Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Regulation of expression of genes associated with nitrate response by osmotic stress and combined osmotic and nitrogen deficiency stress in bread wheat (Triticum aestivum L.)

  • 25 Accesses

Abstract

In drought prone areas, often farmers use less nitrogen, and thus the crop is subjected to combined stress (low N + osmotic stress). Since understanding the regulation of genes involved in nitrate signalling, uptake and assimilation under water-deficit (osmotic stress) is important for improving yield under the combined stress environments, this study analysed the regulation of genes coding for N responses under low N, osmotic stress (OS) and combined stress conditions in seedlings of a wheat. The results revealed that HD2967, a mega wheat variety, was more tolerant to short-term N starvation, OS and combined stress as compared with C306, a drought tolerant check. Interestingly, it was found that low N stress can also lead to accumulation of ABA in wheat seedlings. Real-time RT-qPCR analysis revealed that in addition to low N stress, OS also regulated expression of nitrate signalling genes (TaCIPK8, TaCIPK23, TaNLP4, TaSPL9, TabHLH1 and TaNAC4), HATS gene TaNRT2.1, LATS genes (TaNRT6.5 and TaNPF7.1), nitrate and nitrite assimilation genes and ammonium assimilation genes at least in one tissue of one of the genotypes. Combined stress was found to have significant interaction in regulation genes for nitrate signalling, uptake and assimilation. TabZIP1 and TaPIMP1 TF were identified as new players in low N response in wheat. Thus, osmotic stress and combined stress modulates the genes for N responses, and genotypic variation exists for this in wheat. The common expression pattern of N response genes found under low N and OS may probably regulated, at least in part, by ABA-dependent pathway, as ABA accumulation was induced by both OS and low N stresses. Functional analysis of the osmotic stress regulated genes coding for N response will help enhance tolerance of wheat to combined stress conditions.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

References

  1. Adavi, S. B., & Sathee, L. (2019). Elevated CO2-induced production of nitric oxide differentially modulates nitrate assimilation and root growth of wheat seedlings in a nitrate dose-dependent manner. Protoplasma,256, 147–159.

  2. Balotf, S., Kavoosi, G., & Kholdebarin, B. (2016). Nitrate reductase, nitrite reductase, glutamine synthetase, and glutamate synthase expression and activity in response to different nitrogen sources in nitrogen-starved wheat seedlings. Biotechnology and Applied Biochemistry,63, 220–229.

  3. Bista, D., Heckathorn, S., Jayawardena, D., Mishra, S., & Boldt, J. (2018). Effects of drought on nutrient uptake and the levels of nutrient-uptake proteins in roots of drought-sensitive and-tolerant grasses. Plants,7, 28.

  4. Borgognone, D., Rouphael, Y., Cardarelli, M., Lucini, L., & Colla, G. (2016). Changes in biomass, mineral composition, and quality of cardoon in response to NO3:Cl ratio and nitrate deprivation from the nutrient solution. Frontiers in Plant Science,7, 978.

  5. Britto, D. T., Siddiqi, M. Y., Glass, A. D., & Kronzucker, H. J. (2001). Futile transmembrane NH4+ cycling: A cellular hypothesis to explain ammonium toxicity in plants. Proceedings of the National Academy of Sciences,98, 4255–4258.

  6. Buchner, P., & Hawkesford, M. J. (2014). Complex phylogeny and gene expression patterns of members of the NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family (NPF) in wheat. Journal of Experimental Botany,65, 5697–5710.

  7. Castaings, L., Camargo, A., Pocholle, D., Gaudon, V., Texier, Y., Boutet-Mercey, S., et al. (2009). The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. The Plant Journal,57, 426–435.

  8. Chapin, F. S., III. (1991). Effects of multiple environmental stresses on nutrient availability and use. In H. A. Mooney, W. E. Winner, & E. J. Pell (Eds.), Response of plants to multiple stresses (pp. 67–88). San Diego: Academic Press.

  9. Chaves, M. M., Pereira, J. S., Maroco, J., Rodrigues, M. L., Ricardo, C. P. P., Osório, M. L., et al. (2002). How plants cope with water stress in the field? Photosynthesis and growth. Annals of Botany,89, 907–916.

