Skip to main content
SpringerLink
Log in

A genome‐wide analysis of NPF and NRT2 transporter gene families in bread wheat provides new insights into the distribution, function, regulation and evolution of nitrate transporters

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Nitrate transporters (NRT) in plants are mainly encoded by the NPF and NRT2 gene families. We aimed to reveal the chromosome distribution, collinearity, coexpression and evolution of the NPF and NRT2 genes in the genome of wheat (Triticum aestivum). Nitrate transport activity of representative proteins was also verified.

Methods

Genomic information, collinearity analysis, coexpression network analysis, nitrate transport activity and polymorphism analysis were integrated to identify and characterize the NPF and NRT2 genes.

Results

We identified 331 NPF and 46 NRT2 genes in the wheat genome. Tandem duplication was the main driver of the expansion of the NRT2 genes. The NPF genes were mainly distributed on the 2-, 3- and 7- chromosome groups and in the R2b region. The NRT2 genes were mainly distributed on the 6-chromosome group and in the R1 region. Multiple transcription factor families were coexpressed with NPF and NRT2 genes in wheat. Two NPFs and one NRT2 could transport NO3− under either 0.5 mM or 10 mM nitrate concentrations. One hundred and eighty-five NPF and 27 NRT2 genes fit the neutral selection model. Natural variations in NPF genes resulted in differences in the nitrogen uptake of wheat.

Conclusions

Duplication events are ubiquitous in NPF and NRT2 gene families in the wheat genome. GRAS may be a previously unrecognized transcription factor that regulates NPF genes expression. It is unreliable to predict the activity of NPF and NRT2 proteins based only on their phylogenetic relationships. Polymorphisms in NPF and NRT2 genes mainly accumulate by random drift.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

HATS:

High-affinity transport system

LATS:

Low-affinity transport system

N:

Nitrogen

NUE:

Nitrogen use efficiency

NPF:

Nitrate Transporter 1 and Peptide Transporter Family

NRT:

Nitrate transporter

MFS:

Major facilitator superfamily

IAA:

Auxin

ABA:

Abscisic acid

JAs:

Jasmonates

GAs:

Gibberellins

NAR:

Nitrate-assimilation related

TF:

Transcription factor

SNP:

Single-nucleotide polymorphism

WGCNA:

Weighted gene coexpression network analysis

PCA:

Principal component analysis

GRAVY:

Grand average of hydropathicity

CDS:

Coding sequence

NHI:

N harvest index

References

  • Achaz G, Coissac E, Viari A, Netter P (2000) Analysis of intrachromosomal duplications in yeast Saccharomyces cerevisiae: A possible model for their origin. Mol Biol Evol 17:1268–1275

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Babst BA, Gao F, Acosta-Gamboa LM, Karve A, Schueller MJ, Lorence A (2019) Three NPF genes in Arabidopsis are necessary for normal nitrogen cycling under low nitrogen stress. Plant Physiol Biochem 143:1–10

    Article  CAS  PubMed  Google Scholar 

  • Bagchi R, Salehin M, Adeyemo OS, Salazar C, Shulaev V, Sherrier DJ, Dickstein R (2012) Functional assessment of the Medicago truncatulaNIP/LATD protein demonstrates that it is a high-affinity nitrate transporter. Plant Physiol 160:906–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bajgain P, Russell B, Mohammadi M (2018) Phylogenetic analyses and in-seedling expression of ammonium and nitrate transporters in wheat. Sci Rep 8:7082

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bao SD (2000) Soil and agricultural chemistry analysis. China Agricultural Press, Beijing (in Chiese)

    Google Scholar 

  • Brandt B, Brodsky DE, Xue SW, Negi J, Iba K, Kangasjarvi J, Ghassemian M, Stephan AB, Hu HH, Schroeder JI (2012) Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci U S A 109:10593–10598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchner P, Hawkesford MJ (2014) Complex phylogeny and gene expression patterns of members of the Nitrate Transporter 1/Peptide Transporter family (NPF) in wheat. J Exp Bot 65:5697–5710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Castillo JA, Agathos SN (2019) A genome-wide scan for genes under balancing selection in the plant pathogen Ralstonia solanacearum. BMC Evol Biol 19:123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen YX, Yang MY, Ding WW, Zhao YJ, Li XJ, Xiao K (2017) Wheat ZFP gene TaZFP593;l mediates the N-starvation adaptation of plants through regulating N acquisition and the ROS metabolism. Plant Cell Tissue Organ Cult 129:271–288

