Small BMC Biology 2013, 11:30http://www.biomedcentral.com/1741-7007/11/30

COMMENTARY Open Access

Mitochondrial genomes as living ‘fossils’Ian Small

Abstract

The huge variation between mitochondrial genomesmakes untangling their evolutionary histories difficult.Richardson et al. report on the remarkably unaltered‘fossil’ genome of the tulip tree, giving us many cluesas to how the mitochondrial genomes of floweringplants have evolved over the last 150 million years,and raising questions about how such extraordinarysequence conservation can be maintained.

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were present in the ancestral flowering plant mito-

CommentaryAlthough they are all thought to derive from a singleendosymbiotic relationship, mitochondrial genomesshow extraordinary diversity. They include examples ofthe smallest (non-viral) genomes known and exampleslarger than most bacterial genomes [1]. They includesome of the fastest mutating genomes and some of theslowest [1]. In metazoans, mitochondrial gene order isusually invariant over tens or even hundreds of millionsof years, whereas in plants, mitochondrial gene orderoften differs between organelles in the same cell [2].Some use different genetic codes and some alter thesequence of their RNA to code for proteins that are notcoded in the genome [3]. Together, they offer fascinatinginsights into evolutionary processes at work. The diffi-culty lies in extrapolating backwards from present daydiversity to imagine what the ancestral state at any onepoint might have been. The new paper by Richardsonet al. [4] not only provides yet another record-breakingmitochondrial genome with its share of ‘gee-whizz’ char-acteristics, it also turns out to be an extremely usefulwindow into the past.Richardson et al. chose to study the tulip tree

(Liriodendron tulipifera L.), a native of the eastern

Correspondence: ian.small@uwa.edu.auAustralian Research Council Centre of Excellence in Plant Energy Biology,Bayliss Building, The University of Western Australia, 35 Stirling Highway,Crawley, WA 6009, Australia

© 2013 Small; licensee BioMed Central Ltd. ThCommons Attribution License (http://creativecreproduction in any medium, provided the or

United States, but widely grown elsewhere as a magnificentspecimen tree in parks and gardens (Figure 1a). The spec-tacular flowers (Figure 1b, c) make it clear that this is aflowering plant (Magnoliophyta), but most admirers won’trealize that the tulip tree is a member of an early-branchinglineage, quite separate from the bulk of flowering plants inthe monocot and dicot clades. As all our important cropplants lie in these two dominant clades, they have been thetargets of almost all the sequencing efforts around theworld. As a result, for many of the important moleculartraits that differ between monocots and dicots, we cannottell which is the ancestral state. The new sequencefrom the tulip tree helps to understand what genes

chondrial genome, which ones were clustered together,which ones were captured from chloroplast DNA andwhen, which ones contained introns, and the degreeto which each gene required editing of its RNA tran-scripts. It answers these questions particularly convin-cingly because of its most startling characteristic - themitochondrial genome of the tulip tree (and those ofits relatives, the magnolias) contain the most slowlyevolving genes ever studied. Some of the Magnoliagenes appear to have acquired no mutations at all in50 million years [4]. This ‘fossilized’ genome gives ussome important clues as to what mitochondrial genomeslooked like (and how they functioned) as floweringplants evolved and took over the land in the time ofthe dinosaurs.

‘Fossilizing’ a genomeLike all good science, this work raises as many questionsas it answers, and one obvious one that will exercise theminds of researchers everywhere is how can an organismso effectively prevent its genome from acquiring muta-tions? Mitochondrial genomes are subject to recurrentdamage from reactive oxygen species generated by therespiratory electron transport chain, not to mentionunavoidable polymerase errors during DNA replication[5]. Mitochondria are generally uniparentally inheritedin plants, limiting the possibility of eliminating muta-tions by sexual recombination, and, in any case, plant

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Figure 1. Tulip trees are a popular feature in parks and gardens. (a) The American tulip tree, Liriodendron tulipifera. Photo by Jean-PolGrandmont. (b) Side view of a flower, the shape of which gives the tree its name. (c) Top view of a flower.

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mitochondrial genomes show very low rate of change atsilent sites too, not just functionally important sites.Hence, low mutation rates are largely due to mecha-nisms that suppress or correct mutations, rather than tonatural selection.One factor of uncertain importance is life span.

Genomes of long-lived organisms tend to be copied lessoften, but it is unclear how important this is in plants,which lack a clearly segregated germ line, and can repro-duce at a relatively young age, even in long-lived species.Probably of more importance is that long-lived organ-isms tend to have much stronger defenses againstgenotoxic damage, due to selection against prematuresomatic senescence [6]. Indeed, there is very activeresearch into the possible links between mitochondrialgenome damage and aging in humans [5]. The tulip treecomes from a long line of woody perennials with rela-tively long life spans and can live to 300 to 400 years old(the oldest living organism in New York is reputed tobe a tulip tree, the ‘Queens Giant’). It is likely, therefore,that it possesses excellent biochemical protection (anti-oxidants and the like) against genome damage.Plant mitochondria also possess highly active mis-

match repair and recombination machinery. Recent ad-vances by several labs have identified many of thecomponents of this machinery, some of which are clearlyderived from the original bacterial endosymbiont, someof which appear to be novel. Key players include theDNA mismatch repair protein MSH1 (related to bacter-ial MutS) and a small family of RecA homologs likely to

be involved in DNA strand exchange during homolo-gous recombination [7]. Active strand exchange andgene conversion amongst the multiple copies of themitochondrial genome in a single cell are likely to act tosuppress the fixation of mutations [2], but as yet therehave not been any comparisons between the compo-nents active in species with fast-mutating genomes (forexample, some Silene [1]) or slow-mutating genomes(for example, Liriodendron). As the rate of fixation ofmutations can vary by 5,000-fold [4], we might expectsome fairly obvious differences to be revealed were sucha comparison to be made.

