Investigating biological nitrogen fixation via single-cell transcriptomics

Pereira, Wendell J.; Conde, Daniel; Perron, Noé; Schmidt, Henry W; Dervinis, Christopher; Venado, Rafael E.; Ané, Jean-Michel; Kirst, Matias

doi:10.1093/jxb/erae454

Investigating biological nitrogen fixation via single-cell transcriptomics

Journal Article · Tue Nov 19 23:00:00 EST 2024 · Journal of Experimental Botany

DOI:https://doi.org/10.1093/jxb/erae454· OSTI ID:3005949

^[1]; Conde, Daniel ^[2]; Perron, Noé ^[1]; ^[1]; ^[1]; ^[3]; ^[3]; ^[1]

University of Florida, Gainesville, FL (United States)
Universidad Politécnica de Madrid–Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC) (Spain)
University of Wisconsin, Madison, WI (United States)

The extensive use of nitrogen fertilizers has detrimental environmental consequences, and it is essential for society to explore sustainable alternatives. One promising avenue is engineering root nodule symbiosis, a naturally occurring process in certain plant species within the nitrogen-fixing clade, into non-leguminous crops. Advancements in single-cell transcriptomics provide unprecedented opportunities to dissect the molecular mechanisms underlying root nodule symbiosis at the cellular level. This review summarizes key findings from single-cell studies in Medicago truncatula, Lotus japonicus, and Glycine max. We highlight how these studies address fundamental questions about the development of root nodule symbiosis, including the following findings: (i) single-cell transcriptomics has revealed a conserved transcriptional program in root hair and cortical cells during rhizobial infection, suggesting a common infection pathway across legume species; (ii) characterization of determinate and indeterminate nodules using single-cell technologies supports the compartmentalization of nitrogen fixation, assimilation, and transport into distinct cell populations; (iii) single-cell transcriptomics data have enabled the identification of novel root nodule symbiosis genes and provided new approaches for prioritizing candidate genes for functional characterization; and (iv) trajectory inference and RNA velocity analyses of single-cell transcriptomics data have allowed the reconstruction of cellular lineages and dynamic transcriptional states during root nodule symbiosis.

View Accepted Manuscript (DOE)

Research Organization:: University of Florida, Gainesville, FL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0018247

OSTI ID:: 3005949

Journal Information:: Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 4 Vol. 76; ISSN 1460-2431; ISSN 0022-0957

Publisher:: Oxford University Press (OUP)Copyright Statement

Country of Publication:: United States

Language:: English

References (148)

