Comparative analysis of the complete mitogenome of Geoffroea decorticans: a native tree surviving in the Atacama Desert

Abstract

Chañar (Geoffroea decorticans (Gill., ex Hook. & Arn.) Burkart) has been highly significant for indigenous people in the Atacama Desert for over 3,000 years. Through evolutionary processes, the G. decorticans mitogenome likely underwent changes facilitating its adaptation to the extreme conditions of the Atacama Desert. Here, we compare the mitochondrial genome of G. decorticans with those of other Papilionoideae family species. The complete mitogenome of G. decorticans was sequenced and assembled, making it the first in the genus Geoffroea. The mitogenome contained 383,963 base pairs, consisting of 33 protein coding genes, 21 transfer RNA genes, and 3 ribosomal RNA genes. The Chañar mitogenome is relatively compact, and has two intact genes (sdh4 and nad1) which were not observed in most other species. Additionally, Chañar possessed the highest amount of mitochondrial DNA of plastid origin among angiosperm species. The phylogenetic analysis of the mitogenomes of Chañar and 12 other taxa displayed a high level of consistency in taxonomic classification, when compared to those of the plastid genome. Atp8 was subjected to positive selection, while the ccmFc and rps1 were subjected to neutral selection. This study provides valuable information regarding its ability to survive the extreme environmental conditions of the Atacama Desert.

Full text

Comparative analysis of the
complete mitogenome of
Geoffroea decorticans: a native
tree surviving in the Atacama
Desert
Roberto Contreras-Díaz
1
*, Felipe S. Carevic
2†
and
Liesbeth van den Brink
3
,
4†
1
Núcleo Milenio de Ecología Histórica Aplicada para los Bosques Áridos (AFOREST), CRIDESAT,
Universidad de Atacama, Copiapó, Chile,
2
Laboratorio de Ecología Vegetal, Facultad de Recursos
Naturales Renovables, Núcleo Milenio de Ecología Histórica Aplicada para los Bosques Áridos (AFOREST),
Universidad Arturo Prat, Iquique, Chile,
3
Institute of Evolution and Ecology, Plant Ecology Group,
Universität Tübingen, Tübingen, Germany,
4
Departamento de Botánica, Facultad de Ciencias Naturales y
Oceanográficas, ECOBIOSIS, Universidad de Concepción, Concepción, Chile
Chañar (Geoffroea decorticans (Gill., ex Hook. & Arn.) Burkart) has been highly
significant for indigenous people in the Atacama Desert for over 3,000 years.
Through evolutionary processes, the G. decorticans mitogenome likely
underwent changes facilitating its adaptation to the extreme conditions of the
Atacama Desert. Here, we compare the mitochondrial genome of G. decorticans
with those of other Papilionoideae family species. The complete mitogenome of
G. decorticans was sequenced and assembled, making it the first in the genus
Geoffroea. The mitogenome contained 383,963 base pairs, consisting of
33 protein coding genes, 21 transfer RNA genes, and 3 ribosomal RNA genes.
The Chañar mitogenome is relatively compact, and has two intact genes (sdh4 and
nad1) which were not observed in most other species. Additionally, Chañar
possessed the highest amount of mitochondrial DNA of plastid origin among
angiosperm species. The phylogenetic analysis of the mitogenomes of Chañar and
12 other taxa displayed a high level of consistency in taxonomic classification,
when compared to those of the plastid genome. Atp8 was subjected to positive
selection, while the ccmFc and rps1 were subjected to neutral selection. This study
provides valuable information regarding its ability to survive the extreme
environmental conditions of the Atacama Desert.
KEYWORDS
Atacama Desert, Geoffroea decorticans, mitochondrial genome, stress tolerance,
fabaceae, extremophiles
1 Introduction
Chañar, Geoffroea decorticans (Gill., ex Hook. & Arn.) Burkart, is considered to have
been one of the most important wild trees for the indigenous populations that resided in the
Atacama Desert around 1000 years BP (Ugalde et al., 2021). In the present day, this species is
recognized for its diverse utility as a food resource, furniture material and medicinal product
(Giménez, 2004;Nuñez et al., 2009;Costamagna et al., 2013;Jiménez-Aspee et al., 2017;
Cotabarren et al., 2020). Surviving and providing sustenance to local communities under
OPEN ACCESS
EDITED BY
Ana Luisa Garcia-Oliveira,
The International Maize and Wheat
Improvement Center (CIMMYT), Kenya
REVIEWED BY
Edi Sudianto,
National Cheng Kung University, Taiwan
Romain Yves Olivier Gastineau,
University of Szczecin, Poland
*CORRESPONDENCE
Roberto Contreras-Díaz,
roberto.contreras@uda.cl
†
These authors have contributed equally
to this work
RECEIVED 20 May 2023
ACCEPTED 26 July 2023
PUBLISHED 10 August 2023
CITATION
Contreras-Díaz R, Carevic FS and
van den Brink L (2023), Comparative
analysis of the complete mitogenome of
Geoffroea decorticans: a native tree
surviving in the Atacama Desert.
