Research Article: Immobility in the sedentary plant-parasitic nematode H. glycines is associated with remodeling of neuromuscular tissue

Date Published: August 16, 2018

Publisher: Public Library of Science

Author(s): Ziduan Han, Sita Thapa, Ursula Reuter-Carlson, Hannah Reed, Michael Gates, Kris N. Lambert, Nathan E. Schroeder, Adler Dillman.


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.

Partial Text

The sedentary plant-parasitic nematodes are among the most damaging pathogens to agricultural crop production [1]. For example, the soybean cyst nematode, Heterodera glycines, accounts for over a billion dollars in yield loss yearly [2]. H. glycines hatches as an infective, mobile second-stage juvenile (J2) (Fig 1). Following infection, H. glycines establishes a multinucleated feeding site and develops from a vermiform J2 to lemon-shaped and sausage-shaped J4 females and males, respectively (Fig 1). While feeding, both sexes are restricted in movement to slight head motion at their feeding site [3]. During J4, males undergo extensive morphological remodeling back to a vermiform morphology. Following the final molt, the adult male is fully mobile, while the female remains lemon-shaped and immobile.

We demonstrate that H. glycines undergoes a progressive atrophy of neuromuscular tissue that likely leads to immobility. Elsea (1951) suggested that the absence of body wall muscle in M. hapla adult females was “a result of the sedentary mode of life”; however, this conclusion was based on light microscopy of mobile J2s and adult females. While we cannot entirely rule out that the loss of muscle mass in H. glycines is caused by a lack of movement, our data suggests this is highly unlikely. We demonstrate that muscle atrophy occurs in conjunction with loss of mobility. Furthermore, cyst nematodes, such as H. glycines, are able to survive as fully developed, but inactive J2s, for years in a pre-hatch diapause state [34]. Upon activation by a hatching stimulant, these animals readily resume movement suggesting that inactivity alone does not result in muscle atrophy. We suggest that the combination of muscle atrophy and detachment of muscle from the cuticle combined with changes to neuron structure and gene expression cause immobility in feeding cyst nematodes.