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Comparative Phylogenomics Uncovers The Impact Of Symbiotic Associations On Host Genome Evolution

Pierre-Marc Delaux, Kranthi Varala, P. Edger, G. Coruzzi, J. Pires, Jean-Michel Ané
Published 2014 · Biology, Medicine

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Mutualistic symbioses between eukaryotes and beneficial microorganisms of their microbiome play an essential role in nutrition, protection against disease, and development of the host. However, the impact of beneficial symbionts on the evolution of host genomes remains poorly characterized. Here we used the independent loss of the most widespread plant–microbe symbiosis, arbuscular mycorrhization (AM), as a model to address this question. Using a large phenotypic approach and phylogenetic analyses, we present evidence that loss of AM symbiosis correlates with the loss of many symbiotic genes in the Arabidopsis lineage (Brassicales). Then, by analyzing the genome and/or transcriptomes of nine other phylogenetically divergent non-host plants, we show that this correlation occurred in a convergent manner in four additional plant lineages, demonstrating the existence of an evolutionary pattern specific to symbiotic genes. Finally, we use a global comparative phylogenomic approach to track this evolutionary pattern among land plants. Based on this approach, we identify a set of 174 highly conserved genes and demonstrate enrichment in symbiosis-related genes. Our findings are consistent with the hypothesis that beneficial symbionts maintain purifying selection on host gene networks during the evolution of entire lineages.
This paper references
10.1126/SCIENCE.289.5486.1920
Glomalean fungi from the Ordovician.
D. Redecker (2000)
10.1080/00380768.2001.10408433
Arbuscular mycorrhizal colonization in Lupinus and related genera
H. Oba (2001)
10.1007/s00572-004-0314-5
Red list plants: colonization by arbuscular mycorrhizal fungi and dark septate endophytes
B. Fuchs (2004)
10.1080/10635150590947131
Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary.
M. Lavin (2005)
10.1007/s00438-005-0057-9
Significant microsynteny with new evolutionary highlights is detected between Arabidopsis and legume model plants despite the lack of macrosynteny
Zoltán Kevei (2005)
10.1111/J.1365-313X.2005.02364.X
The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species.
R. Nagy (2005)
10.1093/AOB/MCL154
Nitrogen fixation by white lupin under phosphorus deficiency.
J. Schulze (2006)
10.1126/science.1128691
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
G. Tuskan (2006)
10.1111/J.1095-8339.2006.00580.X
The systematic relationships of glucosinolate‐producing plants and related families: a cladistic investigation based on morphological and molecular characters
L. R. D. Craene (2006)
10.1007/s00572-006-0081-6
Mycorrhizal and dark septate endophytic fungi of Pedicularis species from northwest of Yunnan Province, China
Ai-Rong Li (2006)
10.1534/genetics.105.051185
Tracing Nonlegume Orthologs of Legume Genes Required for Nodulation and Arbuscular Mycorrhizal Symbioses
Hongyan Zhu (2006)
fungi and dark septate endophytes
AR Li (2007)
10.1186/1471-2229-9-10
Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis
S. K. Gomez (2008)
10.1073/pnas.0710618105
SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria
H. Gherbi (2008)
10.1038/nature07271
Strigolactone inhibition of shoot branching
V. Gómez-Roldán (2008)
10.1126/science.1155725
Evolution of Mammals and Their Gut Microbes
R. Ley (2008)
10.1016/j.cell.2008.01.003
Evo-Devo: Variations on Ancestral Themes
E. Robertis (2008)
10.1104/pp.108.124867
Finding and Comparing Syntenic Regions among Arabidopsis and the Outgroups Papaya, Poplar, and Grape: CoGe with Rosids1[W]
Eric Lyons (2008)
10.1038/nrmicro1987
Arbuscular mycorrhiza: the mother of plant root endosymbioses
M. Parniske (2008)
10.1111/j.1365-313X.2008.03575.x
Knock-down of the MEP pathway isogene 1-deoxy-D-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids, and abolishes normal expression of mycorrhiza-specific plant marker genes.