Front. Genet. 14:1226052.
doi: 10.3389/fgene.2023.1226052
COPYRIGHT
© 2023 Contreras-Díaz, Carevic and van
den Brink. This is an open-access article
distributed under the terms of the
Creative Commons Attribution License
(CC BY). The use, distribution or
reproduction in other forums is
permitted, provided the original author(s)
and the copyright owner(s) are credited
and that the original publication in this
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accepted academic practice. No use,
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which does not comply with these terms.
Frontiers in Genetics frontiersin.org01
TYPE Brief Research Report
PUBLISHED 10 August 2023
DOI 10.3389/fgene.2023.1226052

such challenging conditions is a remarkable achievement for any
plant. The Atacama Desert, known as the world`s oldest and driest
desert, presents extreme environmental conditions including high
levels of UV radiation, high temperatures, extreme aridity, and
highly saline and oxidizing soils (Eshel et al., 2021;Azua-Bustos
et al., 2022). Geoffroea decorticans also inhabits other arid and semi-
arid regions in Bolivia, Peru, and Argentina (Contreras Díaz, Porcile
Saavedra and Aguayo Cruces, 2018), which are facing increasing
aridity due to climate change. Drought, salinity, and high
temperatures are highly important environmental factors that
severely restrict plant growth and development (Krasensky and
Jonak, 2012). In response to these abiotic stresses, plants employ
various mechanisms, such as the production of reactive oxygen
species (ROS), which can cause oxidative damage to lipids, proteins,
and nucleic acids, ultimately leading to programmed cell death (Van
Aken et al., 2009;Tang and Zhu, 2023).
Mitochondria play a key role in plant responses to abiotic stress
(Newton et al., 2004;Liberatore et al., 2016). They are involved in
energy production, metabolism, regulation of PCD, and ROS
production (Tang and Zhu, 2023). Compared to plastid genomes,
mitochondrial genomes demonstrate substantial variability in terms
of size, structure (Smith and Keeling, 2015), and gene content
(Liberatore et al., 2016). Plant mitochondrial genomes
(mitogenomes) exhibit distinctive characteristics, including high
rates of point mutations and structural rearrangements, genome
expansion and contraction, integration of foreign DNA, gene loss,
and transfer to the nuclear genome (Palmer et al., 2000;Chevigny
et al., 2020). It is highly likely that the mitogenome structure of G.
decorticans has undergone changes, through evolution, enabling its
adaptation to extreme conditions, and accounting for its remarkable
survival capability. Studying the genetic characteristics of plants that
have adapted to these harsh conditions can contribute to the
preservation of this valuable genetic resource that has sustained
indigenous cultures for millennia. The objective of this study is 1) to
compare the structural characteristics of the mitochondrial genome
of G. decorticans with other species of Papilionoideae family species,
focusing on gene content, genome size, the number of protein-
coding genes with RNA editing, transfer of DNA from plastid
regions, and 2) to confirm its phylogeny.
2 Methods
Fresh leaves of Chañar were collected near Copiapó, Chile. A
subsample was stored in the Index Herbariorum of Universidad de
Chile, with the voucher number EIF13815, and the rest of the leaves
were used for DNA isolation, using a modified
cetyltrimethylammonium bromide (CTAB) protocol (Contreras
et al., 2020). The concentration of the DNA was measured using
a Qubit™3.0 fluorometer and a Qubit™dsDNA HS Assay Kit. To
verify the integrity of the DNA, an Agilent 2100 Bioanalyzer was
used, prior to sequencing. The NGS library was prepared using the
TruSeq DNA LT Kit and sequencing was performed on Illumina
next-generation sequencing (NGS) platforms. Paired-end sequences
of 150 bp were generated for both forward (R1) and reverse (R2)
reads. To filter the reads we used the Trim-Galore software (Krueger,
2019), which eliminates adapter remnants and low quality sequences
(phred value <25). The SPAdes 4 software, version 3.13.0
(Bankevich et al., 2012) was used to assemble the filtered reads.
Additionally, we mapped the reads back to the G. decorticans
mitogenome assembly to visualize the read coverage, using
Geneious Prime v2022.0.1 (Supplementary Figure S1,http://www.
geneious.com;Kearse et al. (2012)). The annotation of the
mitogenome was performed using AGORA (Jung et al., 2018)
and MITOFY (Alverson et al., 2010) software. The circular map
of the mitochondrial genome, along with annotation information,
was generated using OrganellarGenomeDRAW (OGDRAW)
(Greiner et al., 2019). The final annotated mitogenome sequence
of G. decorticans was deposited in the NCBI GenBank, with the
accession number OQ707067.
