The Functional Diversity of the High-Affinity Nitrate Transporter Gene Family in Hexaploid Wheat: Insights from Distinct Expression Profiles
Abstract
:1. Introduction
2. Results
2.1. Wheat NRT2 and NRT3 Gene Family Genome and Phylogeny Analysis
2.2. Phylogenetic Relationship of NRT2 from Wheat and Other Plant Species
2.3. Transcriptional Regulation of NRT2 and NRT3 in Response to N Starvation
2.4. Transcriptional Regulation of NRT2 and NRT3 to Nitrate Provision/Induction
2.5. Spatial Expression Analysis of the NRT2 and NRT3 in Field-Grown Wheat
3. Discussion
3.1. The NRT2 Family in Wheat Consist of Multiple Genes Organized in Three Clades
3.2. Distinct Expression Profiles Revealed Specific Functional Roles
3.2.1. NRT2 Clade 1
3.2.2. NRT2 Clade 2
3.2.3. NRT2 Clade 3
3.2.4. NRT3
3.2.5. Implications in Improving the NUE
4. Materials and Methods
4.1. Identification and Phylogenetic Analysis of the NRT2 and NRT3 Genes in the Wheat Genome
4.2. Secondary Transmembrane Structure Analysis of the NRT2 and NRT3 Protein Sequences
4.3. Plant Material and Hydroponic Culture
4.4. Total RNA Extraction and Total N Analysis
4.5. Quantitative Reverse Transcription-PCR (RT-qPCR)
4.6. Statistical Analysis and Visualization
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Gene | GeneID | Chr | Start | End | Strand | Protein Length (aa) | [26] | [27] | [28] |
---|---|---|---|---|---|---|---|---|---|
TaNRT2.1-6A | TraesCS6A02G031200 | 6A | 15,781,020 | 15,782,725 | −1 | 509 | TaNRT2.1-A6 | TaNRT2-6A6 | TaNRT2-6A.6 |
TaNRT2.1-6B | TraesCS6B02G044000 | 6B | 26,591,111 | 26,592,640 | 1 | 509 | TaNRT2.1-B6 | TaNRT2-6B6 | TaNRT2-6B.1 |
TaNRT2.1-6D | TraesCS6D02G035600 | 6D | 14,618,629 | 14,620,585 | 1 | 509 | TaNRT2.1-D6 | TaNRT2-6D6 | TaNRT2-6D.1 |
TaNRT2.2-6A | TraesCS6A02G031100 | 6A | 15,765,759 | 15,767,783 | 1 | 507 | TaNRT2.1-A4 | TaNRT2-6A5 | TaNRT2-6A.5 |
TaNRT2.2-6B | TraesCS6B02G044100 | 6B | 26,596,252 | 26,597,775 | −1 | 507 | TaNRT2.1-B4 | TaNRT2-6B1 | TaNRT2-6B.2 |
TaNRT2.2-6D | TraesCS6D02G035800LC | 6D | 14,624,460 | 14,625,647 | −1 | 395 | NA | NA | TaNRT2-6D.2 |
TaNRT2.3-6A | TraesCS6A02G031000 | 6A | 15,756,560 | 15,758,437 | 1 | 507 | TaNRT2.1-A3 | TaNRT2-6A4 | TaNRT2-6A.4 |
TaNRT2.3-6B | TraesCS6B02G044200 | 6B | 26,616,491 | 26,618,567 | −1 | 507 | TaNRT2.1-B3 | TaNRT2-6B4 | TaNRT2-6B.3 |
TaNRT2.3-6D | TraesCS6D02G035700 | 6D | 14,631,385 | 14,633,069 | −1 | 507 | TaNRT2.1-D3 | TaNRT2-6D4 | TaNRT2-6D.3 |