  10. Chen, H., Lan, H., Huang, P., Zhang, Y., Yuan, X., Huang, X., et al. (2015). Characterization of OsPM19L1 encoding an AWPM-19-like family protein that is dramatically induced by osmotic stress in rice. Genetic and Molecular Research,14, 11994–12005.

  11. Cui, L. G., Shan, J. X., Shi, M., Gao, J. P., & Lin, H. X. (2014). The miR156-SPL 9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. The Plant Journal,80, 1108–1117.

  12. Dalal, M., Sahu, S., Tiwari, S., Rao, A. R., & Gaikwad, K. (2018). Transcriptome analysis reveals interplay between hormones, ROS metabolism and cell wall biosynthesis for drought-induced root growth in wheat. Plant Physiology and Biochemistry,130, 482–492.

  13. Ding, L., Li, Y., Wang, Y., Gao, L., Wang, M., Chaumont, F., et al. (2016). Root ABA accumulation enhances rice seedling drought tolerance under ammonium supply: Interaction with aquaporins. Frontiers in Plant Science,7, 1206.

  14. El-Rawy, M. A., & Hassan, M. I. (2014). A diallel analysis of drought tolerance indices at seedling stage in bread wheat (Triticum aestivum L.). Plant Breeding and Biotechnology,2(3), 276–288.

  15. Fan, X. L., & Li, Y. K. (2001). Effect of drought stress and drought tolerance heredity on nitrogen efficiency of winter wheat. In W. J. Horst, et al. (Eds.), Plant nutrition (pp. 62–63). Dordrecht: Springer.

  16. Finkelstein, R. (2013). Abscisic acid synthesis and response. The Arabidopsis Book, American Society of Plant Biologists,11, e0166. https://doi.org/10.1199/tab.0166.

  17. Fresneau, C., Ghashghaie, J., & Cornic, G. (2007). Drought effect on nitrate reductase and sucrose-phosphate synthase activities in wheat (Triticum durum L.): Role of leaf internal CO2. Journal of Experimental Botany,58, 2983–2992.

  18. Gallé, A., & Feller, U. (2007). Changes of photosynthetic traits in beech saplings (Fagus sylvatica) under severe drought stress and during recovery. Physiologia Plantarum,131(3), 412–421.

  19. Gamuyao, R., Chin, J. H., Pariasca-Tanaka, J., Pesaresi, P., Catausan, S., Dalid, C., et al. (2012). The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature,488(7412), 535.

  20. Gao, J., Luo, Q., Sun, C., Hu, H., Wang, F., Tian, Z., et al. (2019). Low nitrogen priming enhances photosynthesis adaptation to water-deficit stress in winter wheat (Triticum aestivum L.) seedlings. Frontiers in Plant Science,10, 818.

  21. Guo, J., Jia, Y., Chen, H., Zhang, L., Yang, J., Zhang, J., et al. (2019). Growth, photosynthesis, and nutrient uptake in wheat are affected by differences in nitrogen levels and forms and potassium supply. Scientific Reports, 9, 1248. https://doi.org/10.1038/s41598-018-37838-3.

  22. Guo, S., Zhou, Y., Shen, Q., & Zhang, F. (2007). Effect of ammonium and nitrate nutrition on some physiological processes in higher plants-growth, photosynthesis, photorespiration, and water relations. Plant Biology,9(01), 21–29.

  23. Harris, J. M., & Ondzighi-Assoume, C. A. (2017). Environmental nitrate signals through abscisic acid in the root tip. Plant Signaling & Behavior,12(1), e1273303.

  24. Ho, C. H., Lin, S. H., Hu, H. C., & Tsay, Y. F. (2009). CHL1 functions as a nitrate sensor in plants. Cell,138(6), 1184–1194.

  25. Hsieh, W. P., Hsieh, H. L., & Wu, S. H. (2012). Arabidopsis bZIP16 transcription factor integrates light and hormone signaling pathways to regulate early seedling development. The Plant Cell,24(10), 3997–4011.

  26. Hu, Y., & Schmidhalter, U. (2005). Drought and salinity: A comparison of their effects on mineral nutrition of plants. Journal of Plant Nutrition and Soil Science,168(4), 541–549.