The features of the G. decorticans mitogenome were compared
with ten closely related species in the Papilionoideae subfamily,
i.e., Dalbergia odorifera T.C. Chen (MW441235), Arachis hypogaea
L. (MW448460), Lotus japonicus (Regel) K. Larsen (NC_016743),
Medicago sativa L. (ON782580), Glycine max (L.) Merr., 1917 (NC_
020455), Phaseolus vulgaris L. (MK176514), Vigna angularis
(Willd.) Ohwi & H. Ohashi (NC_021092), Pongamia pinnata (L.)
Pierre (NC_016742), Sophora koreensis Nakai (NC_072933) and
Castanospermum australe A. Cunn. & C. Fraser (MK426679).
Additionally, we compared the G. decorticans mitogenome with
mitogenomes of angiosperm-species from non-polar desert habitats
(Supplementary Table S1). The length of the plastid-derived region
of the mitogenome was evaluated using BLASTN (Johnson et al.,
2008) with default parameters, because plant mitogenomes contain
sequence elements that originate in the plastid genome (plastome),
known as mitochondrial DNA of plastid origin (MIPT). Therefore,
each mitogenome was used as the query versus a database
comprising the plastomes corresponding to the species:
MW672397, KX257487, NC_049008, MT571487, NC_007942,
NC_002694, NC_042841, JN673818, EU196765, AP012598, and
MW628966.
Thirty-three protein-coding gene (PCG) sequences, i.e., nad1,
nad2, nad3, nad4, nad4L, nad5, nad6, nad7, nad9, sdh4, cob, cox1,
cox2, cox3, atp1, atp4, atp6, atp8, atp9, ccmB, ccmC, ccmFc, ccmFn,
rps1, rps3, rps4, rps10, rps12, rps14, rpl5, rpl16, matR, and mttB, were
used in the phylogenetic analysis of G. decorticans along with the
previously mentioned ten Papilionoideae species. In addition, two
Caesalpinioideae species, Leucaena trichandra (Zucc.) Urb. (NC_
039738) and Acacia ligulata A. Cunn. ex Benth. (NC_040998), were
included as outgroups. The 33 PCG sequences were aligned
separately using MAFFT v7 (Katoh and Standley, 2013) and any
gaps in the alignment were trimmed using trimAl v1.4 (Capella-
Gutiérrez et al., 2009). Subsequently, the sequences were
concatenated with Mesquite 3.81 software (Maddison and
Maddison, 2023). The analyses of the mitochondrial genomes’
33 PCG sequences were conducted using the maximum
likelihood (ML) method. We did the same for the complete
plastid genome sequences, using the plastome accessions listed
above (including the outgroup species accessions
NC026134.2 and NC028733) in order to compare the resulting
phylogenetic trees. The best-fitting nucleotide substitution model of
sequence evolution, model TVM + G4, was determined using the
Corrected Akaike Information Criterion (AICc) through Modeltest-
NG on XSEDE (Darriba et al., 2020). The ML analyses were carried
out using RAxML-HPC BlackBox v.8.1.12 (Stamatakis, 2014) with
1,000 bootstrap replicates, using the CIPRES Science Gateway v3.3
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(Miller et al., 2010). Non-parametric bootstrap support (BS) values
were used to measure the internal nodes of the resulting trees. The
ratio of non-synonymous substitution (Ka) to synonymous
substitution (Ks) was calculated for 25 PCGs of G. decorticans
and ten Papilionoideae species, using the KaKs_Calculator tool
3.0 (Zhang, 2022) with the MA model, where Ka/Ks values
of >1 signify that the gene is subjected to positive selection, Ka/
Ks values equal to 1 indicate neutral selection, and Ka/Ks values <
1 signify purification.
3 Results and discussion
We successfully sequenced and assembled the complete
mitogenome of G. decorticans, resulting in a single circular
genome with a length of 383,969 bp (Figure 1; GenBank
accession number OQ707067). The mitogenome sizes of G.
decorticans and ten other Papilionoideae species varied from
290,285 to 592,341 bp (Table 1). Mitogenome sizes can exhibit
significant variation among plant species, for example, among
angiosperm the mitogenome sizes range from 66 kb in the
parasitic plant, Viscum scurruloideum (Skippingtona et al., 2015)
to 11,300 kb in Silene conica (Sloan et al., 2012). According to Choi
et al. (2019), the median size of seed plant mitogenomes is 476 kb.
However, within the Fabaceae family, mitogenome sizes vary
considerably from 271,618 to 729,504 bp. Therefore, G.
decorticans possesses a relatively small mitogenome size
compared to other Papilionoideae species, but it falls within an
intermediate range when compared to angiosperm mitogenomes.
