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Research Article | Open Access

Increased nitrogen use efficiency via amino acid remobilization from source to sink organs in Brassica napus

Guihong Lianga, Yingpeng Huab, Haifei Chena, Jinsong Luoa, Hongkun Xianga, Haixing Songa, Zhenhua Zhanga( )
College of Resources and Environmental Sciences, Hunan Agricultural University, Changsha 410128, Hunan, China
School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450000, Henan, China
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Abstract

Nitrogen (N) is an essential plant growth nutrient whose coordinated distribution from source to sink organs is crucial for seed development and overall crop yield. We compared high and low N use efficiency (NUE) Brassica napus (rapeseed) genotypes. Metabonomics and transcriptomics revealed that leaf senescence induced by N deficiency promoted amino acid allocation from older to younger leaves in the high-NUE genotype at the vegetative growth stage. Efficient source to sink remobilization of amino acids elevated the numbers of branches and pods per plant under a N-deficiency treatment during the reproductive stage. A 15N tracer experiment confirmed that more amino acids were partitioned into seeds from the silique wall during the pod stage in the high-NUE genotype, owing mainly to variation in genes involved in organic N transport and metabolism. We suggest that the greater amino acid source-to-sink allocation efficiency during various growth stages in the high-NUE genotype resulted in higher yield and NUE under N deficiency. These findings support the hypothesis that strong amino acid remobilization in rapeseed leads to high yield, NUE, and harvest index.

Keywords

Amino acidsYieldGenetic variationNitrogenSource-to-sink allocation

References

[1]

M. Perchlik, M. Tegeder, Leaf amino acid supply affects photosynthetic and plant nitrogen use efficiency under nitrogen stress, Plant Physiol. 178 (2018) 174–188.
Crossref Google Scholar
[2]

Y. Ji, W. Huang, B. Wu, Z. Fang, X. Wang, D. Gibbs, The amino acid transporter AAP1 mediates growth and grain yield by regulating neutral amino acid uptake and reallocation in Oryza sativa, J. Exp. Bot. 71 (2020) 4763–4777.
Crossref Google Scholar
[3]

A. Mauceri, L. Bassolino, A. Lupini, F. Badeck, F. Rizza, M. Schiavi, L. Toppino, M.R. Abenavoli, G.L. Rotino, F. Sunseri, Genetic variation in eggplant for nitrogen use efficiency under contrasting NO3– supply, J. Integr. Plant Biol. 62 (2020) 487–508.
Crossref Google Scholar
[4]

C.H. McAllister, P.H. Beatty, A.G. Good, Engineering nitrogen use efficient crop plants: the current status, Plant Biotechnol. J. 10 (2012) 1011–1025.
Crossref Google Scholar
[5]

Y. Dellero, V. Clouet, N. Marnet, A. Pellizzaro, S. Dechaumet, M.F. Niogret, A. Bouchereau, N. Smirnoff, Leaf status and environmental signals jointly regulate proline metabolism in winter oilseed rape, J. Exp. Bot. 71 (2020) 2098–2111.
Crossref Google Scholar
[6]

P. Malagoli, P. Laine, L. Rossato, A. Ourry, Dynamics of nitrogen uptake and mobilization in field-grown winter oilseed rape (Brassica napus) from stem extension to harvest. Ⅱ. An 15N-labelling-based simulation model of N partitioning between vegetative and reproductive tissues, Ann. Bot. 95 (2005) 1187–1198.
Crossref Google Scholar
[7]

J.C. Avice, P. Etienne, Leaf senescence and nitrogen remobilization efficiency in oilseed rape (Brassica napus L.), J. Exp. Bot. 65 (2014) 3813–3824.
Crossref Google Scholar
[8]

W. Diepenbrock, Yield analysis of winter oilseed rape (Brassica napus L.): a review, Field Crops Res. 67 (2000) 35–49.
Crossref Google Scholar
[9]

