Genome-Wide Identification and Analysis of Apple NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER Family (NPF) Genes Reveals MdNPF6.5 Confers High Capacity for Nitrogen Uptake under Low-Nitrogen Conditions
Abstract
:1. Introduction
2. Results
2.1. Identification and Annotation of NPF Genes in Apple
2.2. Phylogenetic Tree of NPF in Apple
2.3. Chromosomal Localization Analysis of NPFs in Apple
2.4. Analyses of Conserved Domains and TM Regions
2.5. Comparison of Exon‒Intron Structures for NPF Genes in Apple and Other Species
2.6. Analysis of Expression for 14 MdNPFs in Response to Different Nitrate Concentrations
2.7. Effect of Low-Nitrogen Treatment on Growth by Apple Calli Tissue
3. Discussion
4. Materials and Methods
4.1. Identification of Apple NPF Genes
4.2. Sequence Alignment and Phylogenetic Analysis
4.3. Analyses of Exon‒Intron Structure and Genome Distribution
4.4. Sequence Logo and Prediction of TM Regions
4.5. Plant Materials and Nitrogen Treatments
4.6. Quantitative Real Time RT-PCR (qRT-PCR) and Gene-Cloning
4.7. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Gene Name | Gene ID a | Chromosome Location | ORF | Protein Length (aa) | MW (kDa) | Theoretical Isoeletrical Point (pI) | GenBank Accession Numbers of Cloned Gene |
---|---|---|---|---|---|---|---|
MdNPF1 | MD15G1190800 | Chr15:15008548-15011039 | 1779 | 593 | 65.21 | 8.90 | |
MdNPF2.1 | MD11G1122200 | Chr11:11243604-11246153 | 1656 | 552 | 60.36 | 8.14 | |
MdNPF2.2 | MD11G1121600 | Chr11:11225429-11227624 | 1404 | 468 | 51.09 | 8.99 | |
MdNPF2.3 | MD07G1180500 | Chr07:25970318-25972596 | 1539 | 513 | 56.69 | 9.27 | |
MdNPF2.4 | MD01G1112600 | Chr01:22682711-22685617 | 1662 | 554 | 60.53 | 9.25 | |
MdNPF2.5 | MD11G1122500 | Chr11:11284715-11290091 | 1698 | 566 | 61.85 | 8.86 | MG021338 |
MdNPF2.6 | MD03G1108900 | Chr03:9496734-9500175 | 1812 | 604 | 66.37 | 8.73 | MG021345 |
MdNPF2.7 | MD03G1108700 | Chr03:9467766-9470916 | 1683 | 561 | 61.53 | 8.96 | |
MdNPF2.8 | MD06G1186800 | Chr06:32435102-32437373 | 1809 | 603 | 67.17 | 9.61 | |
MdNPF2.9 | MD14G1193200 | Chr14:28393718-28396166 | 1866 | 622 | 69.34 | 8.88 | |
MdNPF2.10 | MD04G1137500 | Chr04:22509802-22511767 | 1764 | 588 | 64.55 | 8.76 | |
MdNPF2.11 | MD14G1193100 | Chr14:28376948-28379737 | 1746 | 482 | 64.43 | 9.00 | MG021332 |
MdNPF2.12 | MD06G1186500 | Chr06:32427308-32429277 | 1299 | 433 | 48.04 | 8.86 | |
MdNPF2.13 | MD16G1080100 | Chr16:5611393-5619434 | 1845 | 615 | 68.20 | 8.44 | |
MdNPF2.14 | MD16G1079900 | Chr16:5602664-5605755 | 1818 | 606 | 66.73 | 8.14 | |
MdNPF2.15 | MD16G1080000 | Chr16:5608051-5610469 | 1737 | 579 | 63.71 | 7.82 | |
MdNPF3.1 | MD13G1043200 | Chr13:3030935-3034949 | 1740 | 580 | 64.10 | 8.61 | MG021337 |
MdNPF3.2 | MD13G1043100 | Chr13:3013976-3017053 | 1776 | 592 | 65.47 | 8.61 | |
MdNPF3.3 | MD16G1044000 | Chr16:3127680-3131016 | 1743 | 581 | 64.24 | 8.34 | |