The variations in mitogenome size among plant species can be
attributed to various factors. Mitogenomic chromosome loss, gain of
exogenous DNA through intracellular gene transfer and horizontal
gene transfer, and the acquisition of repetitive DNA are likely
explanations for the increases and decreases observed in
mitogenome sizes in angiosperms (Choi et al., 2019).
Additionally, some studies suggest that changes in mitochondrial
genome size can be influenced by environmental stresses (Xiong
et al., 2022).
FIGURE 1
Mitochondrial maps of Geoffroea decorticans (size: 383,969 bp).
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TABLE 1 General features of mitogenome of Geoffroea decorticans and other ten Papilionoideae species.
Species (subfamily
Papilionoideae)
Genome
length (bp)
GC
(%)
Genes
(*)
tRNA
(**)
rRNA
(**)
Protein-
coding
genes
(PCG) (**)
Genes with
mutation in first
start codon (GM)
Pseudogenes Missing genes Exclusive
gene
MIPT
(bp)
(***)
References
Geoffroea decorticans 383,969 45.3 57 21 3 30 rps4, nad4L, rps10 rpl10, sdh3, rps7, rpl2,
rps19
rps2, rps11, rps13 sdh4, nad1 50,224
(13%)
This study
Arachis hypogaea 592,341 44.7 56 21 3 29 nad1, nad4L, rps10 rpl10, sdh4, rps19 sdh3, rps7, rpl2,
rps2, rps11, rps13
33,237
(5%)
Choi et al.
(2021)
Dalbergia odorifera 435,224 45.1 54 17 4 28 nad4L, rps10, rps14,
mttB, cob
—rpl10, sdh3, rps19,
rps7, rpl2, rps2,
rps11, rps13
sdh4, nad1 17,588
(4%)
Hong et al.
(2021)
Lotus japonicus 380,861 45.4 57 20 3 31 nad1, nad4L, rps10 rpl10, sdh3, rps7, rps19,
nad6, atp6, sdh4, cob
rpl2, rps2, rps11,
rps13
—12,039
(3%)
Kazakoff et al.
(2012)
Medicago sativa 290,285 45.3 54 18 3 32 nad1 —rpl10, sdh3, sdh4,
rps19, rps7, rpl2,
rps2, rps11, rps13
—1,583
(0.5%)
—
Glycine max 402,558 45.0 58 19 3 30 nad1, nad4L-1, nad4L-
2 rps10, ccmFc, mttB
—rpl10, sdh3, sdh4,
rps19, rps7, rpl2,
rps2, rps11, rps13
—5,507
(1,3%)
Chang et al.,
2013
Phaseolus vulgaris 395,516 45.1 52 18 3 26 nad1, nad4L, rps10,
ccmFc, mttB
—rpl10, sdh3, sdh4,
rps19, rps7, rpl2,
rps2, rps11, rps13
—3,092
(0.7%)
—
Vigna angularis 404,466 45.2 45 16 3 21 nad1, nad4L, mttB,
ccmFc, rps10
rpl10, sdh3, sdh4,
rps19, rps7,
rpl2 cox2, rps2,
rps11, rps13
—4,205
(1.0%)
Naito et al.
(2013)
Pongamia pinnata 425,718 45.0 64 24 3 32 nad1, nad4L, rps10,
cox2, mttB
rps19, sdh4, rpl2, nad6,
rps7
rpl10, rps2, rps11,
rps13
—7,338
(1.7%)
Kazakoff et al.
(2012)
Sophora koreensis 519,841 44.5 60 19 3 37 nad1 sdh4 rpl10, rps19, rps2,
rps11, rps13
rpl2, rps7,
sdh3
53,781
(10.3%)
—
Castanospermum australe 542,079 45.3 58 18 3 33 nad1, rps4, rps10, mttB rps19 rpl10, sdh3, rps7,
rpl2, rps2, rps11,
rps13
sdh4 2,586
(0.4%)
Zhang et al.
(2019)
(*) tRNA + rRNA + PCG + GM; (**) intact genes; (***) all DNA sequences of plastid were considered.
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The total GC content of G. decorticans was 45.3%, which was
similar to the other Papilionoideae species, ranging from 44.5% in S.
koreensis to 45.4% in L. japonicus (Table 1). In the mitogenome of G.
decorticans, we identified a total of 57 genes, including 33 protein-
coding genes (PCG), of which 30 were intact PCGs and 3 had
mutations in the first start codon (Table 1). Additionally, there were
21 tRNA genes and 3 rRNA genes (Table 1). The number of genes in
the mitogenomes of other Papilionoideae species varied from
45 genes in V. angularis to 64 genes in P. pinnata (Table 1).
