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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Overexpression of a putative nitrate transporter (StNPF1.11) increases plant height, leaf chlorophyll content and tuber protein content of young potato plants

Michiel T. Klaassen A B , Dianka C. T. Dees A , Rommel M. Garrido Jr. A , Jorge Alemán Báez A , Michiel Schrijen A , Pablo G. Baldeón Mendoza A and Luisa M. Trindade https://orcid.org/0000-0003-1541-2094 A C
+ Author Affiliations
- Author Affiliations

A Wageningen University and Research, Plant Breeding, PO Box 386, 6700 AJ Wageningen, The Netherlands.

B Aeres University of Applied Sciences, Department of Applied Research, PO Box 374, 8250 AJ Dronten, The Netherlands.

C Corresponding author. Email: luisa.trindade@wur.nl

Functional Plant Biology 47(5) 464-472 https://doi.org/10.1071/FP19342
Submitted: 29 November 2019  Accepted: 16 December 2019   Published: 25 March 2020

Abstract

Nitrate (NO3) fertilisers are commonly used to improve the yield and quality of most non-legume crops such as potato (Solanum tuberosum L.). Root cells absorb nitrate from the soil using plasma membrane-bound transporters. In this study, we overexpressed a putative nitrate transporter from potato (StNPF1.11) to study its effect on the level of tuber protein content in potato. At 10 weeks after planting, overexpression of StNPF1.11 increased the mean level of protein content of all n = 23 transformants by 42% compared with the wild-type control. The level of chlorophyll content in leaves (from upper and lower plant parts) also increased for several individuals at 10 weeks. Tuber yield (fresh) was not structurally impaired; however, the mean tuber dry matter content of the transformants was reduced by 3–8% at 19 weeks. At 19 weeks, an overall increase in protein content was not clearly observed. Throughout plant development, half of the transformants were taller than the control. A basic understanding of the mechanisms that regulate plant nitrogen uptake, transport and utilisation, enable the development of tools to improve both crop nutrition and crop quality that are needed to enhance the viability and sustainability of future plant production systems.

Additional keywords: ion transport, plant nutrition, Solanum tuberosum, soluble protein.


References

Aslam M, Travis RL, Huffaker RC (1992) Comparative kinetics and reciprocal inhibition of nitrate and nitrite uptake in roots of uninduced and induced barley (Hordeum vulgare L.) seedlings. Plant Physiology 99, 1124–1133.
Comparative kinetics and reciprocal inhibition of nitrate and nitrite uptake in roots of uninduced and induced barley (Hordeum vulgare L.) seedlings.Crossref | GoogleScholarGoogle Scholar | 11537883PubMed |

Bélanger G, Walsh JR, Richards JE, Milburn PH, Ziadi N (2002) Nitrogen fertilization and irrigation affects tuber characteristics of two potato cultivars. American Journal of Potato Research 79, 269–279.
Nitrogen fertilization and irrigation affects tuber characteristics of two potato cultivars.Crossref | GoogleScholarGoogle Scholar |

Castro Marín IC, Loef I, Bartetzko L, Searle I, Coupland G, Stitt M, Osuna D (2011) Nitrate regulates floral induction in Arabidopsis, acting independently of light, gibberellin and autonomous pathways. Planta 233, 539–552.
Nitrate regulates floral induction in Arabidopsis, acting independently of light, gibberellin and autonomous pathways.Crossref | GoogleScholarGoogle Scholar |

Chiba Y, Shimizu T, Miyakawa S, Kanno Y, Koshiba T, Kamiya Y, Seo M (2015) Identification Arabidopsis thaliana NRT1/PTR FAMILY (NPF) proteins capable of transporting plant hormones. Journal of Plant Research 128, 679–686.
Identification Arabidopsis thaliana NRT1/PTR FAMILY (NPF) proteins capable of transporting plant hormones.Crossref | GoogleScholarGoogle Scholar | 25801271PubMed |

Doddema H, Telkamp G (1979) Uptake of nitrate by mutants of Arabidopsis thaliana, disturbed in uptake or reduction of nitrate: II. Kinetics. Physiologia Plantarum 45, 332–338.
Uptake of nitrate by mutants of Arabidopsis thaliana, disturbed in uptake or reduction of nitrate: II. Kinetics.Crossref | GoogleScholarGoogle Scholar |

Fan X, Tang Z, Tan Y, Zhang Y, Luo B, Yang M, Lian X, Shen Q, Miller AJ, Xu G (2016) Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proceedings of the National Academy of Sciences of the United States of America 113, 7118–7123.
Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields.Crossref | GoogleScholarGoogle Scholar | 27274069PubMed |

Fang R-X, Nagy F, Sivasubramaniam S, Chua N-H (1989) Multiple cis regulatory elements for maximal expression of the cauliflower mosaic virus 35S promoter in transgenic plants. The Plant Cell 1, 141–150.

