Association genetics of the parameters related to nitrogen use efficiency in Brassica juncea L.
G × E interactions
Indian mustard
N transporters
marker trait associations
morphological traits
nitrogen harvest index
Journal
Plant molecular biology
ISSN: 1573-5028
Titre abrégé: Plant Mol Biol
Pays: Netherlands
ID NLM: 9106343
Informations de publication
Date de publication:
Jan 2021
Jan 2021
Historique:
received:
31
03
2020
accepted:
23
09
2020
pubmed:
1
10
2020
medline:
5
1
2021
entrez:
30
9
2020
Statut:
ppublish
Résumé
Genome wide association studies allowed prediction of 17 candidate genes for association with nitrogen use efficiency. Novel information obtained may provide better understanding of genomic controls underlying germplasm variations for this trait in Indian mustard. Nitrogen use efficiency (NUE) of Indian mustard (Brassica juncea (L.) Czern & Coss.) is low and most breeding efforts to combine NUE with crop performance have not succeeded. Underlying genetics also remain unexplored. We tested 92 SNP-genotyped inbred lines for yield component traits, N uptake efficiency (NUPEFF), nitrogen utilization efficiency (NUTEFF), nitrogen harvest index (NHI) and NUE for two years at two nitrogen doses (N
Identifiants
pubmed: 32997301
doi: 10.1007/s11103-020-01076-x
pii: 10.1007/s11103-020-01076-x
doi:
Substances chimiques
Nitrogen
N762921K75
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
161-175Subventions
Organisme : Department of Biotechnology, Govt. of India
ID : BT/01/CEIB/12/I/03
Références
Avice JC, Etienne P (2014) Leaf senescence and nitrogen remobilization efficiency in oilseed rape (Brassica napus L.). J Exp Bot 65:3813–3824
pubmed: 24790115
Bi YM, Kant S, Clark J, Gidda S, Ming F, Xu J et al (2009) Increased nitrogen-use efficiency in transgenic rice plants over-expressing a nitrogen-responsive early nodulin gene identified from rice expression profiling. Plant Cell Environ 32:1749–1760
pubmed: 19682292
Bordes J, Ravel C, Jaubertie JP, Duperrier B, Gardet O, Heumez E, Pissavy AL, Charmet G, Le Gouis J, Balfourier F (2013) Genomic regions associated with the nitrogen limitation response revealed in a global wheat core collection. Theor Appl Genet 126:805–822
pubmed: 23192671
Bouchet AS, Laperche A, Bissuel-Belaygue C, Snowdon R, Nesi N, Stahl A (2016) Nitrogen use efficiency in rapeseed: A review. Agron Sustain Dev 36:38
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) Software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. doi: https://doi.org/10.1093/bioinformatics/btm308
doi: 10.1093/bioinformatics/btm308
pubmed: 17586829
Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81:1084–1097
pubmed: 17924348
pmcid: 2265661
Bruex A, Kainkaryam RM, Wieckowski Y, Kang YH, Bernhardt C, Xia Y et al (2012) A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLOS Genetics 8:e1002446
pubmed: 22253603
pmcid: 3257299
Brugiere N, Dubois F, Masclaux C, Sangwan RS, Hirel B (2000) Immunolocalization of glutamine synthetase in senescing tobacco (Nicotiana tabacum L.) leaves suggests that ammonia assimilation is progressively shifted to the mesophyll cytosol. Planta 211:519–527
pubmed: 11030551
Chamorro AM, Tamagno LN, Bezus R, Sarandon SJ (2002) Nitrogen accumulation, partition and nitrogen use efficiency in canola under different nitrogen availabilities. Commun Soil Sci Plan 33:493–504
Chen LS, Bush DR (1997) LHT1, a lysine- and histidine-specific amino acid transporter in Arabidopsis. Plant Physiol 115:1127–1134
