Abstract

Among land plants, angiosperms have the structurally most labile mitochondrial (mt) genomes. In contrast, the so-called early land plants (e.g., mosses) seem to have completely static mt chromosomes. We assembled the complete mt genomes from 12 mosses spanning the moss tree of life, to assess 1) the phylogenetic depth of the conserved mt gene content and order and 2) the correlation between scattered sequence repeats and gene order lability in land plants. The mt genome of most mosses is approximately 100 kb in size, and thereby the smallest among land plants. Based on divergence time estimates, moss mt genome structure has remained virtually frozen for 350 My, with only two independent gene losses and a single gene relocation detected across the macroevolutionary tree. This is the longest period of mt genome stasis demonstrated to date in a plant lineage. The complete lack of intergenic repeat sequences, considered to be essential for intragenomic recombinations, likely accounts for the evolutionary stability of moss mt genomes.

Introduction

Plants are well known for their large and, in an evolutionary context, labile mitochondrial (mt) genomes (Palmer and Herbon 1988; Palmer et al. 2000; reviewed by Knoop [2004], Knoop et al. [2011], and Mower et al. [2012]), with the structure differing in some cases among congeneric species or even conspecific populations of angiosperms (Allen et al. 2007; Darracq et al. 2010; Chang et al. 2011). Changes in gene order can result from intragenomic nonhomologous recombination between repeat sequences in intergenic spacers, and the phylogenetic frequency of rearrangements may be correlated to the abundance of such repeats (Maréchal and Brisson 2010; Arrieta-Montiel and Mackenzie 2011).

Approximately 50 land plant mt genomes have been fully sequenced, with a severe sampling bias toward angiosperms. Although the structure of the mt genome has been highly dynamic during the diversification of vascular plants, resulting in an average of 31 rearrangements between any two samples, the structure of early land plant (i.e., bryophyte) mt genome has been largely static (Liu, Wang, Li, et al. 2012). The mt genomes of two hornworts that diverged ±100 Ma (Villarreal and Renner 2012) differ by only five changes in gene order (Li et al. 2009; Xue et al. 2010). Among three liverworts spanning the base of the liverwort tree of life, the mt genome varies slightly in gene content but is constant in gene order (Wang et al. 2009). The two mt genomes available for mosses share an identical set of genes and are completely syntenous (Liu et al. 2011). These two taxa belong to two distinct subclasses of the macroevolutionary crown group of mosses (i.e., those with jointed peristomes; Goffinet et al. 2009), whose diversification started ±200 Ma (Newton et al. 2007). Whether the mt genome synteny extends deeper in the moss tree of life and hence, whether the structural integrity of the mt genome in mosses is maintained over long geological time periods remains unknown.

Results and Discussion

Size and Gene Content of Moss mt Genomes

Shotgun sequencing of genomic extracts yielded complete circular mt genomes for all 12 mosses (supplementary table S1, Supplementary Material online) with a sequencing depth of 58–1,404× (supplementary table S2, Supplementary Material online). These moss mt chromosomes are smaller than any of the other land plants (supplementary table S1, Supplementary Material online), with Buxbaumia having the smallest mt genome among all land plants. The moss mt genomes vary between ±101 and 141 kb (supplementary table S3, Supplementary Material online), a range much narrower than that observed among vascular plants (200–11,000 kb; Chang et al. 2011; Sloan et al. 2012). Within mosses, the mt genome is largest in the most basal genus sampled (i.e., Sphagnum, 141 kb), and assuming this is the plesiomorphic condition, rapidly decreases in size through the loss of introns and shortening of intergenic spacers to ±105 kb in peristomate mosses (fig. 1a). This trend contrasts with the general size increase along the land plant tree of life (fig. 1b). In all peristomate mosses, the total exonic component is larger than both the intronic or intergenic components (fig. 1a and supplementary table S3, Supplementary Material online), in contrast to liverworts, hornworts, and lycophytes, where the exonic regions represent the smallest component (fig. 1b). In mosses and other land plants, the size of exonic regions remains fairly constant. Changes in overall genome size in mosses is due to variations in both introns and intergenic spacers, in sharp contrast to other land plants, where variations in total genome size occur mostly through expansions or contractions in intergenic spacers (fig. 1b).

