scholarly journals Heteroplasmy and Patterns of Cytonuclear Linkage Disequilibrium in Wild Carrot

2019 ◽  
Vol 59 (4) ◽  
pp. 1005-1015 ◽  
Author(s):  
Adam J Ramsey ◽  
David E McCauley ◽  
Jennifer R Mandel

Abstract Organellar genomes are considered to be strictly uniparentally-inherited. Uniparental inheritance allows for cytonuclear coevolution and the development of highly coordinated cytonuclear interactions. Yet, instances of biparental inheritance have been documented across eukaryotes. Biparental inheritance in otherwise uniparentally-inherited organelles is termed leakage (maternal or paternal) and allows for the presence of multiple variants of the same organellar genome within an individual, called heteroplasmy. It is unclear what, if any, evolutionary consequences are placed on nuclear and/or organellar genomes due to heteroplasmy. One way of accessing cytonuclear interactions and potential coevolution is through calculating cytonuclear linkage disequilibrium (cnLD), or the non-random association of alleles between nuclear and organellar genomes. Patterns of cnLD can indicate positive or negative cytonuclear selection, coevolution between the nuclear and organellar genomes, non-traditional organellar inheritance, or instances of ancestral heteroplasmy. In plants, cytonuclear interactions have been shown to play a role in cytoplasmic male sterility which occurs in gynodioecious species and is associated with leakage. We used the gynodioecious species, Daucus carota L. spp. carota, or wild carrot, to investigate cnLD. We genotyped a total of 265 individuals from two regions of the USA at 15 nuclear microsatellites, the mitochondrial genes cox1 and atp9, and an intergenic region between trnS and trnG (StoG) in the plastid genome to calculate nuclear–nuclear LD (nucLD), cnLD, and organellar LD (i.e., within the mtDNA and between mtDNA and ptDNA) within the two regions. We were further able to identify cox1 and StoG heteroplasmy and calculate some of the same LD measures within heteroplasmic and homoplasmic (non-heteroplasmic) datasets. We used a Z-transformation test to demonstrate that heteroplasmic individuals display significantly higher levels of cnLD within both regions. In spite of this, within and between organellar LD is low to moderate. Given these patterns of LD in two regions of the USA in which gene flow has been shown to occur between crop and wild carrot, we suggest that heteroplasmy is an evolutionary mechanism which permits the maintenance of cnLD while also acting to disrupt organellar LD.

Database ◽  
2020 ◽  
Vol 2020 ◽  
Author(s):  
Tao Liu ◽  
Yutong Cui ◽  
Xuli Jia ◽  
Jing Zhang ◽  
Ruoran Li ◽  
...  

Abstract Algae are the oldest taxa on Earth, with an evolutionary relationship that spans prokaryotes (Cyanobacteria) and eukaryotes. A long evolutionary history has led to high algal diversity. Their organelle DNAs are characterized by uniparental inheritance and a compact genome structure compared with nuclear genomes; thus, they are efficient molecular tools for the analysis of gene structure, genome structure, organelle function and evolution. However, an integrated organelle genome database for algae, which could enable users to both examine and use relevant data, has not previously been developed. Therefore, to provide an organelle genome platform for algae, we have developed a user-friendly database named Organelle Genome Database for Algae (OGDA, http://ogda.ytu.edu.cn/). OGDA contains organelle genome data either retrieved from several public databases or sequenced in our laboratory (Laboratory of Genetics and Breeding of Marine Organism [MOGBL]), which are continuously updated. The first release of OGDA contains 1055 plastid genomes and 755 mitochondrial genomes. Additionally, a variety of applications have been integrated into this platform to analyze the structural characteristics, collinearity and phylogeny of organellar genomes for algae. This database represents a useful tool for users, enabling the rapid retrieval and analysis of information related to organellar genomes for biological discovery.


2020 ◽  
Vol 111 (6) ◽  
pp. 531-538 ◽  
Author(s):  
Jennifer R Mandel ◽  
Adam J Ramsey ◽  
Jacob M Holley ◽  
Victoria A Scott ◽  
Dviti Mody ◽  
...  

Abstract Plant mitochondria and plastids display an array of inheritance patterns and varying levels of heteroplasmy, where individuals harbor more than 1 version of a mitochondrial or plastid genome. Organelle inheritance in plants has the potential to be quite complex and can vary with plant growth, development, and reproduction. Few studies have sought to investigate these complicated patterns of within-individual variation and inheritance using experimental crosses in plants. We carried out crosses in carrot, Daucus carota L. (Apiaceae), which has previously been shown to exhibit organellar heteroplasmy. We used mitochondrial and plastid markers to begin to disentangle the patterns of organellar inheritance and the fate of heteroplasmic variation, with special focus on cases where the mother displayed heteroplasmy. We also investigated heteroplasmy across the plant, assaying leaf samples at different development stages and ages. Mitochondrial and plastid paternal leakage was rare and offspring received remarkably similar heteroplasmic mixtures to their heteroplasmic mothers, indicating that heteroplasmy is maintained over the course of maternal inheritance. When offspring did differ from their mother, they were likely to exhibit a loss of the genetic variation that was present in their mother. Finally, we found that mitochondrial variation did not vary significantly over plant development, indicating that substantial vegetative sorting did not occur. Our study is one of the first to quantitatively investigate inheritance patterns and heteroplasmy in plants using controlled crosses, and we look forward to future studies making use of whole genome information to study the complex evolutionary dynamics of plant organellar genomes.