    Article  CAS  Google Scholar 

  • Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Chiu CC, Lin CS, Hsia AP, Su RC, Lin HL, Tsay YF (2004) Mutation of a nitrate transporter, AtNRT1: 4, results in a reduced petiole nitrate content and altered leaf development. Plant Cell Physiol 45:1139–1148

    Article  CAS  PubMed  Google Scholar 

  • Choulet F, Alberti A, Theil S, Glover N, Barbe V, Daron J, Pingault L, Sourdille P, Couloux A, Paux E, Leroy P, Mangenot S, Guilhot N, Le Gouis J, Balfourier F, Alaux M, Jamilloux V, Poulain J, Durand C, Bellec A, Gaspin C, Safar J, Dolezel J, Rogers J, Vandepoele K, Aury JM, Mayer K, Berges H, Quesneville H, Wincker P, Feuillet C (2014) Structural and functional partitioning of bread wheat chromosome 3B. Science 345:1249721

    Article  PubMed  CAS  Google Scholar 

  • Corratge-Faillie C, Lacombe B (2017) Substrate (un)specificity of Arabidopsis NRT1/PTR Family (NPF) proteins. J Exp Bot 68:3107–3113

    Article  CAS  PubMed  Google Scholar 

  • Du XQ, Wang FL, Li H, Jing S, Yu M, Li J, Wu WH, Kudla J, Wang Y (2019) The transcription factor MYB59 regulates K+/NO3– translocation in the Arabidopsis response to low K+ stress. Plant Cell 31:699–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan JF, Tian H, Gao YJ (2016) Expression of nitrogen transporter genes in roots of winter wheat (Triticum aestivum L.) in response to soil drought with contrasting nitrogen supplies. Crop Pasture Sci 67:128–136

    Article  CAS  Google Scholar 

  • Fan XR, Naz M, Fan XR, Xuan W, Miller AJ, Xu GH (2017a) Plant nitrate transporters: from gene function to application. J Exp Bot 68:2463–2475

    Article  CAS  PubMed  Google Scholar 

  • Fan XR, Tang Z, Tan YW, Zhang Y, Luo BB, Yang M, Lian XM, Shen QR, Miller AJ, Xu GH (2017b) Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proc Natl Acad Sci U S A 113:7118–7123

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu YL, Yi HY, Bao J, Gong JM (2015) LeNRT2.3 functions in nitrate acquisition and long-distance transport in tomato. FEBS Lett 589:1072–1079

    Article  CAS  PubMed  Google Scholar 

  • Giunta F, Motzo R, Pruneddu G (2007) Trends since 1900 in the yield potential of Italian-bred durum wheat cultivars. Eur J Agron 27:12–24

    Article  Google Scholar 

  • Gooding MJ, Addisu M, Uppal RK, Snape JW, Jones HE (2012a) Effect of wheat dwarfing genes on nitrogen-use efficiency. J Agric Sci 150:3–22

    Article  CAS  Google Scholar 

  • Gooding MJ, Fan MS, McGrath S, Shewry P, Zhao FJ (2012b) Contrasting effects of dwarfing alleles and nitrogen availability on mineral concentrations in wheat grain. Plant Soil 360:93–107

    Article  CAS  Google Scholar 

  • Guo TC, Xuan HM, Yang YY, Wang LN, Wei LT, Wang YH, Kang GZ (2014) Transcription analysis of genes encoding the wheat root transporter NRT1 and NRT2 families during nitrogen starvation. J Plant Growth Regul 33:837–848

    Article  CAS  Google Scholar 

  • He X, Qu BY, Li WJ, Zhao XQ, Teng W, Ma WY, Ren YZ, Li B, Li ZS, Tong YP (2015) The nitrate-inducible NAC transcription factor TaNAC2-5A controls nitrate response and increases wheat yield. Plant Physiol 169:1991–2005

