skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Genome-Wide Analysis of Nitrate Transporter (NRT/NPF) Family in Sugarcane Saccharum spontaneum L.

Abstract

Nitrate is the predominant nitrogen source for plant growth and development. However, sugarcane, globally used as the primary sugar crop and biofuel feedstock, displays a low nitrate use efficiency due to a low capacity in storing nitrate in shoots. It is well studied that the nitrate transporter (NRT/NPF) family functions as the gatekeeper in governing nitrogen uptake and distribution, and optimizing nitrogen utilization in plants. This makes it a promising target for improving nitrogen use efficiency in sugarcane. Here, we carried out a comprehensive analysis of NRT/NPF genes at a genome-wide scale in Saccharum spontaneum. A BLAST search of NRT/NPF genes was initially performed against recently released sugarcane genome, followed by phylogenetic, gene structure and protein motif analysis. Additionally, NRT/NPF gene expression profile from various tissues was obtained from RNA-seq data analysis. As a result, we identified 178 NPF, 20 NRT2, and 6 NRT3 genes which spread across all 8 monoploid chromosomes. NPF and NRT3 exhibit high levels of genetic diversities as opposed to NRT2 which is more evolutionarily conserved. Interestingly, several SsNPF genes are products of gene fusions of several tandem duplications, which provide valuable structural resources for functional characterization of nitrate transporters. Moreover, several genes are tissue-specific expressed,more » indicating roles in tissue-specific nitrate translocations. A substantial number of NRT/NPF genes are heterogeneous in terms of their gene structures and mRNA abundance. Taken together, our work provides a genetic foundation for future investigations of molecular and physiological functions of sugarcane nitrate transporters.« less

Authors:
 [1];  [2];  [1];  [1]; ORCiD logo [1]
  1. Univ. of Illinois, Urbana-Champaign, IL (United States)
  2. Univ. of Illinois, Urbana-Champaign, IL (United States); China Agricultural Univ., Beijing (China)
Publication Date:
Research Org.:
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1497673
Grant/Contract Number:  
SC0018420
Resource Type:
Accepted Manuscript
Journal Name:
Tropical Plant Biology
Additional Journal Information:
Journal Volume: 12; Journal Issue: 3; Journal ID: ISSN 1935-9756
Publisher:
Springer Nature
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Gene duplication and fusion; NRT/NPF; Nitrate transporter; Tissue-specific expression; Sugarcane

Citation Formats

Wang, Jiang, Li, Yaxin, Zhu, Fan, Ming, Ray, and Chen, Li -Qing. Genome-Wide Analysis of Nitrate Transporter (NRT/NPF) Family in Sugarcane Saccharum spontaneum L.. United States: N. p., 2019. Web. https://doi.org/10.1007/s12042-019-09220-8.
Wang, Jiang, Li, Yaxin, Zhu, Fan, Ming, Ray, & Chen, Li -Qing. Genome-Wide Analysis of Nitrate Transporter (NRT/NPF) Family in Sugarcane Saccharum spontaneum L.. United States. https://doi.org/10.1007/s12042-019-09220-8
Wang, Jiang, Li, Yaxin, Zhu, Fan, Ming, Ray, and Chen, Li -Qing. Thu . "Genome-Wide Analysis of Nitrate Transporter (NRT/NPF) Family in Sugarcane Saccharum spontaneum L.". United States. https://doi.org/10.1007/s12042-019-09220-8. https://www.osti.gov/servlets/purl/1497673.
@article{osti_1497673,
title = {Genome-Wide Analysis of Nitrate Transporter (NRT/NPF) Family in Sugarcane Saccharum spontaneum L.},
author = {Wang, Jiang and Li, Yaxin and Zhu, Fan and Ming, Ray and Chen, Li -Qing},
abstractNote = {Nitrate is the predominant nitrogen source for plant growth and development. However, sugarcane, globally used as the primary sugar crop and biofuel feedstock, displays a low nitrate use efficiency due to a low capacity in storing nitrate in shoots. It is well studied that the nitrate transporter (NRT/NPF) family functions as the gatekeeper in governing nitrogen uptake and distribution, and optimizing nitrogen utilization in plants. This makes it a promising target for improving nitrogen use efficiency in sugarcane. Here, we carried out a comprehensive analysis of NRT/NPF genes at a genome-wide scale in Saccharum spontaneum. A BLAST search of NRT/NPF genes was initially performed against recently released sugarcane genome, followed by phylogenetic, gene structure and protein motif analysis. Additionally, NRT/NPF gene expression profile from various tissues was obtained from RNA-seq data analysis. As a result, we identified 178 NPF, 20 NRT2, and 6 NRT3 genes which spread across all 8 monoploid chromosomes. NPF and NRT3 exhibit high levels of genetic diversities as opposed to NRT2 which is more evolutionarily conserved. Interestingly, several SsNPF genes are products of gene fusions of several tandem duplications, which provide valuable structural resources for functional characterization of nitrate transporters. Moreover, several genes are tissue-specific expressed, indicating roles in tissue-specific nitrate translocations. A substantial number of NRT/NPF genes are heterogeneous in terms of their gene structures and mRNA abundance. Taken together, our work provides a genetic foundation for future investigations of molecular and physiological functions of sugarcane nitrate transporters.},
doi = {10.1007/s12042-019-09220-8},
journal = {Tropical Plant Biology},
number = 3,
volume = 12,
place = {United States},
year = {2019},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:

