Abstract
Background Freshwater planarians are well known for their regenerative abilities. Less well known is how planarians maintain spatial patterning in long-lived adult animals or how they re-pattern tissues during regeneration. HOX genes are good candidates to regulate planarian spatial patterning, yet the full complement or genomic clustering of planarian HOX genes has not yet been described, primarily because only a few have been detectable by in situ hybridization, and none have given morphological phenotypes when knocked down by RNAi.ResultsBecause the planarian Schmidteamediterranea (S. mediterranea) is unsegmented, appendage less, and morphologically simple, it has been proposed that it may have a simplified HOX gene complement. Here, we argue against this hypothesis and show that S. mediterranea has a total of 13 HOX genes, which represent homologs to all major axial categories, and can be detected by whole-mount in situ hybridization using a highly sensitive method. In addition, we show that planarian HOX genes do not cluster in the genome, yet 5/13 have retained aspects of axially restricted expression. Finally, we confirm HOX gene axial expression by RNA deep-sequencing 6 anterior–posterior “zones” of the animal, which we provide as a dataset to the community to discover other axially restricted transcripts.ConclusionsFreshwater planarians have an unappreciated HOX gene complexity, with all major axial categories represented. However, we conclude based on adult expression patterns that planarians have a derived body plan and their asexual lifestyle may have allowed for large changes in HOX expression from the last common ancestor between arthropods, flatworms, and vertebrates. Using our in situ method and axial zone RNAseq data, it should be possible to further understand the pathways that pattern the anterior–posterior axis of adult planarians.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-016-0044-8) contains supplementary material, which is available to authorized users.
Highlights
Freshwater planarians are well known for their regenerative abilities
We show that S. mediterranea has a total of 13 HOX genes which represent all major A–P categories
In order to detect the spatial expression of S. mediterranea HOX genes, we developed a very sensitive wholemount in situ hybridization (WISH) technique as well as performed RNA deep sequencing (RNAseq) of 6 A–P zones of the animal to confirm HOX gene whole-mount in situ hybridization (WISH) detection and to provide this as a resource for future gene discovery
Summary
Less well known is how planarians maintain spatial patterning in long-lived adult animals or how they re-pattern tissues during regeneration. HOX genes are good candidates to regulate planarian spatial patterning, yet the full complement or genomic clustering of planarian HOX genes has not yet been described, primarily because only a few have been detectable by in situ hybridization, and none have given morphological phenotypes when knocked down by RNAi. HOX genes are well-known, conserved regulators of axial body patterning during embryogenesis in most studied animals [1,2,3,4,5,6]. HOX genes tend to exist in clusters in the genome in the exact order on the chromosome in which they are spatially expressed along the anterior–posterior (A–P) axis—a mechanism termed “colinearity” [8, 9]. Depending on the organism, HOX genes can be lost (parasitic flatworms: 7 HOX [16,17,18]; C. elegans: 6 HOX [19]