Moreover, V. angularis had the lowest number of PCGs (21) and
S. koreensis the highest (37). The number of tRNA genes ranged
from 16 in V. angularis to 24 in P. pinnata, while the number of
rRNA genes was consistent across most mitogenomes (3 genes),
except for Dalbergia odorifera which had 4 rRNA genes (Table 1).
Interestingly, G. decorticans and A. hypogaea had the second-highest
number of tRNA (21) genes. In angiosperms, mitochondrial tRNA
genes are known to be heterogeneous, with a variable number of
native tRNA genes (typically 11–13 genes) and tRNAs acquired
from different sources through intracellular and horizontal transfers
(Warren et al., 2021). Several studies have suggested a link between
highly accelerated rates of mitochondrial sequence evolution and a
reduced number of tRNA genes. For example, species like Silene
conica and Silene noctiflora and Viscum (mistletoe) have a reduced
tRNA gene content (Skippingtona et al., 2015;Warren et al., 2021).
In these cases, tRNA genes are replaced by nuclear-encoded
homologs, leading to a gene substitution process (Warren et al.,
2021). Therefore, considering the high number of tRNA genes (21)
in G. decorticans, it could be hypothesized that this species exhibits a
reduced rate of mitochondrial sequence evolution.
The presence of genes with mutations in the first start codon was
observed in the mitogenomes of the other Papilionoideae species,
ranging from 1 gene in Medicago sativa and S. koreensis to 6 genes in
G. max (Table 1). These mutations, known as RNA editing (C-to-U
RNA editing) occur at protein genes’first and second codon
positions. The functional significance of RNA editing is not yet
fully understood (Sloan et al., 2012), but it might play a role in the
maintenance and function of gene and genome architecture (Linch,
2007), as well as in gene regulation, protein isoform generation and
modification of active protein complexes (Lo Giudice et al., 2019).
Furthermore, Murayama et al. (2012) suggested that mitochondrial
function, specifically RNA editing at the nad4 gene, interacts with
and regulates the action of stress-related hormones in plants. It was
found that an RNA editing site in mitochondrial nad4 transcripts
was targeted by AHG11, resulting in the production of more
mRNAs for oxidative stress-responsive genes (Murayama et al.,
2012). In G. decorticans, as well as in the other species belonging
to the Papilionoideae family, the nad4 gene remains intact, while in
most of them the nad4L gene undergoes RNA editing.
Generally, vascular plants have been found to contain between
20 and 40 protein-coding genes (PCGs) in their mitogenomes
(Møller et al., 2021). Mitogenomes of the species of the Fabaceae
family have around 30 intact PCGs (Choi et al., 2019). In the case of
the G. decorticans mitogenome, we discovered 30 intact PCGs,
3 PCGs with mutations in the first start codon, 5 pseudogenes
(rpl10, sdh3, rps7, rpl2, and rps19) and 3 lost ribosomal protein genes
(rps2, rps11, and rps13)(Table 1). The number of PCGs in G.
decorticans (30) falls thus within the expected range for the Fabaceae
species. It has been observed before that pseudogenes, truncations
and deletions of the rps7, rps11, rps13, and rps2 genes were prevalent
in numerous Fabaceae species (Choi et al., 2019). This observation
aligns with our findings in G. decorticans and the other
Papilionoideae mitogenomes studied, except for S. koreensis,
which retained an intact rps7 gene. The rps19 gene was missing
in all Papilionoideae species used in our study (Table 1). Similarly,
Wang et al. (2023) reported that most rps genes (rps2,rps7,rps10,
rps11, and rps19) were absent in the mitogenome of Photinia
serratifolia, as well as in some Rosacea species. The loss of
ribosomal protein genes (rps genes) and the occurrence of
putative mutations in the first start codon (RNA editing) can
potentially be compensated for by nuclear genes (Newton et al.,
2004). In fact, nuclear genes have the ability to influence the
organization of mitochondrial genomes and regulate the
expression of mitochondrial genes (Newton et al., 2004). Gene
loss can occur through the transfer of a gene to the nucleus,
functional substitution by a related protein, or loss of the protein
and its function (Adams et al., 2002). In several Fabaceae species, the
presence or absence of genes such as cox2,rpl2,rpl10,rps1,sdh4, and
sdh3 has been found to be variable (Choi et al., 2019). This variability
in gene presence or absence was also observed in the eleven
Papilionoideae species analyzed in our study (Table 1), where
some species retained the genes while others exhibited
pseudogenization or complete loss.
Interestingly, we discovered four Papilionoideae species that
retained the intact sdh genes: D. odorifera (sdh4),
Castanospermum australe (sdh4), G. decorticans (sdh4) and S.
koreensis (sdh3)(Table 1). In contrast, a study by Choi et al.