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194

    Article  CAS  PubMed  Google Scholar 

  • Hu B, Wang W, Ou SJ, Tang JY, Li H, Che RH, Zhang ZH, Chai XY, Wang HR, Wang YQ, Liang CZ, Liu LC, Piao ZZ, Deng QY, Deng K, Xu C, Liang Y, Zhang LH, Li LG, Chu CC (2015) Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nature Genet 47:834–838

    Article  CAS  PubMed  Google Scholar 

  • IWGSC (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788

    Article  CAS  Google Scholar 

  • IWGSC (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:7191

    Article  CAS  Google Scholar 

  • Kotur Z, Mackenzie N, Ramesh S, Tyerman SD, Kaiser BN, Glass AD (2012) Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2.1. New Phytol 194:724–731

    Article  CAS  PubMed  Google Scholar 

  • 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 19:1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Batra R, Gahlaut V, Gautam T, Kumar S, Sharma M, Tyagi S, Singh KP, Balyan HS, Pandey R, Gupta PK (2018)Genome-wide identification and characterization of gene family for RWP-RK transcription factors in wheat (Triticum aestivum L.). PLoS One 13:e0208409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leran S, Varala K, Boyer JC, Chiurazzi M, Crawford N, Daniel-Vedele F, David L, Dickstein R, Fernandez E, Forde B, Gassmann W, Geiger D, Gojon A, Gong JM, Halkier BA, Harris JM, Hedrich R, Limami AM, Rentsch D, Seo M, Tsay YF, Zhang MY, Coruzzi G, Lacombe B (2014) A unified nomenclature of Nitrate Transporter 1/Peptide Transporter family members in plants. Trends Plant Sci 19:5–9

    Article  CAS  PubMed  Google Scholar 

  • Li MJ, Wang RZ, Tian H, Gao YJ (2018) Transcriptome responses in wheat roots to colonization by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Mycorrhiza 28:747–759

    Article  PubMed  Google Scholar 

  • Li WJ, He X, Chen Y, Jing YF, Shen CC, Yang JB, Teng W, Zhao XQ, Hu WJ, Hu MY, Li H, Miller AJ, Tong YP (2020) A wheat transcription factor positively sets seed vigour by regulating the grain nitrate signal. New Phytol 225:1667–1680

    Article  CAS  PubMed  Google Scholar 

  • Liu KH, Tsay YF (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. Embo J 22:1005–1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu KH, Huang CY, Tsay YF (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11:865–874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XQ, Huang DM, Tao JY, Miller AJ, Fan XR, Xu GH (2014) Identification and functional assay of the interaction motifs in the partner protein OsNAR2.1 of the two-component system for high-affinity nitrate transport. New Phytol 204:74–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu ZP, Zhao YJ, Wang XY, Yang MY, Guo CJ, Xiao K (2018)TaNBP1, a guanine nucleotide-binding subunit gene of wheat, is essential in the regulation of N starvation adaptation via modulating N acquisition and ROS homeostasis. BMC Plant Biol 18:167

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Loddo S, Gooding MJ (2012)Semi-dwarfing (Rht-B1b) improves nitrogen-use efficiency in wheat, but not at economically optimal levels of nitrogen availability. Cereal Res Commun 40:116–121

    Article  CAS  Google Scholar 

  • Morere-Le Paven MC, Viau L, Hamon A, Vandecasteele C, Pellizzaro A, Bourdin C, Laffont C, Lapied B, Lepetit M, Frugier F, Legros C, Limami AM (2011) Characterization of a dual-affinity nitrate transporter MtNRT1.3 in the model legume Medicago truncatula. J Exp Bot 62:5595–5605

    Article  CAS  PubMed  Google Scholar 

  • Mu XH, Luo J (2019) Evolutionary analyses of NIN-like proteins in plants and their roles in nitrate signaling. Cell Mol Life Sci 76:3753–3764