Works referenced in this record:

New insights into the evolution and functional divergence of the SWEET family in Saccharum based on comparative genomics
journal, November 2018


The Sorghum bicolor genome and the diversification of grasses
journal, January 2009

  • Paterson, Andrew H.; Bowers, John E.; Bruggmann, Rémy
  • Nature, Vol. 457, Issue 7229
  • DOI: 10.1038/nature07723

Functional consequences of a gene duplication and fusion event in an arginine kinase
journal, May 2003

  • Compaan, D. M.
  • Journal of Experimental Biology, Vol. 206, Issue 9
  • DOI: 10.1242/jeb.00299

Whole Genome Sequencing Reveals Potential New Targets for Improving Nitrogen Uptake and Utilization in Sorghum bicolor
journal, October 2016

  • Massel, Karen; Campbell, Bradley C.; Mace, Emma S.
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.01544

The PTR family: a new group of peptide transporters
journal, June 1995


Functional role of oligomerization for bacterial and plant SWEET sugar transporter family
journal, September 2013

  • Xuan, Y. H.; Hu, Y. B.; Chen, L. -Q.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 39
  • DOI: 10.1073/pnas.1311244110

Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status
journal, January 2011

  • Feng, Huimin; Yan, Ming; Fan, Xiaorong
  • Journal of Experimental Botany, Vol. 62, Issue 7
  • DOI: 10.1093/jxb/erq403

Endophytic nitrogen fixation in sugarcane: present knowledge and future applications
journal, May 2003

  • Boddey, Robert M.; Urquiaga, Segundo; Alves, Bruno J. R.
  • Plant and Soil, Vol. 252, Issue 1
  • DOI: 10.1023/A:1024152126541

Arabidopsis Nitrate Transporter NRT1.9 Is Important in Phloem Nitrate Transport
journal, May 2011


Dichotomy in the NRT Gene Families of Dicots and Grass Species
journal, December 2010


Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.
journal, October 2018


The Organization, Expression, and Evolution of Antibody Genes and Other Multigene Families
journal, December 1975


Characterization of the Arabidopsis Nitrate Transporter NRT1.6 Reveals a Role of Nitrate in Early Embryo Development
journal, December 2008


Root based approaches to improving nitrogen use efficiency in plants
journal, September 2009


Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2.1
journal, March 2012


Disruption of the rice nitrate transporter OsNPF2.2 hinders root-to-shoot nitrate transport and vascular development
journal, April 2015

  • Li, Yuge; Ouyang, Jie; Wang, Ya-Yun
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep09635

Identification and molecular characterization of Medicago truncatula NRT2 and NAR2 families
journal, December 2014

  • Pellizzaro, Anthoni; Clochard, Thibault; Planchet, Elisabeth
  • Physiologia Plantarum, Vol. 154, Issue 2
  • DOI: 10.1111/ppl.12314

Identification and molecular characterization of the Brachypodium distachyon NRT2 family, with a major role of BdNRT2.1
journal, April 2018

  • Wang, Jiang; Hüner, Norman; Tian, Lining
  • Physiologia Plantarum, Vol. 165, Issue 3
  • DOI: 10.1111/ppl.12716

