Pervasive survival of expressed mitochondrial rps14 pseudogenes in grasses and their relatives for 80 million years following three functional transfers to the nucleus

BACKGROUND: Many mitochondrial genes, especially ribosomal protein genes, have been frequently transferred as functional entities to the nucleus during plant evolution, often by an RNA-mediated process. A notable case of transfer involves the rps14 gene of three grasses (rice, maize, and wheat), which has been relocated to the intron of the nuclear sdh2 gene and which is expressed and targeted to the mitochondrion via alternative splicing and usage of the sdh2 targeting peptide. Although this transfer occurred at least 50 million years ago, i.e., in a common ancestor of these three grasses, it is striking that expressed, nearly intact pseudogenes of rps14 are retained in the mitochondrial genomes of both rice and wheat. To determine how ancient this transfer is, the extent to which mitochondrial rps14 has been retained and is expressed in grasses, and whether other transfers of rps14 have occurred in grasses and their relatives, we investigated the structure, expression, and phylogeny of mitochondrial and nuclear rps14 genes from 32 additional genera of grasses and from 9 other members of the Poales. RESULTS: Filter hybridization experiments showed that rps14 sequences are present in the mitochondrial genomes of all examined Poales except for members of the grass subfamily Panicoideae (to which maize belongs). However, PCR amplification and sequencing revealed that the mitochondrial rps14 genes of all examined grasses (Poaceae), Cyperaceae, and Joinvilleaceae are pseudogenes, with all those from the Poaceae sharing two 4-NT frameshift deletions and all those from the Cyperaceae sharing a 5-NT insertion (only one member of the Joinvilleaceae was examined). cDNA analysis showed that all mitochondrial pseudogenes examined (from all three families) are transcribed, that most are RNA edited, and that surprisingly many of the edits are reverse (U→C) edits. Putatively nuclear copies of rps14 were isolated from one to several members of each of these three Poales families. Multiple lines of evidence indicate that the nuclear genes are probably the products of three independent transfers. CONCLUSION: The rps14 gene has, most likely, been functionally transferred from the mitochondrion to the nucleus at least three times during the evolution of the Poales. The transfers in Cyperaceae and Poaceae are relatively ancient, occurring in the common ancestor of each family, roughly 80 million years ago, whereas the putative Joinvilleaceae transfer may be the most recent case of functional organelle-to-nucleus transfer yet described in any organism. Remarkably, nearly intact and expressed pseudogenes of rps14 have persisted in the mitochondrial genomes of most lineages of Poaceae and Cyperaceae despite the antiquity of the transfers and of the frameshift and RNA editing mutations that mark the mitochondrial genes as pseudogenes. Such long-term, nearly pervasive survival of expressed, apparent pseudogenes is to our knowledge unparalleled in any genome. Such survival probably reflects a combination of factors, including the short length of rps14, its location immediately downstream of rpl5 in most plants, and low rates of nucleotide substitutions and indels in plant mitochondrial DNAs. Their survival also raises the possibility that these rps14 sequences may not actually be pseudogenes despite their appearance as such. Overall, these findings indicate that intracellular gene transfer may occur even more frequently in angiosperms than already recognized and that pseudogenes in plant mitochondrial genomes can be surprisingly resistant to forces that lead to gene loss and inactivation

Fall armyworm (Spodoptera frugiperda Smith) feeding elicits differential defense responses in upland and lowland switchgrass