Fig. 1.

Comparison of mt genome size, intergenic, intronic, and exonic contents among (a) mosses, and (b) land plants. The whole genomic size in (a) is denoted by the left-hand axis, and all the other contents (intergenic, intronic, and exonic) are denoted by the right-hand axis. Pseudogenes and ORFs were included in intergenic content only. The species of mosses or the major lineages of land plants in (a) and (b) are sorted by the phylogeny in figure 2. The number of taxa analyzed for each group is indicated in the bracket following each group’s name in (b).

Fig. 1.

Comparison of mt genome size, intergenic, intronic, and exonic contents among (a) mosses, and (b) land plants. The whole genomic size in (a) is denoted by the left-hand axis, and all the other contents (intergenic, intronic, and exonic) are denoted by the right-hand axis. Pseudogenes and ORFs were included in intergenic content only. The species of mosses or the major lineages of land plants in (a) and (b) are sorted by the phylogeny in figure 2. The number of taxa analyzed for each group is indicated in the bracket following each group’s name in (b).

Moss mt genomes comprise three rRNA genes, 24 tRNA genes, and 40 protein-coding genes, except for Tetraphis and Buxbaumia, which independently lost the nad7 gene, and Ptychomnion whose rpl10 gene is pseudogenized (supplementary fig. S1, Supplementary Material online). In contrast to the mt genomes of liverworts, which have incurred some gene losses, or hornworts that retain only 20 protein-coding genes, the gene composition of moss mt genomes stays relatively constant (±1 gene). Some moss mt genes require RNA editings to re-establish their start or stop codons (supplementary table S4, Supplementary Material online). In total, we predicted 26–371 RNA editing sites for the 12 mosses (supplementary table S5, Supplementary Material online), a level higher than in liverworts (Liu et al. 2011) but much lower than in hornworts (Xue et al. 2010) and vascular plants (Liu, Wang, Cui, et al. 2012).

Causes of Size Variations in Moss mt Genomes

Moss mt genomes share 27 introns, including 3 group I and 24 group II introns (supplementary fig. S1, Supplementary Material online). Only Hypnum lacks one of these, the nad7i209g2 intron. Sphagnum harbors three additional introns: Two group II introns in cox1 (cox1i323g2 and cox1i1200g2) and one group I intron in the ribosomal small subunit gene (rrn18i839g1), with the latter occurring also in the “basal” peristomate mosses (i.e., Tetraphis, Atrichum, and Buxbaumia; supplementary fig. S1, Supplementary Material online). Furthermore, the introns of basal moss lineages tend to be longer: cox1i511g2 and cox2i373g2 in Sphagnum and Atrichum are about 1 kb longer than in other mosses and account for the overall larger intron component of their mt genome (fig. 1a).

Size differences in the introns of basal and nonbasal mosses mirror those in the spacers. The spacers make up approximately 54 kb (i.e., 38% of the whole mt gnome) in Sphagnum but only for 32–38 kb (31–35%) in other mosses (table 1). The mt genomes may expand through localized duplication (Liu, Wang, Cui, et al. 2012), acquisition of foreign mt DNA through horizontal gene transfer (Rice et al. 2013), or intracellular transfer of plastid (Richardson et al. 2013) or nuclear DNA (Goremykin et al. 2012). Within the mt genome of Sphagnum, a 200-bp fragment resulting from the pseudogenization of a duplicate atp8 gene was detected between the nad6 and cox2 gene. Similar pseudogenized fragments were also found in the mt genome of Atrichum and Tetraphis, but overall the duplication of mt genes is rare in mosses, in contrast to liverworts and Huperzia with 14–40 and 70 pseudogenized duplicate genes, respectively (Liu et al. 2011; Liu, Wang, Cui, et al. 2012). Transfer of foreign mt genes into any moss mt genome has not been detected (Liu et al. 2014). The mt genomes of many plants harbor promiscuous DNA of plastid origin, representing 0.5–11.5% of the total mt genome (Alverson et al. 2010; Richardson et al. 2013). DNA of plastid origin was never detected in any of the newly sequenced moss mt genomes (table 1; supplementary table S6, Supplementary Material online), which is consistent with previous observations (Terasawa et al. 2007; Liu et al. 2011).

