A two-step adaptive walk rewires nutrient transport in a challenging edaphic environment

Emmanuel Tergemina; Ahmed F. Elfarargi; Paulina Flis; Andrea Fulgione; Mehmet Göktay; Célia Neto; Marleen Scholle; Pádraic J. Flood; Sophie Asako Xerri; Johan Zicola; Nina Döring; Herculano Dinis; Ute Krämer; David E. Salt; Angela M. Hancock

doi:10.1126/sciadv.abm9385

A two-step adaptive walk rewires nutrient transport in a challenging edaphic environment

Emmanuel Tergemina^*, Ahmed F. Elfarargi, Paulina Flis, Andrea Fulgione, Mehmet Göktay, Célia Neto, Marleen Scholle, Pádraic J. Flood, Sophie Asako Xerri, Johan Zicola, Nina Döring, Herculano Dinis, Ute Krämer, David E. Salt, Angela M. Hancock

^*Corresponding author af dette arbejde

Afgrødevidenskab

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

13 Citationer (Scopus)

17 Downloads (Pure)

Abstract

Most well-characterized cases of adaptation involve single genetic loci. Theory suggests that multilocus adaptive walks should be common, but these are challenging to identify in natural populations. Here, we combine trait mapping with population genetic modeling to show that a two-step process rewired nutrient homeostasis in a population of Arabidopsis as it colonized the base of an active stratovolcano characterized by extremely low soil manganese (Mn). First, a variant that disrupted the primary iron (Fe) uptake transporter gene (IRT1) swept quickly to fixation in a hard selective sweep, increasing Mn but limiting Fe in the leaves. Second, multiple independent tandem duplications occurred at NRAMP1 and together rose to near fixation in the island population, compensating the loss of IRT1 by improving Fe homeostasis. This study provides a clear case of a multilocus adaptive walk and reveals how genetic variants reshaped a phenotype and spread over space and time.

Originalsprog	Engelsk
Artikelnummer	eabm9385
Tidsskrift	Science Advances
Vol/bind	8
Udgave nummer	20
Antal sider	15
ISSN	2375-2548
DOI	https://doi.org/10.1126/sciadv.abm9385
Status	Udgivet - 2022

Bibliografisk note

Funding Information:
We thank N. Barton, J. Hermisson, T. Karasov, and S. Laurent for comments on the manuscript. We thank the Instituto Nacional de Investigação e Desenvolvimento Agrário (INIDA) in Cape Verde, in particular, Â. Moreno, and the Max Planck Genome Center for performing the Nanopore sequencing and the digital PCR in this study. We thank B. Bizuayehu, B. Freiin von Loë, and P. Unger for technical assistance. We thank S. Young and S. Vazquez Reina from the Division of Agricultural and Environmental Sciences at the University of Nottingham for performing the ICP-MS analysis of the soil extracts. We thank P. Düchting and the Ruhr-Universität Bochum for the elemental analysis on plates. This work was supported by Max Planck Society funds, ERC-StG CVI_ADAPT 638810, and EPPN2020 CVI_ IONOMICS 114 to A.M.H. and by ERC-AdG 788380 LEAP-EXTREME to U.K. We thank the Max Planck Society for financial support and use of facilities.

Publisher Copyright:
Copyright © 2022 The Authors,

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Citationsformater

Tergemina, E., Elfarargi, A. F., Flis, P., Fulgione, A., Göktay, M., Neto, C., Scholle, M., Flood, P. J., Xerri, S. A., Zicola, J., Döring, N., Dinis, H., Krämer, U., Salt, D. E., & Hancock, A. M. (2022). A two-step adaptive walk rewires nutrient transport in a challenging edaphic environment. Science Advances, 8(20), Artikel eabm9385. https://doi.org/10.1126/sciadv.abm9385

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abstract = "Most well-characterized cases of adaptation involve single genetic loci. Theory suggests that multilocus adaptive walks should be common, but these are challenging to identify in natural populations. Here, we combine trait mapping with population genetic modeling to show that a two-step process rewired nutrient homeostasis in a population of Arabidopsis as it colonized the base of an active stratovolcano characterized by extremely low soil manganese (Mn). First, a variant that disrupted the primary iron (Fe) uptake transporter gene (IRT1) swept quickly to fixation in a hard selective sweep, increasing Mn but limiting Fe in the leaves. Second, multiple independent tandem duplications occurred at NRAMP1 and together rose to near fixation in the island population, compensating the loss of IRT1 by improving Fe homeostasis. This study provides a clear case of a multilocus adaptive walk and reveals how genetic variants reshaped a phenotype and spread over space and time.",

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AU - Fulgione, Andrea

AU - Göktay, Mehmet

AU - Neto, Célia

AU - Scholle, Marleen

AU - Flood, Pádraic J.

AU - Xerri, Sophie Asako

AU - Zicola, Johan

AU - Döring, Nina

AU - Dinis, Herculano

AU - Krämer, Ute

AU - Salt, David E.

AU - Hancock, Angela M.

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AB - Most well-characterized cases of adaptation involve single genetic loci. Theory suggests that multilocus adaptive walks should be common, but these are challenging to identify in natural populations. Here, we combine trait mapping with population genetic modeling to show that a two-step process rewired nutrient homeostasis in a population of Arabidopsis as it colonized the base of an active stratovolcano characterized by extremely low soil manganese (Mn). First, a variant that disrupted the primary iron (Fe) uptake transporter gene (IRT1) swept quickly to fixation in a hard selective sweep, increasing Mn but limiting Fe in the leaves. Second, multiple independent tandem duplications occurred at NRAMP1 and together rose to near fixation in the island population, compensating the loss of IRT1 by improving Fe homeostasis. This study provides a clear case of a multilocus adaptive walk and reveals how genetic variants reshaped a phenotype and spread over space and time.

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