(2019) revealed that all Papilionoideae species had lost the rpl10,
sdh3, and sdh4 genes. The exclusive conservation of functional sdh4
or sdh3 genes, without RNA editing, such as in G. decorticans, may
provide an important advantage for survival in the extreme
conditions of the Atacama Desert. Research has demonstrated
that succinate dehydrogenase (SDH) can activate the expression
of stress-related genes, thereby inducing antioxidant responses and
stress tolerance in plants (Jardim-Messeder et al., 2015). The authors
suggested that SDH plays a crucial role in reactive oxygen species
(ROS) production and in regulating both plant development and
responses to stress (Jardim-Messeder et al., 2015). It is worth noting
that within angiosperms, mitochondrial rps genes (16 genes) and sdh
genes (sdh3 and sdh4) have been lost from the mitochondrial
genome multiple times throughout plant evolution (Adams et al.,
2002). This further underscores the significance of intact genes in
certain plant species.
On the other hand, we found two Papilionoideae species, D.
odorifera and G. decorticans, that have the intact nad1 gene
(Table 1). Similar to what was explained earlier, this gene might
play a crucial role in buffering the stress conditions experienced by
G. decorticans on the Atacama Desert. In fact, a study by Jethva et al.
(2023) investigated the function of alternative NADH
dehydrogenases (nad1) and confirmed that this gene is essential
in preventing excessive ROS formation in mitochondria during
reoxygenation. The absence of nad1 and nad2 led to elevated
ROS production, while their overexpression limited ROS levels
(Jethva et al., 2023).
Plastid-to-mitochondria transfers have been suggested to have
been occurring since the colonization of land by plants.
Mitochondrial DNA of plastid origin (MIPT) is present in
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TABLE 2 General features of mitogenomes of angiosperm-species from non-polar desert habitats.
Species Genome
length (bp)
GC
(%)
Genes
(*)
tRNA
(**)
rRNA
(**)
Protein-
coding genes
(PCG) (**)
Genes with
mutation in first
start codon (GM)
Pseudogenes Missing genes Exclusive
gene
MIPT
(bp)
(***)
References
Rhazya stricta 548,608 43.7 53 12 3 36 atp6, rps10 sdh3 rps2, rps11 nad1 32,810
(6%)
Park et al. (2014)
Neltuma glandulosa 758,210 44.8 58 19 3 34 nad1, rps10 rps7 sdh3, rps2, rps11,
rps13
12,296
(1.6%)
Choi et al. (2021)
Phoenix dactylifera 715,001 45.1 70 30 3 35 nad1, nad4L —rpl10, rps10, sdh3,
sdh4
rps2 73,645
(10.3%)
Fang et al. (2012)
Tylosema
esculentum
399,572 44.7 53 15 3 31 nad1, nad4L, mttB, rps10 rps7, rps19 rpl2, rps2, rps11,
rps13
20,205
(5%)
Li and Cullis
(2021)
Ceratonia siliqua 475,642 45.3 62 21 4 34 nad1, nad4L, rps10 rps7 rps2, rps11, rps13 14,126
(2.9%)
Choi et al. (2021)
Vigna unguiculata 383,314 45.1 51 17 3 28 nad1, nad4L, rps10 rps19, sdh4 rpl10, cox2, rps7,
rpl2, rps2, rps11,
rps13, sdh3
3,122
(0.8%)
Choi et al. (2021)
Glycyrrhiza glabra 440,064 45.2 55 20 3 29 nad1, nad4L, rps10 rpl10, rps19, rps7,
sdh4
rpl2, rps2, rps11,
rps13, sdh3
5,688
(1.3%)
Choi et al. (2021)
Haematoxylum
brasiletto
631,094 44.9 65 24 4 32 nad1, atp6, nad4L, mttB,
rps10
rps7, rps13 rps2, rps11 19,949
(3.1%)
Choi et al. (2019)
Ammopiptanthus
nanus
339,352 45.1 52 16 3 30 nad1, nad4L, rps10 rpl10, rps19, rps7 rpl2, rps2, rps11,
rps13, sdh3
28,069
(8.3%)
Feng et al. (2019)
Acacia ligulata 698,138 45.0 59 20 3 34 nad1, rps10 —rps2, rps7, rps11,
rps13, sdh3
62,850
(9%)
Sanchez-Puerta
et al. (2019)
(*) tRNA + rRNA + PCG + GM; (**) intact genes; (***) all DNA sequences of plastid were considered.
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Contreras-Díaz et al. 10.3389/fgene.2023.1226052

angiosperm mitogenomes in varying amounts, representing 0.1%–
10.3% of the mitogenome (Sloan and Wu, 2014). In our comparative
analysis, we found that the percentage coverage of MIPTs ranged
from 0.4% in C. australe to 13% in G. decorticans (Table 1). It is
surprising to note that G. decorticans exhibits higher MIPT coverage
than any other angiosperm species. Initially, we had doubts
regarding the accuracy of our MIPT coverage values. However,
when comparing our findings, such as the 1.3% coverage in G. max,
with the results of other studies such as Gandini and Sanchez-
Puerta, (2017), we found consistency in the values. This provides
confidence in the reliability of our data. In the past MIPTs were
considered as “junk”sequences and were thought to have no
functional contribution to the mitogenome (Wang et al., 2007).