Table 1.

The Content of Intergenic Spacers of 12 Moss mt Genomes.

Species Spacer Size (bp) (% of the Whole Genome) ORF (%) Repeats (%)a SSR (%) Transposable Element (%) Plastid Origin (%) Nuclear Origin (%)b 
Sphagnum palustre 53,960 (38) 4.9 0.0 0.8 3.5 0.0 19.7 
Atrichum angustatum 37,918 (33) 5.3 0.0 1.1 3.3 0.0 36.7 
Tetraphis pellucida 36,425 (34) 4.0 0.0 0.7 2.2 0.0 29.1 
Buxbaumia aphylla 32,629 (32) 8.0 0.0 1.1 6.2 0.0 26.8 
Funaria hygrometrica 38,477 (35) 9.7 0.0 1.1 3.8 0.0 55.5 
Bartramia pomiformis 34,084 (32) 2.7 0.0 1.6 5.4 0.0 52.1 
Ulota hutchinsiae 32,202 (31) 3.1 0.0 1.3 4.7 0.0 48.6 
Orthotrichum stellatum 31,835 (31) 2.1 0.0 1.3 4.7 0.0 48.1 
Ptychomnion cygnisetum 33,209 (32) 5.3 0.0 1.0 3.4 0.0 46.5 
Climacium americanum 33,148 (32) 2.2 0.0 1.2 3.8 0.0 46.8 
Hypnum imponens 32,935 (32) 5.0 0.0 1.3 3.3 0.0 49.2 
Anomodon attenuatus 32,388 (31) 4.5 0.0 1.0 3.4 0.0 48.0 
Species Spacer Size (bp) (% of the Whole Genome) ORF (%) Repeats (%)a SSR (%) Transposable Element (%) Plastid Origin (%) Nuclear Origin (%)b 
Sphagnum palustre 53,960 (38) 4.9 0.0 0.8 3.5 0.0 19.7 
Atrichum angustatum 37,918 (33) 5.3 0.0 1.1 3.3 0.0 36.7 
Tetraphis pellucida 36,425 (34) 4.0 0.0 0.7 2.2 0.0 29.1 
Buxbaumia aphylla 32,629 (32) 8.0 0.0 1.1 6.2 0.0 26.8 
Funaria hygrometrica 38,477 (35) 9.7 0.0 1.1 3.8 0.0 55.5 
Bartramia pomiformis 34,084 (32) 2.7 0.0 1.6 5.4 0.0 52.1 
Ulota hutchinsiae 32,202 (31) 3.1 0.0 1.3 4.7 0.0 48.6 
Orthotrichum stellatum 31,835 (31) 2.1 0.0 1.3 4.7 0.0 48.1 
Ptychomnion cygnisetum 33,209 (32) 5.3 0.0 1.0 3.4 0.0 46.5 
Climacium americanum 33,148 (32) 2.2 0.0 1.2 3.8 0.0 46.8 
Hypnum imponens 32,935 (32) 5.0 0.0 1.3 3.3 0.0 49.2 
Anomodon attenuatus 32,388 (31) 4.5 0.0 1.0 3.4 0.0 48.0 

Note.—SSR, simple sequence repeat. Taxa are sorted phylogenetically (fig. 2).

aRepeated sequence was detected by BLASTN, sequences with similarity more than 85% and aligned length more than 50 bp were considered as repeat.

bPutative nuclear-derived sequences were detected by blasting the whole-intergenic spacer of each species against the Physcomitrella patens nuclear genome, blast hit with E value ≤ 0.0001 was summarized. For length calculation, overlapped regions in mitochondrial spacers were removed.

