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Overexpression of the nitrate transporter, OsNRT2.3b, improves rice phosphorus uptake and translocation

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Abstract

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Overexpression of OsNRT2.3b in rice can increase Pi uptake and accumulation through advanced root system, enhanced OsPT and OsPHR genes expression, and the phloem pH homeostasis.

Abstract

Nitrogen (N) and phosphorus (P) are two essential macronutrients for plants. Overexpression of the rice nitrate transporter, OsNRT2.3b, can improve rice grain yield and nitrogen use efficiency (NUE). Here, OsNRT2.3b overexpression resulted in increased grain yield, straw yield, and grain:straw ratio, accompanied by increased P concentrations in the leaf blade, leaf sheath, culm, and unfilled rice hulls. Overexpression of OsNRT2.3b significantly increased 33Pi uptake compared with WT under 300-μM Pi but not 10-μM Pi condition in 24 h. Moreover, the OsNRT2.3b-overexpressing rice lines showed increased root and shoot biomass, root:shoot ratio, total root length root surface area and N, P accumulation under 300- and 10-μM Pi supply in hydroponic solution. The levels of OsPT2, OsPT8, and OsPHR2 expression in roots and of OsPT1 and OsPHR2 in shoots were upregulated in OsNRT2.3b-overexpressing rice. These results indicated that OsNRT2.3b overexpression can improve rice P uptake and accumulation, partially through the advanced root system, enhanced gene expression, and the phloem pH regulation function.

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References

  • Ai P, Sun S, Zhao J, Fan X, Xin W, Guo Q, Yu L, Shen Q, Wu P, Miller AJ, Xu G (2009) Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. Plant J 57:798–809

    Article  CAS  PubMed  Google Scholar 

  • Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Plant Biol 24:225–252

    CAS  Google Scholar 

  • Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–45

    Article  CAS  Google Scholar 

  • Bryla DR, Koide RT (1998) Mycorrhizal response of two tomato genotypes relates to their ability to acquire and utilize phosphorus. Ann Bot 82:849–857

    Article  Google Scholar 

  • Cai J, Chen L, Qu H, Lian J, Liu W, Hu Y, Xu G (2012) Alteration of nutrient allocation and transporter genes expression in rice under N, P, K, and Mg deficiencies. Acta Physiol Plant 34(3):939–946

    Article  CAS  Google Scholar 

  • Cai H, Xie W, Lian X (2013) Comparative analysis of differentially expressed genes in rice under nitrogen and phosphorus starvation stress conditions. Plant Mol Biol Rep 31(1):160–173

    Article  CAS  Google Scholar 

  • Catarecha P, Segura MD, Franco-ZorrillaJM García-Ponce B, Lanza M, Solano R, Paz-Ares J, Leyva A (2007) A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19(3):1123–1133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen AQ, Hu J, Sun SB, Xu GH (2007) Conservation and divergence of both phosphate- and mycorrhiza-regulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytol 173:817–831

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Feng H, Hu Q, Qu H, Chen A, Yu L, Xu GH (2015) Improving rice tolerance to potassium deficiency by enhancing OsHAK16p:WOX11-controlled root development. Plant Biotechnol J 13(6):833–848

    Article  CAS  PubMed  Google Scholar 

  • Fan X, Tang Z, Tan Y, Zhang Y, Luo B, Yang M, Lian X, Shen Q, Miller AJ, Xu G (2016) Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proc Natl Acad Sci USA 113(26):7118–7123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forde B, Lorenzo H (2001) The nutritional control of root development. Plant Soil 232:51–68

    Article  CAS  Google Scholar 

  • Franco-Zorrilla JM, Gonzalez E, Bustos R, Linhares F, Leyva A, PazAres J (2004) The transcriptional control of plant responses to phosphate limation. J Exp Bot 55:285–293

    Article  CAS  PubMed  Google Scholar 

  • Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698

    Article  CAS  PubMed  Google Scholar 

  • Güimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci USA 102(22):8066–8070

    Article  PubMed  PubMed Central  Google Scholar 

  • Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11:610–617

    Article  CAS  PubMed  Google Scholar 

  • Hühn M (1993) Comparison of harvest index and grain/straw-ratio with applications to winter oilseed rape. J Agron Crop Sci 170(4):270–280

    Article  Google Scholar 

  • Jia H, Ren H, Gu M, Zhao J, Sun S, Zhang X, Chen J, Wu P, Xu G (2011) The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice. Plant Physiol 156(3):1164–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konvalina P, Stehno Z, Capouchová I, Zechner E, Berger S, Grausgruber H, Janovská D, MoudrýSr J (2014) Differences in grain/straw ratio, protein content and yield in landraces and modern varieties of different wheat species under organic farming. Euphytica 199(1):31–40