‘Fossilizing’ a proteomePlant organelles (both mitochondria and chloroplasts)have a third line of defense in addition to biochemicalprotection from genome damage and post-damage repairof DNA lesions. They can edit their RNA to alter itscoding function, enabling proteins to be produced thatwere ‘incorrectly’ coded in the DNA sequence. RNAediting depends on large numbers of highly specifictrans-factors, each of which is capable of targeting a spe-cific base to be edited (reviewed in [3]). In general, RNAediting restores conserved amino acids and leads to theprotein sequences resembling the ancestral sequencemore closely than the codon sequence in the DNA does.In this way, the proteome of plant organelles is morehighly conserved than the genome. The extent to whichthis process occurs varies widely, with the highest ratesof RNA editing seen in early diverging vascular plants

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such as ferns and lycophytes and the lowest seen in veryearly diverging lineages such as some liverworts [8].Flowering plants have intermediate levels of RNA editing(for example, approximately 500 sites in Arabidopsisorganelles). This has led to proposals that followingrapid accumulation of new editing sites during the evo-lution of land plants, flowering plants may now be losingediting sites through random back-mutation and reversetranscription of edited transcripts (reviewed in [3]).Richardson et al. provide important new data on the

evolution of RNA editing in plants. The Liriodendronmitochondrial transcriptome is edited at at least 781sites, more than in any other flowering plant studied todate [4]. Many of these sites are at identical positions tothose found in monocots, dicots or both, indicating thatthey are ancestral sites, not newly created sites. This isstrong evidence that the earlier proposals are correct(flowering plants are tending to lose more sites than theygain). What could be the drivers for these long-termtendencies in creation and loss of RNA editing sites?Overall, there is a positive correlation between C-to-URNA editing and GC content of the genome [9], so it islikely that it is mutation/repair processes at the genomelevel that are driving changes in editing frequency overevolutionary timescales. One highly speculative theory isthat changes in UV damage (and thus rate of genomicmutation of T to C) may be the primary cause of thesetrends, but it could equally be inherent biases duringgene conversion events [9].

The future is in the pastThe increasing cost-effectiveness of genome and tran-scriptome sequencing is making it easier for re-searchers to strategically choose the most informativespecies rather than having to make do with thosethat are economically important and therefore easiertargets for funding. The coverage of early divergingplants is still far from optimal, with many large andimportant groups still barely sampled (for example,gymnosperms and ferns). Ideally, we would like allthree genomes at once, as a comparison of the twoorganelle genomes is often highly informative, and thenuclear genome provides the sequences of all of thepotential molecular factors influencing the processesunder study. In this context, a particularly excitingdevelopment is the elucidation of the molecular basisfor sequence recognition by RNA editing factors [10],permitting prediction of which factor edits whichRNA site [11]. This breakthrough will greatly acceler-ate comparative genomics of RNA editing and addslots of value to any complete genome sequence. I lookforward to being able to analyze the next molecular‘fossil’ to roll off the sequencing machines!

AcknowledgementsThis research was supported by Australian Research Council grantCE0561495.

References1. Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD,

Taylor DR: Rapid evolution of enormous, multichromosomal genomes inflowering plant mitochondria with exceptionally high mutation rates.PLoS Biol 2012, 10:e1001241.

2. Davila JI, Arrieta-Montiel MP, Wamboldt Y, Cao J, Hagmann J, Shedge V, XuYZ, Weigel D, Mackenzie SA: Double-strand break repair processes driveevolution of the mitochondrial genome in Arabidopsis. BMC Biol 2011,9:64.

3. Fujii S, Small I: The evolution of RNA editing and pentatricopeptiderepeat genes. New Phytol 2011, 191:37–47.

4. Richardson AO, Rice DW, Young GJ, Alverson AJ, Palmer JD: The “fossilized”mitochondrial genome of Liriodendron tulipifera: Ancestral gene contentand order, ancestral editing sites, and extraordinarily low mutation rate.BMC Biol, 11:29.

5. Bratic A, Larsson NG: The role of mitochondria in aging. J Clin Invest 2013,123:951–957.

6. Galtier N, Jobson RW, Nabholz B, Glemin S, Blier PU: Mitochondrial whims:metabolic rate, longevity and the rate of molecular evolution. Biol Lett2009, 5:413–416.

7. Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA: Plantmitochondrial recombination surveillance requires unusual RecA andMutS homologs. Plant Cell 2007, 19:1251–1264.

8. Rudinger M, Volkmar U, Lenz H, Groth-Malonek M, Knoop V: NuclearDYW-type PPR gene families diversify with increasing RNA editingfrequencies in liverwort and moss mitochondria. J Mol Evol 2012, 74:37–51.

9. Smith DR: Updating our view of organelle genome nucleotide landscape.Front Genet 2012, 3:175.

10. Barkan A, Rojas M, Fujii S, Yap A, Chong YS, Bond CS, Small I:A combinatorial amino acid code for RNA recognition bypentatricopeptide repeat proteins. PLoS Genet 2012, 8:e1002910.

11. Yagi Y, Hayashi S, Kobayashi K, Hirayama T, Nakamura T: Elucidation of theRNA recognition code for pentatricopeptide repeat proteins involved inorganelle RNA editing in plants. PLoS One 2013, 8:e57286.

doi:10.1186/1741-7007-11-30Cite this article as: Small I: Mitochondrial genomes as living ‘fossils’.BMC Biology 2013 11:30.

Published: 15 April 2013