Abstract
Background and aims
Nitrogen (N) availability affects water uptake from the roots, which decreases upon N deprivation and increases upon resupply. The aim of this study was to reveal possible mechanisms of regulation of water transport in roots through physiological and morphological adaptations to N availability.
Methods
The effects of continuous N deprivation and following resupply on root morphology, osmotic hydraulic conductivity, and expression of genes for aquaporins (water channels) were examined in rice (Oryza sativa L.) plants. The effect of local N availability was examined by using a split-root system.
Results
N deprivation decreased the expression of root-specific aquaporin genes, whereas N resupply increased their expression. Changes in aquaporin gene expression were correlated with changes in hydraulic conductivity. N deprivation increased dry matter allocation to the roots. In a split-root experiment, the expression of root-specific aquaporin genes was down-regulated in the N-deprived half, whereas it was up-regulated in the N-supplied half.
Conclusion
Our results suggest that expression of genes for root-specific aquaporins underlies the changes in conductivity during continuous N deprivation and resupply. Rice plants seem to adapt to N availability through coordinated adjustment of root proliferation and abundance of aquaporins.
Similar content being viewed by others
Abbreviations
- AMT:
-
Ammonia transporter
- ΔΨs :
-
Difference in osmotic potential between the exuded xylem sap and the hydroponic solution.
- GOGAT:
-
Glutamate synthase
- GS:
-
Glutamine synthetase
- NR:
-
Nitrate reductase
- NRT:
-
Nitrate transporter
- Lp r(os):
-
Osmotic hydraulic conductivity
- PIP:
-
Plasma membrane intrinsic protein
- σ:
-
Reflection coefficient for nutrient salts in the xylem
- TIP:
-
Tonoplast intrinsic protein
- J v :
-
Volumetric xylem sap flow rate per unit root surface area
References
Ahamed A, Murai-Hatano M, Ishikawa-Sakurai J, Hayashi H, Kawamura Y, Uemura M (2012) Cold stress-induced acclimation in rice is mediated by root-specific aquaporins. Plant Cell Physiol 53:1445–1456
Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15:439–447
Araki R, Hasegawa H (2006) Expression of rice (Oryza sativa L.) genes involved in high-affinity nitrate transport during the period of nitrate induction. Breed Sci 56:295–302
Cai H, Lu Y, Xie W, Zhu T, Lian X (2012) Transcriptome response to nitrogen starvation in rice. J Biosci 37:731–747
Carvajal M, Cooke DT, Clarkson DT (1996) Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199:372–381
Chapin FS, Walter CHS, Clarkson DT (1988) Growth response of barley and tomato to nitrogen stress and its control by abscisic acid, water relations and photosynthesis. Planta 173:352–366
Clarkson DT, Carvajal M, Henzler T, Waterhouse RN, Smyth AJ, Cooke DT, Stuedle E (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J Exp Bot 51:61–70
di Pietro M, Vialaret J, Li G-W, Hem S, Prado K, Rossignol M, Maurel C, Santoni V (2013) Coordinated post-translational reponses of aquaporins to abiotic and nutritional stimuli in Arabidopsis roots. Mol Cell Proteomics 12:3886–3897
Fan X, Jia L, Li Y, Smith SJ, Miller AJ, Shen Q (2007) Comparing nitrate storage and remobilization in two rice cultivars that differ in their nitrogen use efficiency. J Exp Bot 58:1729–1740
Feng H, Yan M, Fan X, Li B, Shen Q, Miller AJ, Xu G (2011) Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status. J Exp Bot 62:2319–2332
Gloser V, Zwieniecki MA, Orians CM, Holbrook NM (2007) Dynamic changes in root hydraulic properties in response to nitrate availability. J Exp Bot 58:2409–2415
Gorska A, Ye Q, Holbrook NM, Zwieniecki MA (2008a) Nitrate control of root hydraulic properties in plants: translating local information to whole plant response. Plant Physiol 148:1159–1167