  27. 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(2), 264–278.

  28. Huggins, D. R., & Pan, W. L. (2003). Key indicators for assessing nitrogen use efficiency in cereal-based agroecosystems. Journal of Crop Production,8(1–2), 157–185.

  29. Ji, H., Liu, L., Li, K., Xie, Q., Wang, Z., Zhao, X., et al. (2014). PEG-mediated osmotic stress induces premature differentiation of the root apical meristem and outgrowth of lateral roots in wheat. Journal of Experimental Botany,65(17), 4863–4872.

  30. Kang, G., Wu, Y., Li, G., Wang, P., Han, Q., Wang, Y., et al. (2019). Proteomics combined with BSMV-VIGS methods identified some N deficiency-responsive protein species and ABA role in wheat seedling. Plant and Soil,444(1–2), 177–191.

  31. Karrou, M., & Nachit, M. (2015). Durum wheat genotypic variation of yield and nitrogen use efficiency and its components under different water and nitrogen regimes in the Mediterranean region. Journal of Plant Nutrition,38(14), 2259–2278.

  32. Krouk, G., Mirowski, P., LeCun, Y., Shasha, D. E., & Coruzzi, G. M. (2010). Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate. Genome Biology,11(12), R123.

  33. Kruse, J., Hetzger, I., Hänsch, R., Mendel, R. R., Walch-Liu, P., Engels, C., et al. (2002). Elevated pCO2 favours nitrate reduction in the roots of wild-type tobacco (Nicotiana tabacum cv. Gat.) and significantly alters N-metabolism in transformants lacking functional nitrate reductase in the roots. Journal of Experimental Botany,53(379), 2351–2367.

  34. Liu, K. H., & Tsay, Y. F. (2003). Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. The EMBO Journal,22(5), 1005–1013.

  35. Marchive, C., Roudier, F., Castaings, L., Bréhaut, V., Blondet, E., Colot, V., et al. (2013). Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nature Communications,4, 1713.

  36. Murphy, D. V., Sparling, G. P., & Fillery, I. R. P. (1998). Seasonal fluctuations in gross N mineralisation, ammonium consumption, and microbial biomass in Western Australian soil under different land uses. Australian Journal of Agricultural Research,49(3), 523–536.

  37. Nikonorova, N., Van den Broeck, L., Zhu, S., Van De Cotte, B., Dubois, M., Gevaert, K., et al. (2018). Early mannitol-triggered changes in the Arabidopsis leaf (phospho) proteome reveal growth regulators. Journal of Experimental Botany,69(19), 4591–4607.

  38. Pál, M., Tajti, J., Szalai, G., Peeva, V., Végh, B., & Janda, T. (2018). Interaction of polyamines, abscisic acid and proline under osmotic stress in the leaves of wheat plants. Scientific Reports,8(1), 12839.

  39. Pandey, R., Dubey, K. K., Ahmad, A., Nilofar, R., Verma, R., Jain, V., et al. (2015). Elevated CO2 improves growth and phosphorus utilization efficiency in cereal species under sub-optimal phosphorus supply. Journal of Plant Nutrition,38(8), 1196–1217.

  40. Richard-Molard, C., Krapp, A., Brun, F., Ney, B., Daniel-Vedele, F., & Chaillou, S. (2008). Plant response to nitrate starvation is determined by N storage capacity matched by nitrate uptake capacity in two Arabidopsis genotypes. Journal of Experimental Botany,59(4), 779–791.

  41. Saab, I. N., Sharp, R. E., Pritchard, J., & Voetberg, G. S. (1990). Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiology,93(4), 1329–1336.

  42. Sadras, V. O., Hayman, P. T., Rodriguez, D., Monjardino, M., Bielich, M., Unkovich, M., et al. (2016). Interactions between water and nitrogen in Australian cropping systems: Physiological, agronomic, economic, breeding and modelling perspectives. Crop and Pasture Science,67, 1019–1053.

  43. Sanaullah, M., Rumpel, C., Charrier, X., & Chabbi, A. (2012). How does drought stress influence the decomposition of plant litter with contrasting quality in a grassland ecosystem? Plant and Soil,352, 277–288.

  44. Sardans, J., & Peñuelas, J. (2012). The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant physiology, 160(4), 1741–1761.

