A chromosome‐level genome assembly provides new insights into paternal genome elimination in the cotton mealybug <i>Phenacoccus solenopsis</i>

Li, Meizhen; Tong, Haojie; Wang, Shuping; Ye, Wanyi; Li, Zicheng; Omar, Mohamed A.A.; Ao, Yan; Ding, Simin; Li, Zihao; Wang, Ying; Yin, Chuanlin; Zhao, Xianxin; He, Kang; Liu, Feiling; Chen, Xi; Yang, Mei; Walters, James R.; Jiang, Mingxing; Li, Fēi

doi:10.1111/1755-0998.13232

Cited by 17 publications

(21 citation statements)

References 83 publications

(130 reference statements)

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“…2 D ). To investigate patterns of genetic linkage in relation to parent-of-origin expression, we took advantage of synteny alignments of the PCITRI.V0 assembly to a chromosome-level assembly of another closely related mealybug, Phenacoccus solenopsis ( Li et al. 2020 ) .…”

Section: Resultsmentioning

confidence: 99%

“…It is unclear why hybrid males from the reciprocal cross suffer more strongly from hybrid incompatibilities. Mealybugs do not have differentiated sex chromosomes ( Hughes-Schrader 1948 ; Li et al. 2020 ), but since males are to a great extent hemizygous, Haldane’s rule might explain the differential mortality between hybrid sexes ( Koevoets and Beukeboom 2009 ).…”

Section: Discussionmentioning

confidence: 99%

“…2001 ; Hodson et al. 2017 ; Li et al. 2020 ) indicates that the genome-wide imprinting under PGE is male-specific.…”

Section: Discussionmentioning

confidence: 99%

“…The recent publication of a chromosome level assembly for another mealybug species, P. solenopsis ( Li et al. 2020 ), created an opportunity to investigate chromosomal biases in parent-of-origin expression in P. citri .…”

Section: Methodsmentioning

confidence: 99%

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Males That Silence Their Father’s Genes: Genomic Imprinting of a Complete Haploid Genome

Filia

Mongue

Dorrens

et al. 2021

Molecular Biology and Evolution

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Genetic conflict is considered a key driver in the evolution of reproductive systems with non-Mendelian inheritance, where parents do not contribute equally to the genetic makeup of their offspring. One of the most extraordinary examples of non-Mendelian inheritance is paternal genome elimination (PGE), a form of haplodiploidy which has evolved repeatedly across arthropods. Under PGE, males are diploid but only transmit maternally-inherited chromosomes, while the paternally-inherited homologues are excluded from sperm. This asymmetric inheritance is thought to have evolved through an evolutionary arms race between the paternal and maternal genomes over transmission to future generations. In several PGE clades, such as the mealybugs (Hemiptera: Pseudococcidae), paternal chromosomes are not just eliminated from sperm, but also heterochromatinised early in development and thought to remain inactive, which could result from genetic conflict between parental genomes. Here, we present a parent-of-origin allele-specific transcriptome analysis in male mealybugs showing that expression is globally biased towards the maternal genome. However, up to 70% of somatically-expressed genes are to some degree paternally-expressed, while paternal genome expression is much more restricted in the male reproductive tract, with only 20% of genes showing paternal contribution. We also show that parent-of-origin-specific gene expression patterns are remarkably similar across genotypes, and that genes with completely biparental expression show elevated rates of molecular evolution. Our results provide the clearest example yet of genome-wide genomic imprinting in insects and enhance our understanding of PGE, which will aid future empirical tests of evolutionary theory regarding the origin of this unusual reproductive strategy.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

“…2001 ; Hodson et al. 2017 ; Li et al. 2020 ) indicates that the genome-wide imprinting under PGE is male-specific.…”

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Males That Silence Their Father’s Genes: Genomic Imprinting of a Complete Haploid Genome

Filia

Mongue

Dorrens

et al. 2021

Molecular Biology and Evolution

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“…Our genome assembly shows high completeness, as revealed by the presence of >90% single copy orthologs from the insect and hemipteran BUSCO gene sets. Half of the genome (216.2Mb) consists of repetitive sequences, higher than the 38-45% range estimated in Phenacoccus solenopsis (Li et al, 2020) and Pseudococcus longispinus (Garber et al 2021 publicly available at https://ensembl.mealybug.org/Pseudococcus_longispinus_v1) ) and hemipterans such as Acyrthosiphon pisum or Bemisia tabaci (International Aphid Genomics Consortium, 2010;Chen et al, 2016). The vast majority of repeats (96.6%) are unclassified.…”

Section: Genome Assemblymentioning

confidence: 99%

The B chromosome of Pseudococcus viburni: a selfish chromosome that exploits whole-genome meiotic drive

Vea

Filia

Jaroň

et al. 2021

Preprint

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Meiosis, the key process underlying sexual reproduction, is generally a fair process: each chromosome has a 50% chance of being included into each gamete. However in some organisms meiosis has become highly aberrant with some chromosomes having a higher chance of making it into gametes than others. Yet why and how such systems evolve remains unclear. Here we study the unusual reproductive genetics of mealybugs, in which only maternal-origin chromosomes are included into the gametes during male meiosis, while paternally-derived chromosomes degrade. This whole genome meiotic drive occurs in all males and is evolutionarily conserved. However one species - the obscure mealybug Pseudococcus viburni - has a segregating B chromosome that increases in frequency by escaping paternal genome elimination. Here we present whole-genome and gene expression data from laboratory lines with and without B chromosomes. These data allow us to identify B-linked sequences including >70 protein-coding genes as well as a B-specific satellite repeat that makes up a significant proportion of the chromosome. We also used these data to investigate the evolutionary origin of the B chromosome. The few paralogs between the B and the core genome are distributed throughout the genome, showing that it is unlikely that the B originated through a simple duplication of one of the autosomes. We also find that while many of the B-linked genes do not have paralogs within the P.viburni genome, but they do show orthology with genes in other hemipteran insects suggesting that the B might have originated from fission of one of the autosomes, possibly followed by further translocations of individual genes. Finally in order to understand the mechanisms by which the B is able to escape elimination when paternally-derived we generated gene expression data for males and females with and without B chromosomes. We find that at the developmental stage when meiosis is taking place only a small number of B-linked genes show significant expression. Only one gene was significantly over-expressed during male meiosis, which is when the drive occurs: a acetyltransferase involved in H3K56Ac, which has a putative role in meiosis and is therefore a promising candidate for further studies. Together, these results form a promising foundation for studying the mechanisms of meiotic drive in a system that is uniquely suited for this approach.

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Salinity responses and tolerance mechanisms in underground vegetable crops: an integrative review

Chourasia

Kumar

et al. 2022

Planta

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A chromosome‐level genome assembly provides new insights into paternal genome elimination in the cotton mealybug Phenacoccus solenopsis

Cited by 17 publications

References 83 publications

Males That Silence Their Father’s Genes: Genomic Imprinting of a Complete Haploid Genome

Males That Silence Their Father’s Genes: Genomic Imprinting of a Complete Haploid Genome

The B chromosome of Pseudococcus viburni: a selfish chromosome that exploits whole-genome meiotic drive

Salinity responses and tolerance mechanisms in underground vegetable crops: an integrative review

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