Biol Chem 284:36271–36281. doi:10.1074/jbc.M109.059873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci 93:5624–5628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Froechlich D, Fehr W (1981) Agronomic performance of soybeans with differing levels of iron deficiency chlorosis on calcareous soil. Crop Sci 21:438–441

    Article  Google Scholar 

  • Grant D, Nelson R T, Cannon S B and Shoemaker R C (2009) Soybase, the usda-ars soybean genetics and genomics database. Nucleic acids research, gkp798

  • Hass CS, Lam K, Wold MS (2012) Repair-specific functions of replication protein a. J Biol Chem 287:3908–3918

    Article  CAS  PubMed  Google Scholar 

  • Hong S, Kim SA, Guerinot ML, McClung CR (2013) Reciprocal interaction of the circadian clock with the iron homeostasis network in arabidopsis. Plant Physiol 161:893–903

    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 176:709–714

    Article  CAS  Google Scholar 

  • Kassem M, Shultz J, Meksem K, Cho Y, Wood A, Iqbal M, Lightfoot D (2006) An updated ‘essex’by ‘forrest’linkage map and first composite interval map of qtl underlying six soybean traits. Theor Appl Genet 113:1015–1026

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T and Nishizawa N K (2014) Iron sensors and signals in response to iron deficiency. Plant Science

  • 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 69:81–91. doi:10.1111/j.1365-313X.2011.04772.x

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Itai RN, Nishizawa NK (2014) Iron deficiency responses in rice roots. Rice 7:1

    Article  Google Scholar 

  • Lauter ANM, Peiffer GA, Yin T, Whitham SA, Cook D, Shoemaker RC, Graham MA (2014) Identification of candidate genes involved in early iron deficiency chlorosis signaling in soybean (Glycine max) roots and leaves. BMC Genomics 15:702

    Article  Google Scholar 

  • Li G, Kronzucker HJ, Shi W (2016) The response of the root apex in plant adaptation to iron heterogeneity in soil. Front Plant Sci 7

  • Lin S, Cianzio S, Shoemaker R (1997) Mapping genetic loci for iron deficiency chlorosis in soybean. Mol Breed 3:219–229

    Article  CAS  Google Scholar 

  • Lin SF, Grant D, Cianzio S, Shoemaker R (2000) Molecular characterization of iron deficiency chlorosis in soybean. J Plant Nutr 23:1929–1939

    Article  CAS  Google Scholar 

  • Mamidi S, Lee RK, Goos JR, McClean PE (2014) Genome-wide association studies identifies seven major regions responsible for iron deficiency chlorosis in soybean (Glycine max). PLoS One 9:e107469

    Article  PubMed  PubMed Central  Google Scholar 

  • Marschner H, Romheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–274

    Article  CAS  Google Scholar 

  • Naeve SL (2006) Iron deficiency chlorosis in soybean. Agron J 98:1575–1581

    Article  CAS  Google Scholar 

  • Nozoye T, Kim S, Kakei Y, Takahashi M, Nakanishi H, Nishizawa NK (2014) Enhanced levels of nicotianamine promote iron accumulation and tolerance to calcareous soil in soybean. Biosci Biotechnol Biochem 78:1677–1684

    Article  CAS  PubMed  Google Scholar 

  • O’Rourke JA, Charlson DV, Gonzalez DO, Vodkin LO, Graham MA, Cianzio SR, Grusak MA, Shoemaker RC (2007) Microarray analysis of iron deficiency chlorosis in near-isogenic soybean lines. BMC Genomics 8:1

    Article  Google Scholar 

  • O’Rourke JA, Nelson RT, Grant D, Schmutz J, Grimwood J, Cannon S, Vance CP, Graham MA, Shoemaker RC (2009) Integrating microarray analysis and the soybean genome to understand the soybeans iron deficiency response. BMC Genomics 10:1

    Article  Google Scholar 

  • Oliveira NP, Faquin V, Costa ALd, Livramento KGd, Pinho PJd, Guilherme LRG (2016) Genotypic variation of agronomic traits as well as concentrations of fe, zn, p and phytate in soybean cultivars. Revista Ceres 63:403–411

    Article  Google Scholar 

  • Onaga G, Dramé K N and Ismail A M (2016) Understanding the regulation of iron nutrition: Can it contribute to improving iron toxicity tolerance in rice? Funct. Plant Biol

  • Peiffer GA, King KE, Severin AJ, May GD, Cianzio SR, Lin SF, Lauter NC, Shoemaker RC (2012) Identification of candidate genes underlying an iron efficiency quantitative trait locus in soybean. Plant Physiol 158:1745–1754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prodöhl I (2009) A miracle bean: how soy conquered the west. History 4:475–495

    Google Scholar 

  • Ramamurthy RK, Jedlicka J, Graef GL, Waters BM (2014) Identification of new qtls for seed mineral, cysteine, and methionine concentrations in soybean [Glycine max (l.) merr.]. Mol Breed 34:431–445

    Article  Google Scholar 

  • Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697

    Article  CAS  PubMed  Google Scholar 

  • Rogers EE, Wu X, Stacey G, Nguyen HT (2009) Two mate proteins play a role in iron efficiency in soybean. J Plant Physiol 166:1453–1459

