Please wait a minute...
Journal of Integrative Agriculture  2017, Vol. 16 Issue (12): 2657-2673    DOI: 10.1016/S2095-3119(17)61709-X
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Transgenic approaches for improving use efficiency of nitrogen, phosphorus and potassium in crops
TENG Wan, HE Xue, TONG Yi-ping
State Key Laboratory for Plant Cell and Chromosome Engineering/Institute of Genetics and Developmental Sciences, Chinese Academy of Sciences, Beijing 100101, P.R.China
Download:  PDF (364KB) ( )  
Export:  BibTeX | EndNote (RIS)      
Abstract  The success of the Green Revolution largely relies on fertilizers, and a new Green Revolution is very much needed to use fertilizers more economically and efficiently, as well as with more environmental responsibility. The use efficiency of nitrogen, phosphorus, and potassium is controlled by complex gene networks that co-ordinate uptake, re-distribution, assimilation, and storage of these nutrients. Great progress has been made in breeding nutrient-efficient crops by molecularly engineering root traits desirable for efficient acquisition of nutrients from soil, transporters for uptake, redistribution and homeostasis of nutrients, and enzymes for efficient assimilation. Regulatory and transcription factors modulating these processes are also valuable in breeding crops with improved nutrient use efficiency and yield performance.
Keywords:  nutrient use efficiency        nitrogen        phosphorus        potassium       transgenic approach        crop  
Received: 10 March 2017   Accepted:

This research was supported by the National Key Research and Development Program of China (2016YFD0100706) and the National Transgenic Key Project from the Ministry of Agriculture of China (2016ZX08002-005).

Corresponding Authors:  Correspondence TONG Yi-ping, Tel:+86-10-64806556,Fax:+86-10-64806537,E-mail:   

Cite this article: 

TENG Wan, HE Xue, TONG Yi-ping. 2017. Transgenic approaches for improving use efficiency of nitrogen, phosphorus and potassium in crops. Journal of Integrative Agriculture, 16(12): 2657-2673.

Ahmad I, Devonshire J, Mohamed R, Schultze M, Maathuis F J M. 2016. Overexpression of the potassium channel TPKb in small vacuoles confers osmotic and drought tolerance to rice. New Phytologist, 209, 1040–1048.

Ai P H, Sun S B, Zhao J N, Fan X R, Xin W J, Guo Q, Yu L, Shen Q R, Wu P, Miller A J, Xu G H. 2009. Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. The Plant Journal, 57, 798–809.

Alvarez J M, Riveras E, Vidal E A, Gras D E, Contreras-Lopez O, Tamayo K P, Aceituno F, Gomez I, Ruffel S, Lejay L, Jordana X, Gutierrez R A. 2014. Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. The Plant Journal, 80, 1–13.

An D G, Su J Y, Liu Q Y, Zhu Y G, Tong Y P, Li J M, Jing R L, Li B, Li Z S. 2006. Mapping QTLs for nitrogen uptake in relation to the early growth of wheat (Triticum aestivum L.). Plant and Soil, 284, 73–84.

Arai-Sanoh Y, Takai T, Yoshinaga S, Nakano H, Kojima M, Sakakibara H, Kondo M, Uga Y. 2014. Deep rooting conferred by DEEPER ROOTING 1 enhances rice yield in paddy fields. Scientific Reports, 4, 5563.

Bari R, Pant B D, Stitt M, Scheible W R. 2006. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology, 141, 988–999.

Bieleski R L. 1973. Phosphate pools, phosphate transport, and phosphate availability. Annual Review of Plant Physiology and Plant Molecular Biology, 24, 225–252.

Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Taconnat L, Renou J P, Daniel-Vedele F, Fernandez E, Meyer C, Krapp A. 2009. The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. The Plant Journal, 57, 426–435.

Chen G, Hu Q D, Luo L, Yang T Y, Zhang S, Hu Y B, Yu L, Xu G H. 2015. Rice potassium transporter OsHAK1 is essential for maintaining potassium-mediated growth and functions in salt tolerance over low and high potassium concentration ranges. Plant Cell and Environment, 38, 2747–2765.

Chen G H, Yan W, Yang S P, Wang A, Gai J Y, Zhu Y L. 2015. Overexpression of rice phosphate transporter gene OsPT2 enhances tolerance to low phosphorus stress in soybean. Journal of Agricultural Science and Technology, 17, 469–494.

Chen J, Liu Y, Ni J, Wang Y, Bai Y, Shi J, Gan J, Wu Z, Wu P. 2011. OsPHF1 regulates the plasma membrane localization of low- and high-affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiology, 157, 269–278.

Chen J G, Zhang Y, Tan Y W, Zhang M, Zhu L L, Xu G H, Fan X R. 2016. Agronomic nitrogen-use efficiency of rice can be increased by driving OsNRT2.1 expression with the OsNAR2.1 promoter. Plant Biotechnology Journal, 14, 1705–1715.