MdNPF4.1 | MD05G1164400 | Chr05:29316397-29322734 | 1308 | 436 | 48.37 | 7.39 | |
MdNPF4.2 | MD10G1153900 | Chr10:24150970-24153718 | 1605 | 535 | 59.31 | 9.33 | |
MdNPF4.3 | MD10G1154000 | Chr10:24171779-24174663 | 1602 | 534 | 59.02 | 8.26 | |
MdNPF4.4 | MD08G1248200 | Chr08:31226687-31231330 | 1842 | 614 | 67.84 | 8.30 | MG021342 |
MdNPF4.5 | MD15G1443100 | Chr15:54322869-54325021 | 1482 | 494 | 54.88 | 8.96 | |
MdNPF4.6 | MD05G1000900 | Chr05:293868-298577 | 1845 | 615 | 68.08 | 8.54 | |
MdNPF4.7 | MD13G1079300 | Chr13:5562578-5567885 | 1761 | 587 | 64.77 | 8.58 | |
MdNPF4.8 | MD16G1079100 | Chr16:5547983-5553360 | 1761 | 587 | 64.85 | 8.70 | |
MdNPF4.9 | MD14G1194100 | Chr14:28528146-28530941 | 1758 | 586 | 64.70 | 8.26 | |
MdNPF4.10 | MD08G1040500 | Chr08:2990042-2993173 | 1668 | 556 | 61.30 | 8.22 | |
MdNPF4.11 | MD04G1184500 | Chr04:27539356-27541647 | 1836 | 612 | 68.06 | 9.15 | |
MdNPF4.12 | MD12G1197700 | Chr12:27888187-27890493 | 1653 | 551 | 61.38 | 8.67 | |
MdNPF4.13 | MD10G1271800 | Chr10:36356975-36363499 | 1779 | 593 | 66.11 | 8.08 | |
MdNPF4.14 | MD05G1293900 | Chr05:42659455-42665121 | 1809 | 603 | 67.05 | 8.58 | |
MdNPF5.1 | MD07G1230600 | Chr07:30498119-30501840 | 1776 | 592 | 66.07 | 8.76 | MG021340 |
MdNPF5.2 | MD05G1192100 | Chr05:32036536-32040692 | 1809 | 603 | 67.23 | 9.30 | |
MdNPF5.3 | MD16G1224200 | Chr16:22556239-22559806 | 1644 | 548 | 61.45 | 8.57 | |
MdNPF5.4 | MD13G1218900 | Chr13:21148526-21157623 | 1806 | 602 | 67.12 | 9.36 | |
MdNPF5.5 | MD05G1342600 | Chr05:46297101-46299829 | 1779 | 593 | 66.26 | 9.22 | |
MdNPF5.6 | MD07G1039100 | Chr07:3293256-3295279 | 873 | 291 | 32.36 | 9.39 | |
MdNPF5.7 | MD07G1038900 | Chr07:3272734-3276872 | 1695 | 565 | 62.35 | 9.08 | |
MdNPF5.8 | MD07G1038800 | Chr07:3237655-3247764 | 1731 | 577 | 63.70 | 8.82 | |
MdNPF5.9 | MD07G1038600 | Chr07:3176293-3185619 | 1695 | 565 | 62.63 | 9.01 | |
MdNPF5.10 | MD07G1039600 | Chr07:3353966-3358684 | 1731 | 577 | 63.97 | 8.71 | |
MdNPF5.11 | MD04G1148300 | Chr04:23666705-23668537 | 1635 | 545 | 60.03 | 6.25 | |
MdNPF5.12 | MD04G1138500 | Chr04:22623404-22627516 | 1770 | 590 | 65.59 | 8.62 | |
MdNPF5.13 | MD12G1153900 | Chr12:23405312-23409371 | 1770 | 590 | 65.19 | 8.93 | MG021339 |
MdNPF5.14 | MD07G1205700 | Chr07:28355985-28360202 | 1794 | 598 | 67.03 | 8.77 | MG021344 |
MdNPF5.15 | MD01G1141500 | Chr01:25051572-25054193 | 1785 | 595 | 66.39 | 9.24 | |
MdNPF5.16 | MD17G1041000 | Chr17:2979487-2982673 | 1632 | 544 | 60.48 | 8.35 | MG021336 |
MdNPF5.17 | MD09G1040700 | Chr09:2607173-2618823 | 1581 | 527 | 58.64 | 8.79 | |
MdNPF5.18 | MD08G1218300 | Chr08:28077601-28080578 | 1080 | 360 | 40.06 | 5.25 | |
MdNPF5.19 | MD15G1406700 | Chr15:50693334-50695520 | 1317 | 439 | 48.70 | 6.36 | MG021331 |
MdNPF5.20 | MD15G1406500 | Chr15:50682947-50684829 | 1377 | 459 | 50.92 | 5.76 | |