Switchgrass (Panicum virgatum L.) is a low input, high biomass perennial grass being developed for the bioenergy sector. Upland and lowland cultivars can differ in their responses to insect herbivory. Fall armyworm [FAW; Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae)] is a generalist pest of many plant species and can feed on switchgrass as well. Here, in two different trials, FAW larval mass were significantly reduced when fed on lowland cultivar Kanlow relative to larvae fed on upland cultivar Summer plants after 10 days. Hormone content of plants indicated elevated levels of the plant defense hormone jasmonic acid (JA) and its bioactive conjugate JA-Ile although significant differences were not observed. Conversely, the precursor to JA, 12-oxo-phytodienoic acid (OPDA) levels were significantly different between FAW fed Summer and Kanlow plants raising the possibility of differential signaling by OPDA in the two cultivars. Global transcriptome analysis revealed a stronger response in Kanlow plant relative to Summer plants. Among these changes were a preferential upregulation of several branches of terpenoid and phenylpropanoid biosynthesis in Kanlow plants suggesting that enhanced biosynthesis or accumulation of antifeedants could have negatively impacted FAW larval mass gain on Kanlow plants relative to Summer plants. A comparison of the switchgrass-FAW RNA-Seq dataset to those from maize-FAW and switchgrass-aphid interactions revealed that key components of plant responses to herbivory, including induction of JA biosynthesis, key transcription factors and JA-inducible genes were apparently conserved in switchgrass and maize. In addition, these data affirm earlier studies with FAW and aphids that the cultivar Kanlow can provide useful genetics for the breeding of switchgrass germplasm with improved insect resistance

Evolutionary Significance Of The Loss Of The Chloroplast‐Dna Inverted Repeat In The Leguminosae Subfamily Papilionoideae

Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/137404/1/evo05207.pd

Multigene analyses identify the three earliest lineages of extant flowering plants

AbstractFlowering plants (angiosperms) are by far the largest, most diverse, and most important group of land plants, with over 250,000 species and a dominating presence in most terrestrial ecosystems. Understanding the origin and early diversification of angiosperms has posed a long-standing botanical challenge [1]. Numerous morphological and molecular systematic studies have attempted to reconstruct the early history of this group, including identifying the root of the angiosperm tree. There is considerable disagreement among these studies, with various groups of putatively basal angiosperms from the subclass Magnoliidae having been placed at the root of the angiosperm tree (reviewed in [2–4]). We investigated the early evolution of angiosperms by conducting combined phylogenetic analyses of five genes that represent all three plant genomes from a broad sampling of angiosperms. Amborella, a monotypic, vesselless dioecious shrub from New Caledonia, was clearly identified as the first branch of angiosperm evolution, followed by the Nymphaeales (water lilies), and then a clade of woody vines comprising Schisandraceae and Austrobaileyaceae. These findings are remarkably congruent with those from several concurrent molecular studies [5–7] and have important implications for whether or not the first angiosperms were woody and contained vessels, for interpreting the evolution of other key characteristics of basal angiosperms, and for understanding the timing and pattern of angiosperm origin and diversification

A re-assessment of the distribution of Virginia\u27s warbler in the Black Hills of South Dakota

Virginia’s Warbler (Oreothlypis virginiae) reaches the northeastern limit of its breeding range in the southern Black Hills of South Dakota, where it is considered a species of conservation concern. This population occurs in pine–juniper–shrub habitat in several canyons in extreme western Custer County. Additional such habitat occurs in the southern Black Hills south and east of the documented breeding populations, but these areas have received few systematic surveys, and whether Virginia’s Warbler occupies them was uncertain. Therefore, to define the species’ distribution in the South Dakota Black Hills more precisely, we surveyed with the aid of broadcast song and reviewed other reports. Virginia’s Warblers occurred in appropriate habitats all along the southwestern front (approximately 30 km total) of the Black Hills in Custer County but did not occur in similar habitat along the southeastern front, approximately 25 km distant. The species’ relative abundance in previously and newly identified pine–juniper–shrub habitats was similar. Virginia’s Warbler occurrence was positively associated with shrub cover (primarily mountain-mahogany, Cercocarpus montanus), pine overstory, and slopes of \u3e15°. Its association with the Spotted Towhee (Pipilo maculatus) was negative, with the Yellow-rumped Warbler (Setophaga coronata) tended toward positive, and with the Dusky Flycatcher (Empidonax oberholseri) was variable (negative along the southwestern front but weakly positive across all sites). These data extend the documented breeding range of Virginia’s Warbler in South Dakota by more than 20 km to the southeast. To clarify conservation priorities for this species at the northeastern limit of its range, future studies should delineate local and landscape-level characteristics of this population’s habitat more precisely and address its source–sink population dynamics