H. Liu, Q. Yang, C. Fan, X. Zhao, X. Wang, Y. Zhou, Transcriptomic basis of functional difference and coordination between seeds and the silique wall of Brassica napus during the seed-filling stage, Plant Sci. 233 (2015) 186–199.
Crossref Google Scholar
[10]

R.T. Furbank, R. White, J.A. Palta, N.C. Turner, Internal recycling of respiratory CO2 in pods of chickpea (Cicer arietinum L.): the role of pod wall, seed coat, and embryo, J. Exp. Bot. 55 (2004) 1687–1696.
Crossref Google Scholar
[11]

L. Rossato, P. Lainé, A. Ourry, 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 (2001) 1655–1663.
Crossref Google Scholar
[12]

S. Schiltz, N. Munier-Jolain, C. Jeudy, J. Burstin, C. Salon, Dynamics of exogenous nitrogen partitioning and nitrogen remobilization from vegetative organs in pea revealed by 15N in vivo labeling throughout seed filling, Plant Physiol. 137 (2005) 1463–1473.
Crossref Google Scholar
[13]

G. Xu, X. Fan, A.J. Miller, Plant nitrogen assimilation and use efficiency, Annu. Rev. Plant Biol. 63 (2012) 153–182.
Crossref Google Scholar
[14]

L. Zhang, Q. Tan, R. Lee, A. Trethewy, Y.H. Lee, M. Tegeder, Altered xylem-phloem transfer of amino acids affects metabolism and leads to increased seed yield and oil content in Arabidopsis, Plant Cell 22 (2010) 3603–3620.
Crossref Google Scholar
[15]

J.P. Santiago, M. Tegeder, Connecting source with sink: the role of Arabidopsis AAP8 in phloem loading of amino acids, Plant Physiol. 171 (2016) 508–521.
Crossref Google Scholar
[16]

M. Perchlik, M. Tegeder, Improving plant nitrogen use efficiency through alteration of amino acid transport processes, Plant Physiol. 175 (2017) 235–247.
Crossref Google Scholar
[17]

V.J. Melino, M.A. Tester, M. Okamoto, Strategies for engineering improved nitrogen use efficiency in crop plants via redistribution and recycling of organic nitrogen, Curr. Opin. Biotechnol. 74 (2021) 263–269.
Google Scholar
[18]

M. Tegeder, D. Rentsch, Uptake and partitioning of amino acids and peptides, Mol. Plant 3 (2010) 997–1011.
Crossref Google Scholar
[19]

S.V. The, R. Snyder, M. Tegeder, Targeting nitrogen metabolism and transport processes to improve plant nitrogen use efficiency, Front. Plant Sci. 11 (2021) 628366.
Crossref Google Scholar
[20]

A. Sanders, R. Collier, A. Trethewy, G. Gould, R. Sieker, M. Tegeder, AAP1 regulates import of amino acids into developing Arabidopsis embryos, Plant J. 59 (2009) 540–552.
Crossref Google Scholar
[21]

L. Zhang, M.G. Garneau, R. Majumdar, J. Grant, M. Tegeder, Improvement of pea biomass and seed productivity by simultaneous increase of phloem and embryo loading with amino acids, Plant J. 81 (2015) 134–146.
Crossref Google Scholar
[22]

B. Peng, H. Kong, Y. Li, L. Wang, M. Zhong, L. Sun, G. Gao, Q. Zhang, L. Luo, G. Wang, W. Xie, J. Chen, W. Yao, Y. Peng, L. Lei, X. Lian, J. Xiao, C. Xu, X. Li, Y. He, OsAAP6 functions as an important regulator of grain protein content and nutritional quality in rice, Nat. Commun. 5 (2014) 4847.
Crossref Google Scholar
[23]

X. Jin, B. Feng, Z. Xu, X. Fan, J. liu, Q. Liu, P. Zhu, T. Wang, TaAAP6-3B, a regulator of grain protein content selected during wheat improvement, BMC Plant Biol. 18 (2018) 71.
Crossref Google Scholar
[24]