Lipo-oligosaccharide nodulation factors: A new class of signaling molecules mediating recognition and morphogenesis Dénarié, Jean; Cullimore, Julie Cell, Vol. 74, Issue 6 https://doi.org/10.1016/0092-8674(93)90717-5	journal	September 1993
Silhouettes: A graphical aid to the interpretation and validation of cluster analysis Rousseeuw, Peter J. Journal of Computational and Applied Mathematics, Vol. 20 https://doi.org/10.1016/0377-0427(87)90125-7	journal	November 1987
Evolution of signal transduction in intracellular symbiosis Kistner, Catherine; Parniske, Martin Trends in Plant Science, Vol. 7, Issue 11 https://doi.org/10.1016/S1360-1385(02)02356-7	journal	November 2002
Highly Parallel Genome-wide Expression Profiling of Individual Cells Using Nanoliter Droplets Macosko, Evan Z.; Basu, Anindita; Satija, Rahul Cell, Vol. 161, Issue 5 https://doi.org/10.1016/j.cell.2015.05.002	journal	May 2015
A cis-regulatory atlas in maize at single-cell resolution Marand, Alexandre P.; Chen, Zongliang; Gallavotti, Andrea Cell, Vol. 184, Issue 11 https://doi.org/10.1016/j.cell.2021.04.014	journal	May 2021
The single-cell transcriptome program of nodule development cellular lineages in Medicago truncatula Pereira, Wendell J.; Boyd, Jade; Conde, Daniel Cell Reports, Vol. 43, Issue 2 https://doi.org/10.1016/j.celrep.2024.113747	journal	February 2024
DoubletFinder: Doublet Detection in Single-Cell RNA Sequencing Data Using Artificial Nearest Neighbors McGinnis, Christopher S.; Murrow, Lyndsay M.; Gartner, Zev J. Cell Systems, Vol. 8, Issue 4 https://doi.org/10.1016/j.cels.2019.03.003	journal	April 2019
Single-cell RNA sequencing reveals the landscape of maize root tips and assists in identification of cell type-specific nitrate-response genes Li, Xuhui; Zhang, Xiangbo; Gao, Shuai The Crop Journal, Vol. 10, Issue 6 https://doi.org/10.1016/j.cj.2022.02.004	journal	December 2022
hdWGCNA identifies co-expression networks in high-dimensional transcriptomics data Morabito, Samuel; Reese, Fairlie; Rahimzadeh, Negin Cell Reports Methods, Vol. 3, Issue 6 https://doi.org/10.1016/j.crmeth.2023.100498	journal	June 2023
NODULE INCEPTION Recruits the Lateral Root Developmental Program for Symbiotic Nodule Organogenesis in Medicago truncatula Schiessl, Katharina; Lilley, Jodi L. S.; Lee, Tak Current Biology, Vol. 29, Issue 21 https://doi.org/10.1016/j.cub.2019.09.005	journal	November 2019
Light-sensitive short hypocotyl genes confer symbiotic nodule identity in the legume Medicago truncatula Lee, Tak; Orvosova, Martina; Batzenschlager, Morgane Current Biology, Vol. 34, Issue 4 https://doi.org/10.1016/j.cub.2024.01.018	journal	February 2024
Single-cell RNA sequencing of developing maize ears facilitates functional analysis and trait candidate gene discovery Xu, Xiaosa; Crow, Megan; Rice, Brian R. Developmental Cell, Vol. 56, Issue 4 https://doi.org/10.1016/j.devcel.2020.12.015	journal	February 2021
A single-cell Arabidopsis root atlas reveals developmental trajectories in wild-type and cell identity mutants Shahan, Rachel; Hsu, Che-Wei; Nolan, Trevor M. Developmental Cell, Vol. 57, Issue 4 https://doi.org/10.1016/j.devcel.2022.01.008	journal	February 2022
Single-nucleus sequencing deciphers developmental trajectories in rice pistils Li, Chengxiang; Zhang, Songyao; Yan, Xingying Developmental Cell, Vol. 58, Issue 8 https://doi.org/10.1016/j.devcel.2023.03.004	journal	April 2023
The role of nitrogen in achieving sustainable food systems for healthy diets Leip, Adrian; Bodirsky, Benjamin Leon; Kugelberg, Susanna Global Food Security, Vol. 28 https://doi.org/10.1016/j.gfs.2020.100408	journal	March 2021
Single-nucleus RNA sequencing of Nicotiana tabacum seedlings reveals heterogeneity among cell types Jin, Jingjing; Cheng, Lingtong; Meng, Lijun Industrial Crops and Products, Vol. 208 https://doi.org/10.1016/j.indcrop.2023.117825	journal	February 2024
A reference-free approach for cell type classification with scRNA-seq Sun, Qi; Peng, Yifan; Liu, Jinze iScience, Vol. 24, Issue 8 https://doi.org/10.1016/j.isci.2021.102855	journal	August 2021
Single-cell transcriptome atlas of the leaf and root of rice seedlings Wang, Yu; Huan, Qing; Li, Ke Journal of Genetics and Genomics https://doi.org/10.1016/j.jgg.2021.06.001	journal	June 2021
Global Dynamic Molecular Profiling of Stomatal Lineage Cell Development by Single-Cell RNA Sequencing Liu, Zhixin; Zhou, Yaping; Guo, Jinggong Molecular Plant, Vol. 13, Issue 8 https://doi.org/10.1016/j.molp.2020.06.010	journal	August 2020
Single-nucleus RNA and ATAC sequencing reveals the impact of chromatin accessibility on gene expression in Arabidopsis roots at the single-cell level Farmer, Andrew; Thibivilliers, Sandra; Ryu, Kook Hui Molecular Plant, Vol. 14, Issue 3 https://doi.org/10.1016/j.molp.2021.01.001	journal	March 2021