The mt genomes may acquire DNA transferred from the nuclear genome in the spacers. Blasting the intergenic spacers against the Physcomitrella nuclear genome (Rensing et al 2008), suggests that an average of 42% (i.e., 20–56%) of the intergenic spacers in mosses presents similarities to nuclear regions, a proportion within the range observed in angiosperms (Rodríguez-Moreno et al. 2011; Goremykin et al. 2012). Given the scattered distribution of these sequences within the mt genome, transfers from the nuclear genome likely occurred multiple times within lineages. Our estimate of mt DNA of nuclear origin is preliminary, because the Physcomitrella nuclear genome is the only reference currently available. The comparison of the mt spacers of Funaria to the Physcomitrella genome returned the highest proportion (56%) of similarity as they both belong to the same family (Funariaceae), whereas the spacer regions of the most distantly related taxon (i.e., Sphagnum) revealed only 20%, a conservative estimate likely to increase following intergenomic comparison within Sphagnum. Finally, short tandem repeats or so-called simple sequence repeats, which consist mostly of mononucleotide and dinucleotide repeats (supplementary table S7, Supplementary Material online), account for about 1% of the moss mt intergenic spacers, whereas relicts of transposable elements compose 4% and open-reading frames (ORFs) 5%.

The Stasis of mt Genome Structure in Mosses

Moss mt genomes are largely syntenous (supplementary fig. S2, Supplementary Material online). Among the 14 mt genomes compared here, only one gene relocation was observed (supplementary table S6, Supplementary Material online) and confirmed by polymerase chain reaction and Sanger sequencing. The mt genomes of three liverworts also share an identical gene order, whereas those of two hornworts differ by five rearrangements (Li et al. 2009; Xue et al. 2010). Whether this pattern is indicative of a trend of increased lability, set in hornworts and maintained in their putative sister group, the vascular plants, is not clear, as only one complete lycophyte and one gymnosperm mt genome are currently available. Consistent with such hypothesis is the identical gene order shared by two deeply rooted streptophytes (i.e., Chara and Nitella) and the extensive rearrangements observed among angiosperms (fig. 2), wherein on average, any two mt genomes differ by 31 rearrangements, with many rearrangements observed within genera (to 15 in Brassica, 11 in Oryza, or 26 in Zea; supplementary fig. S3, Supplementary Material online).

Fig. 2.

Heat map of mt genome rearrangements in pairwise comparisons of land plants along a phylogenetic tree based on mt amino acid sequences with divergence times estimated under a relaxed clock model implemented in r8s. Confidence intervals with 95% standard error are shown by bars for the nodes with fossil constraints (supplementary table S8, Supplementary Material online). For age estimates, the age of the crown group of land plants was fixed as 472 Ma. The number of repeats detected from intergenic spacers of each species is listed beside the tree.

Fig. 2.

Heat map of mt genome rearrangements in pairwise comparisons of land plants along a phylogenetic tree based on mt amino acid sequences with divergence times estimated under a relaxed clock model implemented in r8s. Confidence intervals with 95% standard error are shown by bars for the nodes with fossil constraints (supplementary table S8, Supplementary Material online). For age estimates, the age of the crown group of land plants was fixed as 472 Ma. The number of repeats detected from intergenic spacers of each species is listed beside the tree.

The robust phylogenetic tree inferred from the amino acid data set of 40 mt protein-coding genes (fig. 2 and supplementary fig. S3, Supplementary Material online) is congruent with previously published land plant phylogenies (Qiu et al. 2006). Divergence time estimates suggest that mosses arose approximately 470 Ma, and the deepest cladogenic event among extant mosses occurred ±350 Ma (mean = 352 Ma, standard deviation = 8 Ma; fig. 2), congruent with previous inferences (Clarke et al. 2011; Magallón et al. 2013). Consequently, the structure of the mt genome of mosses has remained virtually frozen for 350 My, the longest period of structural stasis of an mt genome during the diversification of land plants. Such stasis may also characterize liverworts should the assembly of the mt genome of derived leafy liverworts reveal a completely syntenous mt genome to that of Pleurozia and thalloid taxa, which compose a basal grade among liverworts.