A Nitrite Transporter Associated with Nitrite Uptake by Higher Plant Chloroplasts
journal, June 2007

  • Sugiura, M.; Georgescu, M. N.; Takahashi, M.
  • Plant and Cell Physiology, Vol. 48, Issue 7
  • DOI: 10.1093/pcp/pcm073

Nitrogen in sugarcane derived from fertilizer under Brazilian field conditions
journal, February 2011

  • Franco, Henrique Coutinho Junqueira; Otto, Rafael; Faroni, Carlos Eduardo
  • Field Crops Research, Vol. 121, Issue 1
  • DOI: 10.1016/j.fcr.2010.11.011

Gene Structure and Expression of the High-affinity Nitrate Transport System in Rice Roots
journal, April 2008


Transporters Involved in Root Nitrate Uptake and Sensing by Arabidopsis
journal, September 2016


The Arabidopsis Nitrate Transporter NRT1.7, Expressed in Phloem, Is Responsible for Source-to-Sink Remobilization of Nitrate
journal, September 2009


Nitrate Transport, Signaling, and Use Efficiency
journal, April 2018


Genesis: cluster analysis of microarray data
journal, January 2002


Sucrose Efflux Mediated by SWEET Proteins as a Key Step for Phloem Transport
journal, December 2011


Dissection of the AtNRT2.1 : AtNRT2.2 Inducible High-Affinity Nitrate Transporter Gene Cluster
journal, November 2006


NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds
journal, August 2012

  • Nour-Eldin, Hussam Hassan; Andersen, Tonni Grube; Burow, Meike
  • Nature, Vol. 488, Issue 7412
  • DOI: 10.1038/nature11285

Large-scale search for genes on which positive selection may operate
journal, May 1996


The Arabidopsis nitrate transporter NRT2.5 plays a role in nitrate acquisition and remobilization in nitrogen-starved plants
journal, August 2014

  • Lezhneva, Lina; Kiba, Takatoshi; Feria-Bourrellier, Ana-Belen
  • The Plant Journal, Vol. 80, Issue 2
  • DOI: 10.1111/tpj.12626

The Evolutionary Fate and Consequences of Duplicate Genes
journal, November 2000


The Arabidopsis root stele transporter NPF2.3 contributes to nitrate translocation to shoots under salt stress
journal, July 2015

  • Taochy, Christelle; Gaillard, Isabelle; Ipotesi, Emilie
  • The Plant Journal, Vol. 83, Issue 3
  • DOI: 10.1111/tpj.12901

CHL1 Functions as a Nitrate Sensor in Plants
journal, September 2009


Analysis of the NRT2 Nitrate Transporter Family in Arabidopsis. Structure and Gene Expression
journal, May 2002

  • Orsel, Mathilde; Krapp, Anne; Daniel-Vedele, Françoise
  • Plant Physiology, Vol. 129, Issue 2
  • DOI: 10.1104/pp.005280

Tonoplast-localized nitrate uptake transporters involved in vacuolar nitrate efflux and reallocation in Arabidopsis
journal, July 2017


The Nitrate Transporter AtNRT1.1 (CHL1) Functions in Stomatal Opening and Contributes to Drought Susceptibility in Arabidopsis
journal, December 2002

  • Guo, Fang-Qing; Young, Jared; Crawford, Nigel M.
  • The Plant Cell, Vol. 15, Issue 1
  • DOI: 10.1105/tpc.006312

Resolution of dual Mechanisms of Potassium Absorption by Barley Roots
journal, May 1963

  • Epstein, E.; Rains, D. W.; Elzam, O. E.
  • Proceedings of the National Academy of Sciences, Vol. 49, Issue 5
  • DOI: 10.1073/pnas.49.5.684

Rice nitrate transporter OsNPF2.4 functions in low-affinity acquisition and long-distance transport
journal, October 2014

  • Xia, Xiudong; Fan, Xiaorong; Wei, Jia
  • Journal of Experimental Botany, Vol. 66, Issue 1
  • DOI: 10.1093/jxb/eru425

Agronomic nitrogen-use efficiency of rice can be increased by driving OsNRT2.1 expression with the OsNAR2.1 promoter
journal, January 2016

