Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep

VanBuren, Robert; Wai, Ching Man; Zhang, Jisen; Han, Jennifer; Arro, Jie; Lin, Zhicong; Liao, Zhenyang; Yu, Qingyi; Wang, Ming Li; Zee, Francis; Moore, Richard C.; Charlesworth, Deborah; Ming, Ray

doi:10.1186/s13059-016-1095-9

Cited by 23 publications

(18 citation statements)

References 54 publications

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“…In papaya (C. papaya), Y h , a Y chromosome variant that contributes to the expression of hermaphroditism (90), exhibits dramatic reduction in genetic diversity. This is indicative of a selective sweep, presumably due to artificial selection during domestication (87,88). A similar scenario has also been proposed in grapevine (Vitis vinifera) (84).…”

Section: The Effect Of Domesticationsupporting

confidence: 64%

One Hundred Ways to Invent the Sexes: Theoretical and Observed Paths to Dioecy in Plants

Henry

Akagi

Tao

et al. 2018

Annu. Rev. Plant Biol.

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Dioecy, the presence of male and female flowers on separate individuals, is both widespread and uncommon within flowering plants, with only a few percent of dioecious species spread across most major phylogenetic taxa. It is therefore safe to assume that dioecy evolved independently in these different groups, which allows us to ask questions regarding the molecular and developmental mechanisms underlying these independent transitions to dioecy. We start this review by examining the problem from the standpoint of a genetic engineer trying to develop dioecy, discuss various potential solutions, and compare them to models proposed in the past and based on genetic and evolutionary considerations. Next, we present recent information regarding candidate sex determinants in three species, acquired using newly established genomic approaches. Although such specific information is still scarce, it is slowly becoming apparent that various genes or pathways can be altered to evolve dioecy.

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Section: The Effect Of Domesticationsupporting

confidence: 64%

One Hundred Ways to Invent the Sexes: Theoretical and Observed Paths to Dioecy in Plants

Henry

Akagi

Tao

et al. 2018

Annu. Rev. Plant Biol.

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“…The gene pairs having long phylogenetic distance showed the high degree of silent site divergence. Using a molecular clock of 7.1 × 10 −9 synonymous substitutions per site per year [ 46 ], corrected by a factor of 0.672 [ 47 ], we estimated the ages of gene duplication events of subfamily III PLCPs in papaya (Fig. 2b , Additional files 7 and 8 ).…”

Section: Resultsmentioning

confidence: 99%

“…DnaSP v5.0 [ 44 ] was used to calculate synonymous substitutions per synonymous site ( Ks ), nonsynonymous substitutions per nonsynonymous site ( Ka ), and synonymous and noncoding (silent) substitutions per silent site ( Ksil ). Divergence times were determined using Ksil and the methods described by Li [ 45 ] using a mean substitution rate of 7.1 × 10 −9 substitutions/site/year estimated in A. thaliana based on mutation accumulation experiments [ 46 ], corrected by a factor of 0.672 for papaya as described by VanBuren et al [ 47 ].…”

Section: Methodsmentioning

confidence: 99%

Papain-like cysteine proteases in Carica papaya: lineage-specific gene duplication and expansion