However, recent research has revealed their significance in
mitochondrial function. For instance, rice MIPTs have been
found to possess promoter sequences that are utilized by the
FIGURE 2
Maximum likelihood phylogeny of thirteen Fabaceae mitogenome based on nucleotide datasets of 33 protein-coding genes (left), and with plastid
genomes (right). Bootstrap values are place on the nodes. Scale indicates number of nucleotide substitutions per site.
FIGURE 3
Box-and-whisker plots of Ka/Ks value of 25 protein-coding genes in G. decorticans and ten Papilionoideae species. Each box (with whiskers) shows
the variation of the Ka/Ks values of a gene, among the 11 species studied using G. decorticans as a reference. Box plots show the median (central line),
mean (dot on the box plot) and outliers.
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Contreras-Díaz et al. 10.3389/fgene.2023.1226052

mitochondrial gene atp9 (Nakazono et al., 1996), and tRNA genes of
MIPTs have also been found to contribute functionally to the
mitogenome (Wang et al., 2012). The unusually high percentage
of MIPTs found in G. decorticans may suggest a substantial
acquisition of genes that could play important roles in
mitogenome functioning. Investigating these genes and their
potential contributes in future research would be highly valuable.
The mitogenomes from other angiosperm species that inhabit non-
polar deserts (Table 2) varied between 339,352 and 758.210 bp. The
mitogenomes contained 51 to 70 genes, 12 to 30 tRNA genes and 0.8%–
10.3% MIPT, and were comparable to the mitogenome of the species in
Table 1. Therefore, we did not find a common pattern that characterizes
the mitogenomes of species that are able to inhabit deserts. Interestingly,
the majority of the mitogenomes of the species from the desert contain
an intact sdh4 gene as is observed in G. decorticans, with the exception of
Phoenix dactylifera,Vigna unguiculata and Glycyrrhiza glabra where
the gene is lost or present as a pseudogene. As stated before, the sdh4
gene plays an important role in the response to environmental stress.
We therefore stress the importance of gaining more insight in why this
gene is retained in most of the angiosperms that inhabit deserts. We
observed that RNA editing had occurred in nad1 gene of the majority of
the angiosperms from deserts, however, R. stricta (an extremophile
plant from the desert in South-West Asia) still had the intact gene,
similar as G. decorticans.Rhazya stricta,asG. decorticans,isableto
survive high temperatures and high salinity (Hajrah et al., 2017). We
therefore recommend to evaluate the nad1 gene in species along salinity
gradients.
Previous studies have used plastid genome data to determine the
molecular phylogeny and position of the genus Geoffroea Jack,
including Geoffroea spinosa and G. decorticans (Lee et al., 2021;
Contreras-Díaz et al., 2022). Additionally, researchers have
developed SSR markers specificforG. decorticans to study the
phylogeny and diversity of populations (Contreras et al., 2019;
Contreras Díaz et al., 2021). However, the phylogenetic relationships
of G. decorticans had not been assessed using mitogenome data. To
address this, we analyzed concatenated sequences from 33 PCGs and
complete plastid genome sequences, which were used in ML
phylogenetic analysis. The resulting ML tree revealed two main
clades: one containing the outgroup species L. trichandra and A.
ligulata (Caesalpinioideae), and the other containing all
11 Papilionoideae species. Both clades were strongly supported with
abootstrapvalueof100(Figure 2). Within the Papilionoideae cluster,
four subclades were identified: the Dalbergieae clade consisting of A.
hypogaea,G. decorticans and D. odorifera (BP = 100); the NPAAA (non-
protein–amino-acid-accumulating) clade including L. japonicus,M.
sativa,G. max,P. vulgaris,V. angularis and P. pinnata (BP = 100);
the Genistoids clade, represented solely by S. koreensis (BP = 100); and
the ADA (Angylocalyceae,Dipterygeae,andAmburaneae)clade,which
solely comprised C. australe (BP = 100) (Figure 2). These results align
with previous phylogenetic studies (Cardoso et al., 2013;Choi et al.,
2022). Within the Dalbergieae clade, two subclades were observed: one
containing D. odorifera and the other containing A. hypogaea and G.
decorticans (BP = 100) (Figure 2). This analysis strongly supported G.
decorticans as a sister species of A. hypogaea (BP = 100) (Figure 2).
These two species belong within the Pterocarpus clade, while D.
odorifera belongswithintheDalbergia clade (Cardoso et al., 2013).
