Identification of nitrogen use efficiency genes in barley: Searching for QTLs controlling complex physiological traits

Frontiers in Plant Science

Volumn 7, Issue OCTOBER2016, 2016, Pages

  Han, Mei ^a,b   Wong, Julia ^a   Su, Tao ^a,b   Beatty, Perrin H ^a   Good, Allen G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b NANJING FORESTRY UNIVERSITY   (China)

Author keywords

Barley; MAS; Nitrogen use efficiency (NUE); Phenotyping; QTL

Indexed keywords

EID: 84992642886     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.01587     Document Type: Article

References (83)

1. Abiko, T., Wakayama, M., Kawakami, A., Obara, M., Kisaka, H., Miwa, T., et al. (2010). Changes in nitrogen assimilation, metabolism, and growth in transgenic rice plants expressing a fungal NADP(H)-dependent glutamate dehydrogenase (gdhA). Planta 232, 299-311. doi: 10.1007/s00425-010-1172-3
2. Allison, D. B., Fernandez, J. R., Heo, M., Zhu, S., Etzel, C., Beasley, T. M., et al. (2002). Bias in estimates of quantitative-trait-locus effect in genome scans: demonstration of the phenomenon and a method-of-moments procedure for reducing bias. Am. J. Hum. Genet. 70, 575-585. doi: 10.1086/339273
3. Ashikari, M., Sakakibara, H., Lin, S., Yamamoto, T., Takashi, T., Nishimura, A., et al. (2005). Cytokinin oxidase regulates rice grain production. Science 309, 741-745. doi: 10.1126/science.1113373
4. Avila-Ospina, L., Marmagne, A., Talbotec, J., Krupinska, K., and Masclaux-Daubresse, C. (2015). The identification of new cytosolic glutamine synthetase and asparagine synthetase genes in barley (Hordeum vulgare L.), and their expression during leaf senescence. J. Exp. Bot. 66, 2013-2026. doi: 10.1093/jxb/erv003
5. Beatty, P. H., Carroll, R. T., Shrawat, A. K., Guevara, D., and Good, A. G. (2013). Physiological analysis of nitrogen-efficient rice overexpressing alanine aminotransferase under different N regimes. Botany 91, 866-883. doi: 10.1139/cjb-2013-0171
6. Berger, G. L., Liu, S., Hall, M. D., Brooks, W. S., Chao, S., Muehlbauer, G. J., et al. (2013). Marker-trait associations in Virginia Tech winter barley identified using genome-wide mapping. Theor. Appl. Genet. 126, 693-710. doi: 10.1007/s00122-012-2011-7
7. Bi, Y. M., 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. doi: 10.1111/j.1365-3040.2009.02032.x
8. Brauer, E. K. B. K., and Shelp, B. J. S. J. (2010). Nitrogen use efficiency: re-consideration of the bioengineering approach. Botany 88, 103-109. doi: 10.1139/B09-111
9. Brauer, E. K., Rochon, A., Bi, Y. M., Bozzo, G. G., Rothstein, S. J., and Shelp, B. J. (2011). Reappraisal of nitrogen use efficiency in rice overexpressing glutamine synthetase1. Physiol. Plant 141, 361-372. doi: 10.1111/j.1399-3054.2011.01443.x
10. Byers, D. L. (2005). Evolution in heterogeneous environments and the potential of maintenance of genetic variation in traits of adaptive significance. Genetica 123, 107-124. doi: 10.1007/s10709-003-2721-5
11. Chao, D.-Y., and Lin, H.-X. (2015). Nitrogen-use efficiency: transport solution in rice variations. Nat. Plants 1, 15096. doi: 10.1038/nplants.2015.96
12. Chen, M., Zhao, Y., Zhuo, C., Lu, S., and Guo, Z. (2015). Overexpression of a NF-YC transcription factor from bermudagrass confers tolerance to drought and salinity in transgenic rice. Plant Biotechnol. J. 13, 482-491. doi: 10.1111/pbi.12270
