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 · 07 April 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

Grant/Contract Number:: NONE; AC02-05CH11231

OSTI ID:: 2335524

Alternate ID(s):: OSTI ID: 2340108

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

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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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
Three Common Symbiotic ABC Subfamily B Transporters inMedicago truncatulaAre Regulated by a NIN-Independent Branch of the Symbiosis Signaling Pathway Roy, Sonali; Breakspear, Andrew; Cousins, Donna Molecular Plant-Microbe Interactions®, Vol. 34, Issue 8 https://doi.org/10.1094/MPMI-02-21-0036-R	journal	August 2021
KIN3 impacts arbuscular mycorrhizal symbiosis and promotes fungal colonisation in Medicago truncatula Irving, Thomas B.; Chakraborty, Sanhita; Ivanov, Sergey The Plant Journal, Vol. 110, Issue 2 https://doi.org/10.1111/tpj.15685	journal	March 2022
Spatially Resolved Transcriptomes—Next Generation Tools for Tissue Exploration Asp, Michaela; Bergenstråhle, Joseph; Lundeberg, Joakim BioEssays, Vol. 42, Issue 10 https://doi.org/10.1002/bies.201900221	journal	May 2020
Nutrient Exchange and Regulation in Arbuscular Mycorrhizal Symbiosis Wang, Wanxiao; Shi, Jincai; Xie, Qiujin Molecular Plant, Vol. 10, Issue 9 https://doi.org/10.1016/j.molp.2017.07.012	journal	September 2017
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
The Comparison of Expressed Candidate Secreted Proteins from Two Arbuscular Mycorrhizal Fungi Unravels Common and Specific Molecular Tools to Invade Different Host Plants Kamel, Laurent; Tang, Nianwu; Malbreil, Mathilde Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00124	journal	February 2017
The CLE53–SUNN genetic pathway negatively regulates arbuscular mycorrhiza root colonization in Medicago truncatula Karlo, Magda; Boschiero, Clarissa; Landerslev, Katrine Gram Journal of Experimental Botany, Vol. 71, Issue 16 https://doi.org/10.1093/jxb/eraa193	journal	April 2020
A transcriptional activator from Rhizophagus irregularis regulates phosphate uptake and homeostasis in AM symbiosis during phosphorous starvation Zhang, Shuyuan; Nie, Yuying; Fan, Xiaoning Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.1114089	journal	January 2023
The Mutualistic Interaction between Plants and Arbuscular Mycorrhizal Fungi Lanfranco, Luisa; Bonfante, Paola; Genre, Andrea Microbiology Spectrum, Vol. 4, Issue 6 https://doi.org/10.1128/microbiolspec.FUNK-0012-2016	journal	December 2016
Evidence of non-tandemly repeated rDNAs and their intragenomic heterogeneity in Rhizophagus irregularis Maeda, Taro; Kobayashi, Yuuki; Kameoka, Hiromu Communications Biology, Vol. 1, Issue 1 https://doi.org/10.1038/s42003-018-0094-7	journal	July 2018
Spatiotemporal Developmental Trajectories in the Arabidopsis Root Revealed Using High-Throughput Single-Cell RNA Sequencing Denyer, Tom; Ma, Xiaoli; Klesen, Simon Developmental Cell, Vol. 48, Issue 6 https://doi.org/10.1016/j.devcel.2019.02.022	journal	March 2019
Molecular and Cellular Aspects of the Arbuscular Mycorrhizal Symbiosis Harrison, Maria J. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.arplant.50.1.361	journal	June 1999

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