Spatial co-transcriptomics reveals discrete stages of the arbuscular mycorrhizal symbiosis

Serrano, Karen; Bezrutczyk, Margaret; Goudeau, Danielle; Dao, Thai; O’Malley, Ronan; Malmstrom, Rex R.; Visel, Axel; Scheller, Henrik V.; Cole, Benjamin

doi:10.1038/s41477-024-01666-3

Title: Spatial co-transcriptomics reveals discrete stages of the arbuscular mycorrhizal symbiosis

Journal Article · Mon Apr 08 00:00:00 EDT 2024 · Nature Plants (Online)

DOI:https://doi.org/10.1038/s41477-024-01666-3· OSTI ID:2335524

; Bezrutczyk, Margaret; Goudeau, Danielle; Dao, Thai;

;

Abstract The symbiotic interaction of plants with arbuscular mycorrhizal (AM) fungi is ancient and widespread. Plants provide AM fungi with carbon in exchange for nutrients and water, making this interaction a prime target for crop improvement. However, plant–fungal interactions are restricted to a small subset of root cells, precluding the application of most conventional functional genomic techniques to study the molecular bases of these interactions. Here we used single-nucleus and spatial RNA sequencing to explore both Medicago truncatula and Rhizophagus irregularis transcriptomes in AM symbiosis at cellular and spatial resolution. Integrated, spatially registered single-cell maps revealed infected and uninfected plant root cell types. We observed that cortex cells exhibit distinct transcriptome profiles during different stages of colonization by AM fungi, indicating dynamic interplay between both organisms during establishment of the cellular interface enabling successful symbiosis. Our study provides insight into a symbiotic relationship of major agricultural and environmental importance and demonstrates a paradigm combining single-cell and spatial transcriptomics for the analysis of complex organismal interactions.

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Sponsoring Organization:: USDOE

OSTI ID:: 2335524

Journal Information:: Nature Plants (Online), Journal Name: Nature Plants (Online) Vol. 10 Journal Issue: 4; ISSN 2055-0278

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Insights into the complex role of GRAS transcription factors in the arbuscular mycorrhiza symbiosis Hartmann, Rico M.; Schaepe, Sieke; Nübel, Daniel Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-40214-4	journal	March 2019
An improved genome release (version Mt4.0) for the model legume Medicago truncatula Tang, Haibao; Krishnakumar, Vivek; Bidwell, Shelby BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-312	journal	January 2014
Ectopic activation of cortical cell division during the accommodation of arbuscular mycorrhizal fungi Russo, Giulia; Carotenuto, Gennaro; Fiorilli, Valentina New Phytologist, Vol. 221, Issue 2 https://doi.org/10.1111/nph.15398	journal	August 2018
A lysin motif effector subverts chitin‐triggered immunity to facilitate arbuscular mycorrhizal symbiosis Zeng, Tian; Rodriguez‐Moreno, Luis; Mansurkhodzaev, Artem New Phytologist, Vol. 225, Issue 1 https://doi.org/10.1111/nph.16245	journal	November 2019
Role of Cytochrome P450 Enzyme in Plant Microorganisms’ Communication: A Focus on Grapevine Minerdi, Daniela; Savoi, Stefania; Sabbatini, Paolo International Journal of Molecular Sciences, Vol. 24, Issue 5 https://doi.org/10.3390/ijms24054695	journal	February 2023
A H+-ATPase That Energizes Nutrient Uptake during Mycorrhizal Symbioses in Rice and Medicago truncatula Wang, Ertao; Yu, Nan; Bano, S. Asma The Plant Cell, Vol. 26, Issue 4 https://doi.org/10.1105/tpc.113.120527	journal	April 2014
PANTHER: Making genome‐scale phylogenetics accessible to all Thomas, Paul D.; Ebert, Dustin; Muruganujan, Anushya Protein Science, Vol. 31, Issue 1, p. 8-22 https://doi.org/10.1002/pro.4218	journal	October 2021
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Earliest Colonization Events of Rhizophagus irregularis in Rice Roots Occur Preferentially in Previously Uncolonized Cells Kobae, Yoshihiro; Fujiwara, Toru Plant and Cell Physiology, Vol. 55, Issue 8 https://doi.org/10.1093/pcp/pcu081	journal	June 2014
Medicago truncatula NIN Is Essential for Rhizobial-Independent Nodule Organogenesis Induced by Autoactive Calcium/Calmodulin-Dependent Protein Kinase Marsh, John F.; Rakocevic, Alexandra; Mitra, Raka M. Plant Physiology, Vol. 144, Issue 1 https://doi.org/10.1104/pp.106.093021	journal	March 2007
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Distinct identities of leaf phloem cells revealed by single cell transcriptomics Kim, Ji-Yun; Symeonidi, Efthymia; Pang, Tin Yau The Plant Cell, Vol. 33, Issue 3 https://doi.org/10.1093/plcell/koaa060	journal	January 2021

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