Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis

Maximilian Griesmann; Yue Chang; Xin Liu; Yue Song; Georg Haberer; Matthew B. Crook; Benjamin Billault-Penneteau; Dominique Lauressergues; Jean Keller; Leandro Imanishi; Yuda Purwana Roswanjaya; Wouter Kohlen; Petar Pujic; Kai Battenberg; Nicole Alloisio; Yuhu Liang; Henk Hilhorst; Marco G. Salgado; Valerie Hocher; Hassen Gherbi; Sergio Svistoonoff; Jeff J. Doyle; Shixu He; Yan Xu; Shanyun Xu; Jing Qu; Qiang Gao; Xiaodong Fang; Yuan Fu; Philippe Normand; Alison M. Berry; Luis G. Wall; Jean Michel Ané; Katharina Pawlowski; Xun Xu; Huanming Yang; Manuel Spannagl; Klaus F.X. Mayer; Gane Ka Shu Wong; Martin Parniske; Pierre Marc Delaux; Shifeng Cheng

doi:10.1126/science.aat1743

Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis

Maximilian Griesmann, Yue Chang, Xin Liu, Yue Song, Georg Haberer, Matthew B. Crook, Benjamin Billault-Penneteau, Dominique Lauressergues, Jean Keller, Leandro Imanishi, Yuda Purwana Roswanjaya, Wouter Kohlen, Petar Pujic, Kai Battenberg, Nicole Alloisio, Yuhu Liang, Henk Hilhorst, Marco G. Salgado, Valerie Hocher, Hassen GherbiSergio Svistoonoff, Jeff J. Doyle, Shixu He, Yan Xu, Shanyun Xu, Jing Qu, Qiang Gao, Xiaodong Fang, Yuan Fu, Philippe Normand, Alison M. Berry, Luis G. Wall, Jean Michel Ané, Katharina Pawlowski, Xun Xu, Huanming Yang, Manuel Spannagl, Klaus F.X. Mayer, Gane Ka Shu Wong, Martin Parniske, Pierre Marc Delaux, Shifeng Cheng

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Abstract

The root nodule symbiosis of plants with nitrogen-fixing bacteria affects global nitrogen cycles and food production but is restricted to a subset of genera within a single clade of flowering plants. To explore the genetic basis for this scattered occurrence, we sequenced the genomes of 10 plant species covering the diversity of nodule morphotypes, bacterial symbionts, and infection strategies. In a genome-wide comparative analysis of a total of 37 plant species, we discovered signatures of multiple independent loss-of-function events in the indispensable symbiotic regulator NODULE INCEPTION in 10 of 13 genomes of nonnodulating species within this clade. The discovery that multiple independent losses shaped the present-day distribution of nitrogen-fixing root nodule symbiosis in plants reveals a phylogenetically wider distribution in evolutionary history and a so-far-underestimated selection pressure against this symbiosis.

Original language	English
Article number	eaat1743
Journal	Science
Volume	361
Issue number	6398
DOIs	https://doi.org/10.1126/science.aat1743
State	Published - 13 Jul 2018

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Griesmann, M., Chang, Y., Liu, X., Song, Y., Haberer, G., Crook, M. B., Billault-Penneteau, B., Lauressergues, D., Keller, J., Imanishi, L., Roswanjaya, Y. P., Kohlen, W., Pujic, P., Battenberg, K., Alloisio, N., Liang, Y., Hilhorst, H., Salgado, M. G., Hocher, V., ... Cheng, S. (2018). Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science, 361(6398), Article eaat1743. https://doi.org/10.1126/science.aat1743

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title = "Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis",

abstract = "The root nodule symbiosis of plants with nitrogen-fixing bacteria affects global nitrogen cycles and food production but is restricted to a subset of genera within a single clade of flowering plants. To explore the genetic basis for this scattered occurrence, we sequenced the genomes of 10 plant species covering the diversity of nodule morphotypes, bacterial symbionts, and infection strategies. In a genome-wide comparative analysis of a total of 37 plant species, we discovered signatures of multiple independent loss-of-function events in the indispensable symbiotic regulator NODULE INCEPTION in 10 of 13 genomes of nonnodulating species within this clade. The discovery that multiple independent losses shaped the present-day distribution of nitrogen-fixing root nodule symbiosis in plants reveals a phylogenetically wider distribution in evolutionary history and a so-far-underestimated selection pressure against this symbiosis.",