S. Liu, D. Wang, Y. Mei, T. Xia, W. Xu, Y. Zhang, X. You, X. Zhang, L. Li, N.N. Wang, Overexpression of GmAAP6a enhances tolerance to low nitrogen and improves seed nitrogen status by optimizing amino acid partitioning in soybean, Plant Biotechnol. J. 18 (2020) 1749–1762.
Crossref Google Scholar
[25]

W.B. Frommer, S. Hummel, M. Unseld, O. Ninnemann, Seed and vascular expression of a high-affinity transporter for cationic amino acids in Arabidopsis, Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 12036–12040.
Crossref Google Scholar
[26]

U.Z. Hammes, E. Nielsen, L.A. Honaas, C.G. Taylor, D.P. Schachtman, AtCAT6, a sink-tissue-localized transporter for essential amino acids in Arabidopsis, Plant J. 48 (2006) 414–426.
Crossref Google Scholar
[27]

H. Zhao, H. Ma, L.i. Yu, X. Wang, J. Zhao, T. Tuller, Genome-wide survey and expression analysis of amino acid transporter gene family in rice (Oryza sativa L.), PLoS ONE 7 (2012) e49210.
Crossref Google Scholar
[28]

L. Cheng, H.Y. Yuan, R. Ren, S.Q. Zhao, Y.P. Han, Q.Y. Zhou, D.X. Ke, Y.X. Wang, L. Wang, Genome-wide identification, classification, and expression analysis of amino acid transporter gene family in Glycine max, Front. Plant Sci. 7 (2016) 515.
Google Scholar
[29]

H. Ma, X. Cao, S. Shi, S. Li, J. Gao, Y. Ma, Q. Zhao, Q. Chen, Genome-wide survey and expression analysis of the amino acid transporter superfamily in potato (Solanum tuberosum L.), Plant Physiol. Biochem. 107 (2016) 164–177.
Crossref Google Scholar
[30]

Y.L. Han, H.X. Song, Q. Liao, Y. Yu, S.F. Jian, J.E. Lepo, Q. Liu, X.M. Rong, C. Tian, J. Zeng, C.Y. Guan, A.M. Ismail, Z.H. Zhang, Nitrogen use efficiency is mediated by vacuolar nitrate sequestration capacity in roots of Brassica napus, Plant Physiol. 170 (2016) 1684–1698.
Crossref Google Scholar
[31]

S. Jian, Q. Liao, H. Song, Q. Liu, J.E. Lepo, C. Guan, J. Zhang, A.M. Ismail, Z. Zhang, NRT1.1-related NH4+ toxicity is associated with a disturbed balance between NH4+ uptake and assimilation, Plant Physiol. 178 (2018) 1473–1488.
Crossref Google Scholar
[32]

G. Liang, H. Song, Y. Xiao, Z. Zhang, Ammonium accumulation caused by reduced tonoplast V-ATPase activity in Arabidopsis thaliana, Int. J. Mol. Sci. 22 (2020) 2.
Crossref Google Scholar
[33]

C. Wang, W. Zhang, Z. Li, Z. Li, Y. Bi, N.M. Crawford, Y. Wang, FIP1 plays an important role in nitrate signaling and regulates CIPK8 and CIPK23 expression in Arabidopsis, Front. Plant Sci. 9 (2018) 593.
Crossref Google Scholar
[34]

A.A. Urquhart, K.W. Joy, Use of Phloem exudate technique in the study of amino acid transport in pea plants, Plant Physiol. 68 (1981) 750–754.
Crossref Google Scholar
[35]

Y.P. Hua, T. Zhou, Q. Liao, H.X. Song, C.Y. Guan, Z.H. Zhang, Genomics-assisted identification and characterization of the genetic variants underlying differential nitrogen use efficiencies in allotetraploid rapeseed genotypes, G3-Genes Genomics Genet. 8 (2018) 2757–2771.
Google Scholar
[36]