TaNRT2.4-6A | TraesCS6A02G030900 | 6A | 15,747,526 | 15,749,383 | 1 | 507 | TaNRT2.1-A5 | TaNRT2-6A3 | TaNRT2-6A.3 |
TaNRT2.4-6B | TraesCS6B02G044300 | 6B | 26,625,403 | 26,626,926 | −1 | 507 | TaNRT2.1-B5 | TaNRT2-6B3 | TaNRT2-6B.4 |
TaNRT2.4-6D | TraesCS6D02G035800 | 6D | 14,655,066 | 14,656,589 | −1 | 507 | TaNRT2.1-D5 | TaNRT2-6D3 | TaNRT2-6D.4 |
TaNRT2.5-6A | TraesCS6A02G030800 | 6A | 15,734,520 | 15,736,043 | 1 | 507 | TaNRT2.1-A2 | TaNRT2-6A2 | TaNRT2-6A.2 |
TaNRT2.5-6B | TraesCS6B02G044400 | 6B | 26,633,039 | 26,634,966 | −1 | 565 | TaNRT2.1-B2 | TaNRT2-6B2 | TaNRT2-6B.5 |
TaNRT2.5-6D | TraesCS6D02G036100LC | 6D | 14,662,011 | 14,664,928 | −1 | 305 | NA | NA | TaNRT2-6D.5 |
TaNRT2.6-6A | TraesCS6A02G030700 | 6A | 15,727,844 | 15,729,367 | 1 | 507 | TaNRT2.1-A1 | TaNRT2-6A1 | TaNRT2-6A.1 |
TaNRT2.6-6B | TraesCS6B02G044500 | 6B | 26,644,113 | 26,645,632 | −1 | 485 | TaNRT2.1-B1 | TaNRT2-6B5 | TaNRT2-6B.6 |
TaNRT2.6-6D | TraesCS6D02G035900 | 6D | 14,679,252 | 14,680,775 | −1 | 507 | TaNRT2.1-D1 | TaNRT2-6D2 | TaNRT2-6D.6 |
TaNRT2.7-6A | TraesCS6A02G032400 | 6A | 15,951,566 | 15,953,536 | −1 | 508 | TaNRT2.2-A2-1 | TaNRT2-6A7 | TaNRT2-6A.7 |
TaNRT2.7-6B | TraesCS6B02G045600 | 6B | 27,122,861 | 27,124,387 | −1 | 508 | TaNRT2.2-B2-1 | TaNRT2-6B7 | TaNRT2-6B.7 |
TaNRT2.7-6D | TraesCS6D02G037200 | 6D | 15,383,513 | 15,385,158 | −1 | 508 | TaNRT2.2-D2-1 | TaNRT2-6D7 | TaNRT2-6D.7 |
TaNRT2.8-6A | TraesCS6A02G032500 | 6A | 16,098,637 | 16,100,163 | −1 | 508 | TaNRT2.2-A2-2 | TaNRT2-6A8 | TaNRT2-6A.8 |
TaNRT2.8-6B | TraesCS6B02G045700 | 6B | 27,169,710 | 27,171,230 | −1 | 506 | TaNRT2.2-B2-2 | TaNRT2-6B8 | TaNRT2-6B.8 |
TaNRT2.8-6D | TraesCS6D02G037300 | 6D | 15,418,086 | 15,419,612 | −1 | 508 | TaNRT2.2-D2-2 | TaNRT2-6D8 | TaNRT2-6D.8 |
TaNRT2.9-6B | 6B | 27,180,298 | 27,181,751 | −1 | NA | NA | NA | ||
TaNRT2.9-6D | 6D | 15,426,752 | 15,427,967 | −1 | NA | NA | NA | ||
TaNRT2.10-6A | TraesCS6A02G032800 | 6A | 16,357,746 | 16,359,603 | 1 | 507 | TaNRT2.2-A1 | TaNRT2-6A9 | TaNRT2-6A.9 |
TaNRT2.10-6B | TraesCS6B02G046500 | 6B | 27,685,182 | 27,687,046 | 1 | 507 | TaNRT2.2-B1 | TaNRT2-6B9 | TaNRT2-6B.9 |
TaNRT2.10-6D | TraesCS6D02G037800 | 6D | 15,658,356 | 15,659,879 | 1 | 507 | TaNRT2.2-D1 | TaNRT2-6D9 | TaNRT2-6D.9 |
TaNRT2.11-6A | TraesCS6A02G032900 | 6A | 16,374,353 | 16,376,212 | −1 | 509 | TaNRT2.2-A4-1 | TaNRT2-6A10 | TaNRT2-6A.10 |