Underlying Causes for the Stasis of Moss mt Genomes

The mt genome rearrangements result from nonhomologous, intragenomic recombination facilitated by nonadjacent sequence repeats longer than 50 bp and 85% or more similar (Andre et al. 1992; Maréchal and Brisson 2010; Arrieta-Montiel and Mackenzie 2011). Only rearrangements anchored by repeats in intergenic versus in genic regions may withstand selection and be maintained. The mt genome of vascular plants holds few to many pairs of such repeated sequences: 12–2,409 in flowering plants, 19–69 in lycophytes, and 14,031 in the sole gymnosperm sampled so far, Cycas (Chaw et al. 2008; fig. 2). In contrast, mt genomes of mosses, except those of Sphagnum and Atrichum, lack intergenic repeats (fig. 2), which may explain their stability. Overall, the number of intergenic repeats is positively correlated with mt genome size in land plants (fig. 3). This pattern vanishes if all green eukaryotes are considered, as the mt genome of many algae is small yet rich in repeated sequences (supplementary table S6, Supplementary Material online).

Fig. 3.

Correlation between the size of the mt genome and the number of repeats (>50 bp; similarity >85%) detected in intergenic spacers within land plants. The taxa are sorted on x-axis in the order of genome sizes. In vascular plants, two extreme outliers (Cucurbita and Cycas) with much higher numbers of repeats (fig. 2) were excluded from the analysis.

Fig. 3.

Correlation between the size of the mt genome and the number of repeats (>50 bp; similarity >85%) detected in intergenic spacers within land plants. The taxa are sorted on x-axis in the order of genome sizes. In vascular plants, two extreme outliers (Cucurbita and Cycas) with much higher numbers of repeats (fig. 2) were excluded from the analysis.

Given that the mt genome of liverworts has a considerable number of repeats in intergenic spacers (9–48), yet maintains its gene order, repeated sequences seem to be necessary but not sufficient to allow for intragenomic recombination. Indeed, the structure of the mt genome is maintained by a set of nuclear genes (Maréchal and Brisson 2010; Arrieta-Montiel and Mackenzie 2011), including the MutS homolog 1 (Arabidopsis; Shedge et al. 2007; Davila et al. 2011) and RecA-like recombinases (Arabidopsis; Miller-Messmer et al. 2012; Physcomitrella; Odahara et al. 2009), and knockouts of these genes lead to an increase in mt genome recombination. Thus, the structural evolution of the mt genome in land plants may be shaped by both the intrinsic (i.e., abundance and distribution of repeats) and extrinsic (i.e., control via nuclear genes) parameters.

The nature of the selective forces that maintain the highly conserved mt genome structure of mosses and liverworts is not known. It is possible that organization of genes is essential to the transcription of polycistronic operons. Angiosperm mt genomes maintain multiple promoters in the upstream region of many genes (Lupold et al. 1999; Kühn et al. 2005; Zhang and Liu 2006), which may insure transcription in case of potential intragenomic rearrangement (Kühn et al. 2005; Liere and Börner 2011). If early land plants lack multiple promoters, strong selection for stable mt genome would prevent disruption of operons and hence the gene transcription due to genic rearrangements.

Materials and Methods

Complete mt genomes from 12 mosses were sequenced using the next-generation sequencing method. The mt genomes have been deposited in the GenBank database (accession numbers: JX402749 and KC784949–KC784959). See supplementary material, Supplementary Material online, for detailed information on taxon sampling, mt genome sequencing, assembly, annotation, and comparative analyses.

