Skip to main content
Log in

Physiological and transcriptional responses in the iron–sulphur cluster assembly pathway under abiotic stress in peach (Prunus persica L.) seedlings

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

As one of the most indispensable element in mineral nutrition of plants, iron (Fe) is closely related to fruits quality and yield. However, molecular mechanisms towards Fe metabolism in fruit trees is largely unclear. In higher plants, iron–sulphur (Fe–S) cluster assembly occurs in chloroplasts, mitochondria and cytosol involving dozens of genes. In this study, we identified 44 putative Fe–S cluster assembly genes in peach (Prunus persica cv. ‘Xiahui6’), and analyzed Fe–S cluster assembly gene expression profiles in response to abiotic stresses. Peach seedlings were more sensitive to iron deficiency, drought and salinity stress, evidenced in reduced photosynthetic performance and altered activity of nitrite reductase, succinate dehydrogenase and aconitase. In addition, Fe–S cluster assembly genes are differentially regulated by abiotic stresses. Iron depletion and drought stress are likely to affect Fe–S cluster assembly genes in leaves. Excess iron toxicity mainly induces Fe–S cluster assembly gene expression in roots, whereas salinity stress massively inhibits Fe–S cluster assembly gene expression in roots. Interestingly, we found that un-functional scaffolds are more prone to disappear during the long-term evolution in perennial woody plants. Our findings directly provide molecular basis for Fe metabolism in peach, and favorably reveal potential candidate genes for further functional determination.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ackrell BA, Kearney EB, Singer TP (1978) Mammalian succinate dehydrogenase. Methods Enzymol 53:466–483

    Article  CAS  PubMed  Google Scholar 

  • Balk J, Lobreaux 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 

  • Bandyopadhyay S, Gama F, Molina-Navarro MM, Gualberto JM, Claxton R, Naik SG, Huynh BH, Herrero E, Jacquot JP, Johnson MK, Rouhier N (2008) Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J 27:1122–1133

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barton LL, Abadia J (2006) Iron nutrition in plants and Rhizospheric microorganisms. Springer, New York, pp 85–101

    Book  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  CAS  PubMed Central  PubMed  Google Scholar 

  • Bernard DG, Netz DJ, Lagny TJ, Pierik AJ, Balk J (2013) Requirements of the cytosolic iron–sulfur cluster assembly pathway in Arabidopsis. Philos Trans R Soc Lond B Biol Sci 368:20120259

    Article  PubMed  Google Scholar 

  • Busi 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 J 48:873–882

    Article  CAS  PubMed  Google Scholar 

  • Bych K, Kerscher S, Netz DJ, Pierik AJ, Zwicker K, Huynen MA, Lill R, Brandt U, Balk J (2008) The iron–sulphur protein Ind1 is required for effective complex I assembly. EMBO J 27:1736–1746

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen S, Sanchez-Fernandez R, Lyver ER, Dancis A, Rea PA (2007) Functional characterization of AtATM1, AtATM2, and AtATM3, a subfamily of Arabidopsis half-molecule ATP-binding cassette transporters implicated in iron homeostasis. J Biol Chem 282:21561–21571

    Article  CAS  PubMed  Google Scholar 

  • Cheng NH, Liu JZ, Brock A, Nelson RS, Hirschi KD (2006) AtGRXcp, an Arabidopsis chloroplastic glutaredoxin, is critical for protection against protein oxidative damage. J Biol Chem 281:26280–26288

    Article  CAS  PubMed  Google Scholar 

  • Ciesielski SJ, Schilke BA, Osipiuk J, Bigelow L, Mulligan R, Majewska J, Joachimiak A, Marszalek J, Craig EA, Dutkiewicz R (2012) Interaction of J-protein co-chaperone Jac1 with Fe-S scaffold Isu is indispensable in vivo and conserved in evolution. J Mol Biol 417:1–12

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Colla G, Roupahel Y, Cardarelli M (2006) Effect of salinity on yield, fruit quality, leaf gas exchange, and mineral composition of grafted watermelon plants. HortScience 41:622–627

    CAS  Google Scholar 

  • Couturier J, Touraine B, Briat JF, Gaymard F, Rouhier N (2013) The iron–sulfur cluster assembly machineries in plants: current knowledge and open questions. Front Plant Sci 24:00259

    Google Scholar 

  • Crisosto CH, Johnson RS, Luza JG, Crisosto GM (1994) Irrigation regimes affect fruit soluble solids concentration and rate of water loss of ‘O’Henry’ peaches. HortScience 29:1169–1171

    Google Scholar 

  • Gelling C, Dawes IW, Richhardt N, Lill R, Muhlenhoff U (2008) Mitochondrial Iba57p is required for Fe/S cluster formation on aconitase and activation of radical SAM enzymes. Mol Cell Biol 28:1851–1861

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gerber J, Muhlenhoff U, Lill R (2003) An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep 4:906–911

