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Gene expression analysis of parthenogenetic embryonic development of the pea aphid, Acyrthosiphon pisum, suggests that aphid parthenogenesis evolved from meiotic oogenesis.

Srinivasan DG, Abdelhady A, Stern DL - PLoS ONE (2014)

Bottom Line: In addition, we observed that asexual aphid tissues accumulated unspliced transcripts of Spo11, whereas sexual aphid tissues accumulated primarily spliced transcripts.In situ hybridization revealed Spo11 transcript in sexual germ cells and undetectable levels of Spo11 transcript in asexual germ cells.Together, these results suggest that parthenogenetic oogenesis evolved from a meiosis-like, and not a mitosis-like, process and that the aphid reproductive polyphenism may involve a modification of Spo11 gene activity.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute and Department of Ecology and Evolutionary Biology, Guyot Hall, Princeton University, Princeton, NJ, 08544, United States of America; Department of Biological Science, Rowan University, 201 Mullica Hill Rd, Glassboro, NJ, 08028, United States of America.

ABSTRACT
Aphids exhibit a form of phenotypic plasticity, called polyphenism, in which genetically identical females reproduce sexually during one part of the life cycle and asexually (via parthenogenesis) during the remainder of the life cycle. The molecular basis for aphid parthenogenesis is unknown. Cytological observations of aphid parthenogenesis suggest that asexual oogenesis evolved either through a modification of meiosis or from a mitotic process. As a test of these alternatives, we assessed the expression levels and expression patterns of canonical meiotic recombination and germline genes in the sexual and asexual ovaries of the pea aphid, Acyrthosiphon pisum. We observed expression of all meiosis genes in similar patterns in asexual and sexual ovaries, with the exception that some genes encoding Argonaute-family members were not expressed in sexual ovaries. In addition, we observed that asexual aphid tissues accumulated unspliced transcripts of Spo11, whereas sexual aphid tissues accumulated primarily spliced transcripts. In situ hybridization revealed Spo11 transcript in sexual germ cells and undetectable levels of Spo11 transcript in asexual germ cells. We also found that an obligately asexual strain of pea aphid produced little spliced Spo11 transcript. Together, these results suggest that parthenogenetic oogenesis evolved from a meiosis-like, and not a mitosis-like, process and that the aphid reproductive polyphenism may involve a modification of Spo11 gene activity.

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Meiosis genes are expressed in asexual aphids.A. Cyclical parthenogenesis among aphidomorph insects evolved from sexual ancestors as shown in this phylogeny (adapted from [3]). Time scale on bottom is in millions of years ago (MYA). B. Structures of an asexual ovariole (top) and a sexual ovariole (bottom) are shown. Ovarioles are oriented with anterior on the left. Scale bars are shown. C. Both sexual and asexual ovaries express meiosis genes. PCR products from cDNA template (+), control template lacking reverse transcriptase (RT) during cDNA synthesis (-), or from no template (NT) are shown. D. PCR of meiosis genes from the Tucson obligately asexual pea aphid strain. Lanes contain products from PCR using Tucson ovary cDNA template (+RT), template from cDNA synthesis reactions lacking RT (-RT), and genomic DNA (gDNA). Primers are the same as those used for C.
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pone-0115099-g001: Meiosis genes are expressed in asexual aphids.A. Cyclical parthenogenesis among aphidomorph insects evolved from sexual ancestors as shown in this phylogeny (adapted from [3]). Time scale on bottom is in millions of years ago (MYA). B. Structures of an asexual ovariole (top) and a sexual ovariole (bottom) are shown. Ovarioles are oriented with anterior on the left. Scale bars are shown. C. Both sexual and asexual ovaries express meiosis genes. PCR products from cDNA template (+), control template lacking reverse transcriptase (RT) during cDNA synthesis (-), or from no template (NT) are shown. D. PCR of meiosis genes from the Tucson obligately asexual pea aphid strain. Lanes contain products from PCR using Tucson ovary cDNA template (+RT), template from cDNA synthesis reactions lacking RT (-RT), and genomic DNA (gDNA). Primers are the same as those used for C.

Mentions: The major differences between asexual and sexual aphids are the structure of the ovaries and the fate of germ cells. Aphid ovaries consist of six to eight ovarioles. The anterior terminus of each ovariole consists of a germarium, which develops from germline precursor cells during embryogenesis into a syncytial collection of presumptive oocyte and trophocyte (nurse cell) nuclei enveloped by somatic follicle cells [7], [8] (Fig. 1B). From the germaria of both sexual and asexual ovaries, each presumptive oocyte nucleus, arrested in prophase, sequentially migrates out to form a follicle. The oocyte grows in size surrounded by the follicular epithelium.