Chen X, Cui Z, Fan M, Vitousek P, Zhao M, Ma W, Wang Z, Zhang W, Yan X, Yang J, Deng X, Gao Q, Zhang Q, Guo S, Ren J, Li S, Ye Y, Wang Z, Huang J, Tang Q, et al. 2014. Producing more grain with lower environmental costs. Nature, 514, 486–489.

Chen X B, Yao Q F, Gao X H, Jiang C F, Harberd N P, Fu X D. 2016. Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Current Biology, 26, 640–646.

Chiba Y, Shimizu T, Miyakawa S, Kanno Y, Koshiba T, Kamiya Y, Seo M. 2015. Identification of Arabidopsis thaliana NRT1/PTR FAMILY (NPF) proteins capable of transporting plant hormones. Journal of Plant Research, 128, 679–686.

Dai X, Wang Y, Yang A, Zhang W H. 2012. OsMYB2P-1, an R2R3 MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiology, 159, 169–183.

Delhaize E, Taylor P, Hocking P J, Simpson R J, Ryan P R, Richardson A E. 2009. Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant Biotechnology Journal, 7, 391–400.

Deng Y, Chen K R, Teng W, Zhan A, Tong Y P, Feng G, Cui Z L, Zhang F S, Chen X P. 2014. Is the inherent potential of maize roots efficient for soil phosphorus acquisition? PLOS ONE, 9, e90287.

de Dorlodot S, Forster B, Pages L, Price A, Tuberosa R, Draye X. 2007. Root system architecture: Opportunities and constraints for genetic improvement of crops. Trends in Plant Science, 12, 474–481.

Drew M C. 1975. Comparison of the effects of a localised supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist, 75, 479–490.

Fan X, Tang Z, Tan Y, Zhang Y, Luo B, Yang M, Lian X, Shen Q, Miller A J, Xu G. 2016. Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proceedings of the National Academy of Sciences of the United States of America, 113, 7118–7123.

Fan X, Xie D, Chen J, Lu H, Xu Y, Ma C, Xu G. 2014. Over-expression of OsPTR6 in rice increased plant growth at different nitrogen supplies but decreased nitrogen use efficiency at high ammonium supply. Plant Science, 227, 1–11.

Fang Z, Xia K, Yang X, Grotemeyer M S, Meier S, Rentsch D, Xu X, Zhang M. 2013. Altered expression of the PTR/NRT1 homologue OsPTR9 affects nitrogen utilization efficiency, growth and grain yield in rice. Plant Biotechnology Journal, 11, 446–458.

Feng H, Fan X, Fan X, Liu X, Miller A J, Xu G. 2011. Multiple roles of nitrate transport accessory protein NAR2 in plants. Plant Signaling and Behavior, 6, 1286–1289.

Forde B G. 2014. Nitrogen signalling pathways shaping root system architecture: An update. Current Opinion in Plant Biology, 21, 30–36.

Fritsche-Neto R, DoVale J C, de Lanes E C M, de Resende M D V, Miranda G V. 2012. Genome-wide selection for tropical maize root traits under conditions of nitrogen and phosphorus stress. Acta Scientiarum-Agronomy, 34, 389–395.

Gamuyao R, Chin J H, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza E M, Wissuwa M, Heuer S. 2012. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature, 488, 535–539.

Giehl R F, von Wiren N. 2014. Root nutrient foraging. Plant Physiology, 166, 509–517.

Good A G, Johnson S J, De Pauw M, Carroll R T, Savidov N. 2007. Engineering nitrogen use efficiency with alanine aminotransferase. Canadian Journal of Botany, 85, 252–262.

Good A G, Shrawat A K, Muench D G. 2004. Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends in Plant Science, 9, 597–605.

Guan P, Wang R, Nacry P, Breton G, Kay S A, Pruneda-Paz J L, Davani A, Crawford N M. 2014. Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. Proceedings of the National Academy of Sciences of the United States of America, 111, 15267–15272.

Guo C J, Guo L, Li X J, Gu J T, Zhao M, Duan W W, Ma C Y, Lu W J, Xiao K. 2014. TaPT2, a high-affinity phosphate transporter gene in wheat (Triticum aestivum L.), is crucial in plant Pi uptake under phosphorus deprivation. Acta Physiologiae Plantarum, 36, 1373–1384.

Guo J H, Liu X J, Zhang Y, Shen J L, Han W X, Zhang W F, Christie P, Goulding K W, Vitousek P M, Zhang F S. 2010. Significant acidification in major Chinese croplands. Science, 327, 1008–1010.

Guo M N, Ruan W Y, Li C Y, Huang F L, Zeng M, Liu Y Y, Yu Y N, Ding X M, Wu Y R, Wu Z C, Mao C Z, Yi K K, Wu P, Mo X R. 2015. Integrative comparison of the role of the PHOSPHATE RESPONSE1 subfamily in phosphate signaling and homeostasis in rice. Plant Physiology, 168, 1762–1776.

Guo W, Zhao J, Li X, Qin L, Yan X, Liao H. 2011. A soybean beta-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. The Plant Journal, 66, 541–552.