Feng H, Li B, Zhi Y, Chen J, Li R, Xia X, Xu G, Fan X (2017) Overexpression of the nitrate transporter, OsNRT2.3b, improves rice phosphorus uptake and translocation. Plant Cell Reports 36, 1287–1296.
Overexpression of the nitrate transporter, OsNRT2.3b, improves rice phosphorus uptake and translocation.Crossref | GoogleScholarGoogle Scholar | 28502056PubMed |

Frommer WB, Hummel S, Rentsch D (1994) Cloning of an Arabidopsis histidine transporting protein related to nitrate and peptide transporters. FEBS Letters 347, 185–189.
Cloning of an Arabidopsis histidine transporting protein related to nitrate and peptide transporters.Crossref | GoogleScholarGoogle Scholar | 8033999PubMed |

Gianquinto G, Goffart JP, Olivier M, Guarda G, Colauzzi M, Dalla Costa L, Delle Vedove G, Vos J, Mackerron DKL (2004) The use of hand-held chlorophyll meters as a tool to assess the nitrogen status and to guide nitrogen fertilization of potato crop. Potato Research 47, 35–80.
The use of hand-held chlorophyll meters as a tool to assess the nitrogen status and to guide nitrogen fertilization of potato crop.Crossref | GoogleScholarGoogle Scholar |

Goyal S, Huffaker R (1986) A novel approach and a fully automated microcomputer‐based system to study kinetics of NO3–, NO2–, and NH4+ transport simultaneously by intact wheat seedlings. Plant, Cell & Environment 9, 209–215.
A novel approach and a fully automated microcomputer‐based system to study kinetics of NO3, NO2, and NH4+ transport simultaneously by intact wheat seedlings.Crossref | GoogleScholarGoogle Scholar |

Hedden P, Proebsting WM (1999) Genetic analysis of gibberellin biosynthesis. Plant Physiology 119, 365–370.
Genetic analysis of gibberellin biosynthesis.Crossref | GoogleScholarGoogle Scholar | 9952430PubMed |

Heilersig BH, Loonen AE, Wolters A-MA, Visser RG (2006) Presence of an intron in inverted repeat constructs does not necessarily have an effect on efficiency of post-transcriptional gene silencing. Molecular Breeding 17, 307–316.
Presence of an intron in inverted repeat constructs does not necessarily have an effect on efficiency of post-transcriptional gene silencing.Crossref | GoogleScholarGoogle Scholar |

Hsu P-K, Tsay Y-F (2013) Two phloem nitrate transporters, NRT1. 11 and NRT1. 12, are important for redistributing xylem-borne nitrate to enhance plant growth. Plant Physiology 163, 844–856.
Two phloem nitrate transporters, NRT1. 11 and NRT1. 12, are important for redistributing xylem-borne nitrate to enhance plant growth.Crossref | GoogleScholarGoogle Scholar | 24006285PubMed |

Hu B, Wang W, Ou S, Tang J, Li H, Che R, Zhang Z, Chai X, Wang H, Wang Y (2015) Variation in NRT1. 1B contributes to nitrate-use divergence between rice subspecies. Nature Genetics 47, 834
Variation in NRT1. 1B contributes to nitrate-use divergence between rice subspecies.Crossref | GoogleScholarGoogle Scholar | 26053497PubMed |

Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M, Koshiba T, Kamiya Y, Seo M (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proceedings of the National Academy of Sciences of the United States of America 109, 9653–9658.
Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor.Crossref | GoogleScholarGoogle Scholar | 22645333PubMed |

Karimi M, Inzé D, Depicker A (2002) GATEWAY™ vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193–195.
GATEWAY™ vectors for Agrobacterium-mediated plant transformation.Crossref | GoogleScholarGoogle Scholar | 11992820PubMed |

Kende H, Zeevaart J (1997) The five ‘classical’ plant hormones. The Plant Cell 9, 1197
The five ‘classical’ plant hormones.Crossref | GoogleScholarGoogle Scholar | 12237383PubMed |

Klaassen MT, Bourke PM, Maliepaard C, Trindade LM (2019a) Multi-allelic QTL analysis of protein content in a bi-parental population of cultivated tetraploid potato. Euphytica 215, 14
Multi-allelic QTL analysis of protein content in a bi-parental population of cultivated tetraploid potato.Crossref | GoogleScholarGoogle Scholar | 30872859PubMed |

