Nitrogen Deficiency Accelerates Rice Leaf Senescence Through ABA Signaling and Sugar Metabolic Shifts

. 2025 Jan-Feb ; 177 (1) : e70124.

Jazyk angličtina Země Dánsko Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39968837

Grantová podpora
CZ.10.03.01/00/22_003/0000003 European Union under the LERCO
32272201 National Natural Science Foundation of China
W2433049 National Natural Science Foundation of China
2022YFD2300700 National Key Research and Development Program of China

Nitrogen (N) deficiency is one of the critical factors that induce leaf senescence by integrating with abscisic acid (ABA) metabolism, which results in a shortened leaf photosynthetic period and markedly lowered grain yield. However, the metabolic pathway by which ABA signaling participates in the regulation of senescence-associated change in sugar metabolism and its relationship with N allocation in plant tissues are not well understood. In this paper, the effect of supply level on leaf C/N allocation and its relation to ABA signalling, sugar metabolism, and N assimilation were investigated by using two rice genotypes subjected to four N treatments. Results indicated that N-deficiency markedly induced PYR1-like (PYL) expression and ABA biosynthesis, consequently leading to the activation of ABA signaling. The increased ABA concentration in leaf tissues triggered the catabolic pathways of sugar and N metabolisms, resulting in the reduced photosynthetic pigments and intensified oxidative damage in N-deficient leaves. ABA signaling induced by N-deficiency upregulates the expression of senescence-associated genes (SAGs) and C/N allocation by mediating several senescence-promoting factors, such as NAC, bZIP, and WRKY TFs, along with the suppression of PP2Cs. Therefore, N-deficiency impairs chlorophyll biosynthesis and triggers chlorophyll degradation to accelerate the timing and rate of leaf senescence. This metabolic network could provide helpful information for understanding the regulatory mechanism of leaf senescence in relation to sugar signaling, N-assimilation and N-use efficiency.

Zobrazit více v PubMed

Agüera, E., Cabello, P., de la Haba, P. 2010. Induction of leaf senescence by low nitrogen nutrition in sunflower (Helianthus annuus) plants. Physiol Plantarum 138:256–267.

Asad, M.A.U., Zakari, S.A., Zhao, Q., Zhou, L., Ye, Y., Cheng, F. 2019. Abiotic sresses intervene with ABA signaling to induce destructive metabolic pathways leading to death: premature leaf senescence in plants. International Journal of Molecular Sciences 20, 256.

Asad, M.A.U., Guan, X., Zhou, L., Qian, Z., Yan, Z., Cheng, F. 2023. Involvement of plant signaling network and cell metabolic homeostasis in nitrogen deficiency‐induced early leaf senescence. Plant Sci. 336:111855

Asad, M.A.U., Yan, Z., Zhou, L., Guan. X., Cheng, F. 2024. How abiotic stresses trigger sugar signaling to modulate leaf senescence? Plant Physiol Biochem 210:108650.

Cohen, M., Hertweck, K., Itkin, M., Malitsky, S., Dassa, B., Fischer, A.M, Fluhr, R. 2022. Enhanced proteostasis, lipid remodeling, and nitrogen remobilization define barley flag leaf senescence, Journal of Experimental Botany 73, 6816–6837.

Dai, Y., Xue, L., Liu, Y., Li, Z., Huang, S., Zeng, M., Guo, W. 2024. Comparative physiological and proteomic analysis reveals different responding mechanisms of phosphate deficiency between two clones of Pinus elliottii × P. caribaea, Industrial Crops and Products 218, 118994.

Fang, C., Zhang, H., Wan, J., Wu, Y., Li, K., Jin, C., Chen, W., Wang, S., Wang, W., Zhang, H., Zhang, P., Zhang, F., Qu, L., Liu, X., Zhou, D.X., Luo, J. 2016. Control of leaf senescence by an MeOH‐Jasmonates cascade that is epigenetically regulated by OsSRT1 in rice. Mol. Plant, 9, pp. 1366–1378.

Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.Y., Cutler, S.R., Sheen, J., Rodriguez, P.L., Zhu, J.K. 2009. In vitro reconstitution of an abscisic acid signalling pathway. Nature 462, 660–664.

Fujita, Y., Nakashima, K., Yoshida, T., Katagiri, T., Kidokoro, S., Kanamori, N., Umezawa, T., Fujita, M., Maruyama, K., Ishiyama, K. 2009. Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50, 2123–2132.

