Kejing Fan
Brett James Ferguson
Nacira Belen Muñoz
Man-Wah Li
Hon-Ming Lam- 1Center for Soybean Research of The State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China
- 2Integrative Legume Research Group, School of Agriculture and Food Sciences, The University of Queensland, St Lucia, Brisbane, QLD, Australia
- 3National Institute of Agricultural Technology, Córdoba, Argentina
Editorial on the Research Topic
Metabolic adjustments and gene expression reprogramming for symbiotic nitrogen fixation in legume nodules, volume II
The increased demand for food and more sustainable agricultural practices have brought increased attention to legume crops, a family of plants that are able to carry out symbiotic nitrogen fixation which provides a reliable source of bioavailable nitrogen. Thus, the cultivation of legumes can effectively reduce the reliance on the not-so-environmentally friendly synthetic nitrogen fertilizer. The legume-rhizobium symbiosis results in the formation of new root organs called nodules, where rhizobia differentiate into bacteroids and carry out symbiotic nitrogen fixation to reduce the atmospheric nitrogen (N2) to ammonia, which can then be used by the host plant (Ferguson et al., 2010; Liu et al., 2018; Roy et al., 2020; Yang et al., 2022). Much effort has been dedicated to researching the legume-rhizobium symbiosis and nitrogen fixation mechanism to understand and improve these beneficial processes.
Nodulation and nitrogen fixation are tightly regulated to balance between the benefits of nitrogen and other critical resources (Ferguson et al., 2019). Nodulation is initiated by the exchange of signals between the plant and the rhizobium (Ferguson and Mathesius, 2014; Yang et al., 2022). Typically, the legume host secretes flavonoids or their derivatives into the rhizosphere to attract the rhizobium (Sprent et al., 2017). The flavonoids induce the rhizobium to release nod factors (NFs), a group of lipochiooliosaccharides, which trigger the transcriptomic reprogramming of the host to initiate the nodulation process (Yang et al., 2022). Nevertheless, the host can choose either to accept the NFs through NF receptors or to decline them by hydrolyzing the NFs into non-intimidating forms (Staehelin et al., 1994; Goormachtig et al., 1998; Ovtsyna et al., 2007; Tian et al., 2013; Zhang et al., 2016). A class-V chitinase (MtCHIT5b) was recently characterized in Medicago truncatula, which can cleave the NF from Sinorhizobium meliloti in the rhizosphere (Li et al.). Increasing MtCHIT5b in the rhizosphere through overexpression led to a significant reduction in nodule formation, demonstrating the NF hydrolase to be a key player at the frontier of the interaction between the legume and the rhizobium for nodulation.
When NFs are successfully perceived by NF receptors, the host cells will undergo massive transcriptomic reprogramming governed by a cocktail of transcription factors for the subsequent organogenesis and nitrogen fixation. The respective subunits of heterotrimeric Nuclear Factor Y (NF-Y) transcription factors have been demonstrated to play crucial roles in nodule formation (Wang et al., 2015; Shrestha et al., 2021). Such an interaction, as that between NF-Y subunit C1 (NF-YC1) and the NF-YC1-interacting protein kinase (NIPK) from Phaseolus vulgaris, was recently identified through yeast two-hybrid screening (Clúa et al.). Although NIPK does not possess the canonical residues for the catalytic activities of kinases, its localization to the plasma membrane and the cytoplasm suggests that it may regulate the function of NF-YC1 through the re-localization of the transcription factor protein. The knockdown of NIPK had significant negative impacts on nodule number and nodule size, resembling the phenotype of NF-YC1-RNAi plants. The silencing of NIPK also impaired the induction of cell cycle-related and nodulation-related genes responsive to rhizobium inoculation, suggesting NIPK’s involvement in the transcription regulation of legume-rhizobium symbiosis.