Supplementary Material

Supplementary materials and methods, figures S1–S3, and tables S1–S8 are available at Molecular Biology and Evolution online (http://www.mbe.oxfordjournals.org/).

Acknowledgments

The authors thank Louise A. Lewis, Lily R. Lewis (UConn), and Wei Wang (IBCAS) for suggestions on an earlier draft of the article, and Yingying Xie (UConn) for assisting with the heat map. They thank University of Connecticut Health Center Translational Genomics Core Facility (Farmington, CT) for use of the Illumina instrument. The UConn Bioinformatics Facility provided computing resources for the phylogenetic and molecular dating analyses. This work was supported by the National Science Foundation grants (DEB-1146295 and 1212505) to B.G.

References

Allen
JO
Fauron
CM
Minx
P
Roark
L
Oddiraju
S
Lin
GN
Meyer
L
Sun
H
Kim
K
Wang
C
Comparisons among two fertile and three male-sterile mitochondrial genomes of maize
Genetics
 , 
2007
, vol. 
177
 (pg. 
1173
-
1192
)
Alverson
AJ
Wei
X
Rice
DW
Stern
DB
Barry
K
Palmer
JD
Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae)
Mol Biol Evol.
 , 
2010
, vol. 
27
 (pg. 
1436
-
1448
)
Andre
C
Levy
A
Walbot
V
Small repeated sequences and the structure of plant mitochondrial genomes
Trends Genet.
 , 
1992
, vol. 
8
 (pg. 
128
-
132
)
Arrieta-Montiel
MP
Mackenzie
SA
Kempken
F
Plant mitochondrial genomes and recombination
Plant mitochondria
 , 
2011
New York
Springer
(pg. 
65
-
82
)
Chang
S
Yang
T
Du
T
Huang
Y
Chen
J
Yan
J
He
J
Guan
R
Mitochondrial genome sequencing helps show the evolutionary mechanism of mitochondrial genome formation in Brassica
BMC Genomics
 , 
2011
, vol. 
12
 pg. 
497
 
Chaw
S-M
Shih
AC-C
Wang
D
Wu
Y-W
Liu
S-M
The mitochondrial genome of the gymnosperm Cycas taitungensis contains a novel family of short interspersed elements, Bpu sequences, and abundant RNA editing sites
Mol Biol Evol.
 , 
2008
, vol. 
25
 (pg. 
603
-
615
)
Clarke
JT
Warnock
R
Donoghue
PC
Establishing a time-scale for plant evolution
New Phytol.
 , 
2011
, vol. 
192
 (pg. 
266
-
301
)
Darracq
A
Varré
J-S
Touzet
P
A scenario of mitochondrial genome evolution in maize based on rearrangement events
BMC Genomics
 , 
2010
, vol. 
11
 pg. 
233
 
Davila
JI
Arrieta-Montiel
MP
Wamboldt
Y
Cao
J
Hagmann
J
Shedge
V
Xu
YZ
Weigel
D
Mackenzie
SA
Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis
BMC Biol.
 , 
2011
, vol. 
9
 pg. 
64
 
