Senjuti Sinharoy
Chang-Fu Tian
Jesús Montiel- 1Plant-Microbe Interaction, National Institute of Plant Genome Research (NIPGR) New Delhi, New Delhi, India
- 2State Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural University, Beijing, China
- 3Center for Genomic Sciences, National Autonomous University of Mexico, Cuernavaca, Mexico
Editorial on the Research Topic
Plant-rhizobia symbiosis and nitrogen fixation in legumes
Nitrogen (N) is essential for life, but eukaryotes lack the ability to access this element, as only prokaryotic enzymes can convert N to ammonia. The Haber-Bosch process revolutionized agriculture by enabling synthetic N-fertilizer production, but its overuse and mismanagement created significant environmental challenges (Rockstrom et al., 2009; Richardson et al., 2023). Biological Nitrogen Fixation (BNF) by diazotrophic bacteria and symbiotic nitrogen fixation (SNF) by N-fixing plants offer age-old solutions to the N-problem (Adams et al., 2018).
In this context, legumes represent a valuable biological resource to migrate into a sustainable agriculture, since in N-deficient soil, they engage in symbiosis with rhizobia. In the rhizosphere, nodulation factors (NFs) secreted by rhizobia prompt mitotic activity in the root cortex cells, triggering de-differentiation and nodule formation. Concurrently, rhizobia invade root hair cells, guided by plant-derived infection threads (ITs), towards dividing plant cells. Once inside, rhizobia are endocytosed and become enclosed by plant membrane leading to the formation of ‘symbiosomes’, where they multiply and function as nitrogen-fixing entities. This Research Topic encompasses eleven articles addressing both bacterial and plant aspects essential for SNF (Kang et al., 2016; Roy et al., 2020), and the agronomical benefits of this mutualistic association.
Legumes
It is estimated that around 25% of nodulating legumes employ an alternative rhizobial colonization process, called intercellular infection, where bacteria invade the host plant between the epidermal cells or by crack entry (Quilbe et al., 2022). Since the molecular basis of this mechanism is largely unknown, García-Soto et al. conducted a large-scale mutant screening to discover genes recruited in the intercellular symbiotic colonization of the Agrobacterium pusense strain IRBG74 on Lotus japonicus roots. The forward genetic approach was followed by sequencing the flanking regions of the mutagen to locate the potential causative genes.
Iron is crucial for various rhizobial and plant enzymes essential for BNF, including regulatory proteins like FixL and FixJ (Gilles-Gonzalez et al., 1991), nitrogen fixing enzymes NifH and NifDK (Dixon, 1998) and plant protein leghemoglobin (Wang et al., 2019; Brear et al., 2013). Iron transfer to nodules occurs through both apoplastic and symplastic routes and involves several transporters (Brear et al., 2013; Kryvoruchko et al., 2018; Tejada-Jiménez et al., 2015). MtVTL8 (Vacuolar Iron Transporter (VIT)-Like) is a major transporter responsible for delivering iron to the symbiosome in Medicago truncatula (Walton et al., 2020). In this Research Topic, Cai et al. highlights MtVTL8’s unconventional mechanism of iron transport across the symbiosome membrane (SM), as revealed through genetic, structural prediction, and biochemical analyses.
The SNF imposes a significant energy burden on plants due to its high photosynthetic cost. Legumes regulate nodule number using a systemic signalling called autoregulation of nodulation (AON). The SUPER NUMERARY NODULES (MtSUNN), a leucine-rich repeat receptor-like kinase in the shoot, perceives root-derived peptide signals (MtCLE12 and MtCLE13) (Kang et al., 2016; Kassaw et al., 2017; Imin et al., 2018). MtCLE12/13 is activated in the root by the master transcription factor of nodulation, Nodule Inception (NIN) (Laffont et al., 2020). Thomas and Frugoli discuss in this Research Topic, how the MtBAM2 protein, an ortholog of the Arabidopsis BARELY ANY MERISTEM family, collaborates with SUNN, crucial for nodule meristem establishment. Additionally, Shen and Feng provide a review detailing NIN’s multifaceted role from infection to symbiosome development and AON.