Differentiation trajectories and biofunctions of symbiotic and un-symbiotic fate cells in root nodules of Medicago truncatula Ye, Qinyi; Zhu, Fugui; Sun, Fanghao Molecular Plant, Vol. 15, Issue 12 https://doi.org/10.1016/j.molp.2022.10.019	journal	December 2022
Cell-specific pathways recruited for symbiotic nodulation in the Medicago truncatula legume Cervantes-Pérez, Sergio Alan; Thibivilliers, Sandra; Laffont, Carole Molecular Plant, Vol. 15, Issue 12 https://doi.org/10.1016/j.molp.2022.10.021	journal	December 2022
Symbiosis and the social network of higher plants Venkateshwaran, Muthusubramanian; Volkening, Jeremy D.; Sussman, Michael R. Current Opinion in Plant Biology, Vol. 16, Issue 1 https://doi.org/10.1016/j.pbi.2012.11.007	journal	February 2013
Tough love: accommodating intracellular bacteria through directed secretion of antimicrobial peptides during the nitrogen-fixing symbiosis Stonoha-Arther, Christina; Wang, Dong Current Opinion in Plant Biology, Vol. 44 https://doi.org/10.1016/j.pbi.2018.04.017	journal	August 2018
Crafting a blueprint for single-cell RNA sequencing Denyer, Tom; Timmermans, Marja C. P. Trends in Plant Science, Vol. 27, Issue 1 https://doi.org/10.1016/j.tplants.2021.08.016	journal	January 2022
Transcriptional landscapes of de novo root regeneration from detached Arabidopsis leaves revealed by time-lapse and single-cell RNA sequencing analyses Liu, Wu; Zhang, Yuyun; Fang, Xing Plant Communications, Vol. 3, Issue 4 https://doi.org/10.1016/j.xplc.2022.100306	journal	July 2022
Combining single-cell RNA sequencing with spatial transcriptome analysis reveals dynamic molecular maps of cambium differentiation in the primary and secondary growth of trees Li, Renhui; Wang, Zhifeng; Wang, Jia-Wei Plant Communications, Vol. 4, Issue 5 https://doi.org/10.1016/j.xplc.2023.100665	journal	September 2023
Single-cell transcriptome atlases of soybean root and mature nodule reveal new regulatory programs that control the nodulation process Cervantes-Pérez, Sergio Alan; Zogli, Prince; Amini, Sahand Plant Communications, Vol. 5, Issue 8 https://doi.org/10.1016/j.xplc.2024.100984	journal	August 2024
Flavones induce expression of nodulation genes in Rhizobium Redmond, John W.; Batley, Michael; Djordjevic, Michael A. Nature, Vol. 323, Issue 6089 https://doi.org/10.1038/323632a0	journal	October 1986
A plant regulator controlling development of symbiotic root nodules Schauser, Leif; Roussis, Andreas; Stiller, Jiri Nature, Vol. 402, Issue 6758 https://doi.org/10.1038/46058	journal	November 1999
Too much of a good thing Sutton, Mark A.; Oenema, Oene; Erisman, Jan Willem Nature, Vol. 472, Issue 7342 https://doi.org/10.1038/472159a	journal	April 2011
A plant receptor-like kinase required for both bacterial and fungal symbiosis Stracke, Silke; Kistner, Catherine; Yoshida, Satoko Nature, Vol. 417, Issue 6892 https://doi.org/10.1038/nature00841	journal	June 2002
A receptor kinase gene regulating symbiotic nodule development Endre, Gabriella; Kereszt, Attila; Kevei, Zoltán Nature, Vol. 417, Issue 6892 https://doi.org/10.1038/nature00842	journal	June 2002
Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases Radutoiu, Simona; Madsen, Lene Heegaard; Madsen, Esben Bjørn Nature, Vol. 425, Issue 6958 https://doi.org/10.1038/nature02039	journal	October 2003
A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals Madsen, Esben Bjørn; Madsen, Lene Heegaard; Radutoiu, Simona Nature, Vol. 425, Issue 6958 https://doi.org/10.1038/nature02045	journal	October 2003
Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development Tirichine, Leïla; Imaizumi-Anraku, Haruko; Yoshida, Satoko Nature, Vol. 441, Issue 7097 https://doi.org/10.1038/nature04862	journal	June 2006
The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells Trapnell, Cole; Cacchiarelli, Davide; Grimsby, Jonna Nature Biotechnology, Vol. 32, Issue 4 https://doi.org/10.1038/nbt.2859	journal	March 2014
Massively parallel digital transcriptional profiling of single cells Zheng, Grace X. Y.; Terry, Jessica M.; Belgrader, Phillip Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14049	journal	January 2017
A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms Werner, Gijsbert D. A.; Cornwell, William K.; Sprent, Janet I. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5087	journal	June 2014
mRNA-Seq whole-transcriptome analysis of a single cell Tang, Fuchou; Barbacioru, Catalin; Wang, Yangzhou Nature Methods, Vol. 6, Issue 5 https://doi.org/10.1038/nmeth.1315	journal	April 2009
SCENIC: single-cell regulatory network inference and clustering Aibar, Sara; González-Blas, Carmen Bravo; Moerman, Thomas Nature Methods, Vol. 14, Issue 11 https://doi.org/10.1038/nmeth.4463	journal	October 2017
Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants Oldroyd, Giles E. D. Nature Reviews Microbiology, Vol. 11, Issue 4 https://doi.org/10.1038/nrmicro2990	journal	March 2013