The translation of the open reading frames of transcripts collectively determines the proteome. Song et al. utilized translating ribosome affinity purification (TRAP) sequencing to capture the actively translated transcripts in the root cortex of soybean in response to Bradyrhizobium japonicum inoculation. They have not only found the well-known nodulation marker genes, but have also discovered a new set of genes potentially important for early nodulation events. These discoveries enable legume researchers to further resolve the interconnected regulation networks for nodule formation.
As an essential macronutrient, phosphorus (P) influences various vital functions in plants. Deficiency in P can be detrimental to nodulation and nitrogen fixation. The effects of different P regimes on the proteome of soybean nodules were determined using a high-throughput proteomic approach (Yao et al.). While comparing nodules with normal P to those with P deficiency, the most affected gene ontologies (GO) and pathways of the differentially expressed proteins (DEP) are mainly related to protein translation. At the other end, carbon and nitrogen metabolism-related GO and pathways are the most affected under high-P conditions. These findings enhance our understanding of how nodules respond to different P conditions at the proteomic level.
Recent evidence revealed that non-coding RNAs (ncRNAs), including microRNAs (miRNAs), long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs), form another layer of regulation of nodulation and nitrogen fixation by controlling the transcription and translation of effector genes (Yan et al., 2013; Yan et al., 2015; Fan et al., 2021). Fan et al. summarized and discussed the current understanding of ncRNAs in legume nodulation and nitrogen fixation in root nodules, focusing on the regulation of hormone signal transduction, the autoregulation of nodulation (AON) pathway and nutrient homeostasis in nodules by ncRNAs. They also touched on the potential applications of ncRNAs in agriculture. Unraveling the roles of ncRNAs in legume nodulation will provide new insights into designing better leguminous crops for sustainable agriculture.
This Research Topic explores the new findings in NF signal transduction, nodule development, nodule metabolic changes upon P stress, and technological breakthroughs in translatomic analyses in nodule formation. The contributing articles collectively shed light on the molecular mechanisms involved in these areas and provide new research directions and scenarios for rhizobium-legume symbiosis.
Author contributions
H-ML coordinated the preparation and completed the final version of this editorial. KF and M-WL wrote the first draft. BF and NM contributed to the editing of this Research Topic and proofreading this editorial. All authors contributed to the article and approved the submitted version.
Funding
Research in the laboratories of the Topic Editors is supported by Hong Kong Research Grants Council Area of Excellence Scheme (AoE/M-403/16) and Lo Kwee-Seong Biomedical Research Fund to H-ML, and Australian Research Council Discovery Project grant (DP190102996) to BF.
Acknowledgments
Any opinions, findings, conclusions or recommendations expressed in this publication do not reflect the views of the Government of the Hong Kong Special Administrative Region or the Innovation and Technology Commission.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
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References
Fan, K., Wong-Bajracharya, J., Lin, X., Ni, M., Ku, Y. S., Li, M. W., et al. (2021). Differentially expressed microRNAs that target functional genes in mature soybean nodules. Plant Genome 14, e20103. doi: 10.1002/TPG2.20103
Ferguson, B. J., Indrasumunar, A., Hayashi, S., Lin, M. H., Lin, Y. H., Reid, D. E., et al. (2010). Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol. 52, 61–76. doi: 10.1111/j.1744-7909.2010.00899.x