TaNRT2.11-6B | TraesCS6B02G059100LC | 6B | 27,709,217 | 27,771,770 | −1 | 197 | NA | NA | NA |
TaNRT2.11-6D | TraesCS6D02G037900 | 6D | 15,696,840 | 15,698,711 | −1 | 509 | TaNRT2.2-D4-1 | TaNRT2-6D10 | TaNRT2-6D.10 |
TaNRT2.11-U | TraesCSU02G507900LC | U | 356,326,164 | 356,329,757 | 1 | 197 | NA | NA | NA |
TaNRT2.12-6D | TraesCS6D02G038000 | 6D | 15,710,039 | 15,711,562 | −1 | 507 | TaNRT2.2-D4-2 | TaNRT2-6D11y | TaNRT2-6D.11 |
TaNRT2.13-6A | TraesCS6A02G033000 | 6A | 16,386,427 | 16,388,254 | −1 | 509 | TaNRT2.2-A4-2 | TaNRT2-6A11 | TaNRT2-6A.11 |
TaNRT2.13-6B | TraesCS6B02G046600 | 6B | 27,778,038 | 27,779,912 | −1 | 509 | TaNRT2.2-B4 | TaNRT2-6B11 | TaNRT2-6B.10 |
TaNRT2.13-6D | TraesCS6D02G038100 | 6D | 15,745,837 | 15,748,091 | −1 | 509 | TaNRT2.2-D4-3 | TaNRT2-6D11x | TaNRT2-6D.12 |
TaNRT2.14A-6A | TraesCS6A02G033100 | 6A | 16,398,961 | 16,400,795 | −1 | 508 | TaNRT2.2-A3-1 | TaNRT2-6A12 | TaNRT2-6A.12 |
TaNRT2.14A-6B | TraesCS6B02G059400LC | 6B | 27,805,416 | 27,805,802 | −1 | 128 | NA | NA | NA |
TaNRT2.14A-6D | TraesCS6D02G038200 | 6D | 15,797,524 | 15,799,374 | −1 | 508 | TaNRT2.2-D3-1 | TaNRT2-6D13 | TaNRT2-6D.13 |
TaNRT2.14B-6A | TraesCS6A02G033200 | 6A | 16,408,185 | 16,410,137 | −1 | 508 | TaNRT2.2-A3-2 | TaNRT2-6A13 | TaNRT2-6A.13 |
TaNRT2.14B-6B | TraesCS6B02G046700 | 6B | 27,818,480 | 27,820,351 | −1 | 508 | TaNRT2.2-B3 | TaNRT2-6B13 | TaNRT2-6B.11 |
TaNRT2.14B-6D | TraesCS6D02G038300 | 6D | 15,807,091 | 15,808,955 | −1 | 508 | TaNRT2.2-D3-2 | TaNRT2-6D12 | TaNRT2-6D.14 |
TaNRT2.14C-6D | 6D | 15,781,861 | 15,784,445 | −1 | 501 | NA | NA | NA | |
TaNRT2.15-2A | TraesCS2A02G074800 | 2A | 33,054,150 | 33,056,031 | 1 | 502 | TaNRT2.3-A1 | TaNRT2-2A1 | TaNRT2-2A |
TaNRT2.15-2D | TraesCS2D02G073500 | 2D | 30,787,486 | 30,789,242 | 1 | 499 | TaNRT2.3-D1 | TaNRT2-2D1 | TaNRT2-2D |
TaNRT2.16-3A | TraesCS3A02G254000 | 3A | 475,304,797 | 475,306,341 | −1 | 514 | TaNRT2.4-A1 | TaNRT2-3A1 | TaNRT2-3A |
TaNRT2.16-3B | TraesCS3B02G285900 | 3B | 457,633,984 | 457,635,782 | −1 | 514 | TaNRT2.4-B1 | TaNRT2-3B1 | TaNRT2-3B |
TaNRT2.16-3D | TraesCS3D02G254900 | 3D | 356,623,041 | 356,624,585 | −1 | 514 | TaNRT2.4-D1 | TaNRT2-3D1 | TaNRT2-3D |
TaNRT2.17-U | TraesCSU02G002800 | (1B) | 2,667,931 | 2,669,478 | −1 | 515 | TaNRT2.4-3 | TaNRT2-Un1 | TaNRT2-U.1 |
TaNRT2.17-1D | TraesCS1D02G035700 | 1D | 16,504,613 | 16,506,169 | 1 | 518 | TaNRT2.4-2 | TaNRT2-1D1 | TaNRT2-1D |
