Improved leaf nitrogen reutilisation and Rubisco activation under short-term nitrogen-deficient conditions promotes photosynthesis in winter wheat (Triticum aestivum L.) at the seedling stage
Jingwen Gao A , Feng Wang A B , Hang Hu A , Suyu Jiang A , Abid Muhammad A , Yuhang Shao A , Chuanjiao Sun A , Zhongwei Tian A , Dong Jiang A and Tingbo Dai A C
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Crop Physiology, Ecology and Production Management, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, P.R. China.
B Center of Excellence for Soil Biology, College of Resources and Environment, Southwest University, Beibei, Chongqing 400715, P.R. China.
C Corresponding author. Email: tingbod@njau.edu.cn
Functional Plant Biology 45(8) 840-853 https://doi.org/10.1071/FP17232
Submitted: 9 April 2017 Accepted: 6 February 2018 Published: 29 March 2018
Abstract
Excess N input results in low N use efficiency and environmental crisis, so nitrogenous fertiliser applications must be reduced. However, this can lead to low-N stress. Previous studies on low N have not explored the unique adjustment strategy to N deficiency in the short term, which is important for developing long-term N deficiency tolerance. In this case, two wheat (Triticum aestivum L.) cultivars with different tolerances to low N, Zaoyangmai (sensitive) and Yangmai158 (tolerant), were exposed to 0.25 mM N as a N-deficient condition with 5.0 mM N as a control. Under long-term N-deficient conditions, a significant decrease in Rubisco content resulted in decreased Rubisco activity and net photosynthetic rate (Pn) in both cultivars. However, the NO3– : soluble protein ratio decreased, and nitrate reductase and glutamine synthetase activity increased under short-term N deficiency, especially in Yangmai158. As a result, Rubisco content was not decreased in Yangmai158, while total N content decreased significantly. Moreover, increased Rubisco activase activity promoted Rubisco activation under short-term N deficiency. In sequence, Rubisco activity and Pn improved under short-term N deficiency. In conclusion, N deficiency-tolerant cultivars can efficiently assimilate N to Rubisco and enhance Rubisco activation to improve photosynthetic capabilities under short-term N deficiency conditions.
Additional keywords: glutamine synthetase; net photosynthetic rate; nitrate reductase; nitrogen deficiency; NO3– remobilisation.
References
Abid M, Tian Z, Ata-Ul-Karim ST, Wang F, Liu Y, Zahoor R, Jiang D, Dai T (2016) Adaptation to and recovery from drought stress at vegetative stages in wheat (Triticum aestivum) cultivars. Functional Plant Biology 43, 1159–1169.| Adaptation to and recovery from drought stress at vegetative stages in wheat (Triticum aestivum) cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVGqsLbN&md5=aee948e429dd4b4e58a4e5ebd982e189CAS |
Andrews M, Morton J, Lieffering M, Bisset L (1992) The partitioning of nitrate assimilation between root and shoot of a range of temperate cereals and pasture grasses. Annals of Botany 70, 271–276.
| The partitioning of nitrate assimilation between root and shoot of a range of temperate cereals and pasture grasses.Crossref | GoogleScholarGoogle Scholar |
Ariz I, Asensio AC, Zamarreno AM, Garcia-Mina JM, Aparicio-Tejo PM, Moran JF (2013) Changes in the C/N balance caused by increasing external ammonium concentrations are driven by carbon and energy availabilities during ammonium nutrition in pea plants: the key roles of asparagine synthetase and anaplerotic enzymes. Physiologia Plantarum 148, 522–537.
| Changes in the C/N balance caused by increasing external ammonium concentrations are driven by carbon and energy availabilities during ammonium nutrition in pea plants: the key roles of asparagine synthetase and anaplerotic enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1ymt73F&md5=6a2775203e466ff396e41cb00bf62b8eCAS |
Azcón-Bieto J (1983) Inhibition of photosynthesis by carbohydrates in wheat leaves. Plant Physiology 73, 681–686.
| Inhibition of photosynthesis by carbohydrates in wheat leaves.Crossref | GoogleScholarGoogle Scholar |
Baki G, Siefritz F, Man HM, Weiner H, Kaldenhoff R, Kaiser W (2000) Nitrate reductase in Zea mays L. under salinity. Plant, Cell & Environment 23, 515–521.
