Functional & Integrative Genomics

, Volume 19, Issue 1, pp 75–90 | Cite as

Genome-wide analysis of oligopeptide transporters and detailed characterization of yellow stripe transporter genes in hexaploid wheat

  • Anil Kumar
  • Gazaldeep Kaur
  • Parul Goel
  • Kaushal Kumar Bhati
  • Mandeep Kaur
  • Vishnu Shukla
  • Ajay Kumar PandeyEmail author
Original Article


Oligopeptide transporters (OPT) are integral cell membrane proteins that play a critical role in the transport of small peptides, secondary amino acids, glutathione conjugates, and mineral uptake. In the present study, 67 putative wheat yellow stripe-like transporter (YSL) proteins belonging to the subfamily of OPT transporters were identified. Phylogeny analysis resulted in the distribution of wheat YSLs into four discrete clades. The highest number of YSLs was present on the A genome and the chromosome 2 of hexaploid wheat. The identified wheat YSL genes showed differential expression in different tissues and during grain development suggesting the importance of this subfamily. Gene expression pattern of TaYSLs during iron starvation experiments suggested an early high transcript accumulation of TaYS1A, TaYS1B, TaYSL3, TaYSL5, and TaYSL6 in roots. In contrast, delayed expression was observed in shoots for TaYS1A, TaYS1B, TaYSL5, TaYSL12, and TaYSL19 as compared to control. Further, their expression under biotic and abiotic response emphasized their alternative functions during the plant growth and development. In conclusion, this work is the first comprehensive study of wheat YSL transporters and would be an important resource for prioritizing genes towards wheat biofortification.


Triticum aestivum Yellow stripe-like transporters Iron transport Biofortification Iron starvation 



The authors would like to thank the Executive Director, NABI, for facilities and support. The authors also thank Mr. Shrikant Mantri for discussion pertaining to bioinformatics work.

Funding information

This research was funded by the NABI-CORE grant to AKP and partial support from DST-SERB grant (PDF/2016/001355) to PG. AK and GK acknowledge NABI-JRF Fellowships. PG thanks DST-SERB grant for fellowship.

