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Soybean Fe–S cluster biosynthesis regulated by external iron or phosphate fluctuation

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Abstract

Key message

Iron and phosphorus are essential for soybean nodulation. Our results suggested that the deficiency of Fe or P impairs nodulation by affecting the assembly of functional iron–sulfur cluster via different mechanisms.

Abstract

Iron (Fe) and phosphorus (P) are important mineral nutrients for soybean and are indispensable for nodulation. However, it remains elusive how the pathways of Fe metabolism respond to the fluctuation of external Fe or P. Iron is required for the iron–sulfur (Fe–S) cluster assembly in higher plant. Here, we investigated the expression pattern of Fe–S cluster biosynthesis genes in the nodulated soybean. Soybean genome encodes 42 putative Fe–S cluster biosynthesis genes, which were expressed differently in shoots and roots, suggesting of physiological relevance. Nodules initiated from roots of soybean after rhizobia inoculation. In comparison with that in shoots, iron concentration was three times higher in nodules. The Fe–S cluster biosynthesis genes were activated and several Fe–S protein activities were increased in nodules, indicating that a more effective Fe–S cluster biosynthesis is accompanied by nodulation. Fe–S cluster biosynthesis genes were massively repressed and some Fe–S protein activities were decreased in nodules by Fe deficiency, leading to tiny nodules. Notably, P deficiency induced a similar Fe-deficiency response in nodules, i.e, certain Fe–S enzyme activity loss and tiny nodules. However, distinct from Fe-deficient nodules, higher iron concentration was accumulated and the Fe–S cluster biosynthesis genes were not suppressed in the P-deficiency-treated nodules. Taken together, our results showed that both Fe deficiency and P deficiency impair nodulation, but they affect the assembly of Fe–S cluster maybe via different mechanisms. The data also suggested that Fe–S cluster biosynthesis likely links Fe metabolism and P metabolism in root and nodule cells of soybean.

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Abbreviations

Fe:

Iron

P:

Phosphorus

Fe–S:

Iron–sulfur

SUF:

Sulfur mobilization

ISC:

Iron–sulfur cluster

CIA:

Cytosolic iron–sulfur cluster assembly

qRT-PCR:

Quantitative real-time PCR

ACO:

Aconitase

XDH:

Xanthine dehydrogenase

AO:

Aldehyde oxidase

NiR:

Nitrite reductase

MV:

Methyl viologen

References

  • Balk J, Lobréaux S (2005) Biogenesis of iron–sulfur proteins in plants. Trends Plant Sci 10:324–331

    Article  CAS  PubMed  Google Scholar 

  • Balk J, Pilon M (2011) Ancient and essential: the assembly of iron–sulfur clusters in plants. Trends Plant Sci 16:218–226

    Article  CAS  PubMed  Google Scholar 

  • Bernard DG, Cheng Y, Zhao Y, Balk J (2009) An allelic mutant series of ATM3 reveals its key role in the biogenesis of cytosolic iron–sulfur proteins in Arabidopsis. Plant Physiol 151:590–602

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brear EM, Day DA, Smith PM (2013) Iron: an essential micronutrient for the legume-rhizobium symbiosis. Front Plant Sci 4. doi:10.3389/fpls.2013.00359

  • Dita MA, Rispail N, Prats E, Rubiales D, Singh KB (2006) Biotechnology approaches to overcome biotic and abiotic stress constraints in legumes. Euphytica 147:1–24

    Article  Google Scholar 

  • Grant D, Nelson RT, Cannon SB, Shoemaker RC (2010) SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 38:D843–D846

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guo W, Zhao J, Li X, Qin L, Yan X, Liao H (2011) A soybean β-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant J 66:541–552. doi:10.1111/j.1365-313X.2011.04511.x

    Article  CAS  PubMed  Google Scholar 

  • Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256 (online)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551

    CAS  PubMed  Google Scholar 

  • Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18

    Article  CAS  Google Scholar 

  • Kaiser BN et al (2003) The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport. Plant J 35:295–304

    Article  CAS  PubMed  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 

  • Koiwai H, Akaba S, Seo M, Komano T, Koshiba T (2000) Functional expression of two Arabidopsis aldehyde oxidases in the yeast Pichia pastoris. J Biochem 127:659–664

    Article  CAS  PubMed  Google Scholar 

  • Koshiba T, Saito E, Ono N, Yamamoto N, Sato M (1996) Purification and properties of flavin-and molybdenum-containing aldehyde oxidase from coleoptiles of maize. Plant Physiol 110:781–789

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lancaster JR, Vega J, Kamin H, Orme-Johnson NR, Orme-Johnson WH, Krueger RJ, Siegel LM (1979) Identification of the iron–sulfur center of spinach ferredoxin–nitrite reductase as a tetranuclear center, and preliminary EPR studies of mechanism. J Biol Chem 254:1268–1272

    CAS  PubMed  Google Scholar 

  • Liang X, Qin L, Liu P, Wang M, Ye H (2013) Genes for iron–sulphur cluster assembly are targets of abiotic stress in rice, Oryza sativa. Plant Cell Environ 37:780–794