Hammes U Z, Meier S, Dietrich D, Ward J M, Rentsch D. 2010. Functional properties of the Arabidopsis peptide transporters AtPTR1 and AtPTR5. The Journal of Biological Chemistry, 285, 39710–39717.

Han Y Y, Zhou S, Chen Y H, Kong X Z, Xu Y, Wang W. 2014. The involvement of expansins in responses to phosphorus availability in wheat, and its potentials in improving phosphorus efficiency of plants. Plant Physiology and Biochemistry, 78, 53–62.

He X, Qu B, Li W, Zhao X, Teng W, Ma W, Ren Y, Li B, Li Z, Tong Y. 2015. The nitrate-inducible NAC transcription factor TaNAC2-5A controls nitrate response and increases wheat yield. Plant Physiology, 169, 1991–2005.

Heffer P. 2013. Assessment of fertilizer use by crop at the global level 2010–2010/11. [2017-02-01].

Den Herder G, Van Isterdael G, Beeckman T, De Smet I. 2010. The roots of a new green revolution. Trends in Plant Science, 15, 600–607.

Ho C H, Lin S H, Hu H C, Tsay Y F. 2009. CHL1 functions as a nitrate sensor in plants. Cell, 138, 1184–1194.

Hong J P, Takeshi Y, Kondou Y, Schachtman D P, Matsui M, Shin R. 2013. Identification and characterization of transcription factors regulating Arabidopsis HAK5. Plant and Cell Physiology, 54, 1478–1490.

Hu B, Wang W, Deng K, Li H, Zhang Z, Zhang L, Chu C. 2015a. MicroRNA399 is involved in multiple nutrient starvation responses in rice. Frontiers in Plant Science, 6, 188.

Hu B, Wang W, Ou S, Tang J, Li H, Che R, Zhang Z, Chai X, Wang H, Wang Y, Liang C, Liu L, Piao Z, Deng Q, Deng K, Xu C, Liang Y, Zhang L, Li L, Chu C. 2015b. Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nature Genetetics, 47, 834–838.

Hu B, Zhu C, Li F, Tang J, Wang Y, Lin A, Liu L, Che R, Chu C. 2011. LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiology, 156, 1101–1115.

Hu H C, Wang Y Y, Tsay Y F. 2009. AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. The Plant Journal, 57, 264–278.

Huang L F, Zhang H C, Zhang H Y, Deng X W, Wei N. 2015. HY5 regulates nitrite reductase 1 (NIR1) and ammonium transporter1;2 (AMT1;2) in Arabidopsis seedlings. Plant Science, 238, 330–339.

Huang X Z, Qian Q, Liu Z B, Sun H Y, He S Y, Luo D, Xia G M, Chu C C, Li J Y, Fu X D. 2009. Natural variation at the DEP1 locus enhances grain yield in rice. Nature Genetics, 41, 494–497.

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 Physiology, 156, 1164–1175.

Jonassen E M, Sevin D C, Lillo C. 2009. The bZIP transcription factors HY5 and HYH are positive regulators of the main nitrate reductase gene in Arabidopsis leaves, NIA2, but negative regulators of the nitrate uptake gene NRT1.1. Journal of Plant Physiology, 166, 2071–2076.

Khademi S, O’Connell J, Remis J, Robles-Colmenares Y, Miericke L J W, Stroud R M. 2004. Mechanism of ammonia transport by Amt/MEP/Rh: Structure of AmtB at 1.3.5 angstrom. Science, 305, 1587–1594.

Komarova N Y, Thor K, Gubler A, Meier S, Dietrich D, Weichert A, Suter Grotemeyer M, Tegeder M, Rentsch D. 2008. AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiology, 148, 856–869.

Kumar A, Kaiser B N, Siddiqi M Y, Glass A D M. 2006. Functional characterisation of OsAMT1.1 overexpression lines of rice, Oryza sativa. Functional Plant Biology, 33, 339–346.

Kurai T, Wakayama M, Abiko T, Yanagisawa S, Aoki N, Ohsugi R. 2011. Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions. Plant Biotechnology Journal, 9, 826–837.

Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao H Y, Lee I, Deng X. 2007. Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. The Plant Cell, 19, 731–749.

Li H, Huang G, Meng Q, Ma L, Yuan L, Wang F, Zhang W, Cui Z, Shen J, Chen X, Jiang R, Zhang F. 2011. Integrated soil and plant phosphorus management for crop and environment in China. A review. Plant and Soil, 349, 157–167.

Li X, Guo C, Gu J, Duan W, Zhao M, Ma C, Du X, Lu W, Xiao K. 2014. Overexpression of VP, a vacuolar H+-pyrophosphatase gene in wheat (Triticum aestivum L.), improves tobacco plant growth under Pi and N deprivation, high salinity, and drought. Journal of Experimental Botany, 65, 683–696.

Li X, Zhao J, Tan Z, Zeng R, Liao H. 2015. GmEXPB2, a cell wall beta-expansin, affects soybean nodulation through modifying root architecture and promoting nodule formation and development. Plant Physiology, 169, 2640–2653.