Ca2+-regulated Ca2+ channels with an RCK gating ring control plant symbiotic associations Kim, Sunghoon; Zeng, Weizhong; Bernard, Shane Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11698-5	journal	August 2019
Trajectory-based differential expression analysis for single-cell sequencing data Van den Berge, Koen; Roux de Bézieux, Hector; Street, Kelly Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14766-3	journal	March 2020
Single-cell transcriptome atlas and chromatin accessibility landscape reveal differentiation trajectories in the rice root Zhang, Tian-Qi; Chen, Yu; Liu, Ye Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-22352-4	journal	April 2021
A 3D gene expression atlas of the floral meristem based on spatial reconstruction of single nucleus RNA sequencing data Neumann, Manuel; Xu, Xiaocai; Smaczniak, Cezary Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-30177-y	journal	May 2022
Benchmarking integration of single-cell differential expression Nguyen, Hai C. T.; Baik, Bukyung; Yoon, Sora Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-37126-3	journal	March 2023
Inference of cell type-specific gene regulatory networks on cell lineages from single cell omic datasets Zhang, Shilu; Pyne, Saptarshi; Pietrzak, Stefan Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-38637-9	journal	May 2023
Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus Frank, Manuel; Fechete, Lavinia Ioana; Tedeschi, Francesca Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-42911-1	journal	November 2023
Decoding the gene regulatory network of endosperm differentiation in maize Yuan, Yue; Huo, Qiang; Zhang, Ziru Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-023-44369-7	journal	January 2024
Shifts in evolutionary lability underlie independent gains and losses of root-nodule symbiosis in a single clade of plants Kates, Heather R.; O’Meara, Brian C.; LaFrance, Raphael Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-024-48036-3	journal	May 2024
Mapping the molecular landscape of Lotus japonicus nodule organogenesis through spatiotemporal transcriptomics Ye, Keyi; Bu, Fengjiao; Zhong, Liyuan Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-024-50737-8	journal	July 2024
An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages Radhakrishnan, Guru V.; Keller, Jean; Rich, Melanie K. Nature Plants, Vol. 6, Issue 3 https://doi.org/10.1038/s41477-020-0613-7	journal	March 2020
Transcriptional and imprinting complexity in Arabidopsis seeds at single-nucleus resolution Picard, Colette L.; Povilus, Rebecca A.; Williams, Ben P. Nature Plants, Vol. 7, Issue 6 https://doi.org/10.1038/s41477-021-00922-0	journal	May 2021
Integrated single-nucleus and spatial transcriptomics captures transitional states in soybean nodule maturation Liu, Zhijian; Kong, Xiangying; Long, Yanping Nature Plants, Vol. 9, Issue 4 https://doi.org/10.1038/s41477-023-01387-z	journal	April 2023
Single-nucleus transcriptomes reveal spatiotemporal symbiotic perception and early response in Medicago Liu, Zhijian; Yang, Jun; Long, Yanping Nature Plants, Vol. 9, Issue 10 https://doi.org/10.1038/s41477-023-01524-8	journal	September 2023
Host-imposed control mechanisms in legume–rhizobia symbiosis Porter, Stephanie S.; Dupin, Simon E.; Denison, R. Ford Nature Microbiology, Vol. 9, Issue 8 https://doi.org/10.1038/s41564-024-01762-2	journal	August 2024
RNA velocity of single cells La Manno, Gioele; Soldatov, Ruslan; Zeisel, Amit Nature, Vol. 560, Issue 7719 https://doi.org/10.1038/s41586-018-0414-6	journal	August 2018
The single-cell transcriptional landscape of mammalian organogenesis Cao, Junyue; Spielmann, Malte; Qiu, Xiaojie Nature, Vol. 566, Issue 7745 https://doi.org/10.1038/s41586-019-0969-x	journal	February 2019
An SHR–SCR module specifies legume cortical cell fate to enable nodulation Dong, Wentao; Zhu, Yayun; Chang, Huizhong Nature, Vol. 589, Issue 7843 https://doi.org/10.1038/s41586-020-3016-z	journal	December 2020
A pan-grass transcriptome reveals patterns of cellular divergence in crops Guillotin, Bruno; Rahni, Ramin; Passalacqua, Michael Nature, Vol. 617, Issue 7962 https://doi.org/10.1038/s41586-023-06053-0	journal	May 2023
A comparison of single-cell trajectory inference methods Saelens, Wouter; Cannoodt, Robrecht; Todorov, Helena Nature Biotechnology, Vol. 37, Issue 5 https://doi.org/10.1038/s41587-019-0071-9	journal	April 2019
Generalizing RNA velocity to transient cell states through dynamical modeling Bergen, Volker; Lange, Marius; Peidli, Stefan Nature Biotechnology, Vol. 38, Issue 12 https://doi.org/10.1038/s41587-020-0591-3	journal	August 2020
Modular, efficient and constant-memory single-cell RNA-seq preprocessing Melsted, Páll; Booeshaghi, A. Sina; Liu, Lauren Nature Biotechnology, Vol. 39, Issue 7 https://doi.org/10.1038/s41587-021-00870-2	journal	April 2021