pubmed: 9390441
pmcid: 158577
Chen X, Cui Z, Fan M, Vitousek P, Zhao M, Ma W, Wang Z, Zhang W, Yan X, Yang J, Deng X, Gao Q et al (2014) Producing more grain with lower environmental costs. Nature 514:486–489
pubmed: 25186728
Chiba A, Ishida H, Nishizawa NK, Makino A, Mae T (2003) Exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts by specific bodies in naturally-senescing leaves of wheat. Plant Cell Physiol 44:914–921
pubmed: 14519773
Cormier F, Le Gouis J, Dubreuil P, Lafarge S, Praud S (2014) A genome-wide identification of chromosomal regions determining nitrogen use efficiency components in wheat (Triticum aestivum L.). Theor Appl Genet 127:2679–2693
pubmed: 25326179
Crawford NM, Forde BG (2002) Molecular and developmental biology of inorganic nitrogen nutrition. Arabidopsis Book 1:e0011
pubmed: 22303192
pmcid: 3243300
Dechorgnat J, Nguyen CT, Armengaud P, Jossier M, Diatloff E, Filleur S, Daniel-Vedele F (2011) From the soil to the seeds: The long journey of nitrate in plants. J Exp Bot 62:1349–1359
pubmed: 21193579
Diaz C, Lemaitre T, Christ A, Azzopardi M, Kato Y, Sato F et al (2008) Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol 147:1437–1449
pubmed: 18467460
pmcid: 2442554
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Duitama J, Quintero JC, Cruz DF et al (2014) An integrated framework for discovery and genotyping of genomic variants from high-throughput sequencing experiments. Nucleic Acids Res 42:e44
pubmed: 24413664
pmcid: 3973327
Edwards D, Batley J, Snowdon RJ (2013) Accessing complex crop genomes with next-generation sequencing. Theor Appl Genet 126:1–11
pubmed: 22948437
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLOS ONE 6:e19379
pubmed: 21573248
pmcid: 3087801
Faes P, Deleu C, Ainouche A, Le Caherec F, Montes E, Clouet V, Gouraud AM, Albert B, Orsel M, Lassalle G, Leport L, Bouchereau A, Niogret MF (2015) Molecular evolution and transcriptional regulation of the oilseed rape proline dehydrogenase genes suggest distinct roles of proline catabolism during development. Planta 241:403–419
pubmed: 25326771
Fan X, Naz M, Fan X, Xuan W, Miller AJ, Xu G (2017) Plant nitrate transporters: from gene function to application. J Exp Bot 68:2463–2475
pubmed: 28158856
Feller U, Anders I, Mae T (2008) Rubisco lytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59:1615–1624
pubmed: 17975207
Fontaine JX, Ravel C, Pageau K, Heumez E, Dubois F, Hirel B, Le Gouis J (2009) A quantitative genetic study for elucidating the contribution of glutamine synthetase, glutamate dehydrogenase and other nitrogen-related physiological traits to the agronomic performance of common wheat. Theor Appl Genet 119:645–662
pubmed: 19513687
Fuchsberger C, Abecasis GR, Hinds DA (2015) minimac2: faster genotype imputation. Bioinformatics 31(5):782–784. doi: https://doi.org/10.1093/bioinformatics/btu704
doi: 10.1093/bioinformatics/btu704
pubmed: 25338720
Gallais A, Coque M (2005) Genetic variation and selection for nitrogen use efficiency in maize: a synthesis. Maydica 50:531
Gallais A, Hirel B (2004) An approach to the genetics of nitrogen use efficiency in maize. J Exp Bot 55:295–306
pubmed: 14739258
Ganeteg U, Ahmad I, Jamtgard S, Aguetoni-Cambui C, Inselsbacher E, Svennerstam H, Schmidt S, Nasholm T (2017) Amino acid transporter mutants of Arabidopsis provides evidence that a non-mycorrhizal plant acquires organic nitrogen from agricultural soil. Plant Cell Environ 40:413–423
pubmed: 27943312