Gorska A, Zwieniecka A, Holbrook NM, Zwieniecki MA (2008b) Nitrate induction of root hydraulic conductivity in maize is not correlated with aquaporin expression. Planta 228:989–998
Goto S, Akagawa T, Kojima S, Hayakawa T, Yamaya T (1998) Organization and structure of NADH-dependent glutamate synthase gene from rice plants. Biochim Biophys Acta 1387:298–308
Ishiyama K, Inoue E, Tabuchi M, Yamaya T, Takahashi H (2004) Biochemical background and compartmentalized functions of cytosolic glutamine synthetase for active ammonium assimilation in rice roots. Plant Cell Physiol 45:1640–1647
Javot H, Lauvergeat V, Santoni V et al (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509–522
Katsuhara M, Koshio K, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K (2003) Over-expression of a barley aquaporin increased the shoot/root ratio and raised salt sensitivity in transgenic rice plants. Plant Cell Physiol 44:1378–1383
Kuwagata T, Ishikawa-Sakurai J, Hayashi H, Nagasuga K, Fukushi K, Ahamed A, Takasugi K, Katsuhara M, Murai-Hatano M (2012) Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants. Plant Cell Physiol 53:1418–1431
Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624
Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36
Miyamoto N, Stuedle E, Hirasawa T, Lafitte R (2001) Hydraulic conductivity of rice roots. J Exp Bot 52:1835–1846
Murai-Hatano M, Kuwagata T, Sakurai J, Nonami H, Ahamed A, Nagasuga K, Matsunami T, Fukushi K, Maeshima M, Okada M (2008) Effect of low root temperature on hydraulic conductivity of rice plants and the possible role of aquaporins. Plant Cell Physiol 49:1294–1305
Radin JW, Ackerson RC (1981) Water relations of cotton plants under nitrogen deficiency. Plant Physiol 67:115–119
Radin JW, Boyer JS (1982) Control of leaf expansion by nitrogen nutrition in sunflower plants. Plant Physiol 69:771–775
Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46:1568–1577
Sakurai J, Ahamed A, Murai M, Maeshima M, Uemura M (2008) Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant Cell Physiol 49:30–39
Sakurai-Ishikawa J, Murai-Hatano M, Hayashi H, Ahamed A, Fukushi K, Matsumoto T, Kitagawa Y (2011) Transpiration from shoots triggers diurnal changes in root aquaporin expression. Plant Cell Environ 34:1150–1163
Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14:869–876
Sonoda Y, Ikeda A, Saiki S, von Wiren N, Yamaya T, Yamaguchi J (2003) Distinct expression and function of three ammonium transporter genes (OsAMT1;1–1;3) in rice. Plant Cell Physiol 44:726–734
Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2:178–186
Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, New York
Wang Y-H, Garvin DF, Kochian LV (2001) Nitrate-induced genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition. Plant Physiol 127:345–359
Wang R, Okamoto M, Xing X, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132:556–567
Yao S-G, Sonoda Y, Tsutsui T, Nakamura H, Ichikawa H, Ikeda, Yamaguchi J (2008) Promoter analysis of OsAMT1;2 and OsAMT1;3 implies their distinct roles in nitrogen utilization in rice. Breed Sci 58:201–207
Acknowledgments
We are grateful to Dr. Kensaku Suzuki (NARO Tohoku Agricultural Research Center) for critically reading the manuscript and his helpful discussion. We also thank Prof. Matsuo Uemura (Iwate University) and Dr. Yukio Kawamura (Iwate University) for providing an opportunity to use their osmometer. This work was supported by JSPS KAKENHI Grant Number 21780235.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Ad C. Borstlap.
Rights and permissions
About this article
Cite this article
Ishikawa-Sakurai, J., Hayashi, H. & Murai-Hatano, M. Nitrogen availability affects hydraulic conductivity of rice roots, possibly through changes in aquaporin gene expression. Plant Soil 379, 289–300 (2014). https://doi.org/10.1007/s11104-014-2070-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-014-2070-4