Microfluidics-free single-cell genomics with templated emulsification Clark, Iain C.; Fontanez, Kristina M.; Meltzer, Robert H. Nature Biotechnology, Vol. 41, Issue 11 https://doi.org/10.1038/s41587-023-01685-z	journal	March 2023
The scverse project provides a computational ecosystem for single-cell omics data analysis Virshup, Isaac; Bredikhin, Danila; Heumos, Lukas Nature Biotechnology, Vol. 41, Issue 5 https://doi.org/10.1038/s41587-023-01733-8	journal	April 2023
Dictionary learning for integrative, multimodal and scalable single-cell analysis Hao, Yuhan; Stuart, Tim; Kowalski, Madeline H. Nature Biotechnology, Vol. 42, Issue 2 https://doi.org/10.1038/s41587-023-01767-y	journal	May 2023
Benchmarking atlas-level data integration in single-cell genomics Luecken, Malte D.; Büttner, M.; Chaichoompu, K. Nature Methods, Vol. 19, Issue 1 https://doi.org/10.1038/s41592-021-01336-8	journal	December 2021
Comparison of transformations for single-cell RNA-seq data Ahlmann-Eltze, Constantin; Huber, Wolfgang Nature Methods, Vol. 20, Issue 5 https://doi.org/10.1038/s41592-023-01814-1	journal	April 2023
Single-cell transcriptome sequencing of plant leaf expressing anti-HER2 VHH–FcK cancer therapeutic protein Kim, Myung-Shin; Lee, Seung-Won; Kim, Kibum Scientific Data, Vol. 10, Issue 1 https://doi.org/10.1038/s41597-023-02833-5	journal	December 2023
From Louvain to Leiden: guaranteeing well-connected communities Traag, V. A.; Waltman, L.; van Eck, N. J. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-41695-z	journal	March 2019
Lotus Base: An integrated information portal for the model legume Lotus japonicus Mun, Terry; Bachmann, Asger; Gupta, Vikas Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep39447	journal	December 2016
Advanced sequencing-based high-throughput and long-read single-cell transcriptome analysis Huang, Shanqing; Shi, Weixiong; Li, Shiyu Lab on a Chip, Vol. 24, Issue 10 https://doi.org/10.1039/D4LC00105B	journal	January 2024
Nuclear membranes control symbiotic calcium signaling of legumes Capoen, W.; Sun, J.; Wysham, D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 34 https://doi.org/10.1073/pnas.1107912108	journal	August 2011
Constitutive activation of a nuclear-localized calcium channel complex in Medicago truncatula Liu, Haiyue; Lin, Jie-Shun; Luo, Zhenpeng Proceedings of the National Academy of Sciences, Vol. 119, Issue 34 https://doi.org/10.1073/pnas.2205920119	journal	August 2022
Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Soltis, D. E.; Soltis, P. S.; Morgan, D. R. Proceedings of the National Academy of Sciences, Vol. 92, Issue 7 https://doi.org/10.1073/pnas.92.7.2647	journal	March 1995
Is the Legume Nodule a Modified Root or Stem or an Organsui generis? Hirsch, Ann M.; Larue, Thomas A.; Doyle, Jeff Critical Reviews in Plant Sciences, Vol. 16, Issue 4 https://doi.org/10.1080/07352689709701954	journal	January 1997
Fast unfolding of communities in large networks Blondel, Vincent D.; Guillaume, Jean-Loup; Lambiotte, Renaud Journal of Statistical Mechanics: Theory and Experiment, Vol. 2008, Issue 10 https://doi.org/10.1088/1742-5468/2008/10/P10008	journal	October 2008
Impacts of European livestock production: nitrogen, sulphur, phosphorus and greenhouse gas emissions, land-use, water eutrophication and biodiversity Leip, Adrian; Billen, Gilles; Garnier, Josette Environmental Research Letters, Vol. 10, Issue 11 https://doi.org/10.1088/1748-9326/10/11/115004	journal	November 2015
webSCST: an interactive web application for single-cell RNA-sequencing data and spatial transcriptomic data integration Zhang, Zilong; Cui, Feifei; Su, Wei Bioinformatics, Vol. 38, Issue 13 https://doi.org/10.1093/bioinformatics/btac350	journal	May 2022
Single-cell RNA-seq: advances and future challenges Saliba, Antoine-Emmanuel; Westermann, Alexander J.; Gorski, Stanislaw A. Nucleic Acids Research, Vol. 42, Issue 14 https://doi.org/10.1093/nar/gku555	journal	July 2014
scFTD-seq: freeze-thaw lysis based, portable approach toward highly distributed single-cell 3′ mRNA profiling Dura, Burak; Choi, Jin-Young; Zhang, Kerou Nucleic Acids Research, Vol. 47, Issue 3 https://doi.org/10.1093/nar/gky1173	journal	November 2018
GRACE: a comprehensive web-based platform for integrative single-cell transcriptome analysis Yu, Hao; Wang, Yuqing; Zhang, Xi NAR Genomics and Bioinformatics, Vol. 5, Issue 2 https://doi.org/10.1093/nargab/lqad050	journal	March 2023
MtExpress, a Comprehensive and Curated RNAseq-based Gene Expression Atlas for the Model Legume Medicago truncatula Carrere, Sebastien; Verdier, Jerome; Gamas, Pascal Plant and Cell Physiology, Vol. 62, Issue 9 https://doi.org/10.1093/pcp/pcab110	journal	July 2021
Evidence for phloem loading via the abaxial bundle sheath cells in maize leaves Bezrutczyk, Margaret; Zöllner, Nora R.; Kruse, Colin P. S. The Plant Cell, Vol. 33, Issue 3 https://doi.org/10.1093/plcell/koaa055	journal	January 2021