author = "Maximilian Griesmann and Yue Chang and Xin Liu and Yue Song and Georg Haberer and Crook, {Matthew B.} and Benjamin Billault-Penneteau and Dominique Lauressergues and Jean Keller and Leandro Imanishi and Roswanjaya, {Yuda Purwana} and Wouter Kohlen and Petar Pujic and Kai Battenberg and Nicole Alloisio and Yuhu Liang and Henk Hilhorst and Salgado, {Marco G.} and Valerie Hocher and Hassen Gherbi and Sergio Svistoonoff and Doyle, {Jeff J.} and Shixu He and Yan Xu and Shanyun Xu and Jing Qu and Qiang Gao and Xiaodong Fang and Yuan Fu and Philippe Normand and Berry, {Alison M.} and Wall, {Luis G.} and An{\'e}, {Jean Michel} and Katharina Pawlowski and Xun Xu and Huanming Yang and Manuel Spannagl and Mayer, {Klaus F.X.} and Wong, {Gane Ka Shu} and Martin Parniske and Delaux, {Pierre Marc} and Shifeng Cheng",

note = "Publisher Copyright: {\textcopyright} The Authors, some rights reserved.",

year = "2018",

month = jul,

day = "13",

doi = "10.1126/science.aat1743",

language = "English",

volume = "361",

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Griesmann, M, Chang, Y, Liu, X, Song, Y, Haberer, G, Crook, MB, Billault-Penneteau, B, Lauressergues, D, Keller, J, Imanishi, L, Roswanjaya, YP, Kohlen, W, Pujic, P, Battenberg, K, Alloisio, N, Liang, Y, Hilhorst, H, Salgado, MG, Hocher, V, Gherbi, H, Svistoonoff, S, Doyle, JJ, He, S, Xu, Y, Xu, S, Qu, J, Gao, Q, Fang, X, Fu, Y, Normand, P, Berry, AM, Wall, LG, Ané, JM, Pawlowski, K, Xu, X, Yang, H, Spannagl, M, Mayer, KFX, Wong, GKS, Parniske, M, Delaux, PM & Cheng, S 2018, 'Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis', Science, vol. 361, no. 6398, eaat1743. https://doi.org/10.1126/science.aat1743

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T1 - Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis

AU - Griesmann, Maximilian

AU - Chang, Yue

AU - Liu, Xin

AU - Song, Yue

AU - Haberer, Georg

AU - Crook, Matthew B.

AU - Billault-Penneteau, Benjamin

AU - Lauressergues, Dominique

AU - Keller, Jean

AU - Imanishi, Leandro

AU - Roswanjaya, Yuda Purwana

AU - Kohlen, Wouter

AU - Pujic, Petar

AU - Battenberg, Kai

AU - Alloisio, Nicole

AU - Liang, Yuhu

AU - Hilhorst, Henk

AU - Salgado, Marco G.

AU - Hocher, Valerie

AU - Gherbi, Hassen

AU - Svistoonoff, Sergio

AU - Doyle, Jeff J.

AU - He, Shixu

AU - Xu, Yan

AU - Xu, Shanyun

AU - Qu, Jing

AU - Gao, Qiang

AU - Fang, Xiaodong

AU - Fu, Yuan

AU - Normand, Philippe

AU - Berry, Alison M.

AU - Wall, Luis G.

AU - Ané, Jean Michel

AU - Pawlowski, Katharina

AU - Xu, Xun

AU - Yang, Huanming

AU - Spannagl, Manuel

AU - Mayer, Klaus F.X.

AU - Wong, Gane Ka Shu

AU - Parniske, Martin

AU - Delaux, Pierre Marc

AU - Cheng, Shifeng

PY - 2018/7/13

Y1 - 2018/7/13

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AB - The root nodule symbiosis of plants with nitrogen-fixing bacteria affects global nitrogen cycles and food production but is restricted to a subset of genera within a single clade of flowering plants. To explore the genetic basis for this scattered occurrence, we sequenced the genomes of 10 plant species covering the diversity of nodule morphotypes, bacterial symbionts, and infection strategies. In a genome-wide comparative analysis of a total of 37 plant species, we discovered signatures of multiple independent loss-of-function events in the indispensable symbiotic regulator NODULE INCEPTION in 10 of 13 genomes of nonnodulating species within this clade. The discovery that multiple independent losses shaped the present-day distribution of nitrogen-fixing root nodule symbiosis in plants reveals a phylogenetically wider distribution in evolutionary history and a so-far-underestimated selection pressure against this symbiosis.

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VL - 361

JO - Science

JF - Science

IS - 6398

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Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis

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