D. Floss (2008)
and dark septate endophytic fungi of Pedicularis species from northwest of Yunnan Province , China
H Gherbi (2008)
10.1126/science.1171644
Reprogramming Plant Cells for Endosymbiosis
G. Oldroyd (2009)
10.1038/nature08530
Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43
K. Maslowski (2009)
10.1890/07-2080.1
Arbuscular mycorrhizal fungi ameliorate temperature stress in thermophilic plants.
Rebecca A Bunn (2009)
10.1016/j.plaphy.2010.08.010
Symbiotic interactions between arbuscular mycorrhizal (AM) fungi and male papaya plants: its status, role and implications.
S. W. Khade (2010)
10.1038/NCOMMS1105
Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants.
Claire P Humphreys (2010)
10.1186/1471-2164-13-316
Development and validation of genic-SSR markers in sesame by RNA-seq
H. Zhang (2011)
10.1105/tpc.111.089771
Strigolactone Biosynthesis in Medicago truncatula and Rice Requires the Symbiotic GRAS-Type Transcription Factors NSP1 and NSP2[W][OA]
Wei Liu (2011)
10.1126/science.1208473
Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis
E. Kiers (2011)
10.1038/nature10158
Genome sequence and analysis of the tuber crop potato
Xun Xu (2011)
10.1371/journal.pgen.1002411
A Functional Phylogenomic View of the Seed Plants
Ernest K. Lee (2011)
10.1093/molbev/msr121
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.
K. Tamura (2011)
10.1093/jxb/erq335
The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events
Coline Balzergue (2011)
10.1016/j.cub.2011.11.011
Transcriptomes of the Parasitic Plant Family Orobanchaceae Reveal Surprising Conservation of Chlorophyll Synthesis
N. Wickett (2011)
Genome sequence and analysis of the tuber crop
X Xu (2011)
10.1371/journal.pone.0036234
Digital Gene Expression Analysis Based on Integrated De Novo Transcriptome Assembly of Sweet Potato [Ipomoea batatas (L.) Lam.]
X. Tao (2012)
10.1016/j.cub.2012.09.043
A Common Signaling Process that Promotes Mycorrhizal and Oomycete Colonization of Plants
Ertao Wang (2012)
10.1111/j.1365-313X.2012.05099.x
The microRNA miR171h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2.
D. Lauressergues (2012)
10.1016/j.cell.2012.04.037
Gut Immune Maturation Depends on Colonization with a Host-Specific Microbiota
H. Chung (2012)
10.1126/science.1223490
Interactions Between the Microbiota and the Immune System
L. Hooper (2012)
10.1371/journal.pbio.1001424
The Evolution of Mutualism in Gut Microbiota Via Host Epithelial Selection
Jonas Schluter (2012)
10.1074/mcp.M112.019208
Rapid Phosphoproteomic and Transcriptomic Changes in the Rhizobia-legume Symbiosis*
C. Rose (2012)
10.1038/nature11552
Functional interactions between the gut microbiota and host metabolism
V. Tremaroli (2012)
10.1073/pnas.1110215109
Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion
N. Pumplin (2012)
10.1105/tpc.112.098475
The Recent Evolution of a Symbiotic Ion Channel in the Legume Family Altered Ion Conductance and Improved Functionality in Calcium Signaling[C][W]
M. Venkateshwaran (2012)
10.1038/nature11119
The tomato genome sequence provides insights into fleshy fruit evolution
S. Sato (2012)
10.1186/1471-2164-13-571
De novo assembly of the pepper transcriptome (Capsicum annuum): a benchmark for in silico discovery of SNPs, SSRs and candidate genes
H. Ashrafi (2012)
The Amborella Genome and the Evolution of Flowering Plants
Steve Rounsley (2013)
10.3732/ajb.1200474
How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae).
