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

Abstract

BackgroundMany 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.ResultsWe 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.ConclusionsThe 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.

Root-knot nematodes demonstrate temporal variation in host penetration

“…On the other hand, earlier developmental stages of nematode do not follow rhythmic pattern. We found no obvious differences in percentage of egg hatch and juvenile mobility over time points in in vitro condition but around 12% of hatch was observed under both constant light and dark conditions after two days suggesting that M. incognita eggs are capable of hatching even without host stimulant, unlike other plant-parasitic nematodes (Wesemael et al, 2006;Thapa et al, 2017).…”

Pattern regulation in a regenerating jellyfish

“…The manubrium, tentacle bulbs and gonads harbor populations of stem cells ( Amiel and Houliston, 2009 ; Denker et al, 2008 ; Leclère et al, 2012 ), have autonomous functions and can be regarded as true organs. The main component of the umbrella is an acellular connective layer, the mesoglea ( Figure 1C ), covered on its external surface, the ‘exumbrella’, by a simple monolayer of epithelial cells ( Kamran et al, 2017 ). The concave face of the umbrella, termed ‘subumbrella’, is composed of three overlapping tissues layers ( Figure 1C ): (i) an inner epithelium associated with the mesoglea, (ii) an overlying cnidarian-specific tissue type comprising radially aligned smooth epitheliomuscular cells (‘radial smooth muscles’), (iii) a ring of striated epitheliomuscular cells at the umbrella periphery which power swimming contractions, and are sandwiched between the other two layers ( Leclère and Röttinger, 2016 ).…”

A species-specific nematocide that results in terminal embryogenesis

“…For example, our result that natural variation in ZTDO susceptibility suggests that embryos of wild P. pacificus populations exposed to a pulse of ZTDO could perhaps delay hatching. In this respect, ZTDO-induced embryonic arrest may be analogous to host-mediated hatching behavior found in the plant parasitic nematode Heterodera glycines, whereby unidentified root exudate from fresh samples stimulates hatching (Tefft and Bone, 1985;Perry, 2002;Thapa et al, 2017). However, whereas host cues increased hatching rate but have no effect on pre-hatching development in H. glycines (Thapa et al, 2017), the early exposure and terminal embryogenesis in P. pacificus suggests that ZTDO affects hatching rate indirectly by disrupting prehatching development, rather than the mechanisms required for hatching per se.…”