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 estab...

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Main Authors: 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
Format: Article
Language:English
Published: Nature Portfolio 2023-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-42911-1
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author 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
author_facet 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
author_sort Manuel Frank
collection DOAJ
description 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.
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spelling doaj.art-51e452f000a84be9a0cd5533069c71842023-11-12T12:22:37ZengNature PortfolioNature Communications2041-17232023-11-0114111110.1038/s41467-023-42911-1Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicusManuel Frank0Lavinia Ioana Fechete1Francesca Tedeschi2Marcin Nadzieja3Malita Malou Malekzadeh Nørgaard4Jesus Montiel5Kasper Røjkjær Andersen6Mikkel H. Schierup7Dugald Reid8Stig Uggerhøj Andersen9Department of Molecular Biology and Genetics, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityBioinformatics Research Centre, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityAbstract 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.https://doi.org/10.1038/s41467-023-42911-1
spellingShingle 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
Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus
Nature Communications
title Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus
title_full Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus
title_fullStr Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus
title_full_unstemmed Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus
title_short Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus
title_sort single cell analysis identifies genes facilitating rhizobium infection in lotus japonicus
url https://doi.org/10.1038/s41467-023-42911-1
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