Goffinet
B
Buck
WR
Shaw
AJ
Goffinet
B
Shaw
AJ
Morphology, anatomy, and classification of the Bryophyta
Bryophyte biology
 , 
2009
2nd ed
Cambridge
Cambridge University Press
(pg. 
55
-
138
)
Goremykin
VV
Lockhart
PJ
Viola
R
Velasco
R
The mitochondrial genome of Malus domestica and the import-driven hypothesis of mitochondrial genome expansion in seed plants
Plant J.
 , 
2012
, vol. 
71
 (pg. 
615
-
626
)
Knoop
V
The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective
Curr Genet.
 , 
2004
, vol. 
46
 (pg. 
123
-
139
)
Knoop
V
Volkmar
U
Hecht
J
Grewe
F
Kempken
F
Mitochondrial genome evolution in the plant lineage
Plant mitochondria
 , 
2011
New York
Springer
(pg. 
3
-
29
)
Kühn
K
Weihe
A
Börner
T
Multiple promoters are a common feature of mitochondrial genes in Arabidopsis
Nucleic Acids Res.
 , 
2005
, vol. 
33
 (pg. 
337
-
346
)
Li
L
Wang
B
Liu
Y
Qiu
YL
The complete mitochondrial genome sequence of the hornwort Megaceros aenigmaticus shows a mixed mode of conservative yet dynamic evolution in early land plant mitochondrial genomes
J Mol Evol.
 , 
2009
, vol. 
68
 (pg. 
665
-
678
)
Liere
K
Börner
T
Kempken
F
Transcription in plant mitochondria
Plant mitochondria
 , 
2011
New York
Springer
(pg. 
85
-
105
)
Liu
Y
Xue
JY
Wang
B
Li
L
Qiu
YL
The mitochondrial genomes of the early land plants Treubia lacunosa and Anomodon rugelii: dynamic and conservative evolution
PLoS One
 , 
2011
, vol. 
6
 pg. 
e25836
 
Liu
Y
Wang
B
Cui
P
Li
L
Xue
JY
Yu
J
Qiu
YL
The mitochondrial genome of the lycophyte Huperzia squarrosa: the most archaic form in vascular plants
PLoS One
 , 
2012
, vol. 
7
 pg. 
e35168
 
Liu
Y
Wang
B
Li
L
Qiu
YL
Xue
JY
Bock
R
Knoop
V
Conservative and dynamic evolution of mitochondrial genomes in early land plants
Genomics of chloroplasts and mitochondria
 , 
2012
The Netherlands
Springer
(pg. 
159
-
174
)
Liu
Y
Cox
CJ
Wang
W
Goffinet
B
Mitochondrial phylogenomics of early land plants: Mitigating the effects of saturation, compositional heterogeneity, and codon-usage bias
Syst Bio.
  
Advance Access published July 28, 2014, doi:10.1093/sysbio/syu049.
Lupold
DS
Caoile
AG
Stern
DB
The maize mitochondrial cox2 gene has five promoters in two genomic regions, including a complex promoter consisting of seven overlapping units
J Biol Chem.
 , 
1999
, vol. 
274
 (pg. 
3897
-
3903
)
Magallón
S
Hilu
KW
Quandt
D
Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates
Am J Bot.
 , 
2013
, vol. 
100
 (pg. 
556
-
573
)
Maréchal
A
Brisson
N
Recombination and the maintenance of plant organelle genome stability
New Phytol.
 , 
2010
, vol. 
186
 (pg. 
299
-
317
)
Miller-Messmer
M
Kühn
K
Bichara
M
Le Ret
M
Imbault
P
Gualberto
JM
RecA-dependent DNA repair results in increased heteroplasmy of the Arabidopsis mitochondrial genome
Plant Physiol.
 , 
2012
, vol. 
159
 (pg. 
211
-
226
)
Mower
JP
Sloan
DB
Alverson
AJ
Wendel
JF
Greilhuber
J
Dolezel
J
Leitch
IJ
Plant mitochondrial genome diversity: the genomics revolution
Plant genome diversity
 , 
2012
, vol. 
Vol. 1
 