Leaf cell-specific and single-cell transcriptional profiling reveals a role for the palisade layer in UV light protection Procko, Carl; Lee, Travis; Borsuk, Aleca The Plant Cell, Vol. 34, Issue 9 https://doi.org/10.1093/plcell/koac167	journal	June 2022
Spatiotemporal cytokinin response imaging and ISOPENTENYLTRANSFERASE 3 function in Medicago nodule development Triozzi, Paolo M.; Irving, Thomas B.; Schmidt, Henry W. Plant Physiology, Vol. 188, Issue 1 https://doi.org/10.1093/plphys/kiab447	journal	September 2021
Single-cell genomics in plants: current state, future directions, and hurdles to overcome Cuperus, Josh T. Plant Physiology, Vol. 188, Issue 2 https://doi.org/10.1093/plphys/kiab478	journal	October 2021
Medicago truncatula IPD3 Is a Member of the Common Symbiotic Signaling Pathway Required for Rhizobial and Mycorrhizal Symbioses Horváth, Beatrix; Yeun, Li Huey; Domonkos, Ágota Molecular Plant-Microbe Interactions, Vol. 24, Issue 11 https://doi.org/10.1094/MPMI-01-11-0015	journal	November 2011
Laser Capture Microdissection Transcriptome Reveals Spatiotemporal Tissue Gene Expression Patterns of Medicago truncatula Roots Responding to Rhizobia Schnabel, Elise; Thomas, Jacklyn; El-Hawaz, Rabia Molecular Plant-Microbe Interactions®, Vol. 36, Issue 12 https://doi.org/10.1094/MPMI-03-23-0029-R	journal	December 2023
A Novel Nuclear Protein Interacts With the Symbiotic DMI3 Calcium- and Calmodulin-Dependent Protein Kinase of Medicago truncatula Messinese, Elsa; Mun, Jeong-Hwan; Yeun, Li Huey Molecular Plant-Microbe Interactions®, Vol. 20, Issue 8 https://doi.org/10.1094/MPMI-20-8-0912	journal	August 2007
Nodule Organogenesis and Symbiotic Mutants of the Model Legume Lotus japonicus Szczyglowski, Krzysztof; Shaw, Robert S.; Wopereis, Judith Molecular Plant-Microbe Interactions®, Vol. 11, Issue 7 https://doi.org/10.1094/MPMI.1998.11.7.684	journal	July 1998
STARsolo: accurate, fast and versatile mapping/quantification of single-cell and single-nucleus RNA-seq data Kaminow, Benjamin; Yunusov, Dinar; Dobin, Alexander bioRxiv https://doi.org/10.1101/2021.05.05.442755	preprint	May 2021
Defining cell types and states with single-cell genomics Trapnell, Cole Genome Research, Vol. 25, Issue 10 https://doi.org/10.1101/gr.190595.115	journal	October 2015
Finding and evaluating community structure in networks Newman, M. E. J.; Girvan, M. Physical Review E, Vol. 69, Issue 2 https://doi.org/10.1103/PhysRevE.69.026113	journal	February 2004
The Medicago truncatula Lysine Motif-Receptor-Like Kinase Gene Family Includes NFP and New Nodule-Expressed Genes Arrighi, Jean-François; Barre, Annick; Ben Amor, Besma Plant Physiology, Vol. 142, Issue 1 https://doi.org/10.1104/pp.106.084657	journal	July 2006
A Robust and Sensitive Synthetic Sensor to Monitor the Transcriptional Output of the Cytokinin Signaling Network in Planta Zürcher, Evelyne; Tavor-Deslex, Deborah; Lituiev, Dmytro Plant Physiology, Vol. 161, Issue 3 https://doi.org/10.1104/pp.112.211763	journal	January 2013
A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis Jardinaud, Marie-Françoise; Boivin, Stéphane; Rodde, Nathalie Plant Physiology, Vol. 171, Issue 3 https://doi.org/10.1104/pp.16.00711	journal	May 2016
DELLA1-Mediated Gibberellin Signaling Regulates Cytokinin-Dependent Symbiotic Nodulation Fonouni-Farde, Camille; Kisiala, Anna; Brault, Mathias Plant Physiology, Vol. 175, Issue 4 https://doi.org/10.1104/pp.17.00919	journal	October 2017
An ERF Transcription Factor in Medicago truncatula That Is Essential for Nod Factor Signal Transduction Middleton, Patrick H.; Jakab, Júlia; Penmetsa, R. Varma The Plant Cell, Vol. 19, Issue 4 https://doi.org/10.1105/tpc.106.048264	journal	April 2007
Lotus japonicus CASTOR and POLLUX Are Ion Channels Essential for Perinuclear Calcium Spiking in Legume Root Endosymbiosis Charpentier, Myriam; Bredemeier, Rolf; Wanner, Gerhard The Plant Cell, Vol. 20, Issue 12 https://doi.org/10.1105/tpc.108.063255	journal	December 2008
Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation Roy, Sonali; Liu, Wei; Nandety, Raja Sekhar The Plant Cell, Vol. 32, Issue 1 https://doi.org/10.1105/tpc.19.00279	journal	October 2019
On Modularity Clustering Brandes, U.; Delling, D.; Gaertler, M. IEEE Transactions on Knowledge and Data Engineering, Vol. 20, Issue 2 https://doi.org/10.1109/TKDE.2007.190689	journal	February 2008
A member of the highly conserved FWL (tomato FW2.2-like) gene family is essential for soybean nodule organogenesis: A soybean FWL essential for nodulation Libault, Marc; Zhang, Xue-Cheng; Govindarajulu, Manjula The Plant Journal, Vol. 62, Issue 5 https://doi.org/10.1111/j.1365-313X.2010.04201.x	journal	March 2010
Molecular Analysis of Legume Nodule Development and Autoregulation Ferguson, Brett J.; Indrasumunar, Arief; Hayashi, Satomi Journal of Integrative Plant Biology, Vol. 52, Issue 1 https://doi.org/10.1111/j.1744-7909.2010.00899.x	journal	January 2010
