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Embryogenesis in the parasitic nematode Heterodera glycines is independent of host-derived hatching stimulation

BACKGROUND: Many parasites regulate their development to synchronize their life cycle with a compatible host. The parasitic nematode Heterodera glycines displays incomplete host-mediated hatching behavior wherein some H. glycines individuals hatch only in the presence of a host-derived cue while oth...

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Autores principales: Thapa, Sita, Patel, Jayna A., Reuter-Carlson, Ursula, Schroeder, Nathan E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5225516/
https://www.ncbi.nlm.nih.gov/pubmed/28077087
http://dx.doi.org/10.1186/s12861-016-0144-7
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author Thapa, Sita
Patel, Jayna A.
Reuter-Carlson, Ursula
Schroeder, Nathan E.
author_facet Thapa, Sita
Patel, Jayna A.
Reuter-Carlson, Ursula
Schroeder, Nathan E.
author_sort Thapa, Sita
collection PubMed
description BACKGROUND: Many parasites regulate their development to synchronize their life cycle with a compatible host. The parasitic nematode Heterodera glycines displays incomplete host-mediated hatching behavior wherein some H. glycines individuals hatch only in the presence of a host-derived cue while others hatch in water alone. Furthermore, H. glycines shows variable hatching behavior based on oviposition location. The mechanisms regulating this hatching variability are unknown. In this study, we established a detailed timeline of the H. glycines pre-hatch development from early embryogenesis to the pre-hatched J2. These descriptive data were then used to test hypotheses regarding the effect of host stimulus and oviposition location on pre-hatch development. RESULTS: We found that H. glycines develops from a single-cell egg to a fully formed J2 in approximately 172 hours. The stylet-based mouthpart, which is used to pierce the eggshell during hatching, is not completely formed until late in pre-hatch J2 development and is preceded by the formation of stylet protractor muscles. We also found that the primary motor nervous system of H. glycines did not complete development until late in pre-hatch J2 development. These data suggest possible structural requirements for H. glycines hatching. As expected, exposure of H. glycines eggs to host-derived cues increased the percentage of nematodes that hatched. However, exposure to hatching cues did not affect pre-hatch development. Similarly, we found no obvious differences in the pre-hatch developmental timeline between eggs laid in an egg sac or retained within the mother. CONCLUSIONS: The pattern of early embryonic development in H. glycines was very similar to that recently described in the related parasitic nematode Meloidogyne incognita. However, the speed of H. glycines pre-hatch development was approximately three times faster than reported for M. incognita. Our results suggest that hatching stimulants do not affect embryogenesis itself but only influence the hatching decision once J2 development is complete. Similarly, the oviposition location does not alter the rate of embryogenesis. These results provide insight into the primary survival mechanism for this important parasite.
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spelling pubmed-52255162017-01-17 Embryogenesis in the parasitic nematode Heterodera glycines is independent of host-derived hatching stimulation Thapa, Sita Patel, Jayna A. Reuter-Carlson, Ursula Schroeder, Nathan E. BMC Dev Biol Research Article BACKGROUND: Many parasites regulate their development to synchronize their life cycle with a compatible host. The parasitic nematode Heterodera glycines displays incomplete host-mediated hatching behavior wherein some H. glycines individuals hatch only in the presence of a host-derived cue while others hatch in water alone. Furthermore, H. glycines shows variable hatching behavior based on oviposition location. The mechanisms regulating this hatching variability are unknown. In this study, we established a detailed timeline of the H. glycines pre-hatch development from early embryogenesis to the pre-hatched J2. These descriptive data were then used to test hypotheses regarding the effect of host stimulus and oviposition location on pre-hatch development. RESULTS: We found that H. glycines develops from a single-cell egg to a fully formed J2 in approximately 172 hours. The stylet-based mouthpart, which is used to pierce the eggshell during hatching, is not completely formed until late in pre-hatch J2 development and is preceded by the formation of stylet protractor muscles. We also found that the primary motor nervous system of H. glycines did not complete development until late in pre-hatch J2 development. These data suggest possible structural requirements for H. glycines hatching. As expected, exposure of H. glycines eggs to host-derived cues increased the percentage of nematodes that hatched. However, exposure to hatching cues did not affect pre-hatch development. Similarly, we found no obvious differences in the pre-hatch developmental timeline between eggs laid in an egg sac or retained within the mother. CONCLUSIONS: The pattern of early embryonic development in H. glycines was very similar to that recently described in the related parasitic nematode Meloidogyne incognita. However, the speed of H. glycines pre-hatch development was approximately three times faster than reported for M. incognita. Our results suggest that hatching stimulants do not affect embryogenesis itself but only influence the hatching decision once J2 development is complete. Similarly, the oviposition location does not alter the rate of embryogenesis. These results provide insight into the primary survival mechanism for this important parasite. BioMed Central 2017-01-11 /pmc/articles/PMC5225516/ /pubmed/28077087 http://dx.doi.org/10.1186/s12861-016-0144-7 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Thapa, Sita
Patel, Jayna A.
Reuter-Carlson, Ursula
Schroeder, Nathan E.
Embryogenesis in the parasitic nematode Heterodera glycines is independent of host-derived hatching stimulation
title Embryogenesis in the parasitic nematode Heterodera glycines is independent of host-derived hatching stimulation
title_full Embryogenesis in the parasitic nematode Heterodera glycines is independent of host-derived hatching stimulation
title_fullStr Embryogenesis in the parasitic nematode Heterodera glycines is independent of host-derived hatching stimulation
title_full_unstemmed Embryogenesis in the parasitic nematode Heterodera glycines is independent of host-derived hatching stimulation
title_short Embryogenesis in the parasitic nematode Heterodera glycines is independent of host-derived hatching stimulation
title_sort embryogenesis in the parasitic nematode heterodera glycines is independent of host-derived hatching stimulation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5225516/
https://www.ncbi.nlm.nih.gov/pubmed/28077087
http://dx.doi.org/10.1186/s12861-016-0144-7
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