Plant and Soil

, Volume 431, Issue 1–2, pp 107–117 | Cite as

Accumulation of ammonium and reactive oxygen mediated drought-induced rice growth inhibition by disturbed nitrogen metabolism and photosynthesis

  • Haifei Chen
  • Quan Zhang
  • Zhifeng Lu
  • Fangsen XuEmail author
Regular Article


Background and aims

Nitrogen (N) deficiency and drought are two key limiting factors for rice production worldwide, but the relationship of drought stress with N homeostasis in rice is rarely advanced. The aim of this study was to dissect the physiological effects of drought stress on rice growth that coupled unbalanced N metabolism.


Water-deficient stress (WD) limited stomatal aperture function and activity of Rubisco carboxylase to photosynthesis. The rate of total electron transport (Jt) and the electron to carboxylation (Jc) were considerably decreased, whereas the proportion of e flow to photorespiration was stimulated by WD, especially at 1600 μmol m−2 s−1 PPFD. Concurrently, the expressions of glycolate oxidase genes (GOX1, GOX5) and glycine decarboxylase complex (GDCH, GDCP and GDCT) were significantly induced in leaves of WD treatment, which led to the accumulation of reactive oxygen species in leaves. With the photosynthetic change, nitrate uptake and reduction were suppressed. Moreover, the enhanced photorespiration generated excess NH3 accumulation in leaves and stimulated the expressions of GS1;1, GS1;2 and GS2, which were tightly coupled with the expressions of PEPC1 and PEPC2 under WD stress.


Our results suggest that the inhibited nitrate reduction associated with diminished electron transport rate, and the photorespiration-associated accumulation of hydrogen peroxide and NH3 were critical in the drought-induced rice growth inhibition.


Water-deficient stress Photosynthesis Nitrogen metabolism Photorespiration Ammonium accumulation Rice 



This work was supported by the National Key Research and Development Program of China (Grant No. 2016YFD0200108).

Supplementary material

11104_2018_3752_MOESM1_ESM.doc (14 kb)
ESM 1 (DOC 14.5 kb)
11104_2018_3752_MOESM2_ESM.doc (33 kb)
ESM 2 (DOC 33 kb)
11104_2018_3752_MOESM3_ESM.doc (774 kb)
ESM 3 (DOC 773 kb)
11104_2018_3752_MOESM4_ESM.doc (42 kb)
ESM 4 (DOC 42.5 kb)
11104_2018_3752_MOESM5_ESM.doc (827 kb)
ESM 5 (DOC 827 kb)
11104_2018_3752_MOESM6_ESM.doc (502 kb)
ESM 6 (DOC 502 kb)