13. Chiasson, D. M., Loughlin, P. C., Mazurkiewicz, D., Mohammadidehcheshmeh, M., Fedorova, E. E., Okamoto, M., et al. (2014). Soybean SAT1 (Symbiotic Ammonium Transporter 1) encodes a bHLH transcription factor involved in nodule growth and NH4+ transport. Proc. Natl. Acad. Sci. U.S.A. 111, 4814-4819. doi: 10.1073/pnas.1312801111
14. Coello, P., Hey, S. J., and Halford, N. G. (2011). The sucrose non-fermenting-1-related (SnRK) family of protein kinases: potential for manipulation to improve stress tolerance and increase yield. J. Exp. Bot. 62, 883-893. doi: 10.1093/jxb/erq331
15. Comadran, J., Russell, J. R., Booth, A., Pswarayi, A., Ceccarelli, S., Grando, S., et al. (2011). Mixed model association scans of multi-environmental trial data reveal major loci controlling yield and yield related traits in Hordeum vulgare in mediterranean environments. Theor. Appl. Genet. 122, 1363-1373. doi: 10.1007/s00122-011-1537-4
16. Duan, P., Rao, Y., Zeng, D., Yang, Y., Xu, R., Zhang, B., et al. (2014). SMALL GRAIN 1, which encodes a mitogen-activated protein kinase kinase 4, influences grain size in rice. Plant J. 77, 547-557. doi: 10.1111/tpj.12405
17. Esposito, S., Guerriero, G., Vona, V., Di Martino Rigano, V., Carfagna, S., and Rigano, C. (2005). Glutamate synthase activities and protein changes in relation to nitrogen nutrition in barley: the dependence on different plastidic glucose-6P dehydrogenase isoforms. J. Exp. Bot. 56, 55-64. doi: 10.1093/jxb/eri006
18. Fan, X., Xie, D., Chen, J., Lu, H., Xu, Y., Ma, C., et al. (2014). Over-expression of OsPTR6 in rice increased plant growth at different nitrogen supplies but decreased nitrogen use efficiency at high ammonium supply. Plant Sci. 227, 1-11. doi: 10.1016/j.plantsci.2014.05.013
19. Gao, G., Zhong, Y., Guo, A., Zhu, Q., Tang, W., Zheng, W., et al. (2006). DRTF: a database of rice transcription factors. Bioinformatics 22, 1286-1287. doi: 10.1093/bioinformatics/btl107
20. G�mez-Cadenas, A., Verhey, S. D., Holappa, L. D., Shen, Q., Ho, T.-H. D., and Walker-Simmons, M. K. (1999). An abscisic acid-induced protein kinase, PKABA1, mediates abscisic acid-suppressed gene expression in barley aleurone layers. Proc. Natl. Acad. Sci. U.S.A. 96, 1767-1772. doi: 10.1073/pnas.96.4.1767
21. Good, A. G., and Beatty, P. H. (2011). “Biotechnological approaches to improving nitrogen use efficiency in plants: alanine aminotransferase as a case study,” in The Molecular and Physiological Basis of Nutrient Use Efficiency in Crops, eds M. J. Hawkesford and P. Barraclough (Oxford, UK: Wiley-Blackwell), 165-191. doi: 10.1002/9780470960707.ch9
22. Good, A. G., Shrawat, A. K., and Muench, D. G. (2004). Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci. 9, 597-605. doi: 10.1016/j.tplants.2004.10.008
23. Han, M., Okamoto, M., Beatty, P. H., Rothstein, S. J., and Good, A. G. (2015). The genetics of nitrogen use efficiency in crop plants. Annu. Rev. Genet. 49, 1-9. doi: 10.1146/annurev-genet-112414-055037
24. Hanke, G. T., Endo, T., Satoh, F., and Hase, T. (2008). Altered photosynthetic electron channelling into cyclic electron flow and nitrite assimilation in a mutant of ferredoxin:NADP(H) reductase. Plant Cell Environ. 31, 1017-1028. doi: 10.1111/j.1365-3040.2008.01814.x