Klaassen MT, Willemsen JH, Vos PG, Visser RG, van Eck HJ, Maliepaard CA, Trindade LM (2019b) Genome-wide association analysis in tetraploid potato reveals four QTLs for protein content. Molecular Breeding 39, 151
Genome-wide association analysis in tetraploid potato reveals four QTLs for protein content.Crossref | GoogleScholarGoogle Scholar |

Krapp A, David LC, Chardin C, Girin T, Marmagne A, Leprince A-S, Chaillou S, Ferrario-Méry S, Meyer C, Daniel-Vedele F (2014) Nitrate transport and signalling in Arabidopsis. Journal of Experimental Botany 65, 789–798.
Nitrate transport and signalling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24532451PubMed |

Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K (2010) Nitrate-regulated auxin transport by NRT1. 1 defines a mechanism for nutrient sensing in plants. Developmental Cell 18, 927–937.
Nitrate-regulated auxin transport by NRT1. 1 defines a mechanism for nutrient sensing in plants.Crossref | GoogleScholarGoogle Scholar | 20627075PubMed |

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |

Lee R, Drew M (1986) Nitrogen-13 studies of nitrate fluxes in barley roots: II. Effect of plant N-status on the kinetic parameters of nitrate influx. Journal of Experimental Botany 37, 1768–1779.
Nitrogen-13 studies of nitrate fluxes in barley roots: II. Effect of plant N-status on the kinetic parameters of nitrate influx.Crossref | GoogleScholarGoogle Scholar |

Liu KH, Tsay YF (2003) Switching between the two action modes of the dual‐affinity nitrate transporter CHL1 by phosphorylation. EMBO Journal 22, 1005–1013.
Switching between the two action modes of the dual‐affinity nitrate transporter CHL1 by phosphorylation.Crossref | GoogleScholarGoogle Scholar | 12606566PubMed |

Liu K-H, Huang C-Y, Tsay Y-F (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. The Plant Cell 11, 865–874.
CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake.Crossref | GoogleScholarGoogle Scholar | 10330471PubMed |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |

Lopez-Pardo R, Ruiz de Galarreta JI, Ritter E (2013) Selection of housekeeping genes for qRT-PCR analysis in potato tubers under cold stress. Molecular Breeding 31, 39–45.
Selection of housekeeping genes for qRT-PCR analysis in potato tubers under cold stress.Crossref | GoogleScholarGoogle Scholar |

Martinoia E, Heck U, Wiemken A (1981) Vacuoles as storage compartments for nitrate in barley leaves. Nature 289, 292
Vacuoles as storage compartments for nitrate in barley leaves.Crossref | GoogleScholarGoogle Scholar |

Meharg A, Blatt M (1995) NO3– transport across the plasma membrane of Arabidopsis thaliana root hairs: kinetic control by pH and membrane voltage. The Journal of Membrane Biology 145, 49–66.
NO3 transport across the plasma membrane of Arabidopsis thaliana root hairs: kinetic control by pH and membrane voltage.Crossref | GoogleScholarGoogle Scholar | 7636885PubMed |

Meyer C, Stitt M (2001) Nitrate reduction and signalling. In ‘Plant nitrogen’. (Eds PJ Lea, JF Morot-Gaudry) pp. 37–59. (Springer: Berlin)

Miller AJ, Smith SJ (1996) Nitrate transport and compartmentation in cereal root cells. Journal of Experimental Botany 47, 843–854.
Nitrate transport and compartmentation in cereal root cells.Crossref | GoogleScholarGoogle Scholar |

Nicot N, Hausman J-F, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. Journal of Experimental Botany 56, 2907–2914.
Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress.Crossref | GoogleScholarGoogle Scholar | 16188960PubMed |

Odell JT, Nagy F, Chua N-H (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313, 810
Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter.Crossref | GoogleScholarGoogle Scholar | 3974711PubMed |

Peng S (1992) Leaf thickness affects the estimation of leaf nitrogen concentration using a chlorophyll meter. International Rice Research Notes 17, 19–20.

Rentsch D, Boorer K, Frommer W (1998) Structure and function of plasma membrane amino acid, oligopeptide and sucrose transporters from higher plants. The Journal of Membrane Biology 162, 177–190.
Structure and function of plasma membrane amino acid, oligopeptide and sucrose transporters from higher plants.Crossref | GoogleScholarGoogle Scholar | 9543490PubMed |

Ruiz-Cristin J, Briskin DP (1991) Characterization of a H+NO3– symport associated with plasma membrane vesicles of maize roots using 36CIO3– as a radiotracer analog. Archives of Biochemistry and Biophysics 285, 74–82.
Characterization of a H+NO3 symport associated with plasma membrane vesicles of maize roots using 36CIO3 as a radiotracer analog.Crossref | GoogleScholarGoogle Scholar | 1990981PubMed |

Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.

