Insights into the Evolution of Mitochondrial Genome Size from Complete Sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae)

132

Bottle gourd (Lagenaria siceraria) was one of the first domesticated plants, and the only one with a global distribution during pre-Columbian times. Although native to Africa, bottle gourd was in use by humans in east Asia, possibly as early as 11,000 y ago (BP) and in the Americas by 10,000 BP. Despite its utilitarian importance to diverse human populations, it remains unresolved how the bottle gourd came to be so widely distributed, and in particular how and when it arrived in the New World. A previous study using ancient DNA concluded that Paleoindians transported already domesticated gourds to the Americas from Asia when colonizing the New World [Erickson et al. (2005) Proc Natl Acad Sci USA 102 (51):18315-18320]. However, this scenario requires the propagation of tropical-adapted bottle gourds across the Arctic. Here, we isolate 86,000 base pairs of plastid DNA from a geographically broad sample of archaeological and living bottle gourds. In contrast to the earlier results, we find that all pre-Columbian bottle gourds are most closely related to African gourds, not Asian gourds.Ocean-current drift modeling shows that wild African gourds could have simply floated across the Atlantic during the Late Pleistocene. Once they arrived in the New World, naturalized gourd populations likely became established in the Neotropics via dispersal by megafaunal mammals. These wild populations were domesticated in several distinct New World locales, most likely near established centers of food crop domestication.long-distance dispersal | New World domestication | archaeogenomics

Section: Resultsmentioning

confidence: 99%

Transoceanic drift and the domestication of African bottle gourds in the Americas

Kistler¹,

Montenegro

Smith

et al. 2014

132

“…Angiosperm mitochondrial genomes harbor tremendous variation in genome size (22,23,34,35). Previous examples of variation within and between species have often been attributed to large sequence duplications (27) or the insertions of large quantities of foreign DNA (23,36,37).…”

Section: Discussionmentioning

confidence: 99%

“…Annotation of the assembled S. noctiflora BRP mitochondrial genome was conducted using Mitofy (35) and direct comparison with the previously generated annotations for S. noctiflora OSR (22). The annotated S. noctiflora BRP mitochondrial chromosome sequences were deposited in GenBank (accession nos.…”

Section: Methodsmentioning

confidence: 99%

The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes

Cuthbert

Taylor

et al. 2015

118

106

Across eukaryotes, mitochondria exhibit staggering diversity in genomic architecture, including the repeated evolution of multichromosomal structures. Unlike in the nucleus, where mitosis and meiosis ensure faithful transmission of chromosomes, the mechanisms of inheritance in fragmented mitochondrial genomes remain mysterious. Multichromosomal mitochondrial genomes have recently been found in multiple species of flowering plants, including Silene noctiflora, which harbors an unusually large and complex mitochondrial genome with more than 50 circular-mapping chromosomes totaling ∼7 Mb in size. To determine the extent to which such genomes are stably maintained, we analyzed intraspecific variation in the mitochondrial genome of S. noctiflora. Complete genomes from two populations revealed a high degree of similarity in the sequence, structure, and relative abundance of mitochondrial chromosomes. For example, there are no inversions between the genomes, and there are only nine SNPs in 25 kb of protein-coding sequence. Remarkably, however, these genomes differ in the presence or absence of 19 entire chromosomes, all of which lack any identifiable genes or contain only duplicate gene copies. Thus, these mitochondrial genomes retain a full gene complement but carry a highly variable set of chromosomes that are filled with presumably dispensable sequence. In S. noctiflora, conventional mechanisms of mitochondrial sequence divergence are being outstripped by an apparently nonadaptive process of whole-chromosome gain/loss, highlighting the inherent challenge in maintaining a fragmented genome. We discuss the implications of these findings in relation to the question of why mitochondria, more so than plastids and bacterial endosymbionts, are prone to the repeated evolution of multichromosomal genomes. meiosis | mitochondrial DNA | mitosis | multichromosomal | multipartite

“…Many mitochondrial genomes abound with horizontally acquired sequences, whereas plastid genomes are conspicuously lacking in foreign DNA (6,81). For instance, ∼13% (∼130 kb) of the zucchini mtDNA is represented by plastid-and nuclear-derived sequences, almost all of which are noncoding (82). Other angiosperms, like Plantago and ginger species, contain mitochondrial gene mosaics, formed by gene conversion between native and foreign homologs (83).…”

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

Smith

Keeling

2015

338

344

Mitochondrial and plastid genomes show a wide array of architectures, varying immensely in size, structure, and content. Some organelle DNAs have even developed elaborate eccentricities, such as scrambled coding regions, nonstandard genetic codes, and convoluted modes of posttranscriptional modification and editing. Here, we compare and contrast the breadth of genomic complexity between mitochondrial and plastid chromosomes. Both organelle genomes have independently evolved many of the same features and taken on similar genomic embellishments, often within the same species or lineage. This trend is most likely because the nuclear-encoded proteins mediating these processes eventually leak from one organelle into the other, leading to a high likelihood of processes appearing in both compartments in parallel. However, the complexity and intensity of genomic embellishments are consistently more pronounced for mitochondria than for plastids, even when they are found in both compartments. We explore the evolutionary forces responsible for these patterns and argue that organelle DNA repair processes, mutation rates, and population genetic landscapes are all important factors leading to the observed convergence and divergence in organelle genome architecture.E ndosymbiosis can dramatically impact cellular and genomic architectures. Mitochondria and plastids exemplify this point. Each of these two types of energy-producing eukaryotic organelle independently arose from the endosymbiosis, retention, and integration of a free-living bacterium into a host cell more than 1.4 billion years ago. Mitochondria came first, evolving from an alphaproteobacterial endosymbiont in an ancestor of all known living eukaryotes, and still exist, in one form or another (1), in all its descendants (2). Plastids came later, via the "primary" endosymbiosis of a cyanobacterium by the eukaryotic ancestor of the Archaeplastida, and then spread laterally to disparate groups through eukaryote-eukaryote endosymbioses (3). Consequently, a significant proportion of the identified eukaryotic diversity has a plastid.With few exceptions (1, 4), mitochondria and plastids contain genomes-chromosomal relics of the bacterial endosymbionts from which they evolved (2, 5). Mitochondrial and plastid DNAs (mtDNAs and ptDNAs) have many traits in common, which is not surprising given their similar evolutionary histories. Both are highly reduced relative to the genomes of extant, free-living alphaproteobacteria and cyanobacteria (2, 5), and both have transferred most of their genes to the host nuclear genome and are therefore reliant on nuclear-encoded, organelle-targeted proteins for the preservation of crucial biochemical pathways and many repair-, replication-, and expression-related functions (6). Both also show a wide and perplexing assortment of genomic architectures (7,8), which has spurred various evolutionary explanations, ranging from ancient inheritance from the RNA world to selection for greater "evolvability" (9, 10).At first glance, genomic complexity w...