25. Hawkesford, M. J. (2012). Improving Nurient Use Efficiency in Crops. Chichester: eLS John Wiley Sons, Ltd, 1-7.
26. Hayes, P. M., Liu, B. H., Knapp, S. J., Chen, F., Jones, B., Blake, T., et al. (1993). Quantitative trait locus effects and environmental interaction in a sample of North American barley germ plasm. Theor. Appl. Genet. 87, 392-401. doi: 10.1007/BF01184929
27. Hirner, A., Ladwig, F., Stransky, H., Okumoto, S., Keinath, M., Harms, A., et al. (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. doi: 10.1105/tpc.106.041012
28. Ivanov, A., Kameka, A., Pajak, A., Bruneau, L., Beyaert, R., Hern�ndez-Sebasti�, C., et al. (2012). Arabidopsis mutants lacking asparaginases develop normally but exhibit enhanced root inhibition by exogenous asparagine. Amino Acids 42, 2307-2318. doi: 10.1007/s00726-011-0973-4
29. Kindu, G. A., Tang, J., Yin, X., and Struik, P. C. (2014). Quantitative trait locus analysis of nitrogen use efficiency in barley (Hordeum vulgare L.). Euphytica 199, 207-221. doi: 10.1007/s10681-014-1138-9
30. Lam, H.-M., Wong, P., Chan, H.-K., Yam, K.-M., Chen, L., Chow, C.-M., et al. (2003). Overexpression of the ASN1 gene enhances nitrogen status in seeds of Arabidopsis. Plant Physiol. 132, 926-935. doi: 10.1104/pp.103.020123
31. Lea, U. S., Leydecker, M.-T., Quiller�, I., Meyer, C., and Lillo, C. (2006). Posttranslational regulation of nitrate reductase strongly affects the levels of free amino acids and nitrate, whereas transcriptional regulation has only minor influence. Plant Physiol. 140, 1085-1094. doi: 10.1104/pp.105.074633
32. L�ran, S., Garg, B., Boursiac, Y., Corratg�-Faillie, C., Brachet, C., Tillard, P., et al. (2015a). AtNPF5.5, a nitrate transporter affecting nitrogen accumulation in Arabidopsis embryo. Sci. Rep. 5:7962. doi: 10.1038/srep07962
33. L�ran, S., Varala, K., Boyer, J.-C., Chiurazzi, M., Crawford, N., Daniel-Vedele, F., et al. (2015b). A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci. 19, 5-9. doi: 10.1016/j.tplants.2013.08.008
34. Li, P., Chen, F., Cai, H., Liu, J., Pan, Q., Liu, Z., et al. (2015). A genetic relationship between nitrogen use efficiency and seedling root traits in maize as revealed by QTL analysis. J. Exp. Bot. 66, 3175-3188. doi: 10.1093/jxb/erv127
35. Li, S., Zhao, B., Yuan, D., Duan, M., Qian, Q., Tang, L., et al. (2013). Rice zinc finger protein DST enhances grain production through controlling Gn1a/OsCKX2 expression. Proc. Natl. Acad. Sci. U.S.A. 110, 3167-3172. doi: 10.1073/pnas.1300359110
36. Liepman, A. H., and Olsen, L. J. (2003). Alanine aminotransferase homologs catalyze the glutamate:glyoxylate aminotransferase reaction in peroxisomes of Arabidopsis. Plant Physiol. 131, 215-227. doi: 10.1104/pp.011460
37. Liu, R., Zhang, H., Zhao, P., Zhang, Z., Liang, W., Tian, Z., et al. (2012). Mining of candidate maize genes for nitrogen use efficiency by integrating gene expression and QTL data. Plant Mol. Biol. Rep. 30, 297-308. doi: 10.1007/s11105-011-0346-x
38. Mansour, E., Casas, A. M., Gracia, M. P., Molina-Cano, J. L., Moralejo, M., Cattivelli, L., et al. (2013). Quantitative trait loci for agronomic traits in an elite barley population for Mediterranean conditions. Mol. Breed. 33, 249-265. doi: 10.1007/s11032-013-9946-5
39. Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L., and Suzuki, A. (2010). Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann. Bot. 105, 1141-1157. doi: 10.1093/aob/mcq028
40. Mayer, K. F. X., Waugh, R., Brown, J. W., Schulman, A., Langridge, P., Platzer, M., et al. (2012). A physical, genetic and functional sequence assembly of the barley genome. Nature 491, 711-716. doi: 10.1038/nature11543
41. McAllister, C. H., Beatty, P. H., and Good, A. G. (2012). Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnol. J. 10, 1011-1025. doi: 10.1111/j.1467-7652.2012.00700.x
42. Mickelson, S., See, D., Meyer, F. D., Garner, J. P., Foster, C. R., Blake, T. K., et al. (2003). Mapping of QTL associated with nitrogen storage and remobilization in barley (Hordeum vulgare L.) leaves. J. Exp. Bot. 54, 801-812. doi: 10.1093/jxb/erg084
43. Mohammadi, M., Blake, T. K., Budde, A. D., Chao, S., Hayes, P. M., Horsley, R. D., et al. (2015). A genome-wide association study of malting quality across eight U.S. barley breeding programs. Theor. Appl. Genet. 128, 705-721. doi: 10.1007/s00122-015-2465-5
44. Mu�oz-Amatria�n, M., Cuesta-Marcos, A., Endelman, J. B., Comadran, J., Bonman, J. M., Bockelman, H. E., et al. (2014). The USDA barley core collection: Genetic diversity, population structure, and potential for genome-wide association studies. PLoS ONE 9:e94688. doi: 10.1371/journal.pone.0094688
45. Mu�oz-Amatria�n, M., Lonardi, S., Luo, M., Madishetty, K., Svensson, J. T., Moscou, M. J., et al. (2015). Sequencing of 15 622 gene-bearing BACs clarifies the gene-dense regions of the barley genome. Plant J. 84, 216-227. doi: 10.1111/tpj.12959
46. Mu�oz-Amatria�n, M., Moscou, M. J., Bhat, P. R., Svensson, J. T., Bartoš, J., Such�nkov�, P., et al. (2011). An improved consensus linkage map of barley based on flow-sorted chromosomes and single nucleotide polymorphism markers. Plant Genome J. 4, 238. doi: 10.3835/plantgenome2011.08.0023
47. Ng, J. M.-S., Han, M., Beatty, P. H., and Good, A. (2016). “‘Genes, meet gases’: the role of plant nutrition and genomics in addressing greenhouse gas emissions,” in Plant Genomics and Climate Change, eds D. Edwards and J. Batley (New York, NY: Springer), 149-172. doi: 10.1007/978-1-4939-3536-9_7
48. Nunes-Nesi, A., Fernie, A. R., and Stitt, M. (2010). Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol. Plant 3, 973-996. doi: 10.1093/mp/ssq049
49. Oaks, A. (1994). Primary nitrogen assimilation in higher plants and its regulation. Can. J. Bot. 72, 739-750. doi: 10.1139/b94-094
50. Orsel, M., Chopin, F., Leleu, O., Smith, S. J., Krapp, A., Daniel-Vedele, F., et al. (2006). Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis. Physiology and protein-protein interaction. Plant Physiol. 142, 1304-1317. doi: 10.1104/pp.106.085209
51. Park, S.-Y., Yu, J.-W., Park, J.-S., Li, J., Yoo, S.-C., Lee, N.-Y., et al. (2007). The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19, 1649-1664. doi: 10.1105/tpc.106.044891
52. Pasam, R. K., Sharma, R., Malosetti, M., van Eeuwijk, F. A., Haseneyer, G., Kilian, B., et al. (2012). Genome-wide association studies for agronomical traits in a world wide spring barley collection. BMC Plant Biol. 12:16. doi: 10.1186/1471-2229-12-16