A. Maillard, P. Etienne, S. Diquélou, J. Trouverie, V. Billard, J.C. Yvin, A. Ourry, Nutrient deficiencies modify the ionomic composition of plant tissues: a focus on cross-talk between molybdenum and other nutrients in Brassica napus, J. Exp. Bot. 67 (2016) 5631–5641.
Crossref Google Scholar
[37]

K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method, Methods 25 (2001) 402–408.
Crossref Google Scholar
[38]

A. Ferrante, R. Savin, G.A. Slafer, Floret development of durum wheat in response to nitrogen availability, J. Exp. Bot. 61 (2010) 4351–4359.
Crossref Google Scholar
[39]

M. Havé, A. Marmagne, F. Chardon, C. Masclaux-Daubresse, Nitrogen remobilization during leaf senescence: lessons from Arabidopsis to crops, J. Exp. Bot. 68 (2017) 2513–2529.
Google Scholar
[40]

A. Girondé, P. Etienne, J. Trouverie, A. Bouchereau, F. Le Cahérec, L. Leport, M. Orsel, M.F. Niogret, N. Nesi, D. Carole, F. Soulay, C. Masclaux-Daubresse, J.C. Avice, The contrasting N management of two oilseed rape genotypes reveals the mechanisms of proteolysis associated with leaf N remobilization and the respective contributions of leaves and stems to N storage and remobilization during seed filling, BMC Plant Biol. 15 (2015) 59.
Crossref Google Scholar
[41]

C. Masclaux-Daubresse, F. Daniel-Vedele, J. Dechorgnat, F. Chardon, L. Gaufichon, A. Suzuki, Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture, Ann. Bot. 105 (2010) 1141–1157.
Crossref Google Scholar
[42]

A. Soltabayeva, S. Srivastava, A. Kurmanbayeva, A. Bekturova, R. Fluhr, M. Sagi, Early senescence in older leaves of low nitrate-grown Atxdh1 uncovers a role for purine catabolism in N supply, Plant Physiol. 178 (2018) 1027–1044.
Crossref Google Scholar
[43]

Y.Y. Wang, P.K. Hsu, Y.F. Tsay, Uptake, allocation and signaling of nitrate, Trends Plant Sci. 17 (2012) 458–467.
Crossref Google Scholar
[44]

G. Liang, Z. Zhang, Reducing the nitrate content in vegetables through joint regulation of short-distance distribution and long-distance transport, Front. Plant Sci. 11 (2020) 1079.
Crossref Google Scholar
[45]

J.Y. Li, Y.L. Fu, S.M. Pike, J. Bao, W. Tian, Y. Zhang, C.Z. Chen, Y. Zhang, H.M. Li, J. Huang, L.G. Li, J.I. Schroeder, W. Gassmann, J.M. Gong, The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance, Plant Cell 22 (2010) 1633–1646.
Crossref Google Scholar
[46]

S.H. Lin, H.F. Kuo, G. Canivenc, C.S. Lin, M. Lepetit, P.K. Hsu, P. Tillard, H.L. Lin, Y.Y. Wang, C.B. Tsai, A. Gojon, Y.F. Tsay, Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport, Plant Cell 20 (2008) 2514–2528.
Crossref Google Scholar
[47]

T. Hildebrandt, A. Nunes Nesi, W. Araújo, H.P. Braun, Amino acid catabolism in plants, Mol. Plant 8 (2015) 1563–1579.
Crossref Google Scholar
[48]

A.J. Barneix, Physiology and biochemistry of source-regulated protein accumulation in the wheat grain, J. Plant Physiol. 164 (2007) 581–590.
Crossref Google Scholar
[49]

C. Masclaux-Daubresse, Q. Chen, M. Havé, Regulation of nutrient recycling via autophagy, Curr. Opin. Plant Biol. 39 (2017) 8–17.
Crossref Google Scholar
[50]

