Treffer: The miR396b-MsGRF1c module positively associates with alfalfa nodule senescence.
Title:
The miR396b-MsGRF1c module positively associates with alfalfa nodule senescence.
Authors:
Yan J; College of Grassland Science and Technology, China Agricultural University, Beijing, 100193, China.; College of Agronomy and Biotechnology, China Agricultural University, Beijing, 100193, China., Liu Y; College of Grassland Science and Technology, China Agricultural University, Beijing, 100193, China., Gao Y; College of Grassland Science and Technology, China Agricultural University, Beijing, 100193, China., Xu M; College of Grassland Science and Technology, China Agricultural University, Beijing, 100193, China., Zhang K; College of Grassland Science and Technology, China Agricultural University, Beijing, 100193, China., Liu Y; National Center of Pratacultural Technology Innovation (Under Preparation), M-Grass Ecology Environment (Group) Co Ltd, Hohhot, 010010, China., Zhang W; College of Grassland Science and Technology, China Agricultural University, Beijing, 100193, China.; College of Grassland Science, Xinjiang Agricultural University, Urumqi, 830052, China.
Source:
The Plant journal : for cell and molecular biology [Plant J] 2025 Sep; Vol. 123 (5), pp. e70468.
Publication Type:
Journal Article
Language:
English
Journal Info:
Publisher: Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology Country of Publication: England NLM ID: 9207397 Publication Model: Print Cited Medium: Internet ISSN: 1365-313X (Electronic) Linking ISSN: 09607412 NLM ISO Abbreviation: Plant J Subsets: MEDLINE
Imprint Name(s):
Original Publication: Oxford : Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology, c1991-
MeSH Terms:
Medicago sativa*/genetics , Medicago sativa*/physiology , Medicago sativa*/metabolism , Medicago sativa*/growth & development , MicroRNAs*/genetics , MicroRNAs*/metabolism , MicroRNAs*/physiology , Root Nodules, Plant*/genetics , Root Nodules, Plant*/physiology , Root Nodules, Plant*/metabolism , Root Nodules, Plant*/growth & development , Plant Proteins*/genetics , Plant Proteins*/metabolism, Reactive Oxygen Species/metabolism ; Gene Expression Regulation, Plant ; Plants, Genetically Modified ; Plant Senescence/genetics ; Nitrogen Fixation ; RNA, Plant/genetics ; RNA, Plant/metabolism ; Glutamate-Ammonia Ligase/genetics ; Glutamate-Ammonia Ligase/metabolism
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Dalton, D.A., Boniface, C., Turner, Z., Lindahl, A., Kim, H.J., Jelinek, L. et al. (2009) Physiological roles of glutathione S‐transferases in soybean root nodules. Plant Physiology, 150, 521–530.
Debernardi, J.M., Mecchia, M.A., Vercruyssen, L., Smaczniak, C., Kaufmann, K., Inze, D. et al. (2014) Post‐transcriptional control of GRF transcription factors by microRNA miR396 and GIF co‐activator affects leaf size and longevity. The Plant Journal, 79, 413–426.
Deng, J., Zhu, F.G., Liu, J.X., Zhao, Y.F., Wen, J.Q., Wang, T. et al. (2019) Transcription factor bHLH2 represses CYSTEINE PROTEASE77 to negatively regulate nodule senescence. Plant Physiology, 181, 1683–1703.
Dixon, R. & Kahn, D. (2004) Genetic regulation of biological nitrogen fixation. Nature Reviews Microbiology, 2, 621–631.
Egli, M.A., Griffith, S.M., Miller, S.S., Anderson, M.P. & Vance, C.P. (1989) Nitrogen assimilating enzyme activities and enzyme protein during development and senescence of effective and plant gene‐controlled ineffective alfalfa nodules. Plant Physiology, 91, 898–904.
Fang, L.F., Liu, T., Li, M.Y., Dong, X.M., Han, Y.L., Xu, C.Z. et al. (2024) MODMS: a multi‐omics database for facilitating biological studies on alfalfa (Medicago sativa L.). Horticulture Research, 11, 245.
Ferela, A., Debernardi, J.M., Rosatti, S., Liebsch, D., Schommer, C. & Palatnik, J.F. (2023) Interplay among ZF‐HD and GRF transcription factors during Arabidopsis leaf development. Plant Physiology, 191, 1789–1802.
Ferreira, S., Moreira, E., Amorim, I., Santos, C. & Melo, P. (2019) Arabidopsis thaliana mutants devoid of chloroplast glutamine synthetase (GS2) have non‐lethal phenotype under photorespiratory conditions. Plant Physiology and Biochemistry, 144, 365–374.
Fukudome, M., Watanabe, E., Osuki, K., Imaizumi, R., Aoki, T., Becana, M. et al. (2019) Stably transformed Lotus japonicus plants overexpressing phytoglobin LjGlb1‐1 show decreased nitric oxide levels in roots and nodules as well as delayed nodule senescence. Plant and Cell Physiology, 60, 816–825.
Guerra, J.C.P., Coussens, G., De Keyser, A., De Rycke, R., Bodt, S., Van De Velde, W. et al. (2010) Comparison of developmental and stress‐induced nodule senescence in Medicago truncatula. Plant Physiology, 152, 1574–1584.
Gupta, M.D. & Nath, U. (2015) Divergence in patterns of leaf growth polarity is associated with the expression divergence of miR396. The Plant Cell, 27, 2785–2799.
Hachiya, T., Inaba, J., Wakazaki, M., Sato, M., Toyooka, K., Miyagi, A. et al. (2021) Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana. Nature Communications, 12, 4944.
Herridge, D.F., Peoples, M.B. & Boddey, R.M. (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil, 311, 1–18.