Ferguson, B. J., Mathesius, U. (2014). Phytohormone regulation of legume-rhizobia interactions. J. Chem. Ecol. 40, 770–790. doi: 10.1007/S10886-014-0472-7
Ferguson, B. J., Mens, C., Hastwell, A. H., Zhang, M. B., Su, H., Jones, C. H., et al. (2019). Legume nodulation: The host controls the party. Plant Cell Environ. 42, 41–51. doi: 10.1111/pce.13348
Goormachtig, S., Lievens, S., Van de Velde, W., Van Montagu, M., Holsters, M. (1998). Srchi13, a novel early nodulin from Sesbania rostrata, is related to acidic class III chitinases. Plant Cell 10, 905–915. doi: 10.1105/TPC.10.6.905
Liu, A., Contador, C. A., Fan, K., Lam, H. M. (2018). Interaction and regulation of carbon, nitrogen, and phosphorus metabolisms in root nodules of legumes. Front. Plant Sci. 871. doi: 10.3389/fpls.2018.01860
Ovtsyna, A. O., Schultze, M., Tikhonovich, I. A., Spaink, H. P., Kondorosi, É., Kondorosi, Á., et al. (2007). Nod factors of Rhizobium leguminosarum bv. viciae and their fucosylated derivatives stimulate a nod factor cleaving activity in pea roots and are hydrolyzed in vitro by plant chitinases at different rates. Mol. Plant Microbe Interact. 13, 799–807. doi: 10.1094/MPMI.2000.13.8.799
Roy, S., Liu, W., Nandety, R. S., Crook, A., Mysore, K. S., Pislariu, C. I., et al. (2020). Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. Plant Cell 32, 15–41. doi: 10.1105/TPC.19.00279
Shrestha, A., Zhong, S., Therrien, J., Huebert, T., Sato, S., Mun, T., et al. (2021). Lotus japonicus nuclear factor YA1, a nodule emergence stage-specific regulator of auxin signalling. New Phytol. 229, 1535–1552. doi: 10.1111/NPH.16950
Sprent, J. I., Ardley, J., James, E. K. (2017). Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytol. 215, 40–56. doi: 10.1111/nph.14474
Staehelin, C., Schultze, M., Kondorosi, É., Mellor, R. B., Boiler, T., Kondorosi, A. (1994). Structural modifications in Rhizobium meliloti nod factors influence their stability against hydrolysis by root chitinases. Plant J. 5, 319–330. doi: 10.1111/J.1365-313X.1994.00319.X
Tian, Y., Liu, W., Cai, J., Zhang, L. Y., Wong, K. B., Feddermann, N., et al. (2013). The nodulation factor hydrolase of Medicago truncatula: Characterization of an enzyme specifically cleaving rhizobial nodulation signals. Plant Physiol. 163, 1179–1190. doi: 10.1104/PP.113.223966
Wang, Y., Li, K., Hen, L., Zou, Y., Liu, H., Tian, Y., et al. (2015). MicroRNA167-directed regulation of the auxin response factors GmARF8a and GmARF8b is required for soybean nodulation and lateral root development. Plant Physiol. 168, 101–116. doi: 10.1104/pp.15.00265
Yang, J., Lan, L., Jin, Y., Yu, N., Wang, D., Wang, E. (2022). Mechanisms underlying legume–rhizobium symbioses. J. Integr. Plant Biol. 64, 244–267. doi: 10.1111/JIPB.13207
Yan, Z., Hossain, M. S., Arikit, S., Valdés-López, O., Zhai, J., Wang, J., et al. (2015). Identification of microRNAs and their mRNA targets during soybean nodule development: functional analysis of the role of miR393j-3p in soybean nodulation. New Phytol. 207, 748–759. doi: 10.1111/nph.13365
Yan, Z., Hossain, M. S., Wang, J., Valdés-López, O., Liang, Y., Libault, M., et al. (2013). miR172 regulates soybean nodulation. Mol. Plant-Microbe Interact. 26, 1371–1377. doi: 10.1094/MPMI-04-13-0111-R
Keywords: legume, nitrogen fixation, nod factor hydrolase, non-coding RNA (ncRNA), nodulation, proteome, transcription regulation, translatome
Citation: Fan K, Ferguson BJ, Muñoz NB, Li M-W and Lam H-M (2023) Editorial: Metabolic adjustments and gene expression reprogramming for symbiotic nitrogen fixation in legume nodules, volume II. Front. Plant Sci. 14:1141269. doi: 10.3389/fpls.2023.1141269
Received: 10 January 2023; Accepted: 16 January 2023;
Published: 24 January 2023.
Edited and Reviewed by:
Andrea Genre, University of Turin, ItalyCopyright © 2023 Fan, Ferguson, Muñoz, Li and Lam. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Hon-Ming Lam, honming@cuhk.edu.hk; Man-Wah Li, limanwah@cuhk.edu.hk