Garcia-Ferris C, Moreno J (1994) Oxidative modification and breakdown of ribulose-1, 5-bisphosphate carboxylase/oxygenase induced in Euglena gracitis by nitrogen starvation. Planta 193:208–215
Glass ADM (2009) Nitrate uptake by plant roots. Botany 87:659
Good AG, Beatty PH (2011) Fertilizing nature: a tragedy of excess in the commons. PLOS Biology 9:e1001124
pubmed: 21857803
pmcid: 3156687
Gotz S, García-Gómez JM, Terol J et al (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435
pubmed: 18445632
pmcid: 2425479
Guiboileau A, Yoshimoto K, Soulay F, Bataille MP, Avice JC, Masclaux-Daubresse C (2012) Autophagy machinery controls nitrogen remobilization at the whole‐plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytol 194:732–740
pubmed: 22404536
Gupta S, Akhatar J, Kaur P, Sharma A, Sharma P, Mittal M, Bharti B, Banga SS (2019) Genetic analyses of nitrogen assimilation enzymes in Brassica juncea (L.) Czern & Coss. Mol Biol Rep 46(4):4235–4244. https://doi.org/10.1007/s11033-019-04878-5
doi: 10.1007/s11033-019-04878-5
pubmed: 31115836
Habash DZ, Massiah AJ, Rong HL, Wallsgrove RM, Leigh RA (2001) The role of cytosolic glutamine synthetase in wheat. Ann Appl Biol 138:83–89
Han Y, Xin M, Hunag K, Xu Y, Liu Z, Hu Z, Yao Y, Peng H, Ni Z, Sun Q (2016) Altered expression of TaRSL4 gene by genome interplay shapes root hair length in allopolyploid wheat. New Phytol 209:721–732
pubmed: 26334764
Hao QN, Zhou XA, Sha AH, Wang C, Zhou R, Chen SL (2011) Identification of genes associated with nitrogen use efficiency by genome-wide transcriptional analysis of two soybean genotypes. BMC Genom 12:525
He H, Yang R, Li Y, Ma A, Cao L, Wu X, Chen B, Tian H, Gao Y (2017) Genotypic variation in nitrogen utilization efficiency of oilseed rape (Brassica napus) under contrasting N supply in pot and field experiments. Front Plant Sci 8:1825
pubmed: 29163565
pmcid: 5664426
Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946
pubmed: 16816136
pmcid: 1533986
Huang XH, Han B (2014) Natural variations and genome-wide association studies in crop plants. Annu Rev Plant Biol 65:531–551
pubmed: 24274033
Ikeyama Y, Tasaka M, Fukaki H (2010) RLF, a cytochrome b5-like heme/steroid binding domain protein, controls lateral root formation independently of ARF7/19‐mediated auxin signaling in Arabidopsis thaliana. Plant J 62:865–875
pubmed: 20230485
Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T (2008) Mobilization of Rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol 148:142–155
pubmed: 18614709
pmcid: 2528122
Izumi M, Wada S, Makino A, Ishida H (2010) The autophagic degradation of chloroplasts via rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiol 154:1196–1209
pubmed: 20807997
pmcid: 2971599
Jan HU, Abbadi A, Lucke S, Nichols RA, Snowdon RJ (2016) Genomic prediction of testcross performance in canola (Brassica napus). PLoS One 11:e0147769
pubmed: 26824924
pmcid: 4732662
Kichey T, Hirel B, Heumez E, Dubois F, Le Gouis J (2007) In winter wheat (Triticum aestivum L.), post-anthesis nitrogen uptake and remobilisation to the grain correlates with agronomic traits and nitrogen physiological markers. Field Crop Res 102:22–32
Kjeldahl J (1883) Neue Methode zur Bestimmung des Stickstoffs in organischen K¨orpern. Fresenius’ Zeitschrift für Analytische Chemie 22:366–382
Laine P, Ourry A, Boucaud J (1995) Shoot control of nitrate uptake rates by roots of Brassica napus L.: Effects of localized nitrate supply. Planta 1961:77–83
Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
