Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus

Manuel Frank; Lavinia Ioana Fechete; Francesca Tedeschi; Marcin Nadzieja; Malita Malou Malekzadeh Nørgaard; Jesus Montiel; Kasper Røjkjær Andersen; Mikkel H Schierup; Dugald Reid; Stig Uggerhøj Andersen

doi:10.1038/s41467-023-42911-1

Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus

Manuel Frank, Lavinia Ioana Fechete, Francesca Tedeschi, Marcin Nadzieja, Malita Malou Malekzadeh Nørgaard, Jesus Montiel, Kasper Røjkjær Andersen, Mikkel H Schierup, Dugald Reid^*, Stig Uggerhøj Andersen^*

^*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

Legume-rhizobium signaling during establishment of symbiotic nitrogen fixation restricts rhizobium colonization to specific cells. A limited number of root hair cells allow infection threads to form, and only a fraction of the epidermal infection threads progress to cortical layers to establish functional nodules. Here we use single-cell analysis to define the epidermal and cortical cell populations that respond to and facilitate rhizobium infection. We then identify high-confidence nodulation gene candidates based on their specific expression in these populations, pinpointing genes stably associated with infection across genotypes and time points. We show that one of these, which we name SYMRKL1, encodes a protein with an ectodomain predicted to be nearly identical to that of SYMRK and is required for normal infection thread formation. Our work disentangles cellular processes and transcriptional modules that were previously confounded due to lack of cellular resolution, providing a more detailed understanding of symbiotic interactions.

Original language	English
Article number	7171
Journal	Nature Communications
Volume	14
Issue	1
ISSN	2041-1723
DOIs	https://doi.org/10.1038/s41467-023-42911-1
Publication status	Published - Dec 2023

Keywords

Rhizobium/metabolism
Root Nodules, Plant/metabolism
Lotus/metabolism
Plant Proteins/genetics
Phenotype
Symbiosis/genetics
Single-Cell Analysis
Gene Expression Regulation, Plant
Plant Roots/metabolism

Access to Document

10.1038/s41467-023-42911-1Licence: CC BY

Cite this

@article{648516d02f3f4a6982181a955007bb1b,

title = "Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus",

abstract = "Legume-rhizobium signaling during establishment of symbiotic nitrogen fixation restricts rhizobium colonization to specific cells. A limited number of root hair cells allow infection threads to form, and only a fraction of the epidermal infection threads progress to cortical layers to establish functional nodules. Here we use single-cell analysis to define the epidermal and cortical cell populations that respond to and facilitate rhizobium infection. We then identify high-confidence nodulation gene candidates based on their specific expression in these populations, pinpointing genes stably associated with infection across genotypes and time points. We show that one of these, which we name SYMRKL1, encodes a protein with an ectodomain predicted to be nearly identical to that of SYMRK and is required for normal infection thread formation. Our work disentangles cellular processes and transcriptional modules that were previously confounded due to lack of cellular resolution, providing a more detailed understanding of symbiotic interactions.",

keywords = "Rhizobium/metabolism, Root Nodules, Plant/metabolism, Lotus/metabolism, Plant Proteins/genetics, Phenotype, Symbiosis/genetics, Single-Cell Analysis, Gene Expression Regulation, Plant, Plant Roots/metabolism",

author = "Manuel Frank and Fechete, {Lavinia Ioana} and Francesca Tedeschi and Marcin Nadzieja and N{\o}rgaard, {Malita Malou Malekzadeh} and Jesus Montiel and Andersen, {Kasper R{\o}jkj{\ae}r} and Schierup, {Mikkel H} and Dugald Reid and Andersen, {Stig Uggerh{\o}j}",

year = "2023",

month = dec,

doi = "10.1038/s41467-023-42911-1",

language = "English",

volume = "14",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Springer Nature",

number = "1",

}

TY - JOUR

T1 - Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus

AU - Frank, Manuel

AU - Fechete, Lavinia Ioana

AU - Tedeschi, Francesca

AU - Nadzieja, Marcin

AU - Nørgaard, Malita Malou Malekzadeh

AU - Montiel, Jesus

AU - Andersen, Kasper Røjkjær

AU - Schierup, Mikkel H

AU - Reid, Dugald

AU - Andersen, Stig Uggerhøj

PY - 2023/12

Y1 - 2023/12

N2 - Legume-rhizobium signaling during establishment of symbiotic nitrogen fixation restricts rhizobium colonization to specific cells. A limited number of root hair cells allow infection threads to form, and only a fraction of the epidermal infection threads progress to cortical layers to establish functional nodules. Here we use single-cell analysis to define the epidermal and cortical cell populations that respond to and facilitate rhizobium infection. We then identify high-confidence nodulation gene candidates based on their specific expression in these populations, pinpointing genes stably associated with infection across genotypes and time points. We show that one of these, which we name SYMRKL1, encodes a protein with an ectodomain predicted to be nearly identical to that of SYMRK and is required for normal infection thread formation. Our work disentangles cellular processes and transcriptional modules that were previously confounded due to lack of cellular resolution, providing a more detailed understanding of symbiotic interactions.

AB - Legume-rhizobium signaling during establishment of symbiotic nitrogen fixation restricts rhizobium colonization to specific cells. A limited number of root hair cells allow infection threads to form, and only a fraction of the epidermal infection threads progress to cortical layers to establish functional nodules. Here we use single-cell analysis to define the epidermal and cortical cell populations that respond to and facilitate rhizobium infection. We then identify high-confidence nodulation gene candidates based on their specific expression in these populations, pinpointing genes stably associated with infection across genotypes and time points. We show that one of these, which we name SYMRKL1, encodes a protein with an ectodomain predicted to be nearly identical to that of SYMRK and is required for normal infection thread formation. Our work disentangles cellular processes and transcriptional modules that were previously confounded due to lack of cellular resolution, providing a more detailed understanding of symbiotic interactions.

KW - Rhizobium/metabolism

KW - Root Nodules, Plant/metabolism

KW - Lotus/metabolism

KW - Plant Proteins/genetics

KW - Phenotype

KW - Symbiosis/genetics

KW - Single-Cell Analysis

KW - Gene Expression Regulation, Plant

KW - Plant Roots/metabolism

UR - http://www.scopus.com/inward/record.url?scp=85175971685&partnerID=8YFLogxK

U2 - 10.1038/s41467-023-42911-1

DO - 10.1038/s41467-023-42911-1

M3 - Journal article

C2 - 37935666

SN - 2041-1723

VL - 14

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 7171

ER -

Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus

Abstract

Keywords

Access to Document

Other files and links

Fingerprint

Cite this