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron–sulfur clusters. Ann Rev Biochem 74:247–281

    Article  CAS  PubMed  Google Scholar 

  • Jung S, Staton M, Lee T, Blenda A, Svancara R, Abbott A, Main D (2008) GDR (Genome Database for Rosaceae): integrated web-database for Rosaceae genomics and genetics data. Nucleic Acids Res 36:D1034–D1040

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kennedy MC, Emptage MH, Dreyer JL, Beinert H (1983) The role of iron in the activation-inactivation of aconitase. J Biol Chem 258:11098–11105

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kumar N, Kumar S, Vats SK, Ahuja PS (2006) Effect of altitude on the primary products of photosynthesis and the associated enzymes in barley and wheat. Photosynth Res 88:63–71

    Article  CAS  PubMed  Google Scholar 

  • Leon S, Touraine B, Ribot C, Briat JF, Lobreaux S (2003) Iron–sulphur cluster assembly in plants: distinct NFU proteins in mitochondria and plastids from Arabidopsis thaliana. Biochem J 371:823–830

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lezhneva L, Amann K, Meurer J (2004) The universally conserved HCF101 protein is involved in assembly of [4Fe-4S]-cluster-containing complexes in Arabidopsis thaliana chloroplasts. Plant J 37:174–185

    Article  CAS  PubMed  Google Scholar 

  • Liang XJ, Qin L, Liu PW, Wang MH, Ye H (2013) Genes for iron–sulphur cluster assembly are targets of abiotic stress in rice, Oryza sativa. Plant Cell Environ 37:780. doi:10.1111/pce.12198

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lill R, Muhlenhoff U (2006) Iron–sulfur protein biogenesis in eukaryotes: components and mechanisms. Ann Rev Cell Dev Biol 22:457–486

    Article  CAS  Google Scholar 

  • Lill R, Muhlenhoff U (2008) Maturation of iron–sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Ann Rev Biochem 77:669–700

    Article  CAS  PubMed  Google Scholar 

  • Lu RK (2000) Analytical methods of soil and agricultural chemistry. Beijing: China Agricultural Science and Technology. pp. 191–196. [in Chinese]

  • Luo D, Bernard DG, Balk J, Hai H, Cui X (2012) The DUF59 family gene AE7 acts in the cytosolic iron–sulfur cluster assembly pathway to maintain nuclear genome integrity in Arabidopsis. Plant Cell 24:4135–4148

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mendlinger S (1994) Effect of increasing plant density and salinity on yield and fruit quality in muskmelon. Sci Hortic 57:41–49

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Murthy NUM, Ollagnier-de-Choudens S, Sanakis Y, Abdel-Ghany SE, Rousset C, Ye H, Fontecave M, Pilon-Smits EAH, Pilon M (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 

  • Ozturk ZN, Talame V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought-and salt-stressed barley. Plant Mol Biol 48:551–573

    Article  CAS  Google Scholar 

  • Pal AK, Acharya K, Vats SK, Kumar S, Ahuja PS (2013) Over-expression of PaSOD in transgenic potato enhances photosynthetic performance under drought. Biol Plantarum 57:359–364

    Article  CAS  Google Scholar 

  • Palmer CM, Guerinot ML (2009) Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol 5:333–340

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pestana M, Beja P, Correia PJ, Varennes AD, Faria EA (2005) Relationships between nutrient composition of flowers and fruit quality in orange trees grown in calcareous soil. Tree Physiol 25:761–767

    Article  CAS  PubMed  Google Scholar 

  • Picciocchi A, Douce R, Alban C (2003) The plant biotin synthase reaction. Identification and characterization of essential mitochondrial accessory protein components. J Biol Chem 278:24966–24975

    Article  CAS  PubMed  Google Scholar 

  • Pilon-Smits EA, Garifullina GF, Abdel-Ghany S, Kato S, Mihara H, Hale KL, Burkhead JL, Esaki N, Kurihara T, Pilon M (2002) Characterization of a NifS-like chloroplast protein from Arabidopsis. Implications for its role in sulfur and selenium metabolism. Plant Physiol 130:1309–1318

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raulfs EC, O’Carroll IP, Dos Santos PC, Unciuleac MC, Dean DR (2008) In vivo iron–sulfur cluster formation. Proc Natl Acad Sci USA 105:8591–8596

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rouault TA, Tong WH (2008) Iron–sulfur cluster biogenesis and human disease. Trends Genet 24:398–407

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schwenkert S, Netz DJ, Frazzon J, Pierik AJ, Bill E, Gross J, Lill R, Meurer J (2010) Chloroplast HCF101 is a scaffold protein for [4Fe–4S] cluster assembly. Biochem J 425:207–214