pubmed: 22388286
pmcid: 3322381
Leleu O, Vuylstecker C, Tetu JF, Degrande D, Champolivier L, Rambour S (2000) Effect of two contrasted N fertilizations on rapeseed growth and nitrate metabolism. Plant Physiol Bioch 38:639–645
Lemaitre T, Gaufichon L, Boutet-Mercey S, Christ A, Masclaux-Daubresse C (2008) Enzymatic and metabolic diagnostic of nitrogen deficiency in Arabidopsis thaliana Wassileskija accession. Plant Cell Physiol 49:1056–1065
pubmed: 18508804
Leran S, Munos S, Brachet C, Tillard P, Gojon A, Lacombe B (2013) Arabidopsis NRT1.1 is a bidirectional transporter involved in root-to-shoot nitrate translocation. Mol Plant 6:1984–1987
pubmed: 23645597
Li H, Hu B, Chu C (2017) Nitrogen use efficiency in crops: lessons from Arabidopsis and rice. J Exp Bot 68:2477–2488
pubmed: 28419301
Li JY, Fu YL, Pike SM, Bao J, Tian W, Zhang Y, Chen CZ, Zhang Y, Li HM, Huang J, Li LG, Schroeder JI, Gassmann W, Gong JM (2010) The Arabidopsis nitrate transporter NRT1. 8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22:1633–1646
pubmed: 20501909
pmcid: 2899866
Li XP, Zhao XQ, He X, Zhao GY, Li B, Liu DC, Zhang AM, Zhang XY, Tong YP, Li ZS (2011) Haplotype analysis of the genes encoding glutamine synthetase plastic isoforms and their association with nitrogen-use and yield-related traits in bread wheat. New Phytol 189:449–458
pubmed: 21039562
Lin J, Nazarenus TJ, Frey JL, Liang X, Wilson MA, Stone JM (2011) A plant DJ-1 homolog is essential for Arabidopsis thaliana chloroplast development. PLoS One 6:e23731
pubmed: 21886817
pmcid: 3160306
Liu X, Zhang Y, Han W et al (2013) Enhanced nitrogen deposition over China. Nature 494:459–462
pubmed: 23426264
Loque D, von Wiren N (2004) Regulatory levels for the transport of ammonium in plant roots. J Exp Bot 55:1293–1305
pubmed: 15133056
Malagoli P, Laine P, Rossato L, Ourry A (2005) Dynamics of nitrogen uptake and mobilization in field-grown winter oilseed rape (Brassica napus) from stem extension to harvest. Ann Bot 95:853–861
pubmed: 15701662
pmcid: 4246740
Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatout C, Dubois F, Balliau T, Valot B, Davanture M, Terce-Laforgue T (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18:3252–3274
pubmed: 17138698
pmcid: 1693956
Masucci JD, Schiefelbein JW (1994) The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin-and ethylene-associated process. Plant Physiol 106:1335–1346
pubmed: 12232412
pmcid: 159671
Mohammadi M, Blake TK, Budde AD, Chao S, Hayes PM, Horsley RD et al (2015) A genome-wide association study of malting quality across eight U.S. Barley breeding programs. Theor Appl Genet 128:705–721
pubmed: 25666272
Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agron J 74:562–564
Mulvaney RL, Khan SA, Ellsworth TR (2009) Synthetic nitrogen fertilizers deplete soil nitrogen: a global dilemma for sustainable cereal production. J Environ Qual 38:2295–2314
pubmed: 19875786
Namai S, Toriyama K, Fukuta Y (2009) Genetic variations in dry matter production and physiological nitrogen use efficiency in rice (Oryza sativa L). varieties Breed Sci 59:269–276
Ng JMS, Han M, Beatty PH, Good A (2016) Genes meet gases: the role of plant nutrition and genomics in addressing green-house gas emissions. In: Edwards D, Batley J (eds) Plant Genomics and Climate Change. Springer Publishers, New York, pp 149–172
Noh Y, Amasino R (1999) Regulation of developmental senescence is conserved between Arabidopsis and Brassica napus. Plant Mol Biol 41:195–206