  45. Sassi-Aydi, S., Aydi, S., & Abdelly, C. (2014). Inorganic nitrogen nutrition enhances osmotic stress tolerance in Phaseolus vulgaris: Lessons from a drought-sensitive cultivar. Hort Science,49, 550–555.

  46. Saud, S., Fahad, S., Yajun, C., Ihsan, M. Z., Hammad, H. M., Nasim, W., et al. (2017). Effects of nitrogen supply on water stress and recovery mechanisms in Kentucky bluegrass plants. Frontiers in Plant Science,8, 983.

  47. Seneviratne, S. I., Nicholls, N., Easterling, D., Goodess, C. M., Kanae, S., Kossin, J., et al. (2012). Changes in climate extremes and their impacts on the natural physical environment. In C. B. Field, V. Barros, T. F. Stocker, D. Qin, D. J. Dokken, K. L. Ebi, M. D. Mastrandrea, K. J. Mach, G.-K. Plattner, A. P. Allen, M. Tignor, & P. M. Midgley (Eds.), Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation. A special report of working groups I and II of the Intergovernmental Panel on Climate Change (IPCC) (pp. 109–230). Cambridge: Cambridge University Press.

  48. Sharma, L., Dalal, M., Verma, R. K., Kumar, S. V., Yadav, S. K., Pushkar, S., et al. (2018a). Auxin protects spikelet fertility and grain yield under drought and heat stresses in rice. Environmental and Experimental Botany,150, 9–24.

  49. Sharma, T., Dreyer, I., & Riedelsberger, J. (2013). The role of K+ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana. Frontiers in Plant Science,4, 224.

  50. Sharma, L., Saha, S., Mondal, T., Pushkar, S., Roy, S., & Chinnusamy, V. (2018b). Standardization and validation of a LC-method for quantification of Indole-3-acetic acid in rice genotypes. Pesticide Research Journal,30(1), 16–23.

  51. Sharp, R. E., Wu, Y., Voetberg, G. S., Saab, I. N., & LeNoble, M. E. (1994). Confirmation that abscisic acid accumulation is required for maize primary root elongation at low water potentials. Journal of Experimental Botany,45, 1743–1751.

  52. Steudle, E., & Peterson, C. A. (1998). How does water get through roots? Journal of Experimental Botany,49(322), 775–788.

  53. Straub, T., Ludewig, U., & Neuhäuser, B. (2017). The kinase CIPK23 inhibits ammonium transport in Arabidopsis thaliana. The Plant Cell,29(2), 409–422.

  54. Teplova, I., Veselov, S., & Kudoyarova, G. (1998). Changes in ABA and IAA content in the roots and shoots of wheat seedlings under nitrogen deficiency. In J. E. Box (Ed.), Root demographics and their efficiencies in sustainable agriculture, grasslands and forest ecosystems (pp. 599–605). Dordrecht: Springer.

  55. Trenberth, K. E., Dai, A., Van Der Schrier, G., Jones, P. D., Barichivich, J., Briffa, K. R., et al. (2014). Global warming and changes in drought. Nature Climate Change,4(1), 17–22.

  56. Varela, M. C., Reinoso, H., Luna, V., & Cenzano, A. M. (2018). Seasonal changes in morphophysiological traits of two native Patagonian shrubs from Argentina with different drought resistance strategies. Plant Physiology and Biochemistry,127, 506–515.

  57. Vidal, E. A., Álvarez, J. M., & Gutiérrez, R. A. (2014). Nitrate regulation of AFB3 and NAC4 gene expression in Arabidopsis roots depends on NRT1. 1 nitrate transport function. Plant Signaling & Behavior,9(6), e28501.

  58. Vidal, E. A., Moyano, T. C., Riveras, E., Contreras-López, O., & Gutiérrez, R. A. (2013). Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proceedings of the National Academy of Sciences,110(31), 12840–12845.

  59. Von Mogel, K. H. (2013). Genotype × environment × management: interactions key to beating future droughts. Crops, Soils, Agronomy News,58(2), 4–9.

  60. Walch-Liu, P. I. A., Ivanov, I. I., Filleur, S., Gan, Y., Remans, T., & Forde, B. G. (2006). Nitrogen regulation of root branching. Annals of Botany,97(5), 875–881.