Li Y T, Zhang J, Zhang X, Fan H M, Gu M, Qu H Y, Xu G H. 2015. Phosphate transporter OsPht1;8 in rice plays an important role in phosphorus redistribution from source to sink organs and allocation between embryo and endosperm of seeds. Plant Science, 230, 23–32.

Li Z, Gao Q, Liu Y, He C, Zhang X, Zhang J. 2011b. Overexpression of transcription factor ZmPTF1 improves low phosphate tolerance of maize by regulating carbon metabolism and root growth. Planta, 233, 1129–1143.

Liang C, Tian J, Lam H M, Lim B L, Yan X, Liao H. 2010. Biochemical and molecular characterization of PvPAP3, a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization. Plant Physiology, 152, 854–865.

Liang C, Wang Y, Zhu Y, Tang J, Hu B, Liu L, Ou S, Wu H, Sun X, Chu J, Chu C. 2014. OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proceedings of the National Academy of Sciences of the United States of America, 111, 10013–10018.

Liang Q A, Cheng X H, Mei M T, Yan X L, Liao H. 2010. QTL analysis of root traits as related to phosphorus efficiency in soybean. Annals of Botany, 106, 223–234.

Liao H, Yan X L, Rubio G, Beebe S E, Blair M W, Lynch J P. 2004. Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Functional Plant Biology, 31, 959–970.

Liu F, Wang Z, Ren H, Shen C, Li Y, Ling H Q, 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. The Plant Journal, 62, 508–517.

Liu K H, Huang C Y, Tsay Y F. 1999. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. The Plant Cell, 11, 865–874.

Liu X J, Zhang Y, Han W X, Tang A H, Shen J L, Cui Z L, Vitousek P, Erisman J W, Goulding K, Christie P, Fangmeier A, Zhang F S. 2013. Enhanced nitrogen deposition over China. Nature, 494, 459–462.

Liu X M, Zhao X L, Zhang L J, Lu W J, Li X J, Xiao K. 2013. TaPht1;4, a high-affinity phosphate transporter gene in wheat (Triticum aestivum), plays an important role in plant phosphate acquisition under phosphorus deprivation. Functional Plant Biology, 40, 329–341.

Lu J, Gao X, Dong Z, Yi J, An L. 2012. Improved phosphorus acquisition by tobacco through transgenic expression of mitochondrial malate dehydrogenase from Penicillium oxalicum. Plant Cell Reports, 31, 49–56.

Ludewig U, Neuhauser B, Dynowski M. 2007. Molecular mechanisms of ammonium transport and accumulation in plants. FEBS Letters, 581, 2301–2308.

Lynch J P. 2007. Roots of the second green revolution. Australian Journal of Botany, 55, 493–512.

Ma W Y, Li J J, Qu B Y, He X, Zhao X Q, Li B, Fu X D, Tong Y P. 2014. Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis. The Plant Journal, 78, 70–79.

Ma X F, Wright E, Ge Y, Bell J, Xi Y, Bouton J H, Wang Z Y. 2009. Improving phosphorus acquisition of white clover (Trifolium repens L.) by transgenic expression of plant-derived phytase and acid phosphatase genes. Plant Science, 176, 479–488.

Ma Z, Liu J, Wang X. 2013. Agrobacterium-mediated transformation of cotton (Gossypium hirsutum) shoot apex with a fungal phytase gene improves phosphorus acquisition. Methods in Molecular Biology, 958, 211–222.

Marchive C, Roudier F, Castaings L, Brehaut V, Blondet E, Colot V, Meyer C, Krapp A. 2013. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nature Communications, 4, 1713.

Marschner H, Marschner P. 2012. Marschner’s Mineral Nutrition of Higher Plants. Elsevier/Academic Press, Waltham, MA, London. p. 651.

Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A. 2010. Nitrogen uptake, assimilation and remobilization in plants: Challenges for sustainable and productive agriculture. Annals of Botany, 105, 1141–1157.

McAllister C H, Beatty P H, Good A G. 2012. Engineering nitrogen use efficient crop plants: The current status. Plant Biotechnology Journal, 10, 1011–1025.

Mi G H, Chen F J, Wu Q P, Lai N W, Yuan L X, Zhang F S. 2010. Ideotype root architecture for efficient nitrogen acquisition by maize in intensive cropping systems. Science China (Life Sciences), 53, 1369–1373.

Miflin B J, Habash D Z. 2002. The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. Journal of Experimental Botany, 53, 979–987.

Miller A E, Bowman W D, Suding K N. 2007. Plant uptake of inorganic and organic nitrogen: Neighbor identity matters. Ecology, 88, 1832–1840.

Nasholm T, Persson J. 2001. Plant acquisition of organic nitrogen in boreal forests. Physiologia Plantarum, 111, 419–426.

Nieves-Cordones M, Aleman F, Martinez V, Rubio F. 2010. The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from Low K+ solutions under saline conditions. Molecular Plant, 3, 326–333.

Nussaume L, Kanno S, Javot H, Marin E, Pochon N, Ayadi A, Nakanishi T M, Thibaud M C. 2011. Phosphate import in plants: focus on the PHT1 transporters. Frontiers in Plant Science, 2, 83.