pubmed: 10579487
O’Neill PM, Shanahan JF, Schepers JS, Caldwell B (2004) Agronomic responses of corn hybrids from different eras to deficit and adequate levels of water and nitrogen. Agron J 96:1660–1667
Okamoto M, Kumar A, Li W, Wang Y, Siddiqi MY, Crawford NM, Glass AD (2006) High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT31. Plant Physiol 140(3):1036–1046
pubmed: 16415212
pmcid: 1400568
Orsel M, Moison M, Clouet V, Thomas J, Leprince F, Canoy AS, Just J, Chalhoub B, Masclaux-Daubresse C (2014) Sixteen cytosolic glutamine synthetase genes identified in the Brassica napus L genome are differentially regulated depending on nitrogen regimes and leaf senescence. J Exp Bot 65:3927–3947
pubmed: 24567494
pmcid: 4106436
Pauli D, Muehlbauer GJ, Smith KP, Cooper B, Hole D, Obert DE et al (2014) Association mapping of agronomic QTLs in US spring barley breeding germplasm. Plant Genome 7:1–15
Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J 50:320–337
pubmed: 17355433
Peoples MB, Dalling MJ (1988) The interplay between proteolysis and amino acid metabolism during senescence and nitrogen reallocation. In: Noodén LD, Leopold AC (eds) Senescence and aging in plants. Academic Press, San Diego, pp 181–217
Perchlik M, Foster J, Tegeder M (2014) Different and overlapping functions of Arabidopsis LHT6 and AAP1 transporters in root amino acid uptake. J Exp Bot 65:5193–5204
pubmed: 25005136
pmcid: 4157705
Perez-Amador MA, Abler ML, De Rocher EJ et al (2000) Identification of BFN1, a bifunctional nuclease induced during leaf and stem senescence in. Arabidopsis Plant Physiol 122:169–180
pubmed: 10631260
Pratelli R, Pilot G (2014) Regulation of amino acid metabolic enzymes and transporters in plants. J Exp Bot 65:5535–5556
pubmed: 25114014
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus. genotype data Genetics 155:945–959
pubmed: 10835412
Prins A, Van Heerden PD, Olmos E, Kunert KJ, Foyer CH (2008) Cysteine proteinases regulate chloroplast protein content and composition in tobacco leaves: a model for dynamic interactions with ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) vesicular bodies. J Exp Bot 59:1935–1950
pubmed: 18503045
Quraishi UM, Abrouk M, Murat F, Pont C, Foucrier S, Desmaizieres G, Confolent C et al (2011) Cross-genome map based dissection of a nitrogen use efficiency ortho-meta QTL in bread wheat unravels concerted cereal genome evolution. Plant J 65:745–756
pubmed: 21251102
R Core Development Team (2013) R: A language and environment for statistical computing; http://www.R-project.org
Rafalski JA (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13:174–180
pubmed: 20089441
Rahman M, McClean P (2013) Genetic analysis on flowering time and root system in Brassica napus. L Crop Sci 53:141
Rathke GW, Behrens T, Diepenbrock W (2006) Integrated nitrogen management strategies to improve seed yield, oil content and nitrogen efficiency of winter oilseed rape (Brassica napus L): a review. Agr Ecosyst Environ 117:80–108
Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett 581:2281–2289
pubmed: 17466985
Rossato L, Laine P, Ourry A (2001) Nitrogen storage and remobilization in Brassica napus L during the growth cycle: nitrogen fluxes within the plant and changes in soluble protein patterns. J Exp Bot 52:1655–1663
pubmed: 11479330
Roshyara NR, Scholz M (2014) FC GENE: a versatile tool for processing and transforming SNP datasets. PLOS ONE 9(7):e97589
pubmed: 25050709
pmcid: 4106754