2019 ◽  
Vol 116 (12) ◽  
pp. 5665-5674 ◽  
Author(s):  
Johanna Sobanski ◽  
Patrick Giavalisco ◽  
Axel Fischer ◽  
Julia M. Kreiner ◽  
Dirk Walther ◽  
...  

In most eukaryotes, organellar genomes are transmitted preferentially by the mother, but molecular mechanisms and evolutionary forces underlying this fundamental biological principle are far from understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of so-called selfish cytoplasmic elements. Those can be, for example, fast-replicating or aggressive chloroplasts (plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show that the ability of plastids to compete against each other is a metabolic phenotype determined by extremely rapidly evolving genes in the plastid genome of the evening primroseOenothera. Repeats in the regulatory region ofaccD(the plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first and rate-limiting step of lipid biosynthesis), as well as inycf2(a giant reading frame of still unknown function), are responsible for the differences in competitive behavior of plastid genotypes. Polymorphisms in these genes influence lipid synthesis and most likely profiles of the plastid envelope membrane. These in turn determine plastid division and/or turnover rates and hence competitiveness. This work uncovers cytoplasmic drive loci controlling the outcome of biparental chloroplast transmission. Here, they define the mode of chloroplast inheritance, as plastid competitiveness can result in uniparental inheritance (through elimination of the “weak” plastid) or biparental inheritance (when two similarly “strong” plastids are transmitted).


2021 ◽  
Author(s):  
Derek Setter ◽  
Sam Ebdon ◽  
Ben Jackson ◽  
Konrad Lohse

Recombination can occur either as a result of crossover or gene conversion events. Population genetic methods for inferring the rate of recombination from patterns of linkage disequilibrium generally assume a simple model of recombination that only involves crossover events and ignore gene conversion. However, distinguishing the two processes is not only necessary for a complete description of recombination, but also essential for understanding the evolutionary consequences of inversions and other genomic partitions in which crossover (but not gene conversion) is reduced. We present heRho, a simple composite likelihood scheme for co-estimating the rate of crossover and gene conversion from individual diploid genomes. The method is based on analytic results for the distance-dependent probability of heterozygous and homozygous states at two loci. We apply heRho to simulations and data from the house mouse Mus musculus castaneus, a well studied model. Our analyses show i) that the rates of crossover and gene conversion can be accurately co-estimated at the level of individual chromosomes and ii) that previous estimates of the population scaled rate of recombination ρ = 4Ner under a pure crossover model are likely biased


1996 ◽  
Vol 10 (2) ◽  
pp. 455-457 ◽  
Author(s):  
Larry W. Mitich

“Cool white, and intricate, Queen Anne's lace hedges our summer highways with spendthrift loveliness. But who of us can imagine the full beauty and wonder of this plant as we speed by?”—Green Immigrants by Claire Shaver Haughton.


2018 ◽  
Author(s):  
Johanna Sobanski ◽  
Patrick Giavalisco ◽  
Axel Fischer ◽  
Julia Kreiner ◽  
Dirk Walther ◽  
...  

AbstractIn most eukaryotes, organellar genomes are transmitted preferentially by the mother, but molecular mechanisms and evolutionary forces underlying this fundamental biological principle are far from understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of so-called selfish cytoplasmic elements. Those can be, for example, fast replicating or aggressive chloroplasts (plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show that the ability of plastids to compete against each other is a metabolic phenotype determined by extremely rapidly evolving genes in the plastid genome of the evening primroseOenothera. Repeats in the regulatory region ofaccD(the plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first and rate limiting step of lipid biosynthesis), as well as inycf2(a giant reading frame of still unknown function), are responsible for the differences in competitive behavior of plastid genotypes. Polymorphisms in these genes influence lipid synthesis and most likely profiles of the plastid envelope membrane. These in turn determine plastid division and/or turn-over rates and hence competitiveness. This work uncovers cytoplasmic drive loci controlling the outcome of biparental chloroplast transmission. Here, they define the mode of chloroplast inheritance, since plastid competitiveness can result in uniparental inheritance (through elimination of the “weak” plastid) or biparental inheritance (when two similarly “strong” plastids are transmitted).Significance statementPlastids and mitochondria are usually uniparentally inherited, typically maternally. When the DNA-containing organelles are transmitted to the progeny by both parents, evolutionary theory predicts that the maternal and paternal organelles will compete in the hybrid. As their genomes do not undergo sexual recombination, one organelle will “try” to outcompete the other, thus favoring the evolution and spread of aggressive cytoplasms. The investigations described here in the evening primrose, a model species for biparental plastid transmission, have discovered that chloroplast competition is a metabolic phenotype. It is conferred by rapidly evolving genes that are encoded on the chloroplast genome and control lipid biosynthesis. Due to their high mutation rate these loci can evolve and become fixed in a population very quickly.


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