    Article  PubMed  Google Scholar 

  • Libault M et al (2010) An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J 63:86–99

    CAS  PubMed  Google Scholar 

  • Lill R (2009) Function and biogenesis of iron–sulphur proteins. Nature 460:831–838

    Article  CAS  PubMed  Google Scholar 

  • Mori S (1999) Iron acquisition by plants. Curr Opin Plant Biol 2:250–253

    Article  CAS  PubMed  Google Scholar 

  • Mühlenhoff U, Gerber J, Richhardt N, Lill R (2003) Components involved in assembly and dislocation of iron–sulfur clusters on the scaffold protein Isu1p. EMBO J 22:4815–4825

    Article  PubMed Central  PubMed  Google Scholar 

  • Murthy N et al (2007) Characterization of Arabidopsis thaliana SufE2 and SufE3 functions in chloroplast iron–sulfur cluster assembly and NAD synthesis. J Biol Chem 282:18254–18264

    Article  CAS  Google Scholar 

  • Netz DJ, Mascarenhas J, Stehling O, Pierik AJ, Lill R (2013) Maturation of cytosolic and nuclear iron–sulfur proteins. Trends Cell Biol 24:303–312

    Article  PubMed  Google Scholar 

  • Qin L et al (2012) The high-affinity phosphate transporter GmPT5 regulates phosphate transport to nodules and nodulation in soybean. Plant Physiol 159:1634–1643

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rodríguez-Celma J, Pan IC, Li W, Lan P, Buckhout TJ, Schmidt W (2013) The transcriptional response of Arabidopsis leaves to Fe deficiency. Front Plant Sci 4. doi:10.3389/fpls.2013.00276

  • Roulin A et al (2013) The fate of duplicated genes in a polyploid plant genome. Plant J 73:143–153

    Article  CAS  Google Scholar 

  • Severin AJ et al (2010) RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10:160

    Article  PubMed Central  PubMed  Google Scholar 

  • Takahashi M, Sasaki Y, Ida S, Morikawa H (2001) Nitrite reductase gene enrichment improves assimilation of NO2 in Arabidopsis. Plant Physiol 126:731–741

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tang C, Robson AD, Dilworth MJ (1990) The role of iron in nodulation and nitrogen fixation in Lupinus angustifolius L. New Phytol 114:173–182

    Article  CAS  Google Scholar 

  • Triplett EW, Blevins DG, Randall DD (1982) Purification and properties of soybean nodule xanthine dehydrogenase. Arch Biochem Biophys 219:39–46

    Article  CAS  PubMed  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447. doi:10.1046/j.1469-8137.2003.00695.x

    Article  CAS  Google Scholar 

  • Wang X, Shen J, Liao H (2010) Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Sci 179:302–306

    Article  CAS  Google Scholar 

  • Xu F, Liu Q, Chen L, Kuang J, Walk T, Wang J, Liao H (2013) Genome-wide identification of soybean microRNAs and their targets reveals their organ-specificity and responses to phosphate starvation. BMC Genomics 14:66

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ye H, Pilon M, Pilon-Smits EA (2006) CpNifS-dependent iron–sulfur cluster biogenesis in chloroplasts. New Phytol 171:285–292

    Article  CAS  PubMed  Google Scholar 

  • Zhao J et al (2004) Characterization of root architecture in an applied core collection for phosphorus efficiency of soybean germplasm. Chin Sci Bull 49:1611–1620

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work is supported by the National Natural Science Foundation of China (31301833) and the 100-Talent Program of Chinese Academy of Sciences.

Conflict of interest

The authors declare that have no conflicts of interest.

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Authors and Affiliations

Authors

Corresponding author

Correspondence to Hong Ye.

Additional information

Communicated by Baochun Li.

L. Qin and M. Wang contributed equally to this work.

Electronic supplementary material

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299_2014_1718_MOESM1_ESM.tif

Supplementary Figure S3 Quantitative determination of enzyme activities from the in-gel assays using Image J. Panel (a): quantitative determination of ACO and AO activities in soybean tissues with or without rhizobia inoculation. Panel (b): quantitative determination of ACO and AO activities in soybean tissues with iron deficiency or iron toxicity treatment. Panel (c): quantitative determination of ACO and AO activities in soybean tissues with P deficiency treatment. (TIFF 1,917 kb)

Supplementary material 2 (TIFF 4,449 kb)

Supplementary material 3 (TIFF 9,238 kb)

Supplementary material 4 (DOC 89 kb)

Supplementary Table S2 Genes and gene-specific primers used in the quantitative real-time PCR experiments. (DOC 118 kb)

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Qin, L., Wang, M., Chen, L. et al. Soybean Fe–S cluster biosynthesis regulated by external iron or phosphate fluctuation. Plant Cell Rep 34, 411–424 (2015). https://doi.org/10.1007/s00299-014-1718-0

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  • DOI: https://doi.org/10.1007/s00299-014-1718-0

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