Legumes also inhibit nodule formation under nitrogen sufficient condition (Kang et al., 2016) and interestingly, this effect can be partially alleviated by the organic macromolecule humic acid (HA). Zhang et al. further explored this phenomenon, by analysing the transcriptomic response of soybean nodules treated with HA under high nitrogen levels. Limited availability of phosphorus has a negative impact on nodule formation (Sulieman et al., 2013). Molecular studies using Arabidopsis have elucidated mechanisms controlling inorganic phosphate homeostasis. Under phosphate sufficiency, PHOSPHATE2 (PHO2) protein facilitate phosphate transporter degradation, limiting uptake. In phosphate deficiency, microRNA399 (miR399) promotes PHO2 degradation (Aung et al., 2006; Bari et al., 2006). Huertas et al. demonstrated that MtPHO2b and MtPHO2c genes play a crucial role in regulating SNF by modulating plant phosphate homeostasis. Importantly, the complex molecular network in the legume-rhizobia symbiosis includes posttranscriptional regulation of gene expression by small RNAs (Roy et al., 2020), which are associated to ARGONAUTE proteins. Sánchez-Correa et al. explored the impact of RNAi-mediated silencing of Argonaute5 in roots and nodules of Phaseolus vulgaris. Additionally, they detected small RNAs bound to PvAGO5 at different stages of the nodulation process.
Rhizobia
Rhizobial nodulation factors (NFs) and type III secretion effectors (T3SEs) are key players in NF-dependent and NF-independent nodulation processes, respectively. It is not rare for rhizobia to harbour both nodulation genes and genes encoding type III secretion system (T3SS) and T3SEs. Available evidence from the intensively studied species Sinorhizobium fredii supports a regulatory network for these key symbiosis genes involving transcriptional factors NodD1, SyrM, NodD2, NolR and TtsI. In this Research Topic, Navarro-Gómez et al. compared transcriptional profiles, symbiotic performance and NF composition of S. fredii HH103 derivatives related to these regulatory genes, and proposed an updated regulatory model. NodD1 activates the transcription of nodulation genes and TtsI that in turn upregulates T3SS/T3SE genes. On the other hand, NodD1 can also activate the transcription of syrM-nodD2 and syrM-nolR modules, and NodD2 and NolR negatively regulate TtsI and NodD1 regulons. Moreover, negative regulation of nodD2 by NolR, feedback repression of syrM by NodD2 and NolR, antagonistic repression between TtsI and SyrM, and autoregulation of NodD1, SyrM, NolR and TtsI were proposed. Further in vivo and in vitro protein-DNA interaction evidence can be helpful for clarifying these regulatory effects as direct and/or indirect output. The work by Navarro-Gómez et al. provides novel insight into the overlooked complexity in the regulation network of key symbiosis genes, which deserves further exploration to guide engineering elite rhizobial inoculants.
Rhizobia can live saprophytically in bulk soils, colonize rhizosphere and rhizoplane, live as host endophytes, enter intracellular symbiosis with compatible legume plants, and release from senescent nodules. In this Research Topic, Agudelo et al. reviewed related literatures on the role of direct or indirect microbial interactions that alter rhizobial fitness in rhizosphere, during nodulation and within nodules. This is a timely summary of multipartite interactions involving legumes, rhizobia and other microorganisms. Authors further highlighted several understudied issues e.g. the significance of microbial interactions within nitrogen-fixing and senescent nodules, and after nodule senescence; genetic bases and eco-evolutionary dynamics underlying microbial interactions. Further efforts in addressing these questions by recruiting a multidisciplinary strategy involving genetics, physiology, molecular biology, ecology and evolution can be helpful.
Agricultural impact
In the last decades the benefits of SNF in agriculture has been largely documented. However, this extraordinary mutualistic association can be further exploited. In this regard, Xu et al. discovered that a mixed planting of Medicago sativa and Bromus inermis resulted in significantly higher hay yield compared to a monoculture grassland. For farmers, a key aspect to implement SNF in the field, is the prediction of the expected yield. This represents a challenging task, considering the biotic and abiotic factors that influence SNF. However, Jemo et al. conducted a multifactorial analysis using mapped soil properties and weather variables, to predict by machine-learning techniques soybean yield in fields supplemented with phosphorus and inoculated with rhizobium.
Author contributions
SS: Conceptualization, Writing – original draft, Writing – review & editing. C-FT: Conceptualization, Writing – original draft, Writing – review & editing. JM: Conceptualization, Writing – original draft, Writing – review & editing.
Funding
The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. NIPGR core grant and SERB Power Grant (SPG/2022/000171) to SS National Key Research and Development Program of China (grant number 2022YFA0912100) and the 2115 Talent Development Program of China Agricultural University to C-FT Dirección General de Asuntos del Personal Académico (DGAPA)-Universidad Nacional Autónoma de México (UNAM) – Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT, grant IA200723) to JM.
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.