    Article  CAS  PubMed Central  Google Scholar 

  • Sheftel AD, Stehling O, Pierik AJ, Netz DJ, Kerscher S, Elsasser HP, Wittig I, Balk J, Brandt U, Lill R (2009) Human ind1, an iron–sulfur cluster assembly factor for respiratory complex I. Mol Cell Biol 29:6059–6073

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sheftel AD, Wilbrecht C, Stehling O, Niggemeyer B, Elsasser HP, Muhlenhoff U, Lill R (2012) The human mitochondrial ISCA1, ISCA2, and IBA57 proteins are required for [4Fe-4S] protein maturation. Mol Biol Cell 23:1157–1166

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stehling O, Vashisht AA, Mascarenhas J, Jonsson ZO, Sharma T, Netz DJA, Pierik AJ, Wohlschlegel JA, Lill R (2012) MMS19 assembles iron–sulfur proteins required for DNA metabolism and genomic integrity. Science 337:195–199

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stockel J, Oelmuller R (2004) A novel protein for photosystem I biogenesis. J Biol Chem 279:10243–10251

    Article  PubMed  Google Scholar 

  • Tagliavini M, Rombolà AD (2001) Iron deficiency and chlorosis in orchard and vineyard ecosystems. Eur J Agron 15:72–92

    Article  Google Scholar 

  • Tagliavini M, Abadía J, Rombolà AD, Abadía A, Tsipouridis C, Marangoni B (2000) Agronomic means for the control of iron deficiency chlorosis in deciduous fruit trees. J Plant Nutr 23:2007–2022

    Article  CAS  Google Scholar 

  • Takahashi M, Sasaki Y, Ida S, Morikawa H (2001) Nitrite reductase gene enrichment improves assimilation of NO(2) in Arabidopsis. Plant Physiol 126:731–741

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Takubo K, Morikawa T, Nonaka Y, Mizutani M, Takenaka S, Takabe K, Takahashi MA, Ohta D (2003) Identification and molecular characterization of mitochondrial ferredoxins and ferredoxin reductase from Arabidopsis. Plant Mol Biol 52:817–830

    Article  CAS  PubMed  Google Scholar 

  • Tone Y, Kawai-Yamada M, Uchimiya H (2004) Isolation and characterization of Arabidopsis thaliana ISU1 gene. Biochim Biophys Acta 1680:171–175

    Article  CAS  PubMed  Google Scholar 

  • Turowski VR, Busi MV, Gomez-Casati DF (2012) Structural and functional studies of the mitochondrial cysteine desulfurase from Arabidopsis thaliana. Mol Plant 5:1001–1010

    Article  CAS  PubMed  Google Scholar 

  • Vazzola V, Losab A, Soavea C, Murgiaa I (2007) Knockout of frataxin gene causes embryo lethality in Arabidopsis. FEBS Lett 581:667–672

    Article  CAS  PubMed  Google Scholar 

  • Vickery LE, Cupp-Vickery JR (2007) Molecular chaperones HscA/Ssq1 and HscB/Jac1 and their roles in iron–sulfur protein maturation. Crit Rev Biochem Mol Biol 42:95–111

    Article  CAS  PubMed  Google Scholar 

  • Xu XM, Møller SG (2006) AtSufE is an essential activator of plastidic and mitochondrial desulfurases in Arabidopsis. EMBO J 25:900–909

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yadav S, Kushwaha HR, Kumar K, Verma PK (2012) Comparative structural modeling of a monothiol GRX from chickpea: insight in iron–sulfur cluster assembly. Int J Biol Macromol 51:266–273

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ye H, Abdel-Ghany SE, Anderson TD, Pilon-Smits EA, Pilon M (2006b) CpSufE activates the cysteine desulfurase CpNifS for chloroplastic Fe–S cluster formation. J Biol Chem 273:13264–13272

    Google Scholar 

Download references

Acknowledgments

We are grateful to Prof. Hong Ye, South China Botanical Garden, Chinese Academy of Sciences, for sincere help during the studies in SCBG. This work was financially supported by grants from China Agriculture Resarch System (CAR-31).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mingliang Yu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11240_2014_452_MOESM1_ESM.doc

Phenotypes and dry weights of peach seedlings after stress treatments. Seedlings were suffered to different treatment for 21 d before examination. (a) Seedlings after iron depletion and excess iron stress. (b) Seedlings after iron depletion and excess iron stress. (c) Seedlings after iron depletion and excess iron stress. Data are random representatives of six independent replicates. (DOC 115 kb)

Supplementary material 2 (JPEG 1367 kb)

Supplementary material 3 (DOC 135 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, Z., Yang, Y., Xu, J. et al. Physiological and transcriptional responses in the iron–sulphur cluster assembly pathway under abiotic stress in peach (Prunus persica L.) seedlings. Plant Cell Tiss Organ Cult 117, 419–430 (2014). https://doi.org/10.1007/s11240-014-0452-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-014-0452-1

Keywords

Navigation