Schjoerring JK, Bock JGH, Gammelvind L, Jensen CR, Mogensen VO (1995) Nitrogen incorporation and remobilization in different shoot components of field-grown winter oilseed rape (Brassica napus L) as affected by rate of nitrogen application and irrigation. Plant Soil 177:255–264
Schulte auf’mErley G, Wijaya KA, Ulas A, Becker H, Wiesler F, Horst WJ (2007) Leaf senescence and N uptake parameters as selection traits for nitrogen efficiency of oilseed rape cultivars. Physiol Plant 130:519–531
Sheorana P, Sardana V, Singh S, Kumara A, Manna A, Sharma P (2016) Agronomic and physiological assessment of nitrogen use, uptake and acquisition in sunflower. Int J Plant Prod 10:109–122
Snowdon RJ, Abbadi A, Kox T, Schmutzer T, Leckband G (2015) Heterotic haplotype capture: precision breeding for hybrid performance. Trends Plant Sci 20:410–413
pubmed: 26027461
Soltabayeva A, Srivastava S, Kurmanbayeva A, Bekturova A, Fluhr R, Sagi M (2018) Early senescence in older leaves of low nitrate-grown Atxdh1 uncovers a role for purine catabolism in N supply. Plant Physiol 178:1027–1044
pubmed: 30190419
pmcid: 6236613
Stitt M, Muller C, Matt P, Gibon Y, Carillo P, Morcuende R et al (2002) Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53:959–970
pubmed: 11912238
Sun H, Qian Q, Wu K, Luo J, Wang S, Zhang C et al (2014) Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet 46:652–656
pubmed: 24777451
Svennerstam H, Ganeteg U, Bellini C, Nasholm T (2007) Comprehensive screening of Arabidopsis mutants suggests the lysine histidine transporter 1 to be involved in plant uptake of amino acids. Plant Physiol 143:1853–1860
pubmed: 17293438
pmcid: 1851813
Sylvester-Bradley R, Kindred DR (2009) Analysing nitrogen responses of cereals to prioritize routes to the improvement of nitrogen use efficiency. J Exp Bot 60:1939–1951
pubmed: 19395389
Tsay YF, Schroeder JI, Feldmann KA, Crawford NM (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible. nitrate transporter Cell 72:705–713
pubmed: 8453665
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301
pubmed: 17124321
pmcid: 4737439
Vijayakumar P, Datta S, Dolan L (2016) ROOT HAIR DEFECTIVE SIX-LIKE4 (RSL4) promotes root hair elongation by transcriptionally regulating the expression of genes required for cell growth. New Phytol 212:944–953
pubmed: 27452638
pmcid: 5111604
Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A (2009) Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol 149:885–893
pubmed: 19074627
pmcid: 2633819
Wang G, Ding G, Li L, Cai H, Ye X, Zou J, Xu F (2014) Identification and characterization of improved nitrogen efficiency in interspecific hybridized new-type Brassica napus. Ann Bot 114:549–559
pubmed: 24989788
pmcid: 4204666
Yang H, Stierhof YD, Ludewig U (2015) The putative Cationic Amino Acid Transporter 9 is targeted to vesicles and may be involved in plant amino acid homeostasis. Front Plant Sci 6:212
pubmed: 25883600
pmcid: 4381505
Yang X, Xia X, Zhang Z, Nong B, Zeng Y, Xiong F, Wu Y, Gao J, Deng G, Li D (2017) QTL Mapping by whole genome re-sequencing and analysis of candidate genes for nitrogen use efficiency in rice. Front Plant Sci 8:1634
pubmed: 28983307
pmcid: 5613164
Zhang Y, Tan L, Zhu Z, Yuan L, Xie D, Sun C (2015) TOND1 confers tolerance to nitrogen deficiency in rice. Plant J 81:367–376
pubmed: 25439309
pmcid: 4329406
Zhao Q, Huang X, Lin Z, Han B (2010) SEG-Map: A novel software for genotype calling and genetic map construction from next generation sequencing Rice 3:98–102