Gene expression analysis of parthenogenetic embryonic development of the pea aphid, Acyrthosiphon pisum, suggests that aphid parthenogenesis evolved from meiotic oogenesis.

Srinivasan DG, Abdelhady A, Stern DL - PLoS ONE (2014)

Meiosis genes are expressed in asexual aphids.A. Cyclical parthenogenesis among aphidomorph insects evolved from sexual ancestors as shown in this phylogeny (adapted from [3]). Time scale on bottom is in millions of years ago (MYA). B. Structures of an asexual ovariole (top) and a sexual ovariole (bottom) are shown. Ovarioles are oriented with anterior on the left. Scale bars are shown. C. Both sexual and asexual ovaries express meiosis genes. PCR products from cDNA template (+), control template lacking reverse transcriptase (RT) during cDNA synthesis (-), or from no template (NT) are shown. D. PCR of meiosis genes from the Tucson obligately asexual pea aphid strain. Lanes contain products from PCR using Tucson ovary cDNA template (+RT), template from cDNA synthesis reactions lacking RT (-RT), and genomic DNA (gDNA). Primers are the same as those used for C.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4264872&req=5

pone-0115099-g001: Meiosis genes are expressed in asexual aphids.A. Cyclical parthenogenesis among aphidomorph insects evolved from sexual ancestors as shown in this phylogeny (adapted from [3]). Time scale on bottom is in millions of years ago (MYA). B. Structures of an asexual ovariole (top) and a sexual ovariole (bottom) are shown. Ovarioles are oriented with anterior on the left. Scale bars are shown. C. Both sexual and asexual ovaries express meiosis genes. PCR products from cDNA template (+), control template lacking reverse transcriptase (RT) during cDNA synthesis (-), or from no template (NT) are shown. D. PCR of meiosis genes from the Tucson obligately asexual pea aphid strain. Lanes contain products from PCR using Tucson ovary cDNA template (+RT), template from cDNA synthesis reactions lacking RT (-RT), and genomic DNA (gDNA). Primers are the same as those used for C.
Mentions: The major differences between asexual and sexual aphids are the structure of the ovaries and the fate of germ cells. Aphid ovaries consist of six to eight ovarioles. The anterior terminus of each ovariole consists of a germarium, which develops from germline precursor cells during embryogenesis into a syncytial collection of presumptive oocyte and trophocyte (nurse cell) nuclei enveloped by somatic follicle cells [7], [8] (Fig. 1B). From the germaria of both sexual and asexual ovaries, each presumptive oocyte nucleus, arrested in prophase, sequentially migrates out to form a follicle. The oocyte grows in size surrounded by the follicular epithelium.

Bottom Line: In addition, we observed that asexual aphid tissues accumulated unspliced transcripts of Spo11, whereas sexual aphid tissues accumulated primarily spliced transcripts.In situ hybridization revealed Spo11 transcript in sexual germ cells and undetectable levels of Spo11 transcript in asexual germ cells.Together, these results suggest that parthenogenetic oogenesis evolved from a meiosis-like, and not a mitosis-like, process and that the aphid reproductive polyphenism may involve a modification of Spo11 gene activity.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute and Department of Ecology and Evolutionary Biology, Guyot Hall, Princeton University, Princeton, NJ, 08544, United States of America; Department of Biological Science, Rowan University, 201 Mullica Hill Rd, Glassboro, NJ, 08028, United States of America.

ABSTRACT
Aphids exhibit a form of phenotypic plasticity, called polyphenism, in which genetically identical females reproduce sexually during one part of the life cycle and asexually (via parthenogenesis) during the remainder of the life cycle. The molecular basis for aphid parthenogenesis is unknown. Cytological observations of aphid parthenogenesis suggest that asexual oogenesis evolved either through a modification of meiosis or from a mitotic process. As a test of these alternatives, we assessed the expression levels and expression patterns of canonical meiotic recombination and germline genes in the sexual and asexual ovaries of the pea aphid, Acyrthosiphon pisum. We observed expression of all meiosis genes in similar patterns in asexual and sexual ovaries, with the exception that some genes encoding Argonaute-family members were not expressed in sexual ovaries. In addition, we observed that asexual aphid tissues accumulated unspliced transcripts of Spo11, whereas sexual aphid tissues accumulated primarily spliced transcripts. In situ hybridization revealed Spo11 transcript in sexual germ cells and undetectable levels of Spo11 transcript in asexual germ cells. We also found that an obligately asexual strain of pea aphid produced little spliced Spo11 transcript. Together, these results suggest that parthenogenetic oogenesis evolved from a meiosis-like, and not a mitosis-like, process and that the aphid reproductive polyphenism may involve a modification of Spo11 gene activity.

Show MeSH
Related in: MedlinePlus