    Article  CAS  PubMed  Google Scholar 

  • Okamoto M, Vidmar JJ, Glass ADM (2003) Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: Responses to nitrate provision. Plant Cell Physiol 44:304–317

    Article  CAS  PubMed  Google Scholar 

  • Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kianian S, Spielmeyer W (2008) A physical map of the 1-Gigabase bread wheat chromosome 3B. Science 322:101–104

    Article  CAS  PubMed  Google Scholar 

  • Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302

    Article  CAS  PubMed  Google Scholar 

  • Sadras VO, Lawson C (2013) Nitrogen and water-use efficiency of Australian wheat varieties released between 1958 and 2007. Eur J Agron 46:34–41

    Article  CAS  Google Scholar 

  • Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, Wakimoto H, Yang C-c, Iwamoto M, Abe T, Yamada Y, Muto A, Inokuchi H, Ikemura T, Matsumoto T, Sasaki T, Itoh T (2013) Rice annotation project database (RAP-DB): an integrative and Interactive Database for Rice Genomics. Plant Cell Physiol 54:e6–e6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun CW, Dong ZD, Zhao L, Ren Y, Zhang N, Chen F (2020) The Wheat 660K SNP array demonstrates great potential for marker-assisted selection in polyploid wheat. Plant Biotechnol J 18:1354–1360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E (2007) The Arabidopsis information resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang WJ, Ye J, Yao XM, Zhao PZ, Xuan W, Tian YL, Zhang YY, Xu S, An HZ, Chen GM, Yu J, Wu W, Ge YW, Liu XL, Li J, Zhang HZ, Zhao YQ, Yang B, Jiang XZ, Peng C, Zhou C, Terzaghi W, Wang CM, Wan JM (2019)Genome-wide associated study identifies NAC42-activated nitrate transporter conferring high nitrogen use efficiency in rice. Nat Commun 10:5279

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Taulemesse F, Le Gouis J, Gouache D, Gibon Y, Allard V (2015)Post-Flowering nitrate uptake in wheat is controlled by N status at flowering, with a putative major role of root nitrate transporter NRT2.1. PLoS One 10:e0120291

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tian H, Yuan XL, Duan JF, Li WH, Zhai BN, Gao YJ (2017) Influence of nutrient signals and carbon allocation on the expression of phosphate and nitrogen transporter genes in winter wheat (Triticum aestivum L.) roots colonized by arbuscular mycorrhizal fungi. PLoS One 12:e0172154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tong YP, Zhou JJ, Li Z, Miller AJ (2005) A two-component high-affinity nitrate uptake system in barley. Plant J 41:442–450

    Article  CAS  PubMed  Google Scholar 

  • Vidal EA, Alvarez JM, Araus V, Riveras E, Brooks MD, Krouk G, Ruffel S, Lejay L, Crawford NM, Coruzzi GM, Gutierrez RA (2020) Nitrate in 2020: thirty years from transport to signaling networks. Plant Cell 32:2094–2119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Wittgenstein NJ, Le CH, Hawkins BJ, Ehlting J (2014) Evolutionary classification of ammonium, nitrate, and peptide transporters in land plants. BMC Evol Biol 14:11

    Article  CAS  Google Scholar 

  • Wang YP, Tang HB, DeBarry JD, Tan X, Li JP, Wang XY, Lee TH, Jin HZ, Marler B, Guo H, Kissinger JC, Paterson AH (2012)MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Zhang PL, Liu Q, Li GJ, Di DW, Xia GM, Kronzucker H, Fang S, Chu JF, Shi WM (2020)TaANR1-TaBG1 and TaWabi5-TaNRT2s/NARs link ABA metabolism and nitrate acquisition in wheat roots. Plant Physiol 182:1440–1453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei J, Zheng Y, Feng H, Qu HM, Fan XR, Yamaji N, Ma JF, Xu GH (2018)OsNRT2.4 encodes a dual-affinity nitrate transporter and functions in nitrate-regulated root growth and nitrate distribution in rice. J Exp Bot 69:1095–1107