| Nitrate reductase in Zea mays L. under salinity.Crossref | GoogleScholarGoogle Scholar |
Blumwald E (2000) Sodium transport and salt tolerance in plants. Current Opinion in Cell Biology 12, 431–434.
| Sodium transport and salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Srtbg%3D&md5=9d389b7af3638fe697141a43e4547c9fCAS |
Boussadia O, Steppe K, Zgallai H, Ben El Hadj S, Braham M, Lemeur R, Van Labeke MC (2010) Effects of nitrogen deficiency on leaf photosynthesis, carbohydrate status and biomass production in two olive cultivars ‘Meski’ and ‘Koroneiki’. Scientia Horticulturae 123, 336–342.
| Effects of nitrogen deficiency on leaf photosynthesis, carbohydrate status and biomass production in two olive cultivars ‘Meski’ and ‘Koroneiki’.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGrsLnL&md5=3a66e703ecc112d48d7b7c45b3a5f26fCAS |
Bracher A, Whitney SM, Hartl FU, Hayer-Hartl M (2017) Biogenesis and metabolic maintenance of Rubisco. Annual Review of Plant Biology 68, 29–60.
| Biogenesis and metabolic maintenance of Rubisco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhs1Kitbk%3D&md5=5e04a5d9cb56c226e989d7e453144f84CAS |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=90b0b14534fb4b0d25711d896ae5505eCAS |
Buysse J, Merckx R (1993) An improved colorimetric method to quantify sugar content of plant tissue. Journal of Experimental Botany 44, 1627–1629.
| An improved colorimetric method to quantify sugar content of plant tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXkvFeiuw%3D%3D&md5=6d7add2ec51daa0087fbfceedcbaa76eCAS |
Carmo-Silva AE, Salvucci ME (2011) The activity of Rubisco’s molecular chaperone, Rubisco activase, in leaf extracts. Photosynthesis Research 108, 143–155.
| The activity of Rubisco’s molecular chaperone, Rubisco activase, in leaf extracts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFCmurfN&md5=63d340e721a5a5b7202b67279aefdd5cCAS |
Cataldo D, Maroon M, Schrader L, Youngs V (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid 1. Communications in Soil Science and Plant Analysis 6, 71–80.
| Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXhs1Kqt7Y%3D&md5=3d1ba79b58c864a1e10cdf11cf9049b2CAS |
Chen B-M, Wang Z-H, Li S-X, Wang G-X, Song H-X, Wang X-N (2004) Effects of nitrate supply on plant growth, nitrate accumulation, metabolic nitrate concentration and nitrate reductase activity in three leafy vegetables. Plant Science 167, 635–643.
| Effects of nitrate supply on plant growth, nitrate accumulation, metabolic nitrate concentration and nitrate reductase activity in three leafy vegetables.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFOqtb0%3D&md5=7421b9d7d17752710993930e442f96b9CAS |
Cheng L, Fuchigami LH (2000) Rubisco activation state decreases with increasing nitrogen content in apple leaves. Journal of Experimental Botany 51, 1687–1694.
| Rubisco activation state decreases with increasing nitrogen content in apple leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVWis74%3D&md5=f0f0eb0bae4cd45429a1c0f19da05962CAS |
Ciompi S, Gentili E, Guidi L, Soldatini GF (1996) The effect of nitrogen deficiency on leaf gas exchange and chlorophyll fluorescence parameters in sunflower. Plant Science 118, 177–184.
| The effect of nitrogen deficiency on leaf gas exchange and chlorophyll fluorescence parameters in sunflower.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XktlSiurY%3D&md5=6f56975f5561c66088d9c657b2114341CAS |
Conn SJ, Hocking B, Dayod M, Xu B, Athman A, Henderson S, Aukett L, Conn V, Shearer MK, Fuentes S, Tyerman SD, Gilliham M (2013) Protocol: optimising hydroponic growth systems for nutritional and physiological analysis of Arabidopsis thaliana and other plants. Plant Methods 9, 4
| Protocol: optimising hydroponic growth systems for nutritional and physiological analysis of Arabidopsis thaliana and other plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotFWru7Y%3D&md5=c0767152bed5f2eab3c223aea3a9fd06CAS |
Cren M, Hirel B (1999) Glutamine synthetase in higher plants regulation of gene and protein expression from the organ to the cell. Plant & Cell Physiology 40, 1187–1193.
