Abstract
Iron (Fe) is a crucial micronutrient in plant metabolism; thus, iron homeostasis is critical for plant development. Permease in chloroplast 1 (PIC1) is the first protein determined in the chloroplast playing a role iron homeostasis. In the present study, the PIC1 gene was investigated at a genome-wide scale in four plant genomes; Arabidopsis, tomato, maize and sorghum. Based on the gene ontology database, 21 GO terms were found related to the PIC1 gene, most of which were involved in iron hemostasis and transport. The digital expression data revealed that the expression of the majority of PIC1 genes (62.5%) in Arabidopsis decreased under abiotic stress conditions. Expression profiles of tomato PIC1 (SlPIC1) and sorghum PIC1 (SbPIC1) genes were also analyzed under salt and drought stress conditions using Real Time-quantitative PCR (RT-qPCR). Our wet-lab studies demonstrated that the SbPIC1 gene was down-regulated under salt and drought stresses in all tissues, while SlPIC1 was up-regulated in all but root tissue under drought stress. Some structural variations were detected in predicted 3D structures of PIC1 proteins and the structural similarity values varied between 0.23 and 0.35. Consequently, these results may contribute to the understanding of the PIC1 gene in iron transport and homeostasis in plants.
Similar content being viewed by others
References
Ashburner M et al (2000) Gene ontology: tool for the unification of biology: the gene ontology consortium. Nat Genet 25:25–29. https://doi.org/10.1038/75556
Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME Suite. Nucleic Acids Res 43:W39–49. https://doi.org/10.1093/nar/gkv416
Balk J, Pilon M (2011) Ancient and essential: the assembly of iron-sulfur clusters in plants. Trends Plant Sci 16:218–226. https://doi.org/10.1016/j.tplants.2010.12.006
Balk J, Schaedler TA (2014) Iron cofactor assembly in plants. Annu Rev Plant Biol 65:125–153. https://doi.org/10.1146/annurev-arplant-050213-035759
Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442. https://doi.org/10.1146/annurev-arplant-050213-040159
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297
Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351–1362. https://doi.org/10.1006/jmbi.1999.3310
Blom N, Sicheritz-Ponten T, Gupta R, Gammeltoft S, Brunak S (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4:1633–1649. https://doi.org/10.1002/pmic.200300771
Bobik K, Burch-Smith TM (2015) Chloroplast signaling within, between and beyond cells. Front Plant Sci 6:781. https://doi.org/10.3389/fpls.2015.00781
Briat JF, Dubos C, Gaymard F (2015) Iron nutrition, biomass production, and plant product quality. Trends Plant Sci 20(1):33–40. https://doi.org/10.1016/j.tplants.2014.07.005
Bruce BD (2000) Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol 10(10):440–447
Calvino M, Bruggmann R, Messing J (2011) Characterization of the small RNA component of the transcriptome from grain and sweet sorghum stems. BMC Genomics 12:356. https://doi.org/10.1186/1471-2164-12-356
Cantu D, Blanco-Ulate B, Yang L, Labavitch JM, Bennett AB, Powell AL (2009) Ripening-regulated susceptibility of tomato fruit to Botrytis cinerea requires NOR but not RIN or ethylene. Plant Physiol 150:1434–1449. https://doi.org/10.1104/pp.109.138701
Collakova E, DellaPenna D (2003) Homogentisate phytyltransferase activity is limiting for tocopherol biosynthesis in Arabidopsis. Plant Physiol 131:632–642. https://doi.org/10.1104/pp.015222
Curie C et al (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103(1):1–11. https://doi.org/10.1093/aob/mcn207
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159. https://doi.org/10.1093/nar/gkr319
Duy D, Wanner G, Meda AR, von Wiren N, Soll J, Philippar K (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19(3):986–1006. https://doi.org/10.1105/tpc.106.047407
Duy D, Stube R, Wanner G, Philippar K (2011) The chloroplast permease PIC1 regulates plant growth and development by directing homeostasis and transport of iron. Plant Physiol 155(4):1709–1722. https://doi.org/10.1104/pp.110.170233
Eklund H, Gleason FK, Holmgren A (1991) Structural and functional relations among thioredoxins of different species. Proteins 11:13–28. https://doi.org/10.1002/prot.340110103
Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8(5):978–984. https://doi.org/10.1110/ps.8.5.978