  1. Bloom AJ, Burger M, Asensio JSR, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899–903CrossRefPubMedGoogle Scholar
  2. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot-London 103:551–560CrossRefGoogle Scholar
  3. Coschigano KT, Melo-Oliveira R, Lim J, Coruzzi GM (1998) Arabidopsis gls mutants and distinct Fd-GOGAT genes: implications for photorespiration and primary nitrogen assimilation. Plant Cell 10:741–752PubMedPubMedCentralGoogle Scholar
  4. Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7:859CrossRefPubMedPubMedCentralGoogle Scholar
  5. Crawford NM, Glass ADM (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci 3(10):389–395Google Scholar
  6. Dai GZ, Qiu BS, Karl F (2014) Ammonium tolerance in the cyanobacterium Synechocystis sp. strain PCC 6803 and the role of the psbA multigene family. Plant Cell Environ 37:840–851CrossRefPubMedGoogle Scholar
  7. Fork DC, Herbert SK (1993) Electron-transport and photophosphorylation by photosystem-I in vivo in plants and cyanobacteria. Photosynth Res 36:149–168CrossRefPubMedGoogle Scholar
  8. Foyer CH, Furbank R, Harbinson J, Horton P (1990) The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynth Res 25:83–100CrossRefPubMedGoogle Scholar
  9. Funayama K, Kojima S, Tabuchi-Kobayashi M, Sawa Y, Nakayama Y, Hayakawa T, Yamaya T (2013) Cytosolic glutamine synthetase1;2 is responsible for the primary assimilation of ammonium in rice roots. Plant Cell Physiol 54:934–943CrossRefPubMedGoogle Scholar
  10. Gonzalez-Dugo V, Durand JL, Gastal F (2010) Water deficit and nitrogen nutrition of crops. A review. Agron Sustain Dev 30:529–544CrossRefGoogle Scholar
  11. Guan M, de Bang TC, Pedersen C, Schjoerring JK (2016) Cytosolic glutamine synthetase Gln1; 2 is the main isozyme contributing to GS1 activity and can be up-regulated to relieve ammonium toxicity. Plant Physiol 171:1921–1933CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gutiérrez RA, Lejay LV, Dean A, Chiaromonte F, Shasha DE, Coruzzi GM (2007) Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol 8:R7CrossRefPubMedPubMedCentralGoogle Scholar
  13. Hachiya T, Watanabe CK, Boom C, Tholen D, Takahara K, Noguchi K (2010) Ammonium dependent respiratory increase is dependent on the cytochrome pathway in Arabidopsis thaliana shoots. Plant Cell Environ 33:1888–1897CrossRefPubMedGoogle Scholar
  14. Heidari B, Matre P, Nemie-Feyissa D, Meyer C, Rognli OA, Møller SG, Lillo C (2011) Protein phosphatase 2A B55 and a regulatory subunits interact with nitrate reductase and are essential for nitrate reductase activation. Plant Physiol 156:165–172CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hoai NTT, Shim IS, Kobayashi K, Kenji U (2003) Accumulation of some nitrogen compounds in response to salt stress and their relationships with salt tolerance in rice (Oryza sativa L.) seedlings. J Plant Growth Regul 41:159–164CrossRefGoogle Scholar
  16. Hodges M, Jossier M, Boex-Fontvieille E, Tcherkez G (2013) Protein phosphorylation and photorespiration. Plant Biol 15(4):694–706CrossRefPubMedGoogle Scholar
  17. Kaiser WM, Huber SC (1994) Posttranslational regulation of nitrate reductase in higher plants. Plant Physiol 106:817CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kim TH, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591CrossRefPubMedPubMedCentralGoogle Scholar
  19. Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384:557–560CrossRefGoogle Scholar
  20. Kumar PA, Parry MA, Mitchell RA (2002) Photosynthesis and nitrogen-use efficiency. Advances in Photosynthesis & Respiration 12:23–34Google Scholar
  21. Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 53(370):773–787CrossRefPubMedGoogle Scholar
  22. Masumoto C, Miyazawa SI, Ohkawa H, Fukuda T, Taniguchi Y, Murayama S, Miyao M (2010) Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation. PNAS 107(11):5226–5231CrossRefPubMedGoogle Scholar
  23. Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566CrossRefPubMedPubMedCentralGoogle Scholar
  24. Nagy Z, Németh E, Guóth A, Bona L, Wodala B, Pécsváradi A (2013) Metabolic indicators of drought stress tolerance in wheat: glutamine synthetase isoenzymes and rubisco. Plant Physiol Biochem 67:48–54CrossRefPubMedGoogle Scholar
  25. Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot-London 89:841–850CrossRefGoogle Scholar
  26. Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3(6):973–996CrossRefPubMedGoogle Scholar
  27. Parry MAJ, Andralojc PJ, Khan S, Lea PJ, Keys AJ (2002) Rubisco activity: effects of drought stress. Ann Bot-London 89:833–839CrossRefGoogle Scholar
  28. Parry MA, Andralojc PJ, Scales JC, Salvucci ME, Carmo-Silva AE, Alonso H, Whitney SM (2012) Rubisco activity and regulation as targets for crop improvement. J Exp Bot 64:717–730CrossRefPubMedGoogle Scholar
  29. Rademacher T, Häusler RE, Hirsch HJ, Zhang L, Lipka V, Weier D, Kreuzaler F, Peterhänsel C (2002) An engineered phosphoenolpyruvate carboxylase redirects carbon and nitrogen flow in transgenic potato plants. Plant J 32:25–39CrossRefPubMedGoogle Scholar
  30. Singh KK, Ghosh S (2013) Regulation of glutamine synthetase isoforms in two differentially drought-tolerant rice (Oryza sativa L.) cultivars under water deficit conditions. Plant Cell Rep 32:183–193CrossRefPubMedGoogle Scholar
  31. Singh NB, Singh D, Singh A (2015) Biological seed priming mitigates the effects of water stress in sunflower seedlings. Physiol Mol Biol Plants 21(2):207–214CrossRefPubMedPubMedCentralGoogle Scholar
  32. Singh M, Singh VP, Prasad SM (2016) Responses of photosynthesis, nitrogen and proline metabolism to salinity stress in Solanum lycopersicum under different levels of nitrogen supplementation. Plant Physiol Biochem 109:72–83CrossRefPubMedGoogle Scholar
  33. Sperling O, Lazarovitch N, Schwartz A, Shapira O (2014) Effects of high salinity irrigation on growth, gas-exchange, and photoprotection in date palms (Phoenix dactylifera L., cv. Medjool). Environ Exp Bot 99:100–109CrossRefGoogle Scholar
  34. Tozzi ES, Easlon HM, Richards JH (2013) Interactive effects of water, light and heat stress on photosynthesis in Fremont cottonwood. Plant Cell Environ 36:1423–1434CrossRefPubMedGoogle Scholar
  35. Uri H, Asfaw D, David T, Gendler T, Nikoloski Z, Rachmilevitch S, Fait A (2013) Metabolite profiling and network analysis reveal coordinated changes in grapevine water stress response. BMC Plant Biol 13:184CrossRefGoogle Scholar
  36. Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philosophical transactions of the Royal Society of London. Series B: Biological Sciences 355:1517–1529Google Scholar
  37. Xu ZZ, Zhou GS (2006) Combined effects of water stress and high temperature on photosynthesis, nitrogen metabolism and lipid peroxidation of a perennial grass Leymus chinensis. Planta 224:1080–1090CrossRefPubMedGoogle Scholar
  38. Yi XP, Zhang YL, Yao HS, Zhang XJ, Luo HH, Gou L, Zhang WF (2014) Alternative electron sinks are crucial for conferring photoprotection in field-grown cotton under water deficit during flowering and boll setting stages. Funct Plant Biol 41:737–747CrossRefGoogle Scholar
  39. Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.National Key Laboratory of Crop Genetic Improvement, and Microelement Research CenterHuazhong Agricultural UniversityWuhanChina
  2. 2.College of Resources and EnvironmentHunan Agricultural UniversityChangshaChina

Personalised recommendations