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roriz M, Carvalho SM, Vasconcelos MW (2014) High relative air humidity influences mineral accumulation and growth in iron deficient soybean plants. Front Plant Sci 5

  • Salomé P A, Bernal M and Krämer U (2014) Circadian life without micronutrients: Effects of altered micronutrient supply on clock function in arabidopsis. In Plant circadian networks. pp 227–238. Springer

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

    Article  CAS  PubMed  Google Scholar 

  • Santos CS, Carvalho SM, Leite A, Moniz T, Roriz M, Rangel AO, Rangel M, Vasconcelos MW (2016) Effect of tris (3-hydroxy-4-pyridinonate) iron (iii) complexes on iron uptake and storage in soybean (Glycine max l.). Plant Physiol Biochem 106:91–100

    Article  CAS  PubMed  Google Scholar 

  • Schenkeveld W and Temminghoff E (2011) The effectiveness of feeddha chelates in mending and preventing iron chlorosis in soil-grown soybean plants. INTECH Open Access Publisher

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  CAS  PubMed  Google Scholar 

  • Shin L-J, Lo J-C, Chen G-H, Callis J, Fu H, Yeh K-C (2013) Irt1 degradation factor1, a ring e3 ubiquitin ligase, regulates the degradation of iron-regulated transporter1 in arabidopsis. The Plant Cell Online 25:3039–3051

    Article  CAS  Google Scholar 

  • Sivitz A, Grinvalds C, Barberon M, Curie C, Vert G (2011) Proteasome-mediated turnover of the transcriptional activator fit is required for plant iron-deficiency responses. Plant J 66:1044–1052. doi:10.1111/j.1365-313X.2011.04565.x

    Article  CAS  PubMed  Google Scholar 

  • Stribe D (2012) Analysis of iron transporters in the soybean (Glycine max (l.) merr.) genome

  • Tan S, Liu F, Pan X-X, Zang Y-P, Jin F, W-X Z, Qi X-T, Xiao W, Yin L-P (2016) Csn6, a subunit of the cop9 signalosome, is involved in early response to iron deficiency in Oryza sativa. Sci rep 6

  • Thomine S, Lanquar V (2011) Iron transport and signaling in plants. In: Transporters and pumps in plant signaling. Eds. M Geisler and K Venema. Springer, Boston, pp. 99–131

    Chapter  Google Scholar 

  • USDA (2016) Usda national nutrient database for standard reference, release 28. Accessed on 08.30.2016: https://ndb.nal.usda.gov/

  • Vasconcelos M, Eckert H, Arahana V, Graef G, Grusak MA, Clemente T (2006) Molecular and phenotypic characterization of transgenic soybean expressing the arabidopsis ferric chelate reductase gene, fro2. Planta 224:1116–1128

    Article  CAS  PubMed  Google Scholar 

  • Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat J-F, Curie C (2002) Irt1, an arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, McClean PE, Lee R, Goos RJ, Helms T (2008) Association mapping of iron deficiency chlorosis loci in soybean (Glycine max l. merr.) advanced breeding lines. Theor Appl Genet 116:777–787

    Article  CAS  PubMed  Google Scholar 

  • Waters B M (2016) Expression profiling of iron deficiency chlorosis (idc) in soybean (Glycine max): Similarities and differences between low iron supply and alkaline stress. In Plant and Animal Genome XXIV Conference. Plant and Animal Genome

  • Weng JB, Guerinot ML (2016) Iron in plants. In: Encyclopedia of inorganic and bioinorganic chemistry. Ed. R a Scott. John Wiley & Sons, New York, pp. 1–14

    Google Scholar 

  • White P (2012) Ion uptake mechanisms of individual cells and roots: short-distance transport. Marschner’s mineral nutrition of higher plants, 3rd edn. Academic, London, pp. 7–47

    Google Scholar 

  • Wold MS (1997) Replication protein a: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66:61–92

    Article  CAS  PubMed  Google Scholar 

  • Yamada T, Takagi K, Ishimoto M (2012) Recent advances in soybean transformation and their application to molecular breeding and genomic analysis. Breed Sci 61:480–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang C, Bradshaw JD, Whitham SA, Hill JH (2010) The development of an efficient multipurpose bean pod mottle virus viral vector set for foreign gene expression and rna silencing. Plant Physiol 153:52–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Itai RN, Yamakawa T, Nakanishi H, Nishizawa NK, Kobayashi T (2014) The bowman–birk trypsin inhibitor ibp1 interacts with and prevents degradation of idef1 in rice. Plant Mol Biol Report:1–11

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Correspondence to Emre Aksoy.

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This study was funded by Omer Halisdemir University (Grant number: FEB 2015/41-BAGEP).

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Author Emre Aksoy has received a speaker honorarium from The Scientific and Technological Research Council of Turkey (Grant number: 115C031).

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Responsible Editor: Lourdes Hernández-Apaolaza.

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Aksoy, E., Maqbool, A., Tindas, İ. et al. Soybean: A new frontier in understanding the iron deficiency tolerance mechanisms in plants. Plant Soil 418, 37–44 (2017). https://doi.org/10.1007/s11104-016-3157-x

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