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Comparative phylogenomics of symbiotic
associations
Author for correspondence:
Pierre-Marc Delaux
Tel: +33 0 5 34 32 38 38
Email: [email protected]
Pierre-Marc Delaux
Laboratoire de Recherche en Sciences Vegetales, Universite de Toulouse, CNRS, UPS, 24 chemin de Borde Rouge, Auzeville, BP42617,
31326, Castanet Tolosan, France
Received: 10 May 2016
Accepted: 19 July 2016
Contents
Summary
89
IV. Discovery of new symbiotic genes
91
I.
Introduction
89
V.
92
II.
AM symbiosis in plants: one gain and multiple losses
90
VI. Conclusion
93
III.
Evolution of AM symbiosis-related genes
90
References
93
Future perspectives
Summary
New Phytologist (2017) 213: 89–94
doi: 10.1111/nph.14161
Key words: arbuscular mycorrhizal (AM)
symbiosis, evolution, genomics, phylogeny,
plant–microbe associations.
Understanding the genetic bases of complex traits has been a main challenge in biology for
decades. Comparative phylogenomics offers an opportunity to identify candidate genes
associated with these complex traits. This approach initially developed in prokaryotes consists in
looking at shared coevolution between genes and traits. It thus requires a precise reconstruction
of the trait evolution, a large genomic sampling in the clades of interest and an accurate definition
of orthogroups. Recently, with the growing body of sequenced plant genomes, comparative
genomics has been successfully applied to plants to study the widespread arbuscular mycorrhizal
symbiosis. Here I will use these findings to illustrate the main principles of comparative
phylogenomic approaches and propose directions to improve our understanding of symbiotic
associations.
I. Introduction
Comparative phylogenomic approaches link genomic features
to traits in a phylogenetic context. While these approaches have
mostly been used to define the evolution of known gene
networks, they have the potential to identify new genetic
components controlling part of the phenotypic variability in the
species space of interest (Eisen, 1998). Initially developed in
bacteria (Pellegrini et al., 1999), it has been successfully
expanded to eukaryotes over the last few years and resulted
in the discovery of genes involved in cilia development (AvidorReiss et al., 2004) or the identification of small-RNA pathway
genes (Tabach et al., 2013). In plants, there has so far been a
limited use of such an approach.
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The arbuscular mycorrhizal (AM) symbiosis is a mutualistic
association formed between plants and fungi of the Glomeromycota, also called AM fungi (Box 1). During this association, the
fungus colonizes the host plant and develops intracellular highly
branched structures known as arbuscules. When established, the
association results in an exchange of nutrients between the two
partners (Parniske, 2008). While plant genes controlling this
association have been identified by genetics in model angiosperms,
the symbiotic gene set remains incomplete (Gutjahr & Parniske,
2013). Comparative phylogenomics is thus a promising option to
identify symbiotic genes in a comprehensive manner.
Rather than providing a methodological guide, the goal here is to
illustrate, with the recent advances made by applying comparative
phylogenomics to the AM symbiosis, the three steps required for a
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Box 1
Viridiplantae – a kingdom also known as the green lineage. Composed
by Chlorophyte algae such as Chlamydomonas reinhardtii or
Ostreococcus spp., the six orders of Charophyte algae (Mesostigmatales, Chlorokybales, Klebsormidiales, Charales, Coleochaetales and
Zygnematales) and Embryophytes.
Embryophytes – these encompass nonvascular plants belonging to the
liverwort, hornwort and moss clades as well as the protracheophytes
(extinct) and tracheophytes (vascular plants). The term is widely used
as a synonym for land plants but some lineages belonging to the
Embryophytes do not actually live on land, such as the sea grass
Zostera marina.
Glomeromycota – a monophyletic group of obligate biotrophic fungi
that all form the arbuscular mycorrhizal symbiosis with most
Embryophytes. They are also called arbuscular mycorrhizal fungi. So
far there is no evidence of nonsymbiotic fungi in this clade.
Ectomycorrhizas (ECM) – beneficial associations between various seed
plants and fungi belonging to the Ascomycota and Basidiomycota.