Ouyang X, Hong X, Zhao X, Zhang W, He X, Ma W, Teng W, Tong Y. 2016. Knock out of the PHOSPHATE 2 gene TaPHO2-A1 improves phosphorus uptake and grain yield under low phosphorus conditions in common wheat. Scientific Reports, 6, 29850.

Qin L, Zhao J, Tian J, Chen L Y, Sun Z A, Guo Y X, Lu X, Gu M A, Xu G H, Liao H. 2012. The high-affinity phosphate transporter GmPT5 regulates phosphate transport to nodules and nodulation in soybean. Plant Physiology, 159, 1634–1643.

Qu B, He X, Wang J, Zhao Y, Teng W, Shao A, Zhao X, Ma W, Wang J, Li B, Li Z, Tong Y. 2015. A wheat CCAAT box-binding transcription factor increases the grain yield of wheat with less fertilizer input. Plant Physiology, 167, 411–423.

Ragel P, Rodenas R, Garcia-Martin E, Andres Z, Villalta I, Nieves-Cordones M, Rivero R M, Martinez V, Pardo J M, Quintero F J, Rubio F. 2015. The CBL-interacting protein kinase CIPK23 regulates HAK5-mediated high-affinity K+ uptake in Arabidopsis roots. Plant Physiology, 169, 2863–2873.

Raghothama K G. 2000. Phosphate transport and signaling. Current Opinion in Plant Biology, 3, 182–187.

Raghothama K G, Karthikeyan A S. 2005. Phosphate acquisition. Plant and Soil, 274, 37–49.

Ranathunge K, El-Kereamy A, Gidda S, Bi Y M, Rothstein S J. 2014. AMT1;1 transgenic rice plants with enhanced NH4+ permeability show superior growth and higher yield under optimal and suboptimal NH4+ conditions. Journal of Experimental Botany, 65, 965–979.

Ren F, Guo Q Q, Chang L L, Chen L, Zhao C Z, Zhong H, Li X B. 2012. Brassica napus PHR1 gene encoding a MYB-like protein functions in response to phosphate starvation. PLOS ONE, 7, e44005.

Ren Y Z, He X, Liu D C, Li J J, Zhao X Q, Li B, Tong Y P, Zhang A M, Li Z S. 2012. Major quantitative trait loci for seminal root morphology of wheat seedlings. Molecular Breeding, 30, 139–148.

Rengel Z, Damon P M. 2008. Crops and genotypes differ in efficiency of potassium uptake and use. Physiologia Plantarum, 133, 624–636.

Rubin G, Tohge T, Matsuda F, Saito K, Scheible W R. 2009. Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. The Plant Cell, 21, 3567–3584.

Schachtman D P, Reid R J, Ayling S M. 1998. Phosphorus uptake by plants: from soil to cell. Plant Physiology, 116, 447–453.

Seo H M, Jung Y, Song S, Kim Y, Kwon T, Kim D H, Jeung S J, Yi Y B, Yi G, Nam M H, Nam J. 2008. Increased expression of OsPT1, a high-affinity phosphate transporter, enhances phosphate acquisition in rice. Biotechnology Letters, 30, 1833–1838.

Sharma S, Xu S Z, Ehdaie B, Hoops A, Close T J, Lukaszewski A J, Waines J G. 2011. Dissection of QTL effects for root traits using a chromosome arm-specific mapping population in bread wheat. Theoretical and Applied Genetics, 122, 759–769.

Shen J B, Yuan L X, Zhang J L, Li H G, Bai Z H, Chen X P, Zhang W F, Zhang F S. 2011. Phosphorus dynamics: From soil to plant. Plant Physiology, 156, 997–1005.

Shrawat A K, Carroll R T, DePauw M, Taylor G J, Good A G. 2008. Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnology Journal, 6, 722–732.

Smith S E, Smith F A. 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Annual Review of Plant Biology, 62, 227–250.

Song Z Z, Yang S Y, Zuo J, Su Y H. 2014. Over-expression of ApKUP3 enhances potassium nutrition and drought tolerance in transgenic rice. Biologia Plantarum, 58, 649–658.

Steele K A, Virk D S, Kumar R, Prasad S C, Witcombe J R. 2007. Field evaluation of upland rice lines selected for QTLs controlling root traits. Field Crops Research, 101, 180–186.

Sun H Y, Qian Q, Wu K, Luo J J, Wang S S, Zhang C W, Ma Y F, Liu Q, Huang X Z, Yuan Q B, Han R X, Zhao M, Dong G J, Guo L B, Zhu X D, Gou Z H, Wang W, Wu Y J, Lin H X, Fu X D. 2014. Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nature Genetics, 46, 652–656.

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

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

Teng W, Deng Y, Chen X P, Xu X F, Chen R Y, Lv Y, Zhao Y Y, Zhao X Q, He X, Li B, Tong Y P, Zhang F S, Li Z S. 2013. Characterization of root response to phosphorus supply from morphology to gene analysis in field-grown wheat. Journal of Experimental Botany, 64, 1403–1411.