A Molecular Reexamination Of Introgression Between Helianthus Annuus And H. Bolanderi (Compositae)

Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/137464/1/evo04127.pd

Extensive variation in synonymous substitution rates in mitochondrial genes of seed plants

<p>Abstract</p> <p>Background</p> <p>It has long been known that rates of synonymous substitutions are unusually low in mitochondrial genes of flowering and other land plants. Although two dramatic exceptions to this pattern have recently been reported, it is unclear how often major increases in substitution rates occur during plant mitochondrial evolution and what the overall magnitude of substitution rate variation is across plants.</p> <p>Results</p> <p>A broad survey was undertaken to evaluate synonymous substitution rates in mitochondrial genes of angiosperms and gymnosperms. Although most taxa conform to the generality that plant mitochondrial sequences evolve slowly, additional cases of highly accelerated rates were found. We explore in detail one of these new cases, within the genus <it>Silene</it>. A roughly 100-fold increase in synonymous substitution rate is estimated to have taken place within the last 5 million years and involves only one of ten species of <it>Silene </it>sampled in this study. Examples of unusually slow sequence evolution were also identified. Comparison of the fastest and slowest lineages shows that synonymous substitution rates vary by four orders of magnitude across seed plants. In other words, some plant mitochondrial lineages accumulate more synonymous change in 10,000 years than do others in 100 million years. Several perplexing cases of gene-to-gene variation in sequence divergence within a plant were uncovered. Some of these probably reflect interesting biological phenomena, such as horizontal gene transfer, mitochondrial-to-nucleus transfer, and intragenomic variation in mitochondrial substitution rates, whereas others are likely the result of various kinds of errors.</p> <p>Conclusion</p> <p>The extremes of synonymous substitution rates measured here constitute by far the largest known range of rate variation for any group of organisms. These results highlight the utility of examining absolute substitution rates in a phylogenetic context rather than by traditional pairwise methods. Why substitution rates are generally so low in plant mitochondrial genomes yet occasionally increase dramatically remains mysterious.</p

Phylogenetic Analysis Of Chloroplast Dna Restriction Site Data At Higher Taxonomic Levels: An Example From The Asteraceae

Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/137492/1/evo04314.pd

Structural rearrangements, including parallel inversions, within the chloroplast genome of Anemone and related genera

Chloroplast DNA cleavage sites for 10 restriction enzymes were mapped for 46 species representing all sections of Anemone , four closely related genera ( Clematis, Pulsatilla, Hepatica , and Knowltonia ), and three more distantly related outgroups (Caltha, Ranunculus , and Adonis ). Comparison of the maps revealed that the chloroplast genomes of Anemone and related genera have sustained an unusual number and variety of rearrangements. A single inversion of a 42-kb segment was found in the large single-copy region of Adonis aestivalis . Two types of rearrangements were found in the chloroplast genome of Clematis , Anemone, Pulsatilla, Hepatica , and Knowltonia : An approximately 4-kb expansion of the inverted repeat and four inversions within the large single-copy region. These rearrangements support the monophyletic status of these genera, clearly separating them from Caltha, Ranunculus , and Adonis . Two further inversions were found in two Clematis species and three Anemone species. While appearing to support a monophyletic grouping for these taxa, these two inversions conflict with data from both chloroplast restriction sites and morphology and are better interpreted as having occurred twice independently. These are the first two documented cases of homoplastic inversions in chloroplast DNA. Finally, the second intron of the chloroplast rps12 gene was shown to have been lost in the common ancestor of the same three Anemone species that feature the two homoplastic inversions.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/48047/1/239_2004_Article_BF00176089.pd