MdNPF5.21 | MD07G1039200 | Chr07:3295281-3306861 | 825 | 275 | 29.88 | 8.94 | |
MdNPF6.1 | MD08G1022500 | Chr08:1648693-1654146 | 1551 | 517 | 57.45 | 9.00 | |
MdNPF6.2 | MD15G1019900 | Chr15:1155213-1159411 | 1869 | 623 | 69.53 | 8.46 | |
MdNPF6.3 | MD16G1142100 | Chr16:10938991-10941873 | 1914 | 638 | 70.17 | 8.56 | MG021341 |
MdNPF6.4 | MD13G1131800 | Chr13:10003867-10006664 | 1914 | 638 | 70.08 | 7.70 | |
MdNPF6.5 | MD15G1173800 | Chr15:13572779-13576346 | 1746 | 582 | 63.62 | 9.30 | MG021346 |
MdNPF6.6 | MD04G1086400 | Chr04:12553185-12555016 | 1011 | 337 | 36.83 | 8.33 | |
MdNPF6.7 | MD17G1103000 | Chr17:8745481-8748650 | 1773 | 591 | 65.11 | 9.24 | MG021333 |
MdNPF7.1 | MD11G1017300 | Chr11:1392309-1395225 | 1866 | 622 | 67.81 | 5.82 | |
MdNPF7.2 | MD03G1016700 | Chr03:1321170-1324060 | 2022 | 674 | 73.81 | 7.30 | |
MdNPF7.3 | MD03G1016400 | Chr03:1307373-1311107 | 1782 | 594 | 65.21 | 6.59 | |
MdNPF7.4 | MD07G1082700 | Chr07:8103711-8110134 | 1815 | 605 | 67.04 | 7.80 | |
MdNPF7.5 | MD02G1228800 | Chr02:27110155-27115346 | 1815 | 605 | 67.22 | 7.64 | |
MdNPF7.6 | MD06G1029400 | Chr06:3504379-3509435 | 1791 | 597 | 66.37 | 7.89 | |
MdNPF7.7 | MD16G1277800 | Chr16:37688341-37693389 | 1788 | 596 | 66.44 | 6.71 | |
MdNPF8.1 | MD12G1160700 | Chr12:24039618-24042029 | 1707 | 569 | 63.32 | 8.60 | MG021334 |
MdNPF8.2 | MD04G1147500 | Chr04:23563075-23568217 | 2061 | 687 | 76.60 | 8.76 | |
MdNPF8.3 | MD11G1081100 | Chr11:6913320-6915864 | 1728 | 576 | 63.96 | 8.11 | |
MdNPF8.4 | MD11G1081200 | Chr11:6931888-6934707 | 1749 | 583 | 64.77 | 8.62 | |
MdNPF8.5 | MD16G1010600 | Chr16:814341-817396 | 1758 | 586 | 64.39 | 7.18 |
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Wang, Q.; Liu, C.; Dong, Q.; Huang, D.; Li, C.; Li, P.; Ma, F. Genome-Wide Identification and Analysis of Apple NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER Family (NPF) Genes Reveals MdNPF6.5 Confers High Capacity for Nitrogen Uptake under Low-Nitrogen Conditions. Int. J. Mol. Sci. 2018, 19, 2761. https://doi.org/10.3390/ijms19092761
Wang Q, Liu C, Dong Q, Huang D, Li C, Li P, Ma F. Genome-Wide Identification and Analysis of Apple NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER Family (NPF) Genes Reveals MdNPF6.5 Confers High Capacity for Nitrogen Uptake under Low-Nitrogen Conditions. International Journal of Molecular Sciences. 2018; 19(9):2761. https://doi.org/10.3390/ijms19092761
Chicago/Turabian StyleWang, Qian, Changhai Liu, Qinglong Dong, Dong Huang, Cuiying Li, Pengmin Li, and Fengwang Ma. 2018. "Genome-Wide Identification and Analysis of Apple NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER Family (NPF) Genes Reveals MdNPF6.5 Confers High Capacity for Nitrogen Uptake under Low-Nitrogen Conditions" International Journal of Molecular Sciences 19, no. 9: 2761. https://doi.org/10.3390/ijms19092761