| Glutamine synthetase in higher plants regulation of gene and protein expression from the organ to the cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVeq&md5=06c322cb48f81325cd8ee189293b1549CAS |
Cruz J, Mosquim P, Pelacani C, Araújo W, DaMatta F (2003) Photosynthesis impairment in cassava leaves in response to nitrogen deficiency. Plant and Soil 257, 417–423.
| Photosynthesis impairment in cassava leaves in response to nitrogen deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXoslWrt7g%3D&md5=d0f4fe39b258c380bf291ba3c34ab6dbCAS |
De Angeli A, Monachello D, Ephritikhine G, Frachisse J, Thomine S, Gambale F, Barbier-Brygoo H (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442, 939–942.
| The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVOgurY%3D&md5=186c3c0c5ec5260d535d3960e1a3f671CAS |
Engineer CB, Kranz RG (2007) Reciprocal leaf and root expression of AtAmt1. 1 and root architectural changes in response to nitrogen starvation. Plant Physiology 143, 236–250.
| Reciprocal leaf and root expression of AtAmt1. 1 and root architectural changes in response to nitrogen starvation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1OntA%3D%3D&md5=9fc86bc297c76141b72f37c255f00fceCAS |
Feng X-P, Chen Y, Qi Y-H, Yu C-L, Zheng B-S, Brancourt-Hulmel M, Jiang D-A (2012) Nitrogen enhanced photosynthesis of Miscanthus by increasing stomatal conductance and phosphoenolpyruvate carboxylase concentration. Photosynthetica 50, 577–586.
| Nitrogen enhanced photosynthesis of Miscanthus by increasing stomatal conductance and phosphoenolpyruvate carboxylase concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvFSgtL3L&md5=127c7cccbddceb691ac2d8505cce00a6CAS |
Fuentes SI, Allen DJ, Ortiz-Lopez A, Hernandez G (2001) Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. Journal of Experimental Botany 52, 1071–1081.
| Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVeisrs%3D&md5=51f165a6121e6774787d5622f2a91322CAS |
Ghannoum O, Evans JR, Chow WS, Andrews TJ, Conroy JP, von Caemmerer S (2005) Faster Rubisco is the key to superior nitrogen-use efficiency in NADP-malic enzyme relative to NAD-malic enzyme C4 grasses. Plant Physiology 137, 638–650.
| Faster Rubisco is the key to superior nitrogen-use efficiency in NADP-malic enzyme relative to NAD-malic enzyme C4 grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1Kqsbk%3D&md5=10fddee4eac5258cbc8601d294a6c289CAS |
Gibson SI (2000) Plant sugar-response pathways. Part of a complex regulatory web. Journal of Experimental Botany 51, 1532–1539.
Gong P, Liang L, Zhang Q (2011) China must reduce fertilizer use too. Nature 473, 284–285.
| China must reduce fertilizer use too.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtleltro%3D&md5=7d3876f527f4b17603c8e1b2016e4cb4CAS |
Guiboileau A, Avila-Ospina L, Yoshimoto K, Soulay F, Azzopardi M, Marmagne A, Lothier J, Masclaux-Daubresse C (2013) Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability. New Phytologist 199, 683–694.
| Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSrurbL&md5=a359637264a258a04a9c2c963d1f7c53CAS |
Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiology 132, 578–596.
| Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslersbo%3D&md5=c7b277e8660d374139f888ca03cc851aCAS |
Harada H, Kuromori T, Hirayama T, Shinozaki K, Leigh RA (2004) Quantitative trait loci analysis of nitrate storage in Arabidopsis leading to an investigation of the contribution of the anion channel gene, AtCLC-c, to variation in nitrate levels. Journal of Experimental Botany 55, 2005–2014.
| Quantitative trait loci analysis of nitrate storage in Arabidopsis leading to an investigation of the contribution of the anion channel gene, AtCLC-c, to variation in nitrate levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsVyitr0%3D&md5=91cb878556268c8b377cd692fd4e01f0CAS |
Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science 11, 610–617.