The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Adams, M. A., Buchmann, N., Sprent, J., Buckley, T. N., Turnbull, T. L. (2018). Crops, nitrogen, water: are legumes friend, foe, or misunderstood ally? Trends Plant Sci. 23, 539–550. doi: 10.1016/j.tplants.2018.02.009
Aung, K., Lin, S. I., Wu, C. C., Huang, Y. T., Su, C. L., Chiou, T. J. (2006). pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol. 141, 1000–1011. doi: 10.1104/pp.106.078063
Bari, R., Datt Pant, B., Stitt, M., Scheible, W. R. (2006). PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141, 988–999. doi: 10.1104/pp.106.079707
Brear, E. M., Day, D. A., Smith, P. M. (2013). Iron: an essential micronutrient for the legume-rhizobium symbiosis. Front. Plant Sci. 4. doi: 10.3389/fpls.2013.00359
Dixon, R. (1998). The oxygen-responsive NIFL-NIFA complex: a novel two-component regulatory system controlling nitrogenase synthesis in gamma-proteobacteria. Arch. Microbiol. 169, 371–380. doi: 10.1007/s002030050585
Gilles-Gonzalez, M. A., Ditta, G. S., Helinski, D. R. (1991). A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature 350, 170–172. doi: 10.1038/350170a0
Imin, N., Patel, N., Corcilius, L., Payne, R. J., Djordjevic, M. A. (2018). CLE peptide tri-arabinosylation and peptide domain sequence composition are essential for SUNN-dependent autoregulation of nodulation in Medicago truncatula. New Phytol. 218, 73–80. doi: 10.1111/nph.15019
Kang, Y., Li, M., Sinharoy, S., Verdier, J. (2016). A snapshot of functional genetic studies in Medicago truncatula. Front. Plant Sci. 7. doi: 10.3389/fpls.2016.01175
Kassaw, T., Nowak, S., Schnabel, E., Frugoli, J. (2017). ROOT DETERMINED NODULATION1 is required for. Plant Physiol. 174, 2445–2456. doi: 10.1104/pp.17.00278
Kryvoruchko, I. S. I. S., Routray, P., Sinharoy, S., Torres-Jerez, I., Tejada-Jiménez, M., Finney, L. A. L. A., et al. (2018). An iron-activated citrate transporter, MtMATE67, is required for symbiotic nitrogen fixation. Plant Physiol. 176, 2315–2329. doi: 10.1104/pp.17.01538
Laffont, C., Ivanovici, A., Gautrat, P., Brault, M., Djordjevic, M. A., Frugier, F. (2020). The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically. Nat. Commun. 11, 3167. doi: 10.1038/s41467-020-16968-1
Quilbe, J., Montiel, J., Arrighi, J. F., Stougaard, J. (2022). Molecular mechanisms of intercellular rhizobial infection: novel findings of an ancient process. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.922982
Richardson, K., Steffen, W., Lucht, W., Bendtsen, J., Cornell, S. E., Donges, J. F., et al. (2023). Earth beyond six of nine planetary boundaries. Sci. Adv. 9, eadh2458. doi: 10.1126/sciadv.adh2458
Rockstrom, J., Steffen, W., Noone, K., Persson, A., Chapin, F. S., 3rd, Lambin, E. F., et al. (2009). A safe operating space for humanity. Nature 461, 472–475. doi: 10.1038/461472a
Sulieman, S., Ha, C. V., Schulze, J., Tran, L. S. (2013). Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability. J. Exp. Bot. 64, 2701–2712. doi: 10.1093/jxb/ert122
Tejada-Jiménez, M., Castro-Rodríguez, R., Kryvoruchko, I., Lucas, M. M., Udvardi, M., Imperial, J., et al. (2015). Medicago truncatula natural resistance-associated macrophage Protein1 is required for iron uptake by rhizobia-infected nodule cells. Plant Physiol. 168, 258–272. doi: 10.1104/pp.114.254672
Walton, J. H., Kontra-Kováts, G., Green, R. T., Domonkos, Á., Horváth, B., Brear, E. M., et al. (2020). The Medicago truncatula Vacuolar iron Transporter-Like proteins VTL4 and VTL8 deliver iron to symbiotic bacteria at different stages of the infection process. New Phytol. 228, 651–666. doi: 10.1111/nph.16735
Keywords: legumes, symbiosis, nodule, rhizobia, nitrogen fixation
Citation: Sinharoy S, Tian C-F and Montiel J (2024) Editorial: Plant-rhizobia symbiosis and nitrogen fixation in legumes. Front. Plant Sci. 15:1392006. doi: 10.3389/fpls.2024.1392006
Received: 26 February 2024; Accepted: 28 February 2024;
Published: 11 March 2024.
Edited and Reviewed by:
Andrea Genre, University of Turin, ItalyCopyright © 2024 Sinharoy, Tian and Montiel. 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: Senjuti Sinharoy, ssinharoy@nipgr.ac.in; Chang-Fu Tian, cftian@cau.edu.cn; Jesús Montiel, jmontiel@ccg.unam.mx