Single‐cell RNA sequencing reveals a high‐resolution cell atlas of xylem in Populus Li, Hui; Dai, Xinren; Huang, Xiong Journal of Integrative Plant Biology, Vol. 63, Issue 11 https://doi.org/10.1111/jipb.13159	journal	October 2021
Single‐cell RNA‐seq of Lotus japonicus provide insights into identification and function of root cell types of legume Sun, Zhanmin; Jiang, Sanjie; Wang, Dan Journal of Integrative Plant Biology, Vol. 65, Issue 5 https://doi.org/10.1111/jipb.13435	journal	January 2023
A high‐resolution transcriptomic atlas depicting nitrogen fixation and nodule development in soybean Sun, Baocheng; Wang, Yu; Yang, Qun Journal of Integrative Plant Biology, Vol. 65, Issue 6 https://doi.org/10.1111/jipb.13495	journal	May 2023
Single‐cell RNA sequencing profiles of stem‐differentiating xylem in poplar Xie, Jianbo; Li, Meng; Zeng, Jingyao Plant Biotechnology Journal, Vol. 20, Issue 3 https://doi.org/10.1111/pbi.13763	journal	December 2021
Single cell‐type transcriptome profiling reveals genes that promote nitrogen fixation in the infected and uninfected cells of legume nodules Wang, Longlong; Zhou, Yu; Li, Runhui Plant Biotechnology Journal, Vol. 20, Issue 4 https://doi.org/10.1111/pbi.13778	journal	January 2022
The Gm FWL1 ( FW2-2-like ) nodulation gene encodes a plasma membrane microdomain-associated protein: A FW2-2-like protein is located in plasma membrane microdomains Qiao, Zhenzhen; Brechenmacher, Laurent; Smith, Benjamin Plant, Cell & Environment, Vol. 40, Issue 8 https://doi.org/10.1111/pce.12941	journal	April 2017
Legume nodulation: The host controls the party Ferguson, Brett J.; Mens, Céline; Hastwell, April H. Plant, Cell & Environment, Vol. 42, Issue 1 https://doi.org/10.1111/pce.13348	journal	June 2018
An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing Roux, Brice; Rodde, Nathalie; Jardinaud, Marie-Françoise The Plant Journal, Vol. 77, Issue 6 https://doi.org/10.1111/tpj.12442	journal	February 2014
Spatial transcriptomics drives a new era in plant research Yin, Ruilian; Xia, Keke; Xu, Xun The Plant Journal, Vol. 116, Issue 6 https://doi.org/10.1111/tpj.16437	journal	August 2023
The Soybean Expression Atlas v2: A comprehensive database of over 5000 RNA‐seq samples Almeida‐Silva, Fabricio; Pedrosa‐Silva, Francisnei; Venancio, Thiago M. The Plant Journal, Vol. 116, Issue 4 https://doi.org/10.1111/tpj.16459	journal	September 2023
LysM Domain Receptor Kinases Regulating Rhizobial Nod Factor-Induced Infection Limpens, E. Science, Vol. 302, Issue 5645 https://doi.org/10.1126/science.1090074	journal	October 2003
Medicago truncatula DMI1 Required for Bacterial and Fungal Symbioses in Legumes Ane, J. -M. Science, Vol. 303, Issue 5662 https://doi.org/10.1126/science.1092986	journal	February 2004
A Putative Ca ²⁺ and Calmodulin-Dependent Protein Kinase Required for Bacterial and Fungal Symbioses Lévy, Julien; Bres, Cécile; Geurts, René Science, Vol. 303, Issue 5662 https://doi.org/10.1126/science.1093038	journal	February 2004
Nodulation Signaling in Legumes Requires NSP2, a Member of the GRAS Family of Transcriptional Regulators Kaló, Péter; Gleason, Cynthia; Edwards, Anne Science, Vol. 308, Issue 5729 https://doi.org/10.1126/science.1110951	journal	June 2005
NSP1 of the GRAS Protein Family Is Essential for Rhizobial Nod Factor-Induced Transcription Smit, Patrick; Raedts, John; Portyanko, Vladimir Science, Vol. 308, Issue 5729 https://doi.org/10.1126/science.1111025	journal	June 2005
A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes Peters, N.; Frost, J.; Long, S. Science, Vol. 233, Issue 4767 https://doi.org/10.1126/science.3738520	journal	August 1986
Single-cell profiling of the developing mouse brain and spinal cord with split-pool barcoding Rosenberg, Alexander B.; Roco, Charles M.; Muscat, Richard A. Science, Vol. 360, Issue 6385 https://doi.org/10.1126/science.aam8999	journal	March 2018
A shared gene drives lateral root development and root nodule symbiosis pathways in Lotus Soyano, Takashi; Shimoda, Yoshikazu; Kawaguchi, Masayoshi Science, Vol. 366, Issue 6468 https://doi.org/10.1126/science.aax2153	journal	November 2019
Ground tissue circuitry regulates organ complexity in maize and Setaria Ortiz-Ramírez, Carlos; Guillotin, Bruno; Xu, Xiaosa Science, Vol. 374, Issue 6572 https://doi.org/10.1126/science.abj2327	journal	December 2021
Brassinosteroid gene regulatory networks at cellular resolution in theArabidopsisroot Nolan, Trevor M.; Vukašinović, Nemanja; Hsu, Che-Wei Science, Vol. 379, Issue 6639 https://doi.org/10.1126/science.adf4721	journal	March 2023
The Mechanism of Biological Nitrogen Fixation Wilson, P. W.; Burris, R. H. Bacteriological Reviews, Vol. 11, Issue 1 https://doi.org/10.1128/br.11.1.41-73.1947	journal	March 1947
