Conserved behavioral and genetic mechanisms in the pre-hatching molt of the nematode Pristionchus pacificus

EvoDevo

Ray L Hong¹  Victor M Lewis¹ 

[1] Department of Biology, California State University, Northridge, 18111 Nordhoff Street, Northridge, CA 91330-8303, USA

关键词: Heterochrony;    Nematode;    Developmental timing;    Ecdysis;    Molting;   

Others  :  1093380
DOI  :  10.1186/2041-9139-5-31

 received in 2014-07-03, accepted in 2014-08-27,  发布年份 2014

【 摘 要 】

Background

During development, juvenile nematodes undergo four molts. Although the number of molts appears to be constant within the Nematoda, the timing of the first molt can occur either before or after hatching. A previous study indicates that, as in some parasitic nematode lineages, a pre-hatching juvenile stage also exists in Diplogastrid nematodes. A detailed description of these sequence of events has yet to be shown for any single species.

Findings

To delineate the timing of the pre-hatching molt in the beetle-associated Pristionchus pacificus, we tracked individual mid-J1 stage worms inside the eggshell through the J1-J2 transition and hatching. We found that active movement ended 21 hours after egg-laying, followed by lethargus and hatching. We inferred that lethargus behavior represents the onset of the first molt, which precedes each post-hatching molt in C. elegans and P. pacificus. The onset of the J1-J2 molt was also marked by the upregulation of the P. pacificus molting marker Ppa-pnhr-1. We further corroborated the pre-hatching molt with the isolation of two genetic mutants that exhibited aberrant molting both inside the egg and after hatching, as characterized by protracted and often-aborted shedding of the old cuticle.

Conclusion

Our results describe in detail the pre-hatching juvenile molt in P. pacificus, provide strong visual evidence of a pre-hatching molt, and show support for common genetic mechanisms regulating molting in the pre-hatching and post-hatching developmental stages. Our findings support the hypothesis that the evolution of pre-hatching development in Diplogastrid nematodes is likely due to a heterochronic shift between the timing of the first molt and hatching.

【 授权许可】

   
2014 Lewis and Hong; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA: Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 1997, 387:489-493.
• [2]Singh R, Sulston J: Some observations on moulting in Caenorhabditis elegans. Nematologica 1978, 24:63-71.
• [3]Lee DL: The Biology of Nematodes. London: Taylor and Francis; 2002.
• [4]Ambros V: A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell 1989, 57:49-57.
• [5]Ambros V, Horvitz HR: Heterochronic mutants of the nematode Caenorhabditis elegans. Science 1984, 226:409-416.
• [6]Felix M, Hill R, Schwarz H, Sternberg PW, Sudhaus W, Sommer RS: Pristionchus pacificus, a nematode with only three juvenile stages, displays major heterochronic changes relative to Caenorhabditis elegans. Proc R Soc London 1999, 266:1617-1621.
• [7]Oh WS, Jeong PY, Joo HJ, Lee JE, Moon YS, Cheon HM, Kim JH, Lee YU, Shim YH, Paik YK: Identification and characterization of a dual-acting antinematodal agent against the pinewood nematode, Bursaphelenchus xylophilus. PLoS One 2009, 4:e7593.
• [8]Palomares-Rius JE, Jones JT, Cock PJ, Castillo P, Blok VC: Activation of hatching in diapaused and quiescent Globodera pallida. Parasitology 2013, 140:445-454.
• [9]Anderson RC: Nematode Parasites of Vertebrates. Their Development and Transmission. Wallingford: CAB International; 1992.
• [10]Fürst Von Lieven A: The embryonic moult in diplogastrids (Nematoda) – homology of developmental stages and heterochrony as a prerequisite for morphological diversity. Zool Anzeiger - A J Comp Zool 2005, 244:79-91.
• [11]Dillman AR, Chaston JM, Adams BJ, Ciche TA: PLoS pathogens: an entomopathogenic nematode by any other name. PLoS Pathog 2012, 8:e1002527.
• [12]Hong RL, Sommer RJ: Pristionchus pacificus: a well-rounded nematode. Bioessays 2006, 28:651-659.
• [13]Altun ZF, Herndon LA, Crocker C, Lints R, Hall DH: WormAtlas. [http://www.wormatlas.org webcite]
• [14]Frand AR, Russel S, Ruvkun G: Functional genomic analysis of C. elegans molting. PLoS Biol 2005, 3:e312.
• [15]Yao TP, Forman BM, Jiang Z, Cherbas L, Chen JD, McKeown M, Cherbas P, Evans RM: Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 1993, 366:476-479.
• [16]Barchuk AR, Maleszka R, Simoes ZL: Apis mellifera ultraspiracle: cDNA sequence and rapid up-regulation by juvenile hormone. Insect Mol Biol 2004, 13:459-467.
• [17]Hannan GN, Hill RJ: Lcusp, an ultraspiracle gene from the sheep blowfly, Lucilia cuprina: cDNA cloning, developmental expression of RNA and confirmation of function. Insect Biochem Mol Biol 2001, 31:771-781.
• [18]Parihar M, Minton RL, Flowers S, Holloway A, Morehead BE, Paille J, Gissendanner CR: The genome of the nematode Pristionchus pacificus encodes putative homologs of RXR/Usp and EcR. Gen Comp Endocrinol 2010, 167:11-17.
• [19]Brenner S: The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.