Supplementary material

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  1. Aggarwal S, Kumar A, Bhati KK, Kaur G, Shukla VK, Tiwari S, Pandey AK (2018) RNAi-mediated downregulation of inositol pentakisphosphate kinase (IPK1) in wheat grains decreases phytic acid levels and increases Fe and Zn accumulation. Front Plant Sci.
  2. Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373CrossRefGoogle Scholar
  3. Banakar R, Fernandez AA, Abadia J, Capell T, Christou P (2017) The expression of heterologous Fe (III) phytosiderophore transporter HvYS1 in rice increases Fe uptake, translocation and seed loading and excludes heavy metals by selective Fe transport. Plant Biotechnol J 15(4):423–432CrossRefGoogle Scholar
  4. Bhati KK, Aggarwal S, Sharma S, Mantri S, Singh SP, Bhalla S, Kaur J, Tiwari S, Roy JK, Tuli R, Pandey AK (2014) Differential expression of structural genes for the late phase of phytic acid biosynthesis in developing seeds of wheat (Triticumaestivum L.). Plant Sci 224:74–85CrossRefGoogle Scholar
  5. Bhati KK, Alok A, Kumar A, Kaur J, Tiwari S, Pandey AK (2016) Silencing of ABCC13 transporter in wheat reveals its involvement in grain development, phytic acid accumulation and lateral root formation. J Exp Bot 67:4379–4389CrossRefGoogle Scholar
  6. Bhatnagar T, Sachdev A, Johari RP (2002) Molecular characterization of glutenins in wheat varieties differing in chapatti quality characteristics. J Plant Biochem & Biotech 11:33–36CrossRefGoogle Scholar
  7. Borg S, Brinch-Pedersen H, Tauris B, Holm P (2009) Iron transport, deposition and bioavailability in the wheat and barley grain. Plant Soil 325:15–24CrossRefGoogle Scholar
  8. Borrill P, Connorton JM, Balk J, Miller AJ, Sanders D, Uauy C (2014) Biofortification of wheat grain with iron and zinc: integrating novel genomic resources and knowledge from model crops. Front Plant Sci 5:53CrossRefGoogle Scholar
  9. Borrill P, Ramirez-Gonzalez R, Uauy C (2016) expVIP: a customizable RNA-seq data analysis and visualization platform. Plant Physiol 170:2172–2186CrossRefGoogle Scholar
  10. Castaings L, Caquot A, Loubet S, Curie C (2016) The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision. Sci Rep 6:37222CrossRefGoogle Scholar
  11. Chen CC, Chien WF, Lin NC, Yeh KC (2014) Alternative functions of Arabidopsis YELLOW STRIPE-LIKE3: from metal translocation to pathogen defense. PLoSOne 9:e98008CrossRefGoogle Scholar
  12. Choulet F, Albert A, Theil S, Glover N, Barbe V, Daron J, Pingault L, Sourdille P, Couloux A, Paux E et al (2014) Structural and functional partitioning of bread wheat chromosome 3B. Science 345:1249721CrossRefGoogle Scholar
  13. Connorton JM, Balk J, Rodríguez-Celma J (2017a) Iron homeostasis in plants – a brief overview. Metallomics 9:813–823CrossRefGoogle Scholar
  14. Connorton JM, Jones ER, Rodríguez-Ramiro I, Fairweather-Tait S, Uauy C, Balk J (2017b) Vacuolar Iron transporter TaVIT2 transports Fe and Mn and is 7 effective for biofortification. Plant Physiol 174:2434–2444CrossRefGoogle Scholar
  15. Curie C, Cassin G, Couch D, Divol F, Higuchi K, Le Jean M, Misson J, Schikora A, Czernic P, Mari S (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103(1):1–11CrossRefGoogle Scholar
  16. 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 409:346–349CrossRefGoogle Scholar
  17. DiDonato RJ, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidopsis yellow stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 39:403–414CrossRefGoogle Scholar
  18. Feng S, Tan J, Zhang Y, Liang S, Xiang S, Wang H, Chai T (2017) Isolation and characterization of a novel cadmium-regulated yellow stripe-like transporter (SnYSL3) in Solanumnigrum. Plant Cell Rep 36:281–296CrossRefGoogle Scholar
  19. Gendre D, Czernic P, Conejero G, Pianelli K, Briat JF, Lebrun M, Mari S (2007) TcYSL3, a member of the YSL gene family from the hyperaccumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. Plant J 49:1–15CrossRefGoogle Scholar
  20. Gross J, Stein RJ, Fett-Neto AG, Fett JP (2003) Iron homeostasis related genes in rice. Genet MolBiol 26:477–497Google Scholar