Thomsen H C, Eriksson D, Moller I S, Schjoerring J K. 2014. Cytosolic glutamine synthetase: A target for improvement of crop nitrogen use efficiency? Trends in Plant Science, 19, 656–663.

Tian J, Wang X R, Tong Y P, Chen X P, Liao H. 2012. Bioengineering and management for efficient phosphorus utilization in crops and pastures. Current Opinion in Biotechnology, 23, 866–871.

Tilman D, Cassman K G, Matson P A, Naylor R, Polasky S. 2002. Agricultural sustainability and intensive production practices. Nature, 418, 671–677.

Tong Y, Zhou J J, Li Z, Miller A J. 2005. A two-component high-affinity nitrate uptake system in barley. The Plant Journal, 41, 442–450.

Trachsel S, Kaeppler S M, Brown K M, Lynch J P. 2013. Maize root growth angles become steeper under low N conditions. Field Crops Research, 140, 18–31.

Tuberosa R, Sanguineti M C, Landi P, Michela Giuliani M, Salvi S, Conti S. 2002. Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Molecular Biology, 48, 697–712.

Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M. 2013. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics, 45, 1097–1102.

Vidal E A, Moyano T C, Riveras E, Contreras-Lopez O, Gutierrez R A. 2013. Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proceedlings of the National Academy of Sciences of the United States of America, 110, 12840–12845.

von Wiren N, Gazzarrini S, Gojon A, Frommer W B. 2000. The molecular physiology of ammonium uptake and retrieval. Current Opinion in Plant Biology, 3, 254–261.

von Wittgenstein N J, Le C H, Hawkins B J, Ehlting J. 2014. Evolutionary classification of ammonium, nitrate, and peptide transporters in land plants. BMC Evolutionary Biology, 14, 11.

Wang C, Ying S, Huang H, Li K, Wu P, Shou H. 2009. Involvement of OsSPX1 in phosphate homeostasis in rice. The Plant Journal, 57, 895–904.

Wang H, Xu Q, Kong Y H, Chen Y, Duan J Y, Wu W H, Chen Y F. 2014. Arabidopsis WRKY45 transcription factor activates PHOSPHATE TRANSPORTER1;1 expression in response to phosphate starvation. Plant Physiology, 164, 2020–2029.

Wang J, Sun J H, Miao J, Guo J K, Shi Z L, He M Q, Chen Y, Zhao X Q, Li B, Han F P, Tong Y P, Li Z S. 2013. A phosphate starvation response regulator Ta-PHR1 is involved in phosphate signalling and increases grain yield in wheat. Annals of Botany, 111, 1139–1153.

Wang X, Wang Y, Pineros M A, Wang Z, Wang W, Li C, Wu Z, Kochian L V, Wu P. 2014. Phosphate transporters OsPHT1;9 and OsPHT1;10 are involved in phosphate uptake in rice. Plant, Cell and Environment, 37, 1159–1170.

Wang X R, Wang Y X, Tian J, Lim B L, Yan X L, Liao H. 2009. Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiology, 151, 233–240.

Wang X Y, Li J, Zou X, Lu L M, Li L Q, Ni S, Liu F. 2011. Ectopic expression of AtCIPK23 enhances tolerance against low-K+ stress in transgenic potato. American Journal of Potato Research, 88, 153–159.

Wang Y, Wu W H. 2013. Potassium transport and signaling in higher plants. Annual Review of Plant Biology, 64, 451–476.

Wasaki J, Maruyama H, Tanaka M, Yamamura T, Dateki H, Shinano T, Ito S, Osaki M. 2009. Overexpression of the LASAP2 gene for secretory acid phosphatase in white lupin improves the phosphorus uptake and growth of tobacco plants. Soil Science and Plant Nutrition, 55, 107–113.

West P C, Gerber J S, Engstrom P M, Mueller N D, Brauman K A, Carlson K M, Cassidy E S, Johnston M, MacDonald G K, Ray D K, Siebert S. 2014. Leverage points for improving global food security and the environment. Science, 345, 325–328.

White P J. 2013. Improving potassium acquisition and utilisation by crop plants. Journal of Plant Nutrition and Soil Science, 176, 305–316.

Wissuwa M, Wegner J, Ae N, Yano M. 2002. Substitution mapping of Pup1: A major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theoretical and Applied Genetics, 105, 890–897.

Xu G H, Fan X R, Miller A J. 2012. Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology, 63, 153–182.

Xu J, Li H D, Chen L Q, Wang Y, Liu L L, He L, Wu W H. 2006. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell, 125, 1347–1360.

Xu N, Wang R, Zhao L, Zhang C, Li Z, Lei Z, Liu F, Guan P, Chu Z, Crawford N M, Wang Y. 2016. The Arabidopsis NRG2 protein mediates nitrate signaling and interacts with and regulates key nitrate regulators. The Plant Cell, 28, 485–504.

Xue G, Lu L M, Yang T Z, Li X H, Xing X X, Xu S X. 2016. Enhanced tolerance to low-K+ stress in tobacco plants, that ectopically express the CBL-interacting protein kinase CIPK23 gene. Czech Journal of Genetics and Plant Breeding, 52, 77–82.