| How do plants respond to nutrient shortage by biomass allocation?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1eqtbzE&md5=10edd9cdfb932238395adfc63cb8a853CAS |
Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. Journal of Experimental Botany 58, 2369–2387.
| The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXos1ykt74%3D&md5=82b39a839d013054d7dc66a286c82c98CAS |
Hubbard NL, Huber SC, Pharr DM (1989) Sucrose phosphate synthase and acid invertase as determinants of sucrose concentration in developing muskmelon (Cucumis melo L.) fruits. Plant Physiology 91, 1527
| Sucrose phosphate synthase and acid invertase as determinants of sucrose concentration in developing muskmelon (Cucumis melo L.) fruits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXnsVSitA%3D%3D&md5=08554ca218766f85bf4dc79b9357c836CAS |
Li D, Tian M, Cui H, Dai T, Jiang D, Jin Q, Cao W (2009a) Genotypic differences of low nitrogen tolerance at wheat early stage. Journal of Triticeae Crops 2, 007
Li Y, Gao Y, Xu X, Shen Q, Guo S (2009b) Light-saturated photosynthetic rate in high-nitrogen rice (Oryza sativa L.) leaves is related to chloroplastic CO2 concentration. Journal of Experimental Botany 60, 2351–2360.
| Light-saturated photosynthetic rate in high-nitrogen rice (Oryza sativa L.) leaves is related to chloroplastic CO2 concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyitbg%3D&md5=74d3fdd9bfec6c88a1e5b63e00618abaCAS |
Li Y, Yang X, Ren B, Shen Q, Guo S (2012) Why nitrogen use efficiency decreases under high nitrogen supply in rice (Oryza sativa L.) seedlings. Journal of Plant Growth Regulation 31, 47–52.
| Why nitrogen use efficiency decreases under high nitrogen supply in rice (Oryza sativa L.) seedlings.Crossref | GoogleScholarGoogle Scholar |
Li D, Tian M, Cai J, Jiang D, Cao W, Dai T (2013) Effects of low nitrogen supply on relationships between photosynthesis and nitrogen status at different leaf position in wheat seedlings. Plant Growth Regulation 70, 257–263.
| Effects of low nitrogen supply on relationships between photosynthesis and nitrogen status at different leaf position in wheat seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptFKhsrg%3D&md5=516a48f524f767826e941d558716fa47CAS |
Mächler F, Oberson A, Grub A, Nösberger J (1988) Regulation of photosynthesis in nitrogen deficient wheat seedlings. Plant Physiology 87, 46–49.
| Regulation of photosynthesis in nitrogen deficient wheat seedlings.Crossref | GoogleScholarGoogle Scholar |
Makino A (2011) Photosynthesis, grain yield, and nitrogen utilization in rice and wheat. Plant Physiology 155, 125–129.
| Photosynthesis, grain yield, and nitrogen utilization in rice and wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFagsbw%3D&md5=c4b6751677cf51cd427257d1109e7a9bCAS |
Makino A, Mae T, Ohira K (1986) Colorimetric measurement of protein stained with Coomassie Brilliant Blue R on sodium dodecyl sulfate-polyacrylamide gel electrophoresis by eluting with formamide. Agricultural and Biological Chemistry 50, 1911–1912.
Martinoia E, Heck U, Wiemken A (1981) Vacuoles as storage compartments for nitrate in barley leaves. Nature 289, 292–294.
| Vacuoles as storage compartments for nitrate in barley leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhslWjsLg%3D&md5=d2ec538c79f9a59344c4bd9f2a216eaaCAS |
Millard P (1988) The accumulation and storage of nitrogen by herbaceous plants. Plant, Cell & Environment 11, 1–8.
| The accumulation and storage of nitrogen by herbaceous plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXitFyqs7w%3D&md5=19d2b67d43142abf806235393d8c0031CAS |
Nguyen NT, McInturf SA, Mendoza-Cózatl DG (2016) Hydroponics: a versatile system to study nutrient allocation and plant responses to nutrient availability and exposure to toxic elements. Journal of Visualized Experiments 113, 54317
Parry MA, Andralojc PJ, Mitchell RA, Madgwick PJ, Keys AJ (2013) Manipulation of Rubisco: the amount, activity, function and regulation. Journal of Experimental Botany 19, 536–538.