  61. Wang, Q., Liu, C., Dong, Q., Huang, D., Li, C., Li, P., et al. (2018). Genome-wide identification and analysis of apple NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER Family (NPF) genes reveals MdNPF6.5 confers high capacity for nitrogen uptake under low-nitrogen conditions. International Journal of Molecular Sciences,19, 2761.

  62. Wei, Y., Shi, A., Jia, X., Zhang, Z., Ma, X., Gu, M., et al. (2018). Nitrogen supply and leaf age affect the expression of TaGS1 or TaGS2 driven by a constitutive promoter in transgenic tobacco. Genes (Basel), 9(8), pii: E406. https://doi.org/10.3390/genes9080406.

  63. Xu, W., Cui, K., Xu, A., Nie, L., Huang, J., & Peng, S. (2015). Drought stress condition increases root to shoot ratio via alteration of carbohydrate partitioning and enzymatic activity in rice seedlings. Acta Physiologiae Plantarum,37(2), 9.

  64. Yamaya, T., Obara, M., Nakajima, H., Sasaki, S., Hayakawa, T., & Sato, T. (2002). Genetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice. Journal of Experimental Botany,53(370), 917–925.

  65. Yang, T., Hao, L., Yao, S., Zhao, Y., Lu, W., & Xiao, K. (2016). TabHLH1, a bHLH-type transcription factor gene in wheat, improves plant tolerance to Pi and N deprivation via regulation of nutrient transporter gene transcription and ROS homeostasis. Plant Physiology and Biochemistry,104, 99–113.

  66. Yu, L. H., Wu, J., Tang, H., Yuan, Y., Wang, S. M., Wang, Y. P., et al. (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.

  67. Zhang, H., & Forde, B. G. (1998). An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science,279(5349), 407–409.

  68. Zhang, Z., Liu, X., Wang, X., Zhou, M., Zhou, X., Ye, X., et al. (2012). An R2R3 MYB transcription factor in wheat, TaPIMP1, mediates host resistance to Bipolaris sorokiniana and drought stresses through regulation of defense- and stress-related genes. New Phytologist,196, 1155–1170.

  69. Zhang, Z., Xiong, S., Wei, Y., Meng, X., Wang, X., & Ma, X. (2017). The role of glutamine synthetase isozymes in enhancing nitrogen use efficiency of N-efficient winter wheat. Scientific Reports,7(1), 1000.

  70. Zhang, Y., Zhang, G., Xia, N., Wang, X. J., Huang, L. L., & Kang, Z. S. (2009). Cloning and characterization of a bZIP transcription factor gene in wheat and its expression in response to stripe rust pathogen infection and abiotic stresses. Physiology and Molecular Plant Pathology, 73, 88–94.

  71. Zhao, Y. J., Weng, B. Q., Wang, Y. X., & Xu, G. Z. (2009). Plant physio-ecological responses to drought stress and its research progress. Fujian Science and Technology of Rice and Wheat,27, 45–50.

  72. Zhao, L., Zhang, W., Yang, Y., Li, Z., Li, N., Qi, S., et al. (2018). The Arabidopsis NLP7 gene regulates nitrate signaling via NRT11-dependent pathway in the presence of ammonium. Scientific Reports,8(1), 1487.

Download references

Acknowledgements

The work was funded by National Agricultural Science Fund (NASF), ICAR, New Delhi, Grant No. NASF/Phen-6005/2016-17, and ICAR-Indian Agricultural Research Institute, New Delhi, Grant No. CRSCIARISIL20144047279.

Author information

Correspondence to Viswanathan Chinnusamy.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mahmoud, D., Pandey, R., Sathee, L. et al. Regulation of expression of genes associated with nitrate response by osmotic stress and combined osmotic and nitrogen deficiency stress in bread wheat (Triticum aestivum L.). Plant Physiol. Rep. (2020). https://doi.org/10.1007/s40502-020-00503-x

Download citation

Keywords

  • Biotic stress
  • Gene expression
  • Low N
  • Nitrate uptake
  • Nitrate metabolism
  • Signalling
  • Osmotic stress
  • Root traits