  21. Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29:1023–1026CrossRefGoogle Scholar
  22. Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. CalifAgrExptStaCirc 347Google Scholar
  23. Hoehenwarter W, Monchgesang S, Neumann S, Majovsky P, Abel S, Muller J (2016) Comparative expression profiling reveals a role of the root apoplast in local phosphate response. BMC Plant Biol 16:106CrossRefGoogle Scholar
  24. Horton P, Park KJ, Obyashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT protein localization predictor. Nucleic Acids Res 35:W585–W587CrossRefGoogle Scholar
  25. Hu YT, Ming F, Chen WW, Yan JY, Xu ZY, Li GX, Xu CY, Yang JL, Zheng SJ (2012) TcOPT3, a member of oligopeptide transporters from the hyperaccumulator Thlaspi caerulescens, is a novel Fe/Zn/cd/cu transporter. PLoS One 6:e38535CrossRefGoogle Scholar
  26. 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 BiolChem 284:3470–3479Google Scholar
  27. Ishimaru Y, Masuda H, Bashir K, Inoue H, Tsukamoto T, Takahashi M, Nakanishi H, Aoki N, Hirose T, Ohsugi R, Nishizawa NK (2010) Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J 62:379–390CrossRefGoogle Scholar
  28. Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation and regulation in higher plants. Annu Rev Plant Biol 63:131–152CrossRefGoogle Scholar
  29. Koh S, Wiles AM, Sharp JS, Naider FR, Becker JM, Stacey G (2002) An oligopeptide transporter gene family in Arabidopsis. Plant Physiol 128:21–29CrossRefGoogle Scholar
  30. 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 39:415–424CrossRefGoogle Scholar
  31. Krishnaapa G, Singh AM, Chaudhary S (2017) Molecular mapping of the grain iron and zinc concentration, protein content and thousand kernel weight in wheat (Triticumaestivum L.). PLoS One 12:e0174972CrossRefGoogle Scholar
  32. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645CrossRefGoogle Scholar
  33. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7. 0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  34. Lan P, Li W, Wen TN, Schmidt W (2012) Quantitative phosphoproteome profiling of iron-deficient Arabidopsis roots. Plant Physiol 159:403–417CrossRefGoogle Scholar
  35. Le Jean M, 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 44:769–782CrossRefGoogle Scholar
  36. Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150:786–800CrossRefGoogle Scholar
  37. Liu T, Zeng J, Xia K, Fan T, Li Y, Wang Y, Xu X, Zhang M (2012) Evolutionary expansion and functional diversification of oligopeptide transporter gene family in rice. Rice 5:12CrossRefGoogle Scholar
  38. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408CrossRefGoogle Scholar
  39. Lopez-Millan AF, Duy D, Philippar K (2016) Chloroplast iron transport proteins - function and impact on plant physiology. Front Plant Sci 7:178CrossRefGoogle Scholar
  40. Lubkowitz M (2011) The oligopeptide transporters: a small gene family with a diverse group of substrates and functions? Mol Plant 4:407–415CrossRefGoogle Scholar
  41. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI et al (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43:D222–D226CrossRefGoogle Scholar
  42. Mori S, Nishizawa N (1987) Methionine as a dominant precursor of phytosiderophores in graminaceae plants. Plant Cell Physiol 28:1081–1092Google Scholar
  43. Morrissey J, Guerinot ML (2009) Iron uptake and transport in plants: the good, the bad, and the ionome. Chem Rev 109:4553–4567CrossRefGoogle Scholar
  44. Murata Y, Ma JF, Yamaji N, Ueno D, Nomoto K, Iwashita T (2006) A specific transporter for iron(III)–phytosiderophore in barley roots. Plant J 46:563–572CrossRefGoogle Scholar
  45. Ogo Y, Itai RN, 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):366–377CrossRefGoogle Scholar
  46. Oono Y, Kobayashi F, Kawahara Y, Yazawa T, Handa H, Itoh T, Matsumoto T (2013) Characterisation of the wheat (triticumaestivum L.) transcriptome by de novo assembly for the discovery of phosphate starvation-responsive genes: gene expression in Pi-stressed wheat. BMC genomics 14:77CrossRefGoogle Scholar