    Article  CAS  PubMed  Google Scholar 

  • Wen Z, Tyerman SD, Dechorgnat J, Ovchinnikova E, Dhugga KS, Kaiser BN (2017) Maize NPF6 proteins are homologs of Arabidopsis CHL1 that are selective for both nitrate and chloride. Plant Cell 29:2581–2596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong HC, Guo HJ, Zhou CY, Guo XT, Xie YD, Zhao LS, Gu JY, Zhao SR, Ding YP, Liu LX (2019) A combined association mapping and t-test analysis of SNP loci and candidate genes involving in resistance to low nitrogen traits by a wheat mutant population. PLoS One 14:e0211492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu K, Chen SJ, Li TF, Ma XS, Liang XH, Ding XF, Liu HY, Luo LJ (2015)OsGRAS23, a rice GRAS transcription factor gene, is involved in drought stress response through regulating expression of stress-responsive genes. BMC Plant Biol 15:141

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang TR, Hao L, Yao SF, Zhao YY, Lu WJ, Xiao K (2016)TabHLH1, a bHLH-type transcription factor gene in wheat, improves plant tolerance to Pi and N deprivation via regulation of nutrient transporter gene transcription and ROS homeostasis. Plant Physiol Biochem 104:99–113

    Article  CAS  PubMed  Google Scholar 

  • Yin L, Li P, Wen B, Taylor D, Berry JO (2007) Characterization and expression of a high-affinity nitrate system transporter gene (TaNRT2.1) from wheat roots, and its evolutionary relationship to other NTR2 genes. Plant Sci 172:621–631

    Article  CAS  Google Scholar 

  • Zhang X, Davidson EA, Mauzerall DL, Searchinger TD, Dumas P, Shen Y (2015) Managing nitrogen for sustainable development. Nature 528:51–59

    Article  CAS  PubMed  Google Scholar 

  • Zhou JJ, Theodoulou FL, Muldin I, Ingemarsson B, Miller AJ (1998) Cloning and functional characterization of a Brassica napus transporter that is able to transport nitrate and histidine. J Biol Chem 273:12017–12023

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The work was funded by the National Natural Science Foundation of China (grant number 31972497) and the National Key R & D Plan (SQ2017ZY060068). We thank the ‘State Key Laboratory of Crop Stress Biology for Arid Areas, NWAFU’ for sharing genotyping data. We thank the high performance computing platform of the Northwest A&F University for supporting WGCNA analysis. We also thank Professor Cun Wang, from College of Life Science, Northwest A&F University, for suppling technical assistance during heterologous expression experiment.

Author information

Authors and Affiliations

  1. Key Laboratory of Plant Nutrition and Agri-environment in Northwest China, Ministry of Agriculture, College of Natural Resources and Environment, Northwest A&F University, Yangling, Shaanxi, China

    Mengjiao Li, Hui Tian & Yajun Gao

Authors
  1. Mengjiao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hui Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yajun Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hui Tian.

Additional information

Responsible Editor: Ad C. Borstlap.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Figure S1

Phylogenetic relationship (A), conserved motifs (B) and exon-intron structure (C) of NPF genes (PNG 5270 kb)

High Resolution Image (TIF 40585 kb)

Figure S2

Phylogenetic relationship (A), conserved motifs (B) and exon-intron structure (C) of NRT2 genes (PNG 922 kb)

High Resolution Image (TIF 36004 kb)

Figure S3

Gene ontology (GO) enrichment analysis of genes in NPF- and NRT2-related modules produced during WGCNA (PNG 1.16 mb)

High Resolution Image (TIF 1.34 mb)

Figure S4

Top 20 enriched GO terms for genes in the NPF- and NRT2-related modules produced during WGCNA (PNG 769 kb)

High Resolution Image (TIF 6064 kb)

ESM 1

(XLSX 1.15 mb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, M., Tian, H. & Gao, Y. A genome‐wide analysis of NPF and NRT2 transporter gene families in bread wheat provides new insights into the distribution, function, regulation and evolution of nitrate transporters. Plant Soil 465, 47–63 (2021). https://doi.org/10.1007/s11104-021-04927-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-021-04927-8

Keywords

Search

Navigation