  • Chen, Jingguang; Zhang, Yong; Tan, Yawen
  • Plant Biotechnology Journal, Vol. 14, Issue 8
  • DOI: 10.1111/pbi.12531

Characterization and the Expression Analysis of Nitrate Transporter (NRT) Gene Family in Pineapple
journal, September 2018


AtNPF2.5 Modulates Chloride (Cl−) Efflux from Roots of Arabidopsis thaliana
journal, January 2017


Identification of a Stelar-Localized Transport Protein That Facilitates Root-to-Shoot Transfer of Chloride in Arabidopsis
journal, December 2015

  • Li, Bo; Byrt, Caitlin; Qiu, Jiaen
  • Plant Physiology, Vol. 170, Issue 2
  • DOI: 10.1104/pp.15.01163

AtPTR3, a wound-induced peptide transporter needed for defence against virulent bacterial pathogens in Arabidopsis
journal, December 2006


The Arabidopsis ATNRT2.7 Nitrate Transporter Controls Nitrate Content in Seeds
journal, May 2007

  • Chopin, Franck; Orsel, Mathilde; Dorbe, Marie-France
  • The Plant Cell, Vol. 19, Issue 5
  • DOI: 10.1105/tpc.107.050542

Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields
journal, June 2016

  • Fan, Xiaorong; Tang, Zhong; Tan, Yawen
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 26
  • DOI: 10.1073/pnas.1525184113

Crystal structure of the plant dual-affinity nitrate transporter NRT1.1
journal, February 2014

  • Sun, Ji; Bankston, John R.; Payandeh, Jian
  • Nature, Vol. 507, Issue 7490
  • DOI: 10.1038/nature13074

The Arabidopsis NPF3 protein is a GA transporter
journal, May 2016

  • Tal, Iris; Zhang, Yi; Jørgensen, Morten Egevang
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11486

A high affinity nitrate transport system from Chlamydomonas requires two gene products
journal, January 2000


Mutation of a Nitrate Transporter, AtNRT1:4, Results in a Reduced Petiole Nitrate Content and Altered Leaf Development
journal, September 2004

  • Chiu, Chi-Chou; Lin, Choun-Sea; Hsia, An-Ping
  • Plant and Cell Physiology, Vol. 45, Issue 9
  • DOI: 10.1093/pcp/pch143

Members of the NPF3 Transporter Subfamily Encode Pathogen-Inducible Nitrate/Nitrite Transporters in Grapevine and Arabidopsis
journal, December 2013

  • Pike, Sharon; Gao, Fei; Kim, Min Jung
  • Plant and Cell Physiology, Vol. 55, Issue 1
  • DOI: 10.1093/pcp/pct167

Plant Nitrogen Assimilation and Use Efficiency
journal, June 2012


Characterization of a Two-Component High-Affinity Nitrate Uptake System in Arabidopsis. Physiology and Protein-Protein Interaction
journal, September 2006

  • Orsel, Mathilde; Chopin, Franck; Leleu, Olivier
  • Plant Physiology, Vol. 142, Issue 3
  • DOI: 10.1104/pp.106.085209

NRT1.1B improves selenium concentrations in rice grains by facilitating selenomethinone translocation
journal, January 2019

  • Zhang, Lianhe; Hu, Bin; Deng, Kun
  • Plant Biotechnology Journal, Vol. 17, Issue 6
  • DOI: 10.1111/pbi.13037

An Arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake
journal, January 2001


A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants
journal, January 2014


Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1
journal, February 2014


Functional Assessment of the Medicago truncatula NIP/LATD Protein Demonstrates That It Is a High-Affinity Nitrate Transporter
journal, August 2012

  • Bagchi, Rammyani; Salehin, Mohammad; Adeyemo, O. Sarah
  • Plant Physiology, Vol. 160, Issue 2
  • DOI: 10.1104/pp.112.196444

The Nitrate Transporter (NRT) Gene Family in Poplar
journal, August 2013


N availability modulates the role of NPF3.1, a gibberellin transporter, in GA-mediated phenotypes in Arabidopsis
journal, August 2016


The Arabidopsis Nitrate Transporter NRT2.4 Plays a Double Role in Roots and Shoots of Nitrogen-Starved Plants
journal, January 2012

  • Kiba, Takatoshi; Feria-Bourrellier, Ana-Belen; Lafouge, Florence
  • The Plant Cell, Vol. 24, Issue 1
  • DOI: 10.1105/tpc.111.092221