Paul MJ, Driscoll SP (1997) Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source : sink imbalance. Plant, Cell & Environment 20, 110–116.
| Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source : sink imbalance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsV2msLY%3D&md5=4526d0e41057809b6b024a1301015699CAS |
Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany 54, 539–547.
| Carbon metabolite feedback regulation of leaf photosynthesis and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFKgtbY%3D&md5=d7b7e0d264985a11847ec5c8ad4a6046CAS |
Paul M, Stitt M (1993) Effects of nitrogen and phosphorus deficiencies on levels of carbohydrates, respiratory enzymes and metabolites in seedlings of tobacco and their response to exogenous sucrose. Plant, Cell & Environment 16, 1047–1057.
| Effects of nitrogen and phosphorus deficiencies on levels of carbohydrates, respiratory enzymes and metabolites in seedlings of tobacco and their response to exogenous sucrose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXisVSiu7c%3D&md5=54e8fff4452007d76f727ac028573916CAS |
Pego JV (2000) Photosynthesis, sugars and the regulation of gene expression. Journal of Experimental Botany 51, 407–416.
| Photosynthesis, sugars and the regulation of gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsVKqu7Y%3D&md5=92c89298eaff8fc3a2f80bf30d323cecCAS |
Peng M, Bi Y-M, Zhu T, Rothstein SJ (2007) Genome-wide analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA. Plant Molecular Biology 65, 775–797.
| Genome-wide analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlCntLjN&md5=2baa9cde2b1983156f2e169692ff3cc3CAS |
Portis AR (2003) Rubisco activase – Rubisco’s catalytic chaperone. Photosynthesis Research 75, 11–27.
| Rubisco activase – Rubisco’s catalytic chaperone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1Krurk%3D&md5=d76f4c7b069f7c0913156d1eceb8cca1CAS |
Radin JW, Parker LL, Guinn G (1982) Water relations of cotton plants under nitrogen deficiency V. Environmental control of abscisic acid accumulation and stomatal sensitivity to abscisic acid. Plant Physiology 70, 1066–1070.
| Water relations of cotton plants under nitrogen deficiency V. Environmental control of abscisic acid accumulation and stomatal sensitivity to abscisic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XlvFOntL0%3D&md5=69527d6c8e258ffe1dcf098ea30f0477CAS |
Raines CA, Horsnell PR, Holder C, Lloyd JC (1992) Arabidopsis thaliana carbonic anhydrase: cDNA sequence and effect of CO2 on mRNA levels. Plant Molecular Biology 20, 1143–1148.
| Arabidopsis thaliana carbonic anhydrase: cDNA sequence and effect of CO2 on mRNA levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkvV2qsb0%3D&md5=0229093cb4ffc2e7472703c0b53433c9CAS |
Richter J, Roelcke M (2000) The N-cycle as determined by intensive agriculture – examples from central Europe and China. Nutrient Cycling in Agroecosystems 57, 33–46.
| The N-cycle as determined by intensive agriculture – examples from central Europe and China.Crossref | GoogleScholarGoogle Scholar |
Sage RF, Pearcy RW (1987) The nitrogen use efficiency of C3 and C4 plants II. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiology 84, 959–963.
| The nitrogen use efficiency of C3 and C4 plants II. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album (L.) and Amaranthus retroflexus (L.).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhslOisQ%3D%3D&md5=f38b6380a45db0bcf19e4ac5616b8ddcCAS |
Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annual Review of Plant Biology 58, 47–69.
| Nutrient sensing and signaling: NPKS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsVahs74%3D&md5=ce52981059c639a46e1776d104bcdf06CAS |
Setién I, Fuertes-Mendizabal T, González A, Aparicio-Tejo PM, González-Murua C, González-Moro MB, Estavillo JM (2013) High irradiance improves ammonium tolerance in wheat plants by increasing N assimilation. Journal of Plant Physiology 170, 758–771.