et al. 2018

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BackgroundPapain-like cysteine proteases (PLCPs), a large group of cysteine proteases structurally related to papain, play important roles in plant development, senescence, and defense responses. Papain, the first cysteine protease whose structure was determined by X-ray crystallography, plays a crucial role in protecting papaya from herbivorous insects. Except the four major PLCPs purified and characterized in papaya latex, the rest of the PLCPs in papaya genome are largely unknown.ResultsWe identified 33 PLCP genes in papaya genome. Phylogenetic analysis clearly separated plant PLCP genes into nine subfamilies. PLCP genes are not equally distributed among the nine subfamilies and the number of PLCPs in each subfamily does not increase or decrease proportionally among the seven selected plant species. Papaya showed clear lineage-specific gene expansion in the subfamily III. Interestingly, all four major PLCPs purified from papaya latex, including papain, chymopapain, glycyl endopeptidase and caricain, were grouped into the lineage-specific expansion branch in the subfamily III. Mapping PLCP genes on chromosomes of five plant species revealed that lineage-specific expansions of PLCP genes were mostly derived from tandem duplications. We estimated divergence time of papaya PLCP genes of subfamily III. The major duplication events leading to lineage-specific expansion of papaya PLCP genes in subfamily III were estimated at 48 MYA, 34 MYA, and 16 MYA. The gene expression patterns of the papaya PLCP genes in different tissues were assessed by transcriptome sequencing and qRT-PCR. Most of the papaya PLCP genes of subfamily III expressed at high levels in leaf and green fruit tissues.ConclusionsTandem duplications played the dominant role in affecting copy number of PLCPs in plants. Significant variations in size of the PLCP subfamilies among species may reflect genetic adaptation of plant species to different environments. The lineage-specific expansion of papaya PLCPs of subfamily III might have been promoted by the continuous reciprocal selective effects of herbivore attack and plant defense.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4394-y) contains supplementary material, which is available to authorized users.

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“…More generally, a variety of evolutionary forces have also been invoked to explain patterns of genetic variability on the X chromosome versus autosomes in model species through empirical data analyses ( Andolfatto 2001 ; Lu and Wu 2005 ; Singh and Petrov 2007 ; Cox et al. 2010 ; Corl and Ellegren 2012 ; VanBuren et al. 2016 ) and statistical modeling ( Betancourt et al.…”

Section: Introductionmentioning

confidence: 99%

Contrasting Patterns of Genomic Diversity Reveal Accelerated Genetic Drift but Reduced Directional Selection on X-Chromosome in Wild and Domestic Sheep Species

Chen

Zhang

et al. 2018

Genome Biology and Evolution

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Analyses of genomic diversity along the X chromosome and of its correlation with autosomal diversity can facilitate understanding of evolutionary forces in shaping sex-linked genomic architecture. Strong selective sweeps and accelerated genetic drift on the X-chromosome have been inferred in primates and other model species, but no such insight has yet been gained in domestic animals compared with their wild relatives. Here, we analyzed X-chromosome variability in a large ovine data set, including a BeadChip array for 943 ewes from the world’s sheep populations and 110 whole genomes of wild and domestic sheep. Analyzing whole-genome sequences, we observed a substantially reduced X-to-autosome diversity ratio (∼0.6) compared with the value expected under a neutral model (0.75). In particular, one large X-linked segment (43.05–79.25 Mb) was found to show extremely low diversity, most likely due to a high density of coding genes, featuring highly conserved regions. In general, we observed higher nucleotide diversity on the autosomes, but a flat diversity gradient in X-linked segments, as a function of increasing distance from the nearest genes, leading to a decreased X: autosome (X/A) diversity ratio and contrasting to the positive correlation detected in primates and other model animals. Our evidence suggests that accelerated genetic drift but reduced directional selection on X chromosome, as well as sex-biased demographic events, explain low X-chromosome diversity in sheep species. The distinct patterns of X-linked and X/A diversity we observed between Middle Eastern and non-Middle Eastern sheep populations can be explained by multiple migrations, selection, and admixture during the domestic sheep’s recent postdomestication demographic expansion, coupled with natural selection for adaptation to new environments. In addition, we identify important novel genes involved in abnormal behavioral phenotypes, metabolism, and immunity, under selection on the sheep X-chromosome.

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Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep

Cited by 23 publications

References 54 publications

One Hundred Ways to Invent the Sexes: Theoretical and Observed Paths to Dioecy in Plants

One Hundred Ways to Invent the Sexes: Theoretical and Observed Paths to Dioecy in Plants

Papain-like cysteine proteases in Carica papaya: lineage-specific gene duplication and expansion

Contrasting Patterns of Genomic Diversity Reveal Accelerated Genetic Drift but Reduced Directional Selection on X-Chromosome in Wild and Domestic Sheep Species

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