Gonzalez‐Guzman M, Pizzio G.A., Antoni, R., Vera‐Sirera, F., Merilo, E., Bassel, G.W., Fernández, M.A., Holdsworth, M.J., Perez‐Amador, M.A., Kollist, H., Rodriguez, P.L. 2012. Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell 24, 2483–2496

Granot, D., Kelly, G., Stein, O., David‐Schwartz, R. 2014. Substantial roles of hexokinase and fructokinase in the effects of sugars on plant physiology and development. J. Exp. Bot. 65, 809–819.

Hawkesford, M., Horst, W., Kichey, T., Lambers, H., Schjoerring, J., Møller, I.S., White, P. 2012. Chapter 6‐Functions of macronutrients. in marschner's mineral nutrition of higher plants, 3rd ed.; Marschner, P., Ed.; Academic Press: San Diego, CA, USA.

He, Y., Hao, Q., Li, W., Yan, C., Yan, N., Yin, P. 2014. Identification and characterization of ABA receptors in Oryza sativa. PLoS ONE 9, e95246.

Hermans, C., Hammond, J.P., White, P.J., Verbruggen, N. 2006. How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci. 11, 610–617.

Huang, A., Sang, Y., Sun, W., Fu, Y., Yang, Z. 2016. Transcriptomic analysis of responses to imbalanced carbon: nitrogen availabilities in rice seedlings. PLOS ONE 11, e0165732.

Kaminskyy, V., Zhivotovsky, B. 2012. Proteases in autophagy. Biochim Biophys Acta. 1824, 44–50.

Kim, D.G., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., Salzberg, S.L. 2012. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36.

Knetsch, M., Wang, M., Snaar‐Jagalska, B.E., Heimovaara‐Dijkstra, S. 1996. Abscisic acid induces mitogen‐activated protein kinase activation in barley aleurone protoplasts. Plant Cell, 8:1061–1067.

Kojima, M., Kamada‐Nobusada, T., Komatsu, H., Takei, K., Kuroha, T., Mizutani, M., Ashikari, M., Ueguchi‐Tanaka, M., Matsuoka, M., Suzuki, K. 2009. Highly sensitive and high‐throughput analysis of plant hormones using MS‐probe modification and liquid chromatography–tandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant and Cell Physiology 50, 1201–1214.

Kräutler, B. 2016. Breakdown of chlorophyll in higher plants‐phyllobilins as abundant, yet hardly visible signs of ripening, senescence, and cell death. Angew. Chem. Int. Ed., 55, 4882–4907.

Lee, S.C., Lan, W., Buchanan, B.B., Luan, S. 2009. A protein kinase‐phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci USA 106:21419–21424

Lea, U S., Leydecker, M., Quilleré, I., Meyer, C. Lillo, C. 2006. Posttranslational regulation of nitrate reductase strongly affects the levels of free amino acids and nitrate, whereas transcriptional regulation has only minor influence. Plant Physiology 140, 1085–1094.

Li, B., Qu, S., Kang, J., Peng, Y., Yang, N., Ma, B., Ruan, Y.‐L., Ma, F., Li, M. and Zhu, L. 2024. The MdCBF1/2‐MdTST1/2 module regulates sugar accumulation in response to low temperature in apple. Plant J. 118, 787–801.

Li, J., Chen, G., Zhang, J., Shen, H., Kang, J., Feng, P., Xie, Q., Hu. Z. 2020. Suppression of a hexokinase gene, SlHXK1, leads to accelerated leaf senescence and stunted plant growth in tomato. Plant Sci. 298.

Li, W., Liu, Y., Liu, M, Zheng, Q., Li, B., Li, Z., Li, H. 2019. Sugar accumulation is associated with leaf senescence induced by long‐term high light in wheat. Plant Sci. 287.

Liang, C., Chen, L., Wang, Y., Liu, J., Xu, G., Li, T. 2011. High temperature at grain‐filling stage affects nitrogen metabolism enzyme activities in grains and grain nutritional quality in rice. Rice Sci. 18, 210–216.

Lichtenthaler, H.K. 1987. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology, Vol. 148: Academic Press, 350‐382.