H. Lambers (2013)
10.1371/journal.pone.0073767
De Novo Assembly of the Peanut (Arachis hypogaea L.) Seed Transcriptome Revealed Candidate Unigenes for Oil Accumulation Pathways
Dongmei Yin (2013)
10.1371/journal.pone.0064799
Draft Genome Sequence, and a Sequence-Defined Genetic Linkage Map of the Legume Crop Species Lupinus angustifolius L
H. Yang (2013)
10.1111/nph.12340
NSP1 is a component of the Myc signaling pathway.
P. Delaux (2013)
10.1111/pce.12102
Arbuscular mycorrhizal fungi reduce growth and infect roots of the non-host plant Arabidopsis thaliana.
RITA S. L. Veiga (2013)
10.1016/j.tplants.2013.01.008
Evolution of the plant-microbe symbiotic 'toolkit'.
P. Delaux (2013)
10.1073/pnas.1219690110
Disruption of the petal identity gene APETALA3-3 is highly correlated with loss of petals within the buttercup family (Ranunculaceae)
R. Zhang (2013)
10.1111/pce.12117
Interactions between arbuscular mycorrhizal and non-mycorrhizal plants: do non-mycorrhizal species at both extremes of nutrient availability play the same game?
H. Lambers (2013)
10.1126/science.1240537
The Intestinal Microbiota Modulates the Anticancer Immune Effects of Cyclophosphamide
S. Viaud (2013)
10.1126/science.1241089
The Amborella Genome and the Evolution of Flowering Plants
Amborella Genome (2013)
10.4161/psb.25637
Sl-IAA27 gene expression is induced during arbuscular mycorrhizal symbiosis in tomato and in Medicago truncatula
C. Bassa (2013)
10.1111/nph.12198
NFP, a LysM protein controlling Nod factor perception, also intervenes in Medicago truncatula resistance to pathogens.
T. Rey (2013)
10.1038/nature12132
Architecture and evolution of a minute plant genome
E. Ibarra-Laclette (2013)
10.1126/science.340.6137.1156-a
Mysteries of development.
J. Travis (2013)
10.1126/science.340.6137.1159
Mysteries of development. How do microbes shape animal development?
E. Pennisi (2013)
10.1104/pp.113.234864
De Novo Assembly and Characterization of the Transcriptome of the Parasitic Weed Dodder Identifies Genes Associated with Plant Parasitism1[C][W][OPEN]
A. Ranjan (2014)
10.1111/nph.12636
The symbiotic transcription factor MtEFD and cytokinins are positively acting in the Medicago truncatula and Ralstonia solanacearum pathogenic interaction.
S. Moreau (2014)
R: A language and environment for statistical computing.
R. Team (2014)
10.1038/nature12817
The genome of the recently domesticated crop plant sugar beet (Beta vulgaris)
J. Dohm (2014)
De novo assembly and characterization of the transcriptome of the parasitic weed Cuscuta pentagona identifies genes associated with plant parasitism
A Ranjan (2014)



This paper is referenced by
10.1007/s11103-021-01143-x
A coumarin exudation pathway mitigates arbuscular mycorrhizal incompatibility in Arabidopsis thaliana.
M. Cosme (2021)
10.1093/gbe/evab042
A De Novo Transcriptome Assembly of Ceratopteris richardii Provides Insights into the Evolutionary Dynamics of Complex Gene Families in Land Plants
Y. Geng (2021)
10.1101/2021.02.18.431885
Detailed characterization of the UMAMITs provides insight into their evolution, functional properties as amino acid transporters and role in the plant
Chengsong Zhao (2021)
10.3389/fmicb.2021.645784
Soil Microsite Outweighs Cultivar Genotype Contribution to Brassica Rhizobacterial Community Structure
Scott A. Klasek (2021)
10.1038/s41598-021-93626-6
Important innate differences in determining symbiotic responsiveness in host and non-hosts of arbuscular mycorrhiza
Shalini Vasan (2021)
10.1126/science.aba6605
Plant evolution driven by interactions with symbiotic and pathogenic microbes
Pierre-Marc Delaux (2021)
10.1007/978-3-030-51849-3_15
Early Molecular Dialogue Between Legumes and Rhizobia: Why Are They So Important?