The Arabidopsis Nitrate Transporter NRT1.8 Functions in Nitrate Removal from the Xylem Sap and Mediates Cadmium Tolerance
journal, May 2010


Gene duplication and fusion have occurred frequently in the evolution of phosphagen kinases – a two-domain arginine kinase from the clam Pseudocardium sachalinensis
journal, October 1998

  • Suzuki, Tomohiko; Kawasaki, Yoshitada; Unemi, Yukiko
  • Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1388, Issue 1
  • DOI: 10.1016/S0167-4838(98)00167-8

Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies
journal, June 2015

  • Hu, Bin; Wang, Wei; Ou, Shujun
  • Nature Genetics, Vol. 47, Issue 7
  • DOI: 10.1038/ng.3337

AtNPF5.5, a nitrate transporter affecting nitrogen accumulation in Arabidopsis embryo
journal, January 2015

  • Léran, Sophie; Garg, Bharti; Boursiac, Yann
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep07962

Cloning and Functional Characterization of an Arabidopsis Nitrate Transporter Gene That Encodes a Constitutive Component of Low-Affinity Uptake
journal, August 1999

  • Huang, Nien-Chen; Liu, Kun-Hsiang; Lo, Hau-Jan
  • The Plant Cell, Vol. 11, Issue 8
  • DOI: 10.1105/tpc.11.8.1381

CHL1 Is a Dual-Affinity Nitrate Transporter of Arabidopsis Involved in Multiple Phases of Nitrate Uptake
journal, May 1999

  • Liu, Kun-Hsiang; Huang, Chi-Ying; Tsay, Yi-Fang
  • The Plant Cell, Vol. 11, Issue 5
  • DOI: 10.1105/tpc.11.5.865

The response of the maize nitrate transport system to nitrogen demand and supply across the lifecycle
journal, February 2013

  • Garnett, Trevor; Conn, Vanessa; Plett, Darren
  • New Phytologist, Vol. 198, Issue 1
  • DOI: 10.1111/nph.12166

Cloning and Functional Characterization of a Constitutively Expressed Nitrate Transporter Gene, OsNRT1 , from Rice
journal, February 2000

  • Lin, Chung-Ming; Koh, Serry; Stacey, Gary
  • Plant Physiology, Vol. 122, Issue 2
  • DOI: 10.1104/pp.122.2.379

Nitrate-Regulated Auxin Transport by NRT1.1 Defines a Mechanism for Nutrient Sensing in Plants
journal, June 2010


A Functional Phylogenomic View of the Seed Plants
journal, December 2011

  • Lee, Ernest K.; Cibrian-Jaramillo, Angelica; Kolokotronis, Sergios-Orestis
  • PLoS Genetics, Vol. 7, Issue 12
  • DOI: 10.1371/journal.pgen.1002411

Effects of Nitrogen on Mesophyll Cell Division and Epidermal Cell Elongation in Tall Fescue Leaf Blades
journal, February 1989

  • MacAdam, Jennifer W.; Volenec, Jeffrey J.; Nelson, Curtis J.
  • Plant Physiology, Vol. 89, Issue 2
  • DOI: 10.1104/pp.89.2.549

Nutrient limitations alter cell division control and chromosome segregation through growth-related kinases and phosphatases
journal, December 2011

  • Yanagida, Mitsuhiro; Ikai, Nobuyasu; Shimanuki, Mizuki
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 366, Issue 1584
  • DOI: 10.1098/rstb.2011.0124

Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor
journal, May 2012

  • Kanno, Y.; Hanada, A.; Chiba, Y.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 24
  • DOI: 10.1073/pnas.1203567109

The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues
journal, September 2005

  • Little, D. Y.; Rao, H.; Oliva, S.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 38, p. 13693-13698
  • DOI: 10.1073/pnas.0504219102

A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport
journal, January 1993


CHL1 Is a Dual-Affinity Nitrate Transporter of Arabidopsis Involved in Multiple Phases of Nitrate Uptake
journal, May 1999

  • Liu, Kun-Hsiang; Huang, Chi-Ying; Tsay, Yi-Fang
  • The Plant Cell, Vol. 11, Issue 5
  • DOI: 10.2307/3870820