Ling, L., Li, X., Wang, K., Cai, M., Jiang, Y., Cao, C. 2019. Carbon and nitrogen partitioning of transgenic rice T2A‐1 (Cry2A*) with different nitrogen treatments. Sci Rep. 9, 5351.

Liu, C., Cheng, J., Zhuang, Y., Ye, L., Li, Z., Wang, Y., Qi, M., Zhang, Y. 2019. Polycomb repressive complex 2 attenuates ABA‐induced senescence in Arabidopsis. Plant J. 97, 368–377.

Ma, Y., Szostkiewicz I., Korte, A., Moes, D., Yang, Y., Christmann, A., Grill, E. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science. 324:1064–8.

Moore, B., Moore, B., Zhou, L., Rolland, F., Hall, Q. 2013. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 332.

Mu, X., Chen, Q., Chen, F., Yuan, L., Mi, G. 2018. Dynamic remobilization of leaf nitrogen components in relation to photosynthetic rate during grain filling in maize. Plant Physiol Bioch. 129, 27–34.

Nakamura, Y., Yuki, K., Park, S.Y., Ohya, T. 1989. Carbohydrate metabolism in the developing endosperm of rice grains. Plant and Cell Physiology 30, 833–839.

Nam, M.H., Huh, S.M., Kim, K.M., Park, W.J., Seo, J.B., Cho, K., et al. 2012. Comparative proteomic analysis of early salt stress‐responsive proteins in roots of SnRK2 transgenic rice. Proteome Sci. 10:25

Ning, P., Yang, L., Li, C., Fritschi, F.B. 2018. Post‐silking carbon partitioning under nitrogen deficiency revealed sink limitation of grain yield in maize. J Exp Bot. 69, 1707–1719.

Nuruzzaman, M., Sharoni, A.M., Kikuchi, S. 2013. Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol. 4, 248.

Pal, M., Rao, L.S., Jain, V., Srivastava, A.C., Pandey, R., Raj, A., Singh, K.P. 2005. Effects of elevated CO2 and nitrogen on wheat growth and photosynthesis. Biol Plantarum 49, 467–470.

Park, S.Y., Fung, P., Nishimura, N., Jensen, D.R., Fujii, H., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Chow, T.F., Alfred, S.E., Bonetta, D., Finkelstein, R., Provart, N.J., Desveaux, D., Rodriguez, P.L., McCourt, P., Zhu, J.K., Schroeder, J.I., Volkman, B.F., Cutler, S.R. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068–1071.

Plant, B.D., Musialak‐Lange, M., Nuc, P., May, P., Buhtz, A., Kehr, J., Walther, D., Scheible, W.R. 2009. Identification of nutrient‐responsive Arabidopsis and rapeseed microRNAs by comprehensive real‐time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol. 150, 1541–1555.

Rao, X., Huang, X., Zhou, Z., Lin, X. 2013. An improvement of the 2^(−delta delta CT) method for quantitative real‐time polymerase chain reaction data analysis. Biostat Bioinform Biomath 3:71–85.

Rao, M.V., Lee, H., Creelman, R.A., Mullet, J.E., Davis, K.R. 2000. Jasmonic acid signaling modulates ozone‐induced hypersensitive cell death. The Plant Cell 12, 1633–1646.

Scheible, W.R. Morcuende, R., Czechowski, T., Fritz, C., Osuna, D., Palacios‐Rojas, N., Schindelasch, D., Thimm, O., Udvardi, M.K., Stitt, M. 2004. Genome‐wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 136, 2483–2499.

Sekhon, R.S., Childs, K.L., Santoro, N., Foster, C.E., Buell, C.R., de Leon, N., Kaeppler, S.M. 2012. Transcriptional and metabolic analysis of senescence induced by preventing pollination in maize. Plant Physiol. 159, 1730–1744.

Sultana, N., Islam, S., Juhasz, A. Ma, W., 2021. Wheat leaf senescence and its regulatory gene network. Crop J., 9, 703–717.

Sun, X., Chen, F., Yuan, L., Mi, G. 2020. The physiological mechanism underlying root elongation in response to nitrogen deficiency in crop plants. Planta 251, 84.

Wang, F., Liu, J., Zhou, L., Pan, G., Li, Z., Zaidi, S.H.R, Cheng, F. 2017. Senescence‐specific change in ROS scavenging enzyme activities and regulation of various SOD isozymes to ROS levels in psf mutant rice leaves. Plant Physiology and Biochemistry 109, 248–261.