Eudes A et al (2010) Identification of transport-critical residues in a folate transporter from the folate-biopterin transporter (FBT) family. J Biol Chem 285(4):2867–2875. https://doi.org/10.1074/jbc.m109.063651
Friso G, van Wijk KJ (2015) Posttranslational protein modifications in plant metabolism. Plant Physiol 169:1469–1487. https://doi.org/10.1104/pp.15.01378
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915–925
Fukao Y (2012) Protein-protein interactions in plants. Plant Cell Physiol 53:617–625. https://doi.org/10.1093/pcp/pcs026
Geourjon C, Deleage G (1995) SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput Appl Biosci 11(6):681–684
Ghasemi S, Khoshgoftarmanesh AH, Afyuni M, Hadadzadeh H (2014) Iron (II)–amino acid chelates alleviate salt-stress induced oxidative damages on tomato grown in nutrient solution culture. Sci Hortic 165:91–98
Giri A, Heckathorn S, Mishra S, Krause C (2017) Heat stress decreases levels of nutrient-uptake and -assimilation proteins in tomato roots. Plants 6(1):6. https://doi.org/10.3390/plants6010006
Gong X, Guo C, Terachi T, Cai H, Yu D (2015) Tobacco PIC1 mediates iron transport and regulates chloroplast development. Plant Mol Biol Rep 33(3):401–413
Goodstein DM et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186. https://doi.org/10.1093/nar/gkr944
Gould SB, Waller RR, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517. https://doi.org/10.1146/annurev.arplant.59.032607.092915
Goupil P, Souguir D, Ferjani E, Faure O, Hitmi A, Ledoigt G (2009) Expression of stress-related genes in tomato plants exposed to arsenic and chromium in nutrient solution. J Plant Physiol 166:1446–1452. https://doi.org/10.1016/j.jplph.2009.01.015
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series. Information Retrieval Ltd., London, pp 95–98
Harrison C (2003) GrpE, a nucleotide exchange factor for DnaK. Cell Stress Chaperones 8(3):218–224
Hashiguchi A, Komatsu S (2016) Impact of post-translational modifications of crop proteins under abiotic stress. Proteomes 4(4):42. https://doi.org/10.3390/proteomes4040042
Hatzfeld Y, Saito K (2000) Evidence for the existence of rhodanese (thiosulfate:cyanide sulfurtransferase) in plants: preliminary characterization of two rhodanese cDNAs from Arabidopsis thaliana. FEBS Lett 470(2):147–150
Hruz T et al (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform 2008:420747. https://doi.org/10.1155/2008/420747
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Jeong J, Guerinot ML (2009) Homing in on iron homeostasis in plants. Trends Plant Sci 14:280–285. https://doi.org/10.1016/j.tplants.2009.02.006
Ji YY, Li YQ (2010) The role of secondary structure in protein structure selection. Eur Phys J 32:103–107. https://doi.org/10.1140/epje/i2010-10591-5
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282
Kanai S, Kikuno R, Toh H, Ryo H, Todo T (1997) Molecular evolution of the photolyase-blue-light photoreceptor family. J Mol Evol 45:535–548
Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371. https://doi.org/10.1038/nprot.2009.2
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis Version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Leister D (2003) Chloroplast research in the genomic age. Trends Genet 19:47–56
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402–408
Lopez-Millan AF, Duy D, Philippar K (2016) Chloroplast iron transport proteins—function and impact on plant physiology. Front Plant Sci 7:178. https://doi.org/10.3389/fpls.2016.00178
Makita Y, Shimada S, Kawashima M, Kondou-Kuriyama T, Toyoda T, Matsui M (2015) MOROKOSHI: transcriptome database in Sorghum bicolor. Plant Cell Physiol 56(1):e6. https://doi.org/10.1093/pcp/pcu187
Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57
Nazar R, Iqbal N, Masood A, Syeed S, Khan NA (2011) Understanding the significance of sulfur in improving salinity tolerance in plants. Environ Exp Bot 70:80–87
Obayashi T, Aoki Y, Tadaka S, Kagaya Y, Kinoshita K (2017) ATTED-II in 2018: a plant coexpression database based on investigation of the statistical property of the mutual rank index. Plant Cell Physiol 59(1):e3
Ozaki S et al (2010) Coexpression analysis of tomato genes and experimental verification of coordinated expression of genes found in a functionally enriched coexpression module. DNA Res 17:105–116. https://doi.org/10.1093/dnares/dsq002