Our phylogenetic analysis using the mitogenome database was backed
up by the analysis using the plastid genome database (Figure 2),
confirming the taxonomic classification of G. decorticans.
Phylogenetic analysis of Fabaceae species, along with other
angiosperms suggests that in certain legumes the presence of rpl2,
rps19,andsdh3 genes can be attributed to remnants of a native ancestral
gene (Choi et al., 2019). In our study, we found intact sdh4 and nad1
genes only in G. decorticans and D. odorifera but not in A. hypogaea.
Although these two species do not belong to the same Pterocarpus clade
(Contreras-Díaz et al., 2022), it is possible that these intact genes have
been preserved from a common native ancestor.
Ka/Ks ratios can be used to reflect the natural selective pressure of
protein-coding genes during evolution (Feng et al., 2019). We compared
the Ka/Ks ratio for 25 protein-coding genes in the mitogenomes,
comparing G. decorticans and the ten Papilionoideae species that
were used in our phylogenetic analysis (Figure 3). The mean Ka/Ks
valueinmostprotein-codinggeneswaslessthan1(Figure 3),
suggesting that these genes are purified to keep the genes functional
and remove deleterious mutations. However, the mean Ka/Ks value of
atp8 (1.41) was greater than 1, (Figure 3), indicating that this gene was
subjected to positive selection. Similarly,Ka/Ksvaluesgreaterthan1in
the atp8 gene were founded in the xerophytic legume species,
Ammopiptanthus mongolicus (sister of Ammopiptanthus nanus)
from the desert in northwest China (Feng et al., 2019); and the
authors of this study have speculated that the atp8 gene might play
a role in the adaptation to dry environments. Furthermore, in the same
study the evaluation of the mitogenome of A. mongolicus showed that
the sdh4 gene was found to be intact and unaltered (similar to G.
decorticans),whileinotherlegumesthegenewaslostorpseudogenized
(Feng et al., 2019). Further research is needed to understand why these
two legume species (G. decorticans and A. mongolicus) from deserts on
different continents show similar positive selection of some genes (atp8)
and retention of other genes (such as sdh4).
4 Conclusion
Phylogenetic analysis conducted using the mitogenomes of Chañar
and 12 other taxa revealed a remarkable level of consistency in
taxonomic classification. When compared to other Papilionoideae
species, the structure of the Geoffroea decorticans mitogenome
exhibited minimal changes in terms of gene content, genome size
and functional genes. However, it is important to note that the
mitogenome of G. decorticans displayed distinct rearrangements,
directionality, and organization in comparison to the other
Papilionoideae species. One notable aspect is the conservation of
native mitochondrial DNA in G. decorticans,asshownbypositive
selection for some genes, such as atp8, during evolution. The retention
of the intact sdh4,nad1 and nad4 genes in G. decorticans suggests they
might be important in drought tolerance mechanisms, and therefore in
the species’ability to cope with arid environments, as they have been
lost in many plants that grow under more favorable conditions.
Furthermore, Chañar stands out for possessing the highest amount
of mitochondrial DNA of plastid origin (MIPTs) identified in any
known mitogenome to date. MIPTs are involved in mitogenome
functionality, and their abundance in Chañar is likely a result of the
species’evolutionary adaptation to the extreme environmental
conditions of the Atacama Desert. The acquisition of additional
DNA from other organelles, such as plastids, through horizontal
gene transfer, provides Chañar with unique genetic material that
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Contreras-Díaz et al. 10.3389/fgene.2023.1226052

potentially contributes to its survival strategies. The combination of
conserved genes that facilitate drought stress responses and the
acquisition of plastid material has likely contributed to the
exceptional characteristics of G. decorticans. This species not only
survives, but also provides sustenance to the inhabitants of the driest
desert on Earth, making it an example of adaptation in challenging
environments.
Data availability statement
The datasets presented in this study can be found in online
repositories. The names of the repository/repositories and accession
number(s) can be found below: https://www.ncbi.nlm.nih.gov/
nuccore/OQ707067.1/. The raw reads have been deposited in
NCBI SRA with the number “PRJNA719569”.
Author contributions
RC-D conceptualized, executed the analyses and wrote the first
draft. LvdB and FC provided comments and suggestions for
improvement, and edited the final version. All authors
contributed to the article and approved the submitted version.
Funding
This work was supported by the Universidad de Atacama
(DIUDA 22423), and ANID—MILENIO—NCS 2022_024.
Acknowledgments
We thank José Luis Gutiérrez Alvarado for his picture of the
Chañar tree used in Figure 1. RC-D and FC thanks to AFOREST, a
Millennium Nucleus supported by ANID—MILENIO—NCS
2022_024.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online
at: https://www.frontiersin.org/articles/10.3389/fgene.2023.1226052/
full#supplementary-material
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