Anatomical analysis of the development and distribution of Rhizobium infections in soybean roots Calvert, Harry E.; Pence, Mark K.; Pierce, Margaret Canadian Journal of Botany, Vol. 62, Issue 11 https://doi.org/10.1139/b84-324	journal	November 1984
WGCNA: an R package for weighted correlation network analysis Langfelder, Peter; Horvath, Steve BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-559	journal	December 2008
Asc-Seurat: analytical single-cell Seurat-based web application Pereira, W. J.; Almeida, F. M.; Conde, D. BMC Bioinformatics, Vol. 22, Issue 1 https://doi.org/10.1186/s12859-021-04472-2	journal	November 2021
Slingshot: cell lineage and pseudotime inference for single-cell transcriptomics Street, Kelly; Risso, Davide; Fletcher, Russell B. BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4772-0	journal	June 2018
SCANPY: large-scale single-cell gene expression data analysis Wolf, F. Alexander; Angerer, Philipp; Theis, Fabian J. Genome Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s13059-017-1382-0	journal	February 2018
EmptyDrops: distinguishing cells from empty droplets in droplet-based single-cell RNA sequencing data Lun, Aaron T. L.; Riesenfeld, Samantha; Andrews, Tallulah Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1662-y	journal	March 2019
PAGA: graph abstraction reconciles clustering with trajectory inference through a topology preserving map of single cells Wolf, F. Alexander; Hamey, Fiona K.; Plass, Mireya Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1663-x	journal	March 2019
Vireo: Bayesian demultiplexing of pooled single-cell RNA-seq data without genotype reference Huang, Yuanhua; McCarthy, Davis J.; Stegle, Oliver Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1865-2	journal	December 2019
Over 1000 tools reveal trends in the single-cell RNA-seq analysis landscape Zappia, Luke; Theis, Fabian J. Genome Biology, Vol. 22, Issue 1 https://doi.org/10.1186/s13059-021-02519-4	journal	October 2021
Transcriptional landscape of highly lignified poplar stems at single-cell resolution Chen, Yang; Tong, Shaofei; Jiang, Yuanzhong Genome Biology, Vol. 22, Issue 1 https://doi.org/10.1186/s13059-021-02537-2	journal	November 2021
Single-cell transcriptomics unveils xylem cell development and evolution Tung, Chia-Chun; Kuo, Shang-Che; Yang, Chia-Ling Genome Biology, Vol. 24, Issue 1 https://doi.org/10.1186/s13059-022-02845-1	journal	January 2023
Fate map of Medicago truncatula root nodules Xiao, T. T.; Schilderink, S.; Moling, S. Development, Vol. 141, Issue 18 https://doi.org/10.1242/dev.110775	journal	September 2014
Gene expression variation in Arabidopsis embryos at single-nucleus resolution Kao, Ping; Schon, Michael A.; Mosiolek, Magdalena Development, Vol. 148, Issue 13 https://doi.org/10.1242/dev.199589	journal	July 2021
Single-nuclei transcriptome analysis of the shoot apex vascular system differentiation in Populus Conde, Daniel; Triozzi, Paolo M.; Pereira, Wendell J. Development, Vol. 149, Issue 21 https://doi.org/10.1242/dev.200632	journal	October 2022
Doublet identification in single-cell sequencing data using scDblFinder Germain, Pierre-Luc; Lun, Aaron; Macnair, Will F1000Research, Vol. 10 https://doi.org/10.12688/f1000research.73600.1	journal	September 2021
Dancing to a different tune, can we switch from chemical to biological nitrogen fixation for sustainable food security? Jhu, Min-Yao; Oldroyd, Giles E. D. PLOS Biology, Vol. 21, Issue 3 https://doi.org/10.1371/journal.pbio.3001982	journal	March 2023
Inferring Regulatory Networks from Expression Data Using Tree-Based Methods Huynh-Thu, Vân Anh; Irrthum, Alexandre; Wehenkel, Louis PLoS ONE, Vol. 5, Issue 9 https://doi.org/10.1371/journal.pone.0012776	journal	September 2010
RNA velocity—current challenges and future perspectives Bergen, Volker; Soldatov, Ruslan A.; Kharchenko, Peter V. Molecular Systems Biology, Vol. 17, Issue 8 https://doi.org/10.15252/msb.202110282	journal	August 2021
Gene expression variations and allele-specific expression of two rice and their hybrid in caryopses at single-nucleus resolution Zhou, Han; Deng, Xing Wang; He, Hang Frontiers in Plant Science, Vol. 14 https://doi.org/10.3389/fpls.2023.1171474	journal	May 2023
Single-Cell Transcriptome and Network Analyses Unveil Key Transcription Factors Regulating Mesophyll Cell Development in Maize Tao, Shentong; Liu, Peng; Shi, Yining Genes, Vol. 13, Issue 2 https://doi.org/10.3390/genes13020374	journal	February 2022
Current Progress in Nitrogen Fixing Plants and Microbiome Research Mahmud, Kishan; Makaju, Shiva; Ibrahim, Razi Plants, Vol. 9, Issue 1 https://doi.org/10.3390/plants9010097	journal	January 2020
UMAP: Uniform Manifold Approximation and Projection for Dimension Reduction McInnes, Leland; Healy, John; Melville, James arXiv https://doi.org/10.48550/arXiv.1802.03426	preprint	January 2018

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