Petrillo E et al (2014) A chloroplast retrograde signal regulates nuclear alternative splicing. Science 344:427–430. https://doi.org/10.1126/science.1250322
Rasmussen S et al (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol 161:1783–1794. https://doi.org/10.1104/pp.112.210773
Raven JA, Evans MC, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60(2–3):111–150
Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697. https://doi.org/10.1038/17800
Rouhier N et al (2007) Functional, structural, and spectroscopic characterization of a glutathione-ligated [2Fe-2S] cluster in poplar glutaredoxin C1. Proc Natl Acad Sci USA 104(18):7379–7384. https://doi.org/10.1073/pnas.0702268104
Saito H, Kashida S, Inoue T, Shiba K (2007) The role of peptide motifs in the evolution of a protein network. Nucleic Acids Res 35:6357–6366. https://doi.org/10.1093/nar/gkm692
Santi S, Cesco S, Varanini Z, Pinton R (2005) Two plasma membrane H(+)-ATPase genes are differentially expressed in iron-deficient cucumber plants. Plant Physiol Biochem 43(3):287–292. https://doi.org/10.1016/j.plaphy.2005.02.007
Sattler SE, Cahoon EB, Coughlan SJ, DellaPenna D (2003) Characterization of tocopherol cyclases from higher plants and cyanobacteria. Evolutionary implications for tocopherol synthesis and function. Plant Physiol 132:2184–2195
Scandalios JG (1990) Response of plant antioxidant defense genes to environmental stress. Adv Genet 28:1–41
Schmid M et al (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506. https://doi.org/10.1038/ng1543
Schnell DJ, Blobel G, Keegstra K, Kessler F, Ko K, Soll J (1997) A consensus nomenclature for the protein-import components of the chloroplast envelope. Trends Cell Biol 7:303–304. https://doi.org/10.1016/S0962-8924(97)01111-2
Shi R, Weber G, Koster J, Reza-Hajirezaei M, Zou C, Zhang F, von Wiren N (2012) Senescence-induced iron mobilization in source leaves of barley (Hordeum vulgare) plants. New Phytol 195(2):372–383. https://doi.org/10.1111/j.1469-8137.2012.04165.x
Sjögren LL, Stanne TM, Zheng B, Sutinen S, Clarke AK (2006) Structural and functional insights into the chloroplast ATP-dependent Clp protease in Arabidopsis. Plant Cell 18:2635–2649
Stacey MG et al (2008) The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol 146(2):589–601. https://doi.org/10.1104/pp.107.108183
Sudhakar Reddy P, Srinivas Reddy D, Sivasakthi K, Bhatnagar-Mathur P, Vadez V, Sharma KK (2016) Evaluation of sorghum [Sorghum bicolor (L.)] reference genes in various tissues and under abiotic stress conditions for quantitative real-time PCR data normalization. Front Plant Sci 7:529
Swami AK, Alam SI, Sengupta N, Sarin R (2011) Differential proteomic analysis of salt stress response in Sorghum bicolor leaves. Environ Exp Bot 71:321–328
Szklarczyk D et al (2017) The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res 45:D362–D368. https://doi.org/10.1093/nar/gkw937
Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tanoue R, Kobayashi M, Katayama K, Nagata N, Wada H (2014) Phosphatidylglycerol biosynthesis is required for the development of embryos and normal membrane structures of chloroplasts and mitochondria in Arabidopsis. FEBS Lett 588:1680–1685
Tripathi DK et al (2018) Acquisition and homeostasis of iron in higher plants and their probable role in abiotic stress tolerance. Front Environ Sci 5:86
Tusnady GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849–850
Wada H, Murata N (2007) The essential role of phosphatidylglycerol in photosynthesis. Photosynth Res 92:205–215. https://doi.org/10.1007/s11120-007-9203-z
Watterson G (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276
Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552
Zhang Y, Skolnick J (2005) TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res 33(7):2302–2309. https://doi.org/10.1093/nar/gki524
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Filiz, E., Aydın Akbudak, M. Investigation of PIC1 (permease in chloroplasts 1) gene’s role in iron homeostasis: bioinformatics and expression analyses in tomato and sorghum. Biometals 33, 29–44 (2020). https://doi.org/10.1007/s10534-019-00228-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10534-019-00228-x