53. Pauli, D., Muehlbauer, G. J., Smith, K. P., Cooper, B., Hole, D., Obert, D. E., et al. (2014). Association mapping of agronomic QTLs in US Spring Barley Breeding Germplasm. Plant Genome 7, 1-15. doi: 10.3835/plantgenome2013.11.0037
54. Quraishi, U. M., Abrouk, M., Murat, F., Pont, C., Foucrier, S., Desmaizieres, G., et al. (2011). Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. Plant J. 65, 745-756. doi: 10.1111/j.1365-313X.2010.04461.x
55. Ray, D. K., Ramankutty, N., Mueller, N. D., West, P. C., and Foley, J. A. (2012). Recent patterns of crop yield growth and stagnation. Nat. Commun. 3, 1293. doi: 10.1038/ncomms2296
56. Rothstein, S. J., Bi, Y.-M., Coneva, V., Han, M., and Good, A. (2014). The challenges of commercializing second-generation transgenic crop traits necessitate the development of international public sector research infrastructure. J. Exp. Bot. 65, 5673-5682. doi: 10.1093/jxb/eru236
57. Rubio-Wilhelmi, M. D. M., Sanchez-Rodriguez, E., Rosales, M. A., Blasco, B., Rios, J. J., Romero, L., et al. (2011). Cytokinin-dependent improvement in transgenic P SARK::IPT Tobacco under nitrogen deficiency. J. Agric. Food Chem. 59, 10491-10495. doi: 10.1021/jf202604k
58. Schofield, R. A., Bi, Y. M., Kant, S., and Rothstein, S. J. (2009). Over-expression of STP13, a hexose transporter, improves plant growth and nitrogen use in Arabidopsis thaliana seedlings. Plant Cell Environ. 32, 271-285. doi: 10.1111/j.1365-3040.2008.01919.x
59. Seiler, C., Harshavardhan, V. T., Reddy, P. S., Hensel, G., Kumlehn, J., Eschen-Lippold, L., et al. (2014). Abscisic Acid Flux alterations result in differential abscisic acid signaling responses and impact assimilation efficiency in barley under terminal drought stress. Plant Physiol. 164, 1677-1696. doi: 10.1104/pp.113.229062
60. Shen, J., Li, C., Mi, G., Li, L., Yuan, L., Jiang, R., et al. (2013). Maximizing root/rhizosphere efficiency to improve crop productivity and nutrient use efficiency in intensive agriculture of China. J. Exp. Bot. 64, 1181-1192. doi: 10.1093/jxb/ers342
61. Shrawat, A. K., Carroll, R. T., DePauw, M., Taylor, G. J., and Good, A. G. (2008). Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol. J. 6, 722-732. doi: 10.1111/j.1467-7652.2008.00351.x
62. Stitt, M., M�ller, 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. doi: 10.1093/jexbot/53.370.959
63. 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. doi: 10.1038/ng.2958
64. 2 in Arabidopsis. Plant Physiol. 126, 731-741. doi: 10.1104/pp.126.2.731
65. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
66. Tamura, W., Kojima, S., Toyokawa, A., Watanabe, H., Tabuchi-Kobayashi, M., Hayakawa, T., et al. (2011). Disruption of a Novel NADH-Glutamate Synthase2 gene caused marked reduction in spikelet number of rice. Front. Plant Sci. 2:57. doi: 10.3389/fpls.2011.00057
67. Terao, T., Nagata, K., Morino, K., and Hirose, T. (2010). A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice. Theor. Appl. Genet. 120, 875-893. doi: 10.1007/s00122-009-1218-8
68. Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R., and Polasky, S. (2002). Agricultural sustainability and intensive production practices. Nature 418, 671-677. doi: 10.1038/nature01014