Scott R, Ogunremi E, Ivins J, Mendham N (1973) The effect of fertilizers and harvest date on growth and yield of oilseed rape sown in autumn and spring. The Journal of Agricultural Science 81, 287–293.
The effect of fertilizers and harvest date on growth and yield of oilseed rape sown in autumn and spring.Crossref | GoogleScholarGoogle Scholar |

Takken FL, Luderer R, Gabriëls SH, Westerink N, Lu R, De Wit PJ, Joosten MH (2000) A functional cloning strategy, based on a binary PVX‐expression vector, to isolate HR‐inducing cDNAs of plant pathogens. The Plant Journal 24, 275–283.
A functional cloning strategy, based on a binary PVX‐expression vector, to isolate HR‐inducing cDNAs of plant pathogens.Crossref | GoogleScholarGoogle Scholar | 11069701PubMed |

Touraine B, Glass AD (1997) NO3– and ClO3– fluxes in the chl1-5 mutant of Arabidopsis thaliana (Does the CHL1-5 gene encode a low-affinity NO3– transporter?). Plant Physiology 114, 137–144.
NO3 and ClO3 fluxes in the chl1-5 mutant of Arabidopsis thaliana (Does the CHL1-5 gene encode a low-affinity NO3 transporter?).Crossref | GoogleScholarGoogle Scholar | 9159946PubMed |

Varala K, Marshall-Colón A, Cirrone J, Brooks MD, Pasquino AV, Léran S, Mittal S, Rock TM, Edwards MB, Kim GJ (2018) Temporal transcriptional logic of dynamic regulatory networks underlying nitrogen signaling and use in plants. Proceedings of the National Academy of Sciences of the United States of America 115, 6494–6499.
Temporal transcriptional logic of dynamic regulatory networks underlying nitrogen signaling and use in plants.Crossref | GoogleScholarGoogle Scholar | 29769331PubMed |

Visser RG, Stolte A, Jacobsen E (1991) Expression of a chimaeric granule-bound starch synthase-GUS gene in transgenic potato plants. Plant Molecular Biology 17, 691–699.
Expression of a chimaeric granule-bound starch synthase-GUS gene in transgenic potato plants.Crossref | GoogleScholarGoogle Scholar | 1912493PubMed |

Wang YY, Cheng YH, Chen KE, Tsay YF (2018) Nitrate transport, signaling, and use efficiency. Annual Review of Plant Biology 69, 85–122.
Nitrate transport, signaling, and use efficiency.Crossref | GoogleScholarGoogle Scholar | 29570365PubMed |

Werij JS (2011) Genetic analysis of potato tuber quality traits. PhD thesis, Wageningen University, Wageningen, The Netherlands. Available at http://edepot.wur.nl/183746 [Verified 19 February 2020]

Westermann D, Tindall T, James D, Hurst R (1994) Nitrogen and potassium fertilization of potatoes: yield and specific gravity. American Potato Journal 71, 417–431.
Nitrogen and potassium fertilization of potatoes: yield and specific gravity.Crossref | GoogleScholarGoogle Scholar |

Williamson JD, Hirsch-Wyncott ME, Larkins BA, Gelvin SB (1989) Differential accumulation of a transcript driven by the CaMV 35S promoter in transgenic tobacco. Plant Physiology 90, 1570–1576.
Differential accumulation of a transcript driven by the CaMV 35S promoter in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 16666967PubMed |

Withrow AP (1945) The interrelationship of nitrogen supply and photoperiod on the flowering, growth and stem anatomy of certain long and short day plants. Butler University Botanical Studies 7, 40–64.

Xu X, Dechesne A, Visser RG, Trindade LM (2016) Expression of an (engineered) 4,6-α-glucanotransferase in potato results in changes in starch characteristics. PLoS One 11, e0166981
Expression of an (engineered) 4,6-α-glucanotransferase in potato results in changes in starch characteristics.Crossref | GoogleScholarGoogle Scholar | 28005970PubMed |

Zebarth B, Rosen CJ (2007) Research perspective on nitrogen BMP development for potato. American Journal of Potato Research 84, 3–18.
Research perspective on nitrogen BMP development for potato.Crossref | GoogleScholarGoogle Scholar |

Zhou J-J, Fernández E, Galván A, Miller AJ (2000) A high affinity nitrate transport system from Chlamydomonas requires two gene products. FEBS Letters 466, 225–227.
A high affinity nitrate transport system from Chlamydomonas requires two gene products.Crossref | GoogleScholarGoogle Scholar | 10682832PubMed |

Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In ‘Evolving genes and proteins’. (Eds V Bryson, HJ Vogel) pp. 97–166. (Academic Press: New York)