Wang, F., Liu, J., Chen, M., Zhou, L., Li, Z., Zhao, Q., Pan, G., Zaidi, S.H., Cheng, F. 2016. Involvement of Abscisic Acid in PSII Photodamage and D1 Protein Turnover for Light‐Induced Premature Senescence of Rice Flag Leaves. PLoS One. 11:e0161203.

Wen, B.B., Li, C., Fu, X.L., Li, D.M., Gao, D.S. 2019. Effects of nitrate deficiency on nitrate assimilation and chlorophyll synthesis of detached apple leaves. Plant Physiol Biochem. 142, 363–371.

Wen, B.B., Xiao, W., Mu, Q., Li, D., Chen, X., Wu, H., Li, L., Peng, F. 2020. How does nitrate regulate plant senescence? Plant Physiology and Biochemistry, 157, 60–69.

Wingler, A. 2018. Transitioning to the next phase: the role of sugar signaling throughout the plant life cycle. Plant Physiol., 176, 1075–1084.

Yang, H.C., Kan, C.C., Hung, T.H., Hsieh, P.H., Wang, S.Y., Hsieh, W.Y., Hsieh, M.H. 2017. Identification of early ammonium nitrate‐responsive genes in rice roots. Sci Rep. 7, 16885.

Yang, J., Zhang, J., Wang, Z., Zhu, Q., Liu, L. 2004a. Activities of fructan‐ and sucrose‐metabolizing enzymes in wheat stems subjected to water stress during grain filling. Planta, 220, 331–343.

Yang, J., Zhang, J., Wang, Z., Xu, G., Zhu, Q. 2004b. Activities of key enzymes in sucrose‐to‐starch conversion in wheat grains subjected to water deficit during grain filling. Plant Physiology, 135, 1621–1629.

Yin, H.Y. Yang, F., He, X.Y. Du, X.Y. Mu, P. Ma, W.J. 2022. Advances in the functional study of glutamine synthetase in plant abiotic stress tolerance response. Crop J, 10, 917–923.

Zakari, S.A., Zaidi, S.H.R., Sunusi, M., Dauda, K.D. 2021 Nitrogen deficiency regulates premature senescence by modulating flag leaf function, ROS homeostasis, and intercellular sugar concentration in rice during grain filling. J Genet Eng Biotechnol. 19, 177.

Zakari, A., Asad, M.A.U., Han, Z., Zhao, Q., Cheng, F., 2020. Relationship of nitrogen deficiency‐induced leaf senescence with ROS generation and ABA concentration in rice flag leaves. J. Plant Growth Regul. 1503–1517.

Zhao, Y., Zhang, Z., Gao, J., Wang, P., Hu, T., Wang, Z., Hou, Y.J., Wan, Y., Liu, W., Xie, S., Lu, T., Xue, L., Liu, Y., Macho, A.P., Tao, W.A., Bressan, R.A., Zhu, J.K. 2018 Arabidopsis Duodecuple Mutant of PYL ABA Receptors Reveals PYL Repression of ABA‐Independent SnRK2 Activity. Cell Rep. 23:3340–3351.

Zhao, D., Reddy, K.R., Kakani, V.G., Reddy, V.R. 2005. Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorghum. Eur J Agron. 22:391–403.

Zhao, Y., Chan, Z., Gao, J., Xing, L., Cao, M., Yu, C., Hu, Y., You, J., Shi, H., Zhu, Y., et al. 2016. ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc Natl Acad Sci. USA. 113, 1949–1954.

Zhang, K., Gan, S.S. 2012. An abscisic acid‐AtNAP transcription factor‐SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol. 158, 158–961.

Zhang, L.H., Zhu, L.C, Yu, X.U, Long, L.V, Li, X.G, Li, W.H, Liu, W.D., Li, M.J, Han, D.G. 2023. Genome‐wide identification and function analysis of the sucrose phosphate synthase MdSPS gene family in apple. J. Integr. Agric. 22, 2080–2093.

Zhou D., Li, T., Yang, Y., Qu, Z., Ouyang, L., Jiang, Z., Lin, X., Zhu, C., Peng, L., Fu, J., Peng, X., Bian, J., Tang, W., Xu, J., He, H., 2020. OsPLS4 is involved in cuticular wax biosynthesis and affects leaf senescence in rice. Frontiers in Plant Science 11.

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...