69. Tobin, A. K., and Yamaya, T. (2001). Cellular compartmentation of ammonium assimilation in rice and barley. J. Exp. Bot. 52, 591-604. doi: 10.1093/jexbot/52.356.591
70. Tong, Y., Zhou, J.-J., Li, Z., and Miller, A. J. (2005). A two-component high-affinity nitrate uptake system in barley. Plant J. 41, 442-450. doi: 10.1111/j.1365-313X.2004.02310.x
71. Uauy, C., Distelfeld, A., Fahima, T., Blechl, A., and Dubcovsky, J. (2006). A NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314, 1298-1301. doi: 10.1126/science.1133649
72. Vanoni, M. A., and Curti, B. (1999). Glutamate synthase: a complex iron-sulfur flavoprotein. Cell. Mol. Life Sci. 55, 617-638. doi: 10.1007/s000180050319
73. Varshney, R. K., Paulo, M. J., Grando, S., van Eeuwijk, F. A, Keizer, L. C. P., Guo, P., et al. (2012). Genome wide association analyses for drought tolerance related traits in barley (Hordeum vulgare L.). Field Crops Res. 126, 171-180. doi: 10.1016/j.fcr.2011.10.008
74. Wang, E., Wang, J., Zhu, X., Hao, W., Wang, L., Li, Q., et al. (2008). Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat. Genet. 40, 1370-1374. doi: 10.1038/ng.220
75. Wang, M., Jiang, N., Jia, T., Leach, L., Cockram, J., Waugh, R., et al. (2012a). Genome-wide association mapping of agronomic and morphologic traits in highly structured populations of barley cultivars. Theor. Appl. Genet. 124, 233-246. doi: 10.1007/s00122-011-1697-2
76. Wang, X., Peng, F., Li, M., Yang, L., and Li, G. (2012b). Expression of a heterologous SnRK1 in tomato increases carbon assimilation, nitrogen uptake and modifies fruit development. J. Plant Physiol. 169, 1173-1182. doi: 10.1016/j.jplph.2012.04.013
77. Wuebbles, D. J. (2009). Nitrous oxide: no laughing matter. Science 326, 56-57. doi: 10.1126/science.1179571
78. Xia, X., Fan, X., Wei, J., Feng, H., Qu, H., Xie, D., et al. (2015). Rice nitrate transporter OsNPF2.4 functions in low-affinity acquisition and long-distance transport. J. Exp. Bot. 66, 317-331. doi: 10.1093/jxb/eru425
79. Yan, M., Fan, X., Feng, H., Miller, A. J., Shen, Q., and Xu, G. (2011). Rice OsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3a nitrate transporters to provide uptake over high and low concentration ranges. Plant Cell Environ. 34, 1360-1372. doi: 10.1111/j.1365-3040.2011.02335.x
80. Yang, J., Worley, E., Ma, Q., Li, J., Torres-Jerez, I., Li, G., et al. (2016). Nitrogen remobilization and conservation, and underlying senescence-associated gene expression in the perennial switchgrass Panicum virgatum. New Phytol. 211, 75-89. doi: 10.1111/nph.13898
81. Yuan, L., Loqu�, D., Ye, F., Frommer, W. B., and von Wir�n, N. (2007). Nitrogen-dependent posttranscriptional regulation of the ammonium transporter AtAMT1;1. Plant Physiol. 143, 732-744. doi: 10.1104/pp.106.093237
82. Zhao, S. P., Ye, X. Z., and Shi, W. M. (2014). Expression of OsAMT1 (1.1-1.3) in rice varieties differing in nitrogen accumulation. Russ. J. Plant Physiol. 61, 707-713. doi: 10.1134/S1021443714040220
83. Zhou, Y., Cai, H., Xiao, J., Li, X., Zhang, Q., and Lian, X. (2009). Over-expression of aspartate aminotransferase genes in rice resulted in altered nitrogen metabolism and increased amino acid content in seeds. Theor. Appl. Genet. 118, 1381-1390. doi: 10.1007/s00122-009-0988-3