Oswaldo Valdés-López (2020)
10.1038/s41396-020-0606-6
Genetic variation and evolutionary history of a mycorrhizal fungus regulate the currency of exchange in symbiosis with the food security crop cassava
R. Savary (2020)
10.1007/s00572-020-00997-1
Ignored diversity of arbuscular mycorrhizal fungi in co-occurring mycotrophic and non-mycotrophic plants
Yutao Wang (2020)
10.1093/nar/gkaa1041
A network-based comparative framework to study conservation and divergence of proteomes in plant phylogenies
Junha Shin (2020)
10.1002/9781119505457.CH3
Seed Microbiome and Its Implication in Plant Growth Promotion and Health
P. Tallapragada (2020)
10.1038/s41477-020-0613-7
An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages
Guru V. Radhakrishnan (2020)
10.1007/s00572-020-00978-4
The arbuscular mycorrhizal mycelium from barley differentially influences various defense parameters in the non-host sugar beet under co-cultivation
R. Hajiboland (2020)
10.1016/j.xplc.2019.100019
A Roadmap toward Engineered Nitrogen-Fixing Nodule Symbiosis
R. Huisman (2020)
10.1111/mpp.12983
Structural specificity in plant–filamentous pathogen interactions
Aline Lacaze (2020)
10.1101/2020.07.25.221283
Arabidopsis thaliana interaction with Ensifer meliloti can support plant growth under N-deficiency
Grace Armijo (2020)
10.1111/nph.16729
Independent evolutionary changes in fine-root traits among main clades during the diversification of seed plants.
O. Valverde-Barrantes (2020)
10.1007/s11104-020-04627-9
Resolving the mycorrhizal status of important northern hemisphere trees
M. Brundrett (2020)
10.1007/s00572-020-00934-2
Orchids and their mycorrhizal fungi: an insufficiently explored relationship
Quentin Favre-Godal (2020)
10.1101/2020.03.26.009910
Developmental atlas of white lupin cluster roots
Cécilia Gallardo (2020)
10.1002/ecs2.3100
Indolic glucosinolate pathway provides resistance to mycorrhizal fungal colonization in a non‐host Brassicaceae
M. A. Anthony (2020)
10.1242/dev.184762
VAPYRIN-like is required for development of the moss Physcomitrella patens
Ursina Rathgeb (2020)
10.1111/nph.16569
FungalRoot: Global online database of plant mycorrhizal associations.
Nadejda A. Soudzilovskaia (2020)
10.1126/science.aba0196
A plant’s diet, surviving in a variable nutrient environment
G. Oldroyd (2020)
10.1093/jxb/eraa007
Evo-physio: on stress responses and the earliest land plants
J. M. Fürst-Jansen (2020)
10.1016/b978-0-12-818469-1.00021-3
Arbuscular mycorrhiza, a fungal perspective
Jelle van Creij (2020)
10.1104/pp.19.01420
Duplication of Symbiotic Lysin Motif Receptors Predates the Evolution of Nitrogen-Fixing Nodule Symbiosis1
Luuk Rutten (2020)
10.1101/2020.12.14.422721
Transcriptional responses to arbuscular mycorrhizal symbiosis development are conserved in the early divergent Marchantia paleacea
Mara Sgroi (2020)
10.1086/706187
Mutualism as a Plant Functional Trait: Linking Variation in the Mycorrhizal Symbiosis to Climatic Tolerance, Geographic Range, and Population Dynamics
H. Maherali (2020)
10.1038/s41477-020-0618-2
Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts
F. Li (2020)
10.1007/s00203-020-01915-x
The potential of arbuscular mycorrhizal fungi in C cycling: a review
Manoj Parihar (2020)
10.1093/aobpla/plz060
Insights from invasion ecology: Can consideration of eco-evolutionary experience promote benefits from root mutualisms in plant production?
J. Ramoneda (2019)
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