TaNRT2.18-7A | TraesCS7A02G428500 | 7A | 621,910,950 | 621,913,739 | 1 | 468 | TaNRT2.5-A1 | TaNRT2-7A1 | TaNRT2-7A |
TaNRT2.18-7B | TraesCS7B02G328700 | 7B | 583,923,053 | 583,926,829 | 1 | 486 | TaNRT2.5-B1 | TaNRT2-7B1 | TaNRT2-7B |
TaNRT2.18-7D | TraesCS7D02G420900 | 7D | 540,617,018 | 540,627,808 | 1 | 483 | TaNRT2.5-D1 | TaNRT2-7D1 | TaNRT2-7D |
TaNRT3.1-6A | TraesCS6A02G209900 | 6A | 380,361,041 | 380,362,225 | −1 | 198 | TaNAR2.1-A1 | NA | NA |
TaNRT3.1-6B | TraesCS6B02G238700 | 6B | 415,788,848 | 415,790,024 | −1 | 198 | TaNAR2.1-B1 | NA | NA |
TaNRT3.1-6D | TraesCS6D02G193100 | 6D | 267,236,634 | 267,237,837 | −1 | 198 | TaNAR2.1-D1 | NA | NA |
TaNRT3.2-6A | TraesCS6A02G210000 | 6A | 381,025,658 | 381,028,549 | −1 | 251 | TaNAR2.2-A1 | NA | NA |
TaNRT3.2-6B | TraesCS6B02G238800 | 6B | 415,863,369 | 415,864,548 | −1 | 198 | TaNAR2.2-B1 | NA | NA |
TaNRT3.2-6D | TraesCS6D02G193200 | 6D | 267,514,716 | 267,515,418 | −1 | 198 | TaNAR2.2-D1 | NA | NA |
TaNRT3.3-4A | TraesCS4A02G367300 | 4A | 640,232,228 | 640,233,158 | 1 | 255 | TaNAR2.3-A1 | NA | NA |
TaNRT3.3-5B | TraesCS5B02G719500LC | 5B | 671,187,506 | 671,188,471 | −1 | 236 | NA | NA | NA |
TaNRT3.3-5D | TraesCS5D02G506100 | 5D | 531,971,003 | 531,972,109 | −1 | 199 | TaNAR2.3-D1 | NA | NA |
TaNRT3.4-5B | TraesMAC5B03G03000180 | 5B | 671,130,989 | 671,138,061 | −1 | 181 | NA | NA | NA |
TaNRT3.4-5D | TraesMAC5D03G03214570 | 5D | 531,900,482 | 531,902,366 | −1 | 190 | NA | NA | NA |
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Sigalas, P.P.; Buchner, P.; Kröper, A.; Hawkesford, M.J. The Functional Diversity of the High-Affinity Nitrate Transporter Gene Family in Hexaploid Wheat: Insights from Distinct Expression Profiles. Int. J. Mol. Sci. 2024, 25, 509. https://doi.org/10.3390/ijms25010509
Sigalas PP, Buchner P, Kröper A, Hawkesford MJ. The Functional Diversity of the High-Affinity Nitrate Transporter Gene Family in Hexaploid Wheat: Insights from Distinct Expression Profiles. International Journal of Molecular Sciences. 2024; 25(1):509. https://doi.org/10.3390/ijms25010509
Chicago/Turabian StyleSigalas, Petros P., Peter Buchner, Alex Kröper, and Malcolm J. Hawkesford. 2024. "The Functional Diversity of the High-Affinity Nitrate Transporter Gene Family in Hexaploid Wheat: Insights from Distinct Expression Profiles" International Journal of Molecular Sciences 25, no. 1: 509. https://doi.org/10.3390/ijms25010509