Vienna
Springer
(pg. 
123
-
144
)
Newton
AE
Wikström
N
Bell
N
Forrest
LL
Ignatov
MS
Newton
AE
Tangney
RS
Dating the diversification of the pleurocarpous mosses
Pleurocarpous mosses, systematics and evolution
 , 
2007
Boca Raton (FL)
CRC Press
(pg. 
337
-
366
)
Odahara
M
Kuroiwa
H
Kuroiwa
T
Sekine
Y
Suppression of repeat-mediated gross mitochondrial genome rearrangements by RecA in the moss Physcomitrella patens
Plant Cell
 , 
2009
, vol. 
21
 (pg. 
1182
-
1194
)
Palmer
JD
Adams
KL
Cho
Y
Parkinson
CL
Qiu
YL
Song
K
Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates
Proc Natl Acad Sci U S A.
 , 
2000
, vol. 
97
 (pg. 
6960
-
6966
)
Palmer
JD
Herbon
LA
Plant mitochondrial DNA evolved rapidly in structure, but slowly in sequence
J Mol Evol.
 , 
1988
, vol. 
28
 (pg. 
87
-
97
)
Qiu
YL
Li
L
Wang
B
Chen
Z
Knoop
V
Groth-Malonek
M
Dombrovska
O
Lee
J
Kent
L
Rest
J
, et al.  . 
The deepest divergences in land plants inferred from phylogenomic evidence
Proc Natl Acad Sci U S A.
 , 
2006
, vol. 
103
 (pg. 
15511
-
15516
)
Rensing
SA
Lang
D
Zimmer
AD
Terry
A
Salamov
A
Shapiro
H
Nishiyama
T
Perroud
P-F
Lindquist
EA
Kamisugi
Y
, et al.  . 
The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants
Science
 , 
2008
, vol. 
319
 (pg. 
64
-
69
)
Rice
DW
Alverson
AJ
Richardson
AO
Young
GJ
Sanchez-Puerta
MV
Munzinger
J
Barry
K
Boore
JL
Zhang
Y
Knox
EB
Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella
Science
 , 
2013
, vol. 
342
 (pg. 
1468
-
1473
)
Richardson
AO
Rice
DW
Young
GJ
Alverson
AJ
Palmer
JD
The “fossilized” mitochondrial genome of Liriodendron tulipifera: ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate
BMC Biol.
 , 
2013
, vol. 
11
 pg. 
29
 
Rodríguez-Moreno
L
González
V
Benjak
A
Martí
MC
Puigdomènech
P
Aranda
M
Garcia-Mas
J
Determination of the melon chloroplast and mitochondrial genome sequences reveals that the largest reported mitochondrial genome in plants contains a significant amount of DNA having a nuclear origin
BMC Genomics
 , 
2011
, vol. 
12
 pg. 
424
 
Shedge
V
Arrieta-Montiel
M
Christensen
AC
Mackenzie
SA
Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs
Plant Cell
 , 
2007
, vol. 
19
 (pg. 
1251
-
1264
)
Sloan
DB
Alverson
AJ
Chuckalovcak
JP
Wu
M
McCauley
DE
Palmer
JD
Taylor
DR
Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates
PLoS Biol.
 , 
2012
, vol. 
10
 pg. 
e1001241
 
Terasawa
K
Odahara
M
Kabeya
Y
Kikugawa
T
Sekine
Y
Fujiwara
M
Sato
N
The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants
Mol Biol Evol.
 , 
2007
, vol. 
24
 (pg. 
699
-
709
)
Villarreal
JC
Renner
SS
Hornwort pyrenoids, carbon-concentrating structures, evolved and were lost at least five times during the last 100 million years
Proc Natl Acad Sci U S A.
 , 
2012
, vol. 
109
 (pg. 
18873
-
18878
)
Wang
B
Xue
JY
Li
L
Liu
Y
Qiu
YL
The complete mitochondrial genome sequence of the liverwort Pleurozia purpurea reveals extremely conservative mitochondrial genome evolution in liverworts
Curr Genet.
 , 
2009
, vol. 
55
 (pg. 
601
-
609
)
Xue
JY
Liu
Y
Li
L
Wang
B
Qiu
YL
The complete mitochondrial genome sequence of the hornwort Phaeoceros laevis: retention of many ancient pseudogenes and conservative evolution of mitochondrial genomes in hornworts
Curr Genet.
 , 
2010
, vol. 
56
 (pg. 
53
-
61
)
Zhang
QY
Liu
YG
Rice mitochondrial genes are transcribed by multiple promoters that are highly diverged
J Integr Plant Biol.
 , 
2006
, vol. 
48
 (pg. 
1473
-
1477
)

Author notes

Associate editor: Brandon Gaut