C. Diaz, T. Lemaître, A. Christ, M. Azzopardi, Y. Kato, F. Sato, J.F. Morot-Gaudry, F. Le Dily, C. Masclaux-Daubresse, Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition, Plant Physiol. 147 (2008) 1437–1449.
Crossref Google Scholar
[51]

S.C. Fan, C.S. Lin, P.K. Hsu, S.H. Lin, Y.F. Tasy, The Arabidopsis nitrate transporter NRT1.7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate, Plant Cell 21 (2009) 2750–2761.
Crossref Google Scholar
[52]

T. Zhou, C.P. Yue, J.Y. Huang, J.Q. Cui, Y. Liu, W.M. Wang, C. Tian, Y.P. Hua, Genome-wide identification of the amino acid permease genes and molecular characterization of their transcriptional responses to various nutrient stresses in allotetraploid rapeseed, BMC Plant Biol. 20 (2020) 151.
Crossref Google Scholar
[53]

L. Rossato, C. le Dantec, P. Laine, A. Ourry, Nitrogen storage and remobilization in Brassica napus L. during the growth cycle: identification, characterization and immunolocalization of a putative taproot storage glycoprotein, J. Exp. Bot. 53 (2002) 265–275.
Crossref Google Scholar
[54]

H. Yang, M. Krebs, Y.D. Stierhof, U. Ludewig, Characterization of the putative amino acid transporter genes AtCAT2,3,4: The tonoplast localized AtCAT2 regulates soluble leaf amino acids, J. Plant Physiol. 171 (2014) 594–601.
Crossref Google Scholar
[55]

A. Sato, T. Kimura, K. Hondo, M. Kawano-Kawada, T. Sekito, The vacuolar amino acid transport system is a novel, direct target of GATA transcription factors, Biosci. Biotechnol. Biochem. 24 (2021) 587–599.
Google Scholar
[56]

T. Chahomchuen, K. Hondo, M. Ohsaki, T. Sekito, Y. Kakinuma, Evidence for Avt6 as a vacuolar exporter of acidic amino acids in Saccharomyces cerevisiae cells, J. Gen. Appl. Microbiol. 55 (2009) 409–417.
Crossref Google Scholar
[57]

Y. Liu, H. Wang, Z. Jiang, W. Wang, R. Xu, Q. Wang, Z. Zhang, A. Li, Y. Liang, S. Ou, X. Liu, S. Cao, H. Tong, Y. Wang, F. Zhou, H. Liao, B. Hu, C. Chu, Genomic basis of geographical adaptation to soil nitrogen in rice, Nature 590 (2021) 600–605.
Crossref Google Scholar
[58]

M. Tegeder, C. Masclaux-Daubresse, Source and sink mechanisms of nitrogen transport and use, New Phytol. 217 (2018) 35–53.
Crossref Google Scholar
[59]

Y.L. Han, Q. Liao, Y. Yu, H.X. Song, Q. Liu, X.M. Rong, J.D. Gu, J.E. Lepo, C.Y. Guan, Z.H. Zhang, Nitrate reutilization mechanisms in the tonoplast of two Brassica napus genotypes with different nitrogen use efficiency, Acta Physiol. Plant. 37 (2015) 42.
Crossref Google Scholar
The Crop Journal
Volume 11 Issue 1,
February 2023
Pages 119-131
DOI: 10.1016/j.cj.2022.05.011
Cite this article:
Liang G, Hua Y, Chen H, et al. Increased nitrogen use efficiency via amino acid remobilization from source to sink organs in Brassica napus. The Crop Journal, 2023, 11(1): 119-131. https://doi.org/10.1016/j.cj.2022.05.011

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Received: 24 February 2022
Revised: 28 March 2022
Accepted: 17 June 2022
Published: 03 July 2022
© 2022 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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