Yamaji N, Takemoto Y, Miyaji T, Mitani-Ueno N, Yoshida K T, Ma J F. 2017. Reducing phosphorus accumulation in rice grains with an impaired transporter in the node. Nature, 541, 92–95.

Yan M, Fan X, Feng H, Miller A J, Shen Q, 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 and Environment, 34, 1360–1372.

Yan W, Chen G H, Yang L F, Gai J Y, Zhu Y L. 2014. Overexpression of the rice phosphate transporter gene OsPT6 enhances tolerance to low phosphorus stress in vegetable soybean. Scientia Horticulturae, 177, 71–76.

Yanagisawa S. 2000. Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. The Plant Journal, 21, 281–288.

Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T. 2004. Metabolic engineering with Dof1 transcription factor in plants: Improved nitrogen assimilation and growth under low-nitrogen conditions. Proceedings of the National Academy of Sciences of the United States of America, 101, 7833–7838.

Yanagisawa S, Sheen J. 1998. Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. The Plant Cell, 10, 75–89.

Yang T Y, Zhang S, Hu Y B, Wu F C, Hu Q D, Chen G, Cai J, Wu T, Moran N, Yu L, Xu G H. 2014. The role of a potassium transporter OsHAK5 in potassium acquisition and transport from roots to shoots in rice at low potassium supply levels. Plant Physiology, 166, 945–959.

Yao Z F, Tian J, Liao H. 2014. Comparative characterization of GmSPX members reveals that GmSPX3 is involved in phosphate homeostasis in soybean. Annals of Botany, 114, 477–488.

Ye Y, Yuan J, Chang X, Yang M, Zhang L, Lu K, Lian X. 2015. The phosphate transporter gene OsPht1;4 is involved in phosphate homeostasis in rice. PLOS ONE, 10, e0126186.

Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P. 2005. OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiology, 138, 2087–2096.

Yu C Y, Liu Y H, Zhang A D, Su S, Yan A, Huang L, Ali I, Liu Y, Forde B G, Gan Y B. 2015. MADS-box transcription factor OsMADS25 regulates root development through affection of nitrate accumulation in rice. PLOS ONE, 10, e0135196.

Yu L H, Wu J, Tang H, Yuan Y, Wang S M, Wang Y P, Zhu Q S, Li S G, Xiang C B. 2016. Overexpression of Arabidopsis NLP7 improves plant growth under both nitrogen-limiting and -sufficient conditions by enhancing nitrogen and carbon assimilation. Scientific Reports, 6, 27795.

Zeng Y J, Ying J, Liu J Z, Sun J H, Li B, Xiao H S, Li Z S. 2002. Function analysis of a wheat phosphate transporter in yeast mutant. Acta Genetica Sinica, 29, 1017–1020.

Zhang D, Song H N, Cheng H, Hao D R, Wang H, Kan G Z, Jin H X, Yu D Y. 2014. The acid phosphatase-encoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. PLoS Genetics, 10, e1004061.

Zhang F, Wu X N, Zhou H M, Wang D F, Jiang T T, Sun Y F, Cao Y, Pei W X, Sun S B, Xu G H. 2014. Overexpression of rice phosphate transporter gene OsPT6 enhances phosphate uptake and accumulation in transgenic rice plants. Plant and Soil, 384, 259–270.

Zhang F S, Chen X P, Vitousek P. 2013. An experiment for the world. Nature, 497, 33–35.

Zhang H, Forde B G. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science, 279, 407–409.

Zhang Q F. 2007. Strategies for developing green super rice. Proceedings of the National Academy of Sciences of the United States of America, 104, 16402–16409.

Zhang Y, Tan L, Zhu Z, Yuan L, Xie D, Sun C. 2015. TOND1 confers tolerance to nitrogen deficiency in rice. The Plant Journal, 81, 367–376.

Zhang Z, Liao H, Lucas W J. 2014. Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. Journal of Integrative Plant Biology, 56, 192–220.

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

Zhou J, Xie J, Liao H, Wang X. 2014. Overexpression of beta-expansin gene GmEXPB2 improves phosphorus efficiency in soybean. Physiologia Plantarum, 150, 194–204.