    Article  Google Scholar 

  • Liu Y, Mi GH, Chen FJ, Zhang JH, Zhang FS (2004) Rhizosphere effect and root growth of two maize (Zea mays L.) genotupes with contrasting P efficiency at low P availability. Plant Sci 167(2):217–223

    Article  CAS  Google Scholar 

  • Liu F, Wang Z, Ren H, Shen C, Li Y, Ling HQ, Wu C, Lian X, Wu P (2010) OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. Plant J 62(3):508–517

    Article  CAS  PubMed  Google Scholar 

  • López-Bucio J, Cruz-RamíRez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6(3):280–287

    Article  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London

    Google Scholar 

  • Misson J, Thibaud MC, Bechtold N, Raghothama K, Nussaume L (2004) Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Mol Biol 55:727–741

    Article  CAS  PubMed  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 99:13324–13329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49

    Article  CAS  Google Scholar 

  • Robertson GP, Vitousek PM (2009) Nitrogen in agriculture: balancing the cost of an essential resource. Annu Rev Environ Resour 34:97–125

    Article  Google Scholar 

  • Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Physiol 58:47–69

    CAS  Google Scholar 

  • Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642

    Article  CAS  PubMed  Google Scholar 

  • Sun S, Gu M, Cao Y, Huang X, Zhang X, Ai P, Zhao J, Fan X, Xu G (2012) A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphate-replete rice. Plant Physiol 159:1571–1581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang Z, Fan X, Li Q, Feng H, Miller AJ, Shen Q, Xu G (2012) Knockdown of a rice stelar nitrate transporter alters long-distance translocation but not root influx. Plant Physiol 160:2052–2063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Ying S, Huang H, Li K, Wu P, Shou H (2009) Involvement of OsSPX1 in phosphate homeostasis in rice. Plant J 57:895–904

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wang Y, Piñeros MA, Wang Z, Wang W, Li C, Wu Z, Kochian LV, Wu P (2014) Phosphate transporters OsPHT1;9 and OsPHT1;10 are involved in phosphate uptake in rice. Plant Cell Environ 37:1159–1170

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Sun R, Cao Y, Pei W, Sun Y, Zhou H, Wu X, Zhang F, Luo L, Shen Q, Xu G, Sun S (2015) Ossiz1, a sumo e3 ligase gene, is involved in the regulation of the responses to phosphate and nitrogen in rice. Plant Cell Physiol 56(12):2381–2395

    Article  CAS  PubMed  Google Scholar 

  • Wu P, Shou H, Xu G, Lian X (2013) Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr Opin Plant Biol 16:205–212

    Article  CAS  PubMed  Google Scholar 

  • Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182

    Article  CAS  PubMed  Google Scholar 

  • Yang XJ, Finnegan PM (2010) Regulation of phosphate starvation responses in higher plants. Ann Bot 105:513–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Sun Y, Pei W, Jain A, Sun R, Cao Y, Wu X, Jiang T, Zhang L, Fan X, Chen A, Shen Q, Xu G, Sun S (2015) Involvement of OsPht1;4 in phosphate acquisition and mobilization facilitates embryo development in rice. Plant J 82:556–569

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Jiao F, Wu Z, Li Y, Wang X, He X, Zhong W, Wu P (2008) OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146:1673–1686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31401938, 31372122), the Transgenic Project (2016ZX08001003-008), and the Fundamental Research Funds for the Central Universities (Y0201500014 and Y201500191) and the Outstanding Youth of Jiangsu Province (BK20160030). The English in this document has been checked by at least two professional editors, both native speakers of English, please see: http://www.textcheck.com/certificate/FRARHO.

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Authors and Affiliations

  1. Jiangsu Key Lab of Marine Biology, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, China

    Huimin Feng, Yang Zhi & Ran Li

  2. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, China

    Bin Li, Jingguang Chen, Guohua Xu & Xiaorong Fan

  3. Key Laboratory of Plant Nutrition and Fertilization in Low-Middle Reaches of the Yangtze River, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, 210095, China

    Bin Li, Jingguang Chen, Guohua Xu & Xiaorong Fan

  4. Institute of Agro-Product Processing, Jiangsu Academy of Agricultural Sciences, Nanjing, Jiangsu, People’s Republic of China

    Xiudong Xia

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  1. Huimin Feng
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  2. Bin Li
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  3. Yang Zhi
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Correspondence to Xiaorong Fan.

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Communicated by Amit Dhingra.

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Feng, H., Li, B., Zhi, Y. et al. Overexpression of the nitrate transporter, OsNRT2.3b, improves rice phosphorus uptake and translocation. Plant Cell Rep 36, 1287–1296 (2017). https://doi.org/10.1007/s00299-017-2153-9

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  • DOI: https://doi.org/10.1007/s00299-017-2153-9

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