  47. Pearce S, Tabbita F, Cantu D, Buffalo V, Avni R, Vazquez-Gross H, Zhao R, Conley JC, Distelfeld A, Dubcovksy J (2014) Regulation of Zn and Fe transporters by the GPC1 gene during early wheat monocarpic senescence. BMC Plant Biol 14:368CrossRefGoogle Scholar
  48. Pearce S, Vazquez-Gross S, Herin SY, Hane D, Wang Y, Gu YQ, Dubcovsky J (2015) WheatExp: an RNA-seq expression database for polyploid wheat. BMC Plant Biol 15:299CrossRefGoogle Scholar
  49. Pfeifer M, Kugler KG, Sandve SR, Zhan B, Rudi H, Hvidsten TR (2014) Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345:1250091CrossRefGoogle Scholar
  50. Saenchai C, Bouain N, Kisko M, Prom-u-thai C, Doumas P, Rouached H (2015) The involvement of OsPHO1;1 in the regulation of iron transport through integration of phosphate and zinc deficiency signaling. Front Plant Sci 28(6):290Google Scholar
  51. Santi S, Cesco S, Varanini Z, Pinton R (2005) Two plasma membrane H+-ATPase genes are differentially expressed in iron-deficient cucumber plants. Plant PhysiolBiochem 43:287–292Google Scholar
  52. Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton exclusion in Arabidopsis roots. New Phytol 183:1072–1084CrossRefGoogle Scholar
  53. Sasaki A, Yamaji N, Xia J, Ma JF (2011) OsYSL6 is involved in the detoxification of excess manganese in rice. Plant Physiol 157:1832–1840CrossRefGoogle Scholar
  54. Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, vonWiren N (2004) ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J BiolChem 279:9091–9096Google Scholar
  55. Singh SP, Keller B, Gruissem W, Bhullar NK (2017) Rice NICOTIANAMINE SYNTHASE 2 expression improves dietary iron and zinc levels in wheat. TheorAppl Genet 130:283–292CrossRefGoogle Scholar
  56. Sperotto RA, Boffa T, Duartea GL, Santos LS, Grusak MA, Fett JP (2010) Identification of putative target genes to manipulate Fe and Zn concentrations in rice grains. J Plant Physiol 167:1500–1506CrossRefGoogle Scholar
  57. Stacey MG, Osawa H, Patel A, Gassmann G, Stacey G (2006) Expression analysis of Arabidopsis oligopeptide transporters during seed germination, vegetative growth and reproduction. Planta 223:291–305CrossRefGoogle Scholar
  58. Sui X, Zhao Y, Wang S, Duan X, Xu L, Liang R (2012) Improvement Fe content of wheat (Triticumaestivum) grain by soybean ferritin expression cassette without vector backbone sequence. J AgricBiotechnol 20:766–773Google Scholar
  59. Upadhyaya HD, Bajaj D, Das S, Kuma V, Gowda CLL, Sharma S, Tyagi AK, Parida SK (2016) Genetic dissection of seed-iron and zinc concentrations in chickpea. Sci Rep 6:24050CrossRefGoogle Scholar
  60. Wasaki J, Yonetani R, Kuroda S. Shinano T, Yazaki J, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, et al. 2003 Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26:1515–1523Google Scholar
  61. 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 141:1446–1458CrossRefGoogle Scholar
  62. Yordem BK, Conte SS, Ma JF, Yokosho K, Vasques KA, Gopalsamy SN, Walker EL (2011) Brachypodium distachyon as a new model system for understanding iron homeostasis in grasses: phylogenetic and expression analysis of yellow stripe-like (YSL) transporters. Ann Bot 108:821–833CrossRefGoogle Scholar
  63. Zanin L, Venuti S, Zamboni A, Varanini Z, Tomasi N, Pinton R (2017) Transcriptional and physiological analyses of Fe deficiency response in maize reveal the presence of strategy I components and Fe/P interactions. BMC Genomics 18:154CrossRefGoogle Scholar
  64. Zhai Z, Gayomba SR, Jung HI, Vimalakumari NK, Pineros M, Craft E, Rutzke MA, Danku J, Lahner B, Punshon T et al (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 26:2249–2264CrossRefGoogle Scholar
  65. Zuo Y, Zhang F (2011) Soil and crop management strategies to prevent iron deficiency in crops. Plant Soil 339:83–95CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiotechnologyNational Agri-Food Biotechnology InstituteMohaliIndia
  2. 2.Department of BiotechnologyPanjab UniversityChandigarhIndia
  3. 3.Copenhagen Plant Science Centre, PLENUniversity of CopenhagenFrederiksberg CDenmark

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