Zhu W L, Yang L F, Yang S P, Gai J Y, Zhu Y L. 2016. Overexpression of rice phosphate transporter gene OsPT2 enhances nitrogen fixation and ammonium assimilation in transgenic soybean under phosphorus deficiency. Journal of Plant Biology, 59, 172–181.
[1] MAO Hui, QUAN Yu-Rong, FU Yong. Risk preferences and the low-carbon agricultural technology adoption: Evidence from rice production in China[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2577-2590.
[2] ZHANG Chong, WANG Dan-dan, ZHAO Yong-jian, XIAO Yu-lin, CHEN Huan-xuan, LIU He-pu, FENG Li-yuan, YU Chang-hao, JU Xiao-tang. Significant reduction of ammonia emissions while increasing crop yields using the 4R nutrient stewardship in an intensive cropping system[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1883-1895.
[3] HAN Yu-ling, GUO Dong, MA Wei, GE Jun-zhu, LI Xiang-ling, Ali Noor MEHMOOD, ZHAO Ming, ZHOU Bao-yuan. Strip deep rotary tillage combined with controlled-release urea improves the grain yield and nitrogen use efficiency of maize in the North China Plain[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2559-2576.
[4] ZHANG Hua, WU Hai-yan, TIAN Rui, KONG You-bin, CHU Jia-hao, XING Xin-zhu, DU Hui, JIN Yuan, LI Xi-huan, ZHANG Cai-ying. Genome-wide association and linkage mapping strategies reveal genetic loci and candidate genes of phosphorus utilization in soybean[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2521-2537.
[5] HUI Jing, LIU Zhi, DUAN Feng-ying, ZHAO Yang, LI Xue-lian, AN Xia, WU Xiang-yu, YUAN Li-xing. Ammonium-dependent regulation of ammonium transporter ZmAMT1s expression conferred by glutamine levels in roots of maize[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2413-2421.
[6] LI Ting-ting, LU Na, SHAO Yu-xin, ZHANG Li-yang, LU Lin, LIU Zong-ping, LUO Xu-gang, LIAO Xiu-dong. Effect of the gene silencing of phosphorus transporters on phosphorus absorption across primary cultured duodenal epithelial cell monolayers of chick embryos[J]. >Journal of Integrative Agriculture, 2022, 21(7): 2076-2085.
[7] TIAN Xue-liang, LIU Jia-jia, LIU Quan-cheng, XIA Xin-yao, PENG Yong, Alejandra I. HUERTA, YAN Jian-bing, LI Hui, LIU Wen-de. The effects of soil properties, cropping systems and geographic location on soil prokaryotic communities in four maize production regions across China [J]. >Journal of Integrative Agriculture, 2022, 21(7): 2145-2157.
[8] Muhammad QASWAR, Waqas AHMED, HUANG Jing, LIU Kai-lou, ZHANG Lu, HAN Tian-fu, DU Jiang-xue, Sehrish ALI, Hafeez UR-RAHIM, HUANG Qing-hai, ZHANG Hui-min. Interaction of soil microbial communities and phosphorus fractions under long-term fertilization in paddy soil [J]. >Journal of Integrative Agriculture, 2022, 21(7): 2134-2144.
[9] TIAN Chang, SUN Ming-xue, ZHOU Xuan, LI Juan, XIE Gui-xian, YANG Xiang-dong, PENG Jian-wei. Increase in yield and nitrogen use efficiency of double rice with long-term application of controlled-release urea[J]. >Journal of Integrative Agriculture, 2022, 21(7): 2106-2118.
[10] WU Xiao-li, LIU Miao, LI Chao-su, Allen David (Jack) MCHUGH, LI Ming, XIONG Tao, LIU Yu-bin, TANG Yong-lu. Source–sink relations and responses to sink–source manipulations during grain filling in wheat[J]. >Journal of Integrative Agriculture, 2022, 21(6): 1593-1605.
[11] Muhammad QASWAR, LI Dong-chu, HUANG Jing, HAN Tian-fu, Waqas AHMED, Sehrish ALI, Muhammad Numan KHAN, Zulqarnain Haider KHAN, XU Yong-mei, LI Qian, ZHANG Hui-min, WANG Bo-ren, Ahmad TAUQEER. Dynamics of organic carbon and nitrogen in deep soil profile and crop yields under long-term fertilization in wheat-maize cropping system[J]. >Journal of Integrative Agriculture, 2022, 21(3): 826-839.
[12] YU Xiao-jing, CHEN Qi, SHI Wen-cong, GAO Zheng, SUN Xiao, DONG Jing-jing, LI Juan, WANG Heng-tao, GAO Jian-guo, LIU Zhi-guang, ZHANG Min. Interactions between phosphorus availability and microbes in a wheat–maize double cropping system: a reduced fertilization scheme[J]. >Journal of Integrative Agriculture, 2022, 21(3): 840-854.
[13] LI Shuang, FENG Shi-qian, Hidayat ULLAH, TU Xiong-bing, ZHANG Ze-hua. IPM - Biological and integrated management of desert locust[J]. >Journal of Integrative Agriculture, 2022, 21(12): 3467-3487.
[14] HUANG Li-ying, Li Xiao-xiao, ZHANG Yun-bo, Shah FAHAD, WANG Fei. dep1 improves rice grain yield and nitrogen use efficiency simultaneously by enhancing nitrogen and dry matter translocation[J]. >Journal of Integrative Agriculture, 2022, 21(11): 3185-3198.
[15] Muhammad Amjad BASHIR, ZHAI Li-mei, WANG Hong-yuan, LIU Jian, Qurat-Ul-Ain RAZA, GENG Yu-cong, Abdur REHIM, LIU Hong-bin. Apparent variations in nitrogen runoff and its uptake in paddy rice under straw incorporation[J]. >Journal of Integrative Agriculture, 2022, 21(11): 3356-3367.
No Suggested Reading articles found!