| High irradiance improves ammonium tolerance in wheat plants by increasing N assimilation.Crossref | GoogleScholarGoogle Scholar |
Shangguan ZP, Shao MG, Dyckmans J (2000) Effects of nitrogen nutrition and water deficit on net photosynthetic rate and chlorophyll fluorescence in winter wheat. Journal of Plant Physiology 156, 46–51.
| Effects of nitrogen nutrition and water deficit on net photosynthetic rate and chlorophyll fluorescence in winter wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhslyns74%3D&md5=38f17e145bc53687f4ebb9f477ffb754CAS |
Sharwood RE, Sonawane BV, Ghannoum O, Whitney SM (2016) Improved analysis of C4 and C3 photosynthesis via refined in vitro assays of their carbon fixation biochemistry. Journal of Experimental Botany 67, 3137–3148.
| Improved analysis of C4 and C3 photosynthesis via refined in vitro assays of their carbon fixation biochemistry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFSrsb7M&md5=fb8591378e33fc962e8c94154a60b547CAS |
Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant & Cell Physiology 46, 1350–1357.
| Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXps1Omsro%3D&md5=53577384f29b7c5c51ae56b7b17cc331CAS |
Smolders E, Merckx R (1992) Growth and shoot : root partitioning of spinach plants as affected by nitrogen supply. Plant, Cell & Environment 15, 795–807.
| Growth and shoot : root partitioning of spinach plants as affected by nitrogen supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXotVSlsg%3D%3D&md5=94f6a6763148f6b387a86624cf4fc879CAS |
Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annual Review of Plant Biology 53, 449–475.
| Rubisco: structure, regulatory interactions, and possibilities for a better enzyme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhurk%3D&md5=17ec454d97d96cdc074b66549639d95eCAS |
Tobin AK, Yamaya T (2001) Cellular compartmentation of ammonium assimilation in rice and barley. Journal of Experimental Botany 52, 591–604.
| Cellular compartmentation of ammonium assimilation in rice and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksFKht7k%3D&md5=5ba136a3f206fa4920074d038c2cbc01CAS |
van der Leij M, Smith SJ, Miller AJ (1998) Remobilization of vacuole stored nitrate in barley root cells. Planta 205, 64–72.
| Remobilization of vacuole stored nitrate in barley root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXislGitrY%3D&md5=26c7c7e1bf8d9356bf6bbfb78add46daCAS |
Wallsgrove RM, Keys AJ, Lea PJ, Miflin BJ (2006) Photosynthesis, photorespiration and nitrogen metabolism. Plant, Cell & Environment 6, 301–309.
Wang Y-Y, Hsu P-K, Tsay Y-F (2012) Uptake, allocation and signaling of nitrate. Trends in Plant Science 17, 458–467.
| Uptake, allocation and signaling of nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVeku7o%3D&md5=6994636ffe1b4e3fc058eb85ad67be89CAS |
Wang F, Gao J, Tian Z, Liu Y, Abid M, Jiang D, Cao W, Dai T (2016) Adaptation to rhizosphere acidification is a necessary prerequisite for wheat (Triticum aestivum L.) seedling resistance to ammonium stress. Plant Physiology and Biochemistry 108, 447–455.
| Adaptation to rhizosphere acidification is a necessary prerequisite for wheat (Triticum aestivum L.) seedling resistance to ammonium stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVakt7vM&md5=b243257d9929df0281d7f1e7a890a12eCAS |
Xing G, Zhu Z (2000) An assessment of N loss from agricultural fields to the environment in China. Nutrient Cycling in Agroecosystems 57, 67–73.
| An assessment of N loss from agricultural fields to the environment in China.Crossref | GoogleScholarGoogle Scholar |
Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology 63, 153–182.
| Plant nitrogen assimilation and use efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1ams7w%3D&md5=333e2d79c5805361a00f92a821148ebfCAS |
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.
| Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOksrk%3D&md5=64406e9f9f2b07f45fffe746bba5eda4CAS |
Zhao D, Reddy KR, Kakani VG, Reddy VR (2005) Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorghum. European Journal of Agronomy 22, 391–403.
| Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorghum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1Wjsrs%3D&md5=f03ee0e01a07882e18e6f28e9304909cCAS |