During these interactions the ECM fungus colonizes plant roots to form
a hyphal network between epidermal and cortical cells, known as the
Hartig net.
successful analysis: clearly define the evolution of the trait; identify
the phylogenetic pattern of known genes linked to the trait; and
identify genome-wide genes following that specific pattern (Fig. 1).
Directions in which these approaches could be expanded in the
future are also proposed.
II. AM symbiosis in plants: one gain and multiple
losses
Reconstructing the evolution of a trait relies on a robust species tree.
For Embryophytes (Box 1), several nodes remain debated, such as
the position of liverworts, mosses and hornworts relative to the
tracheophytes or the branching order between the main Gymnosperm lineages (Wickett et al., 2014). These uncertainties need
to be taken into account when investigating trait or gene evolution
(Sayou et al., 2014). Given its widespread occurrence in 80% of the
Embryophytes, including liverworts and hornworts, it has been
proposed that the AM symbiosis has a single and ancient origin at
the base of the Embryophytes (Bonfante & Genre, 2008; Field
et al., 2015). In addition, the fossil record confirmed the presence of
AM fungi and AM-like associations in the earliest land plant fossils
(Remy et al., 1994; Redecker et al., 2000; Strullu-Derrien et al.,
2014). While ancestral state reconstruction of the AM symbiosis in
Embryophytes remains to be performed to further test this
hypothesis, the other evolutionary scenario – independent gains
– is currently not supported. With the AM symbiosis as the likely
ancestral trait in Embryophytes, its absence in various clades would
correspond to independent losses. Identifying losses requires a
precise phenotyping in controlled conditions. Several events have
been well characterized. For instance, studying 36 Lupinus species
and 10 closely related species, it has been demonstrated that the loss
of AM symbiosis occurred at the base of this genus (Oba et al.,
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2012). Similarly, a loss occurred in the Brassicales order just before
the divergence of the Limnanthaceae (Delaux et al., 2014).
These specific evolutionary features, origin in first land plants
and the subsequent losses in various lineages, define a phylogenetic
context to study the evolution of the associated gene networks.
III. Evolution of AM symbiosis-related genes
Genetic analyses conducted in angiosperms led to the identification
of plant genes regulating the AM symbiosis. With the evolution of
AM symbiosis well mapped on the species tree for several clades, as
indicated earlier, phylogenetic studies on these symbiotic genes
would allow the reconstruction of their evolution in plants. Given
the ancient origin of the AM symbiosis, the entire Viridiplantae
lineage is an appropriate scale to conduct such analyses. A
consistent phylogenetic analysis relies on the comprehensive
coverage of the species space with an appropriate sequencing
depth. Until recently, genomic and transcriptomic data were
available for only a limited number of taxa, mostly angiosperm
species with only a few exceptions such as the moss Physcomitrella
patens (Lang et al., 2008).While recently sequenced genomes
improved this coverage (i.e. Amborella trichopoda, Chamala et al.,
2013; Klebsormidium flaccidum, Hori et al., 2014) many clades still
lack sampling. To tackle this limitation, the 1 KP initiative (https://
sites.google.com/a/ualberta.ca/onekp/) sequenced transcriptomes
for over 1400 species covering the entire breadth of the green
lineage. This dataset already resulted in a strong improvement of
our understanding of plant phylogeny (Wickett et al., 2014;
Rothfels et al., 2015) and of the evolution of key proteins such as
photoreceptors (Li et al., 2014). Using these combined datasets, it
has been possible to infer the origin and evolution of genes
previously identified in angiosperms for their involvement in AM
symbiosis (Delaux et al., 2015). Two main evolutionary origins for
symbiotic genes were found. Genes involved in colonization and
arbuscule formation evolved in first land plants, probably together
with the AM symbiosis itself (Bonfante & Genre, 2008; Delaux
et al., 2015). More surprising was the finding of orthologs of genes
involved in the initial recognition of AM fungi, and downstream
early signaling, in advanced charophyte algae, the closest relative to
embryophytes not known to associate with AM fungi (Delaux et al.,
2015). This suggests that the last common ancestor of
embryophytes and charophytes already had the genes involved in
early symbiotic signaling that were later recruited for AM symbiosis
during the terrestrialization process. Besides defining their origins,
the accumulation of plant genomes and transcriptomes allowed the
conservation of the symbiotic genes in nonhost species to be
studied. By combining phylogenetic and synteny analyses, it has
been determined that the loss of AM symbiosis in multiple
angiosperm lineages perfectly correlates with the loss of most AM
symbiosis-related genes (Delaux et al., 2014), a finding recently
confirmed using independent phylogenetic approaches (Favre
et al., 2014; Bravo et al., 2016). This suggests that conservation of
these genes over millions of years might only have been driven by
the symbiotic association.
