Immobility in the sedentary plant-parasitic nematode H. glycines is associated with remodeling of neuromuscular tissue.
The sedentary plant-parasitic nematodes are considered among the most economically damaging pathogens of plants. Following infection and the establishment of a feeding site, sedentary nematodes become immobile. Loss of mobility is reversed in adult males while females never regain mobility. The stru...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2018-08-01
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| Series: | PLoS Pathogens |
| Online Access: | https://doi.org/10.1371/journal.ppat.1007198 |
| _version_ | 1819007597117702144 |
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| author | Ziduan Han Sita Thapa Ursula Reuter-Carlson Hannah Reed Michael Gates Kris N Lambert Nathan E Schroeder |
| author_facet | Ziduan Han Sita Thapa Ursula Reuter-Carlson Hannah Reed Michael Gates Kris N Lambert Nathan E Schroeder |
| author_sort | Ziduan Han |
| collection | DOAJ |
| description | The sedentary plant-parasitic nematodes are considered among the most economically damaging pathogens of plants. Following infection and the establishment of a feeding site, sedentary nematodes become immobile. Loss of mobility is reversed in adult males while females never regain mobility. The structural basis for this change in mobility is unknown. We used a combination of light and transmission electron microscopy to demonstrate cell-specific muscle atrophy and sex-specific renewal of neuromuscular tissue in the sedentary nematode Heterodera glycines. We found that both females and males undergo body wall muscle atrophy and loss of attachment to the underlying cuticle during immobile developmental stages. Male H. glycines undergo somatic muscle renewal prior to molting into a mobile adult. In addition, we found developmental changes to the organization and number of motor neurons in the ventral nerve cord correlated with changes in mobility. To further examine neuronal changes associated with immobility, we used a combination of immunohistochemistry and molecular biology to characterize the GABAergic nervous system of H. glycines during mobile and immobile stages. We cloned and confirmed the function of the putative H. glycines GABA synthesis-encoding gene hg-unc-25 using heterologous rescue in C. elegans. We found a reduction in gene expression of hg-unc-25 as well as a reduction in the number of GABA-immunoreactive neurons during immobile developmental stages. Finally, we found evidence of similar muscle atrophy in the phylogenetically diverged plant-parasitic nematode Meloidogyne incognita. Together, our data demonstrate remodeling of neuromuscular structure and function during sedentary plant-parasitic nematode development. |
| first_indexed | 2024-12-21T00:27:06Z |
| format | Article |
| id | doaj.art-abfc87d041064314bb3068da4358fe50 |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-12-21T00:27:06Z |
| publishDate | 2018-08-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-abfc87d041064314bb3068da4358fe502022-12-21T19:21:58ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742018-08-01148e100719810.1371/journal.ppat.1007198Immobility in the sedentary plant-parasitic nematode H. glycines is associated with remodeling of neuromuscular tissue.Ziduan HanSita ThapaUrsula Reuter-CarlsonHannah ReedMichael GatesKris N LambertNathan E SchroederThe sedentary plant-parasitic nematodes are considered among the most economically damaging pathogens of plants. Following infection and the establishment of a feeding site, sedentary nematodes become immobile. Loss of mobility is reversed in adult males while females never regain mobility. The structural basis for this change in mobility is unknown. We used a combination of light and transmission electron microscopy to demonstrate cell-specific muscle atrophy and sex-specific renewal of neuromuscular tissue in the sedentary nematode Heterodera glycines. We found that both females and males undergo body wall muscle atrophy and loss of attachment to the underlying cuticle during immobile developmental stages. Male H. glycines undergo somatic muscle renewal prior to molting into a mobile adult. In addition, we found developmental changes to the organization and number of motor neurons in the ventral nerve cord correlated with changes in mobility. To further examine neuronal changes associated with immobility, we used a combination of immunohistochemistry and molecular biology to characterize the GABAergic nervous system of H. glycines during mobile and immobile stages. We cloned and confirmed the function of the putative H. glycines GABA synthesis-encoding gene hg-unc-25 using heterologous rescue in C. elegans. We found a reduction in gene expression of hg-unc-25 as well as a reduction in the number of GABA-immunoreactive neurons during immobile developmental stages. Finally, we found evidence of similar muscle atrophy in the phylogenetically diverged plant-parasitic nematode Meloidogyne incognita. Together, our data demonstrate remodeling of neuromuscular structure and function during sedentary plant-parasitic nematode development.https://doi.org/10.1371/journal.ppat.1007198 |
| spellingShingle | Ziduan Han Sita Thapa Ursula Reuter-Carlson Hannah Reed Michael Gates Kris N Lambert Nathan E Schroeder Immobility in the sedentary plant-parasitic nematode H. glycines is associated with remodeling of neuromuscular tissue. PLoS Pathogens |
| title | Immobility in the sedentary plant-parasitic nematode H. glycines is associated with remodeling of neuromuscular tissue. |
| title_full | Immobility in the sedentary plant-parasitic nematode H. glycines is associated with remodeling of neuromuscular tissue. |
| title_fullStr | Immobility in the sedentary plant-parasitic nematode H. glycines is associated with remodeling of neuromuscular tissue. |
| title_full_unstemmed | Immobility in the sedentary plant-parasitic nematode H. glycines is associated with remodeling of neuromuscular tissue. |
| title_short | Immobility in the sedentary plant-parasitic nematode H. glycines is associated with remodeling of neuromuscular tissue. |
| title_sort | immobility in the sedentary plant parasitic nematode h glycines is associated with remodeling of neuromuscular tissue |
| url | https://doi.org/10.1371/journal.ppat.1007198 |
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