Horvath, B., Domonkos, A., Kereszt, A., Szucs, A., Abraham, E., Ayaydin, F. et al. (2015) Loss of the nodule‐specific cysteine rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf7 mutant. Proceedings of the National Academy of Sciences of the United States of America, 112, 15232–15237.
Kim, J.H. (2019) Biological roles and an evolutionary sketch of the GRF‐GIF transcriptional complex in plants. BMB Reports, 52, 227–238.
Kim, J.H., Choi, D.S. & Kende, H. (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. The Plant Journal, 36, 94–104.
Kobercova, E., Melo, P. & Fischer, L. (2023) Validating the role of glutamine synthetase GLN2 during photorespiration in Arabidopsis thaliana. Plant Physiology, 194, 324–328.
Kumagai, H., Hakoyama, T., Umehara, Y., Sato, S., Kaneko, T., Tabata, S. et al. (2007) A novel ankyrin‐repeat membrane protein, IGN1, is required for persistence of nitrogen‐fixing symbiosis in root nodules of Lotus japonicus. Plant Physiology, 143, 1293–1305.
Lea, P.J. & Miflin, B.J. (2011) Nitrogen assimilation and its relevance to crop improvement. Annual Plant Reviews online, 42, 1–40.
Li, S., Tian, Y.H., Wu, K., Ye, Y.F., Yu, J.P., Zhang, J.Q. et al. (2018) Modulating plant growth‐metabolism coordination for sustainable agriculture. Nature, 560, 595–600.
Li, Y.X., Zhou, L., Li, Y.G., Chen, D.S., Tan, X.J., Lei, L. et al. (2008) A nodule‐specific plant cysteine proteinase, AsNODF32, is involved in nodule senescence and nitrogen fixation activity of the green manure legume Astragalus sinicus. New Phytologist, 180, 185–192.
Liao, H., Lee, K., Chung, Y., Chen, S., Hung, Y. & Hsieh, M. (2024) Glutamine induces lateral root initiation, stress responses, and disease resistance in Arabidopsis. Plant Physiology, 195, 2289–2308.
Liebsch, D. & Palatnik, J.F. (2020) MicroRNA miR396, GRF transcription factors and GIF co‐regulators: a conserved plant growth regulatory module with potential for breeding and biotechnology. Current Opinion in Plant Biology, 53, 31–42.
Liu, Y.R., Cen, H.F., Yan, J.P., Zhang, Y.W. & Zhang, W.J. (2015) Inside out: high‐efficiency plant regeneration and Agrobacterium‐mediated transformation of upland and lowland switchgrass cultivars. Plant Cell Reports, 34, 1099–1108.
Liu, Y.R., Yan, J.P., Wang, K.X., Li, D.Y., Yang, R., Luo, H. et al. (2021) MiR396‐GRF module associates with switchgrass biomass yield and feedstock quality. Plant Biotechnology Journal, 19, 1523–1536.
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real‐time quantitative PCR and the 2−ΔΔCt method. Methods, 25, 402–408.
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Grant Information:
CCPTZX2023B01 National Center of Pratacultural Technology Innovation (under preparation); CCPTZX2024GJ02-3 National Center of Pratacultural Technology Innovation (under preparation); 2023ZD0406003 Ministry of Science and Technology of China
Contributed Indexing:
Keywords: Medicago sativa; MsGRF1c; MsGS2; miR396b; nodule senescence; reactive oxygen species
Substance Nomenclature:
0 (MicroRNAs)
0 (Reactive Oxygen Species)
0 (Plant Proteins)
0 (RNA, Plant)
EC 6.3.1.2 (Glutamate-Ammonia Ligase)
0 (Reactive Oxygen Species)
0 (Plant Proteins)
0 (RNA, Plant)
EC 6.3.1.2 (Glutamate-Ammonia Ligase)
Entry Date(s):
Date Created: 20250912 Date Completed: 20250916 Latest Revision: 20250916
Update Code:
20250916
DOI:
10.1111/tpj.70468
PMID:
40939583
Database:
MEDLINE
Weitere Informationen
The miR396-GRF module plays a vital role in the growth and development of plant organs. However, its function in the development of leguminous nodules remains unclear. Here, we observed significant upregulation of miR396b in alfalfa (Medicago sativa L.) senescent nodules, especially in the upper part of the nitrogen fixation region. Transgenic lines overexpressing or sequestering miR396b were generated to examine its role in nodule senescence. Here, we report that miR396b acts as a positive regulator in nodule senescence by affecting the accumulation of reactive oxygen species (ROS) in different regions of a nodule. Among the 10 miR396b-targeted MsGRFs, MsGRF1c showed the most significant transcriptional suppression by miR396b in nodules. By overexpressing rMsGRF1c (a synonymous mutation of MsGRF1c resistant to miR396b cleavage) and suppression of MsGRF1c activity via MsGRF1c-SRDX overexpression in alfalfa, we confirmed that MsGRF1c delayed nodule senescence by regulating ROS distribution and promoted alfalfa above-ground biomass yield after sinorhizobium inoculation. A glutamine synthetase gene (MsGS2), which showed differentially expressed in the RNA sequencing data, was markedly upregulated in the nodule senescent region and repressed by MsGRF1c. Then, MsGS2 was experimentally validated as a direct transcriptional target of MsGRF1c. Transient interference of MsGS2 expression in nodules via antisense oligodeoxynucleotide treatment proved its essential role in regulating ROS distribution and nitrogen fixation efficiency in alfalfa nodules. Our results shed light on the miR396b-MsGRF1c-MsGS2 pathway that plays a vital role in regulating alfalfa nodule senescence by affecting ROS distribution, and we propose an alternative way to create new alfalfa germplasm with enhanced nitrogen fixation capacity and biomass yield.
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