Taken together, these findings define a specific phylogenetic
pattern for the known AM symbiosis-related genes. They are all
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Angiosperms
Species tree
Review 91
Trait
Gymnosperms
Lycophytes
Protracheophytes
Hornworts
Embryophytes
Monilophytes
Trait evolution
Genes
Mosses
Liverworts
Charophytes
Limnanthaceae
Caricaceae
Phylogenetic
pattern
Brassicales
Later-diverging
Brassicales
Candidate genes
and pathways
Moringaceae
Malvaceae
Symbiotic
genes
Lupinus spp.
Cytisus
Genista
Other
Papilionoideae
Legumes
Laburnum
Genomes
Hosts
Nonhost
Nonhost
Nonhost
c. 150 candidates
Fig. 1 Principles of comparative phylogenomics illustrated with arbuscular mycorrhizal (AM) symbiosis. Comparative phylogenomics relies on three aspects:
trait evolution, phylogenetic pattern of known genes, and identification of candidate genes and pathways. Trait evolution is determined by inferring the
occurrence of a trait on a species tree. Left-hand (orange) box, AM symbiosis evolved only once after the divergence of the Charophyte algae and the
Embryophytes and got lost multiple times independently (red branches) at multiple levels: a large clade (Mosses), an order (most families in the Brassicales), or a
genus (Lupinus). A phylogenetic pattern is determined by comparing the occurrence of known genes with the occurrence of the trait. Middle (green) box, AM
symbiosis-related genes are conserved in host species (blue rectangles) and absent from nonhost species (red rectangles). Identification of candidate genes and
pathways relies on genome comparisons to identify genes following the phylogenetic pattern. Right-hand (brown) box, genes present in all host species are
identified (blue circle) and their presence in the genome of nonhost species (red circles) is determined. This comparison allowed for the identification of c. 150
candidate genes (Delaux et al., 2014; Bravo et al., 2016).
ancestral to the radiation of the angiosperms and most of them are
absent in nonrelated, nonhost species.
Box 2
IV. Discovery of new symbiotic genes
Orthogroup – in a given set of species, a group of genes that are
descended from a single gene in their last common ancestor.
The remaining step was to identify genes following the specific
phylogenetic pattern defined earlier in a genome-wide manner
using so-called comparative phylogenomic approaches (Eisen,
1998). Recently, three studies conducted such an approach to
identify candidate symbiotic genes (Delaux et al., 2014; Favre et al.,
2014; Bravo et al., 2016). In other words, these studies tried to
determine for each gene present in the genomes of all host plants
whether an orthologous gene is present in even a single genome of
nonhost species. For this purpose, orthogroups (Box 2) were
defined and the ones containing genes from nonhost species or only
a few host species were filtered out. Over the two last decades,
several algorithms have been developed to accurately define
orthogroups, the most popular ones being based on the
INPARANOID method (Remm et al., 2001). These approaches
start with the collection of homologous sequences by BLAST on the
species of interest, using as a query all protein models from one of
them. In classic analysis, the MCL algorithm, or a derivative, then
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Species tree – a phylogenetic tree showing the relationship between
taxa sharing a common ancestor.
Symbiotic trait – refers to the ability of an organism to participate in a
given symbiotic association.
clusters highly similar sequences in groups (Emms & Kelly, 2015).
However, this clustering step is intrinsically dependent on its
stringency parameters and may result on the exclusion of
orthologous but divergent genes. In the Delaux et al. study this
step resulted in the exclusion of nonhost sequences from
orthogroups. As these genes were excluded at this stage, the
phylogenetic tree generated for each orthogroup in the subsequent
step was obviously devoid of these nonhost species and thus
included in the list of candidate symbiotic genes absent from
nonhost species (Delaux et al., 2014). By contrast, Bravo et al.
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(2016) did not include such a clustering step and directly built
phylogenetic trees on the collected sequences after a single curation
step to reduce the total number of sequences while maintaining
species diversity. This ultimately resulted in the conservation of
more divergent sequences in the dataset used to generate phylogenetic trees. In both cases, phylogenetic trees were constructed
with each orthogroup, reconciled with the species tree and rooted.
Various pipelines have been designed to then identify orthogroups
matching the pattern of interest (Lee et al., 2011; Nagy et al.,
2014). In the case of the AM symbiosis, this pattern was the
conservation in host dicots, absence in nonhost species and
presence in monocots. While the three studies searched this pattern,
the main differences in the species used resulted in striking
differences. Similarly to the use of a clustering method, as described
earlier, a reduced number of nonhost species results in the
identification of a large number of false positives in the list of
candidate genes (i.e. genes actually present in nonhost species and
thus not specific to host species). For instance, Favre et al. (2014)
used only three nonhost Brassicaceae, resulting in the identification
of > 5000 candidate genes. Most of them are Brassicaceae-specific
losses, not consistently related to the loss of the AM symbiosis. The
two other studies used different sets of nonhost species. In the
future, combining these two sets will provide the potential to
improve the list of predicted symbiotic genes. It is worth noting
here that the species included have to be carefully checked for their
symbiotic behavior and for the occurrence of the correlation
between absence of known genes and loss of the trait. For instance,
the presence of the symbiotic gene DMI3 in Nelumbo nucifera
suggests that the selection on symbiotic genes in this species might
be different from that in other nonhost species, as has been
described in mosses (Wang et al., 2010).
These studies provided lists of candidate genes and, more
importantly, proved that comparative phylogenomics has the
potential to strongly improve our understanding of plant–microbe
associations.
V. Future perspectives
With its presumed single origin and multiple losses, the AM
symbiosis has been a very tractable model for comparative
phylogenomics. Expansion in two directions is now required to
fully benefit from this approach. First, while the initial analyses
focused mainly on the correlation between trait loss and gene loss,
more subtle evolutionary patterns could be tracked. Indeed, it can
be anticipated that genes involved in multiple pathways will be
retained in nonhost species after the loss of the AM symbiosis.
However, despite their conservation, features specific to their
symbiotic function are likely to be lost in nonhost lineages,
potentially leading to a detectable switch in selection. Supporting
this idea, it has been found that NSP1 and NSP2, two symbiotic
GRAS transcription factors also controlling the biosynthesis of the
plant hormone strigolactones (Liu et al., 2011), are under relaxed
selection in the Brassicaceae (Delaux et al., 2013). Expanding this
analysis to genome-wide comparisons would lead to the identification of additional symbiotic components. Even beyond selective
pressure on codons, detecting discriminating synonymous
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mutations between host and nonhost species could be extremely
informative.
The second way in which comparative phylogenomics could be
expanded is for the study of other beneficial plant–microbe
interactions. The phylogenetic pattern so far supported for the AM
symbiosis on the plant side, a single origin and multiple losses, was
the most favorable option to study. Indeed, convergent losses are
detectable, assuming a reliable identification of orthogroups.
Unfortunately, most other described symbiotic plant–microbe
interactions followed completely different evolutionary trajectories. Even staying with the AM symbiosis but switching from the
plant side to the AM fungi side leads to a more complicated picture.
As for plants, there is evidence of a single origin, at the base of the
Glomeromycota. However, no loss has been identified. Thus,
looking for genome-wide presence/absence patterns between AM
fungi and their closest relatives would result in the identification of
genes associated with the evolution of the Glomeromycota without
specificity for the symbiotic ones. Facing the same issue of single
evolution of a trait in a given lineage, evolutionary developmental
studies have integrated transcriptomics in the same evolutionary
context (Ichihashi et al., 2014). Combining comparative transcriptomics of various AM fungi in symbiotic conditions and comparative phylogenomics of AM fungi and their close relatives thus
offers a unique opportunity to understand the basis of symbiosis in
this fungal clade. By contrast to the single origin of AM symbiosis in
the Glomeromycota, the ability to form ectomycorrhizal symbiosis
evolved independently > 60 times in Fungi and resulted in very
similar associations at the phenotypic and even physiologic levels, a
clear example of convergent evolution (Tedersoo et al., 2010). A
massive genomic effort has been undertaken for these fungi and
their close saprotrophic relatives, allowing for comparative
phylogenomic approaches to be performed (Kohler et al., 2015).
Using this unique dataset, Kohler et al. (2015) investigated
convergent evolution of ectomycorrhizas (ECM) in nine fungal
lineages. Transcriptomics conducted on the same species space,
revealed many features specific to each ECM lineage, highlighting
the multiple molecular ways to reach the same trait in a convergent
manner. It can be now anticipated that these combinations of
phylogenomics and transcriptomics will shed light on the mechanisms allowing the evolution of other well described beneficial
plant–microbe interactions, such as root nodulation, plant–
cyanobacteria symbioses (Adams & Duggan, 2008), the plant side
of the ectomycorrhizal symbioses (Garcia et al., 2015) or the ericoid
and orchid mycorrhizae (Weiß et al., 2016). Although they
probably represent the most successful ones, based on their spread
and ecological benefits, beneficial associations can no longer be
restricted to these described symbioses. As exemplified by the
specialized interaction recently described between Colletotrichum
tofeldiae and Arabidopsis thaliana, other associations benefiting the
plant partner occur in a species- or clade-specific manner (Hiruma
et al., 2016). With metagenomic approaches strongly improving
the ability to detect associated microbes, it is now possible to
envision creating catalogs of interacting microorganisms for the
entire plant lineage. The coverage of the genomic space provided by
projects such as the 1KP initiative, and the sequencing of more
plant genomes that are more reliable than transcriptomic data, or
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the 1K fungal genome project (http://1000.fungalgenomes.org)
will provide the basis for defining genomic features associated with
taxa in a comprehensive manner. In the earlier mentioned
association between Colletotrichum and Arabidopsis, the authors
found that Colletotrichum was not able to interact symbiotically
with another Brassicaceae, Capsella rubella, that does not produce
indole glucosinolate, which is important in Arabidopsis to restrict
fungal growth (Hiruma et al., 2016). By contrast, Cardamine
hirsuta, which produces indole glucosinolate-like Arabidopsis, fully
benefits from the association (Hiruma et al., 2016). Such a
correlation could be extended to other Brassicales species and
should correlate, if valid, with the presence/absence of the enzymes
specifically controlling the production of these glucosinolates.
Similarities between microbial communities associated with distantly related species such as Barley and Arabidopsis have been
observed (Hacquard et al., 2015). This suggests the existence of
potential highly conserved associations in plants that, in addition to
being characterized as beneficial, neutral or pathogen, could be
functionally studied using comparative phylogenomics to identify
candidate genes.
VI. Conclusion
Genetic, transcriptomic and genomic approaches have led to
huge advances in our understanding of symbiotic associations.
The genomic coverage of the embryophytes has improved
significantly over the last few years together with pipelines
allowing more accurate orthogroup identification. In parallel,
metagenomics performed on field-collected samples allows for
an in-depth characterization of the microorganisms associated
with plants. We can now envision the determination of a
kingdom-wide correlation between genomic features and plant–
microorganism interactions, which will need to be experimentally confirmed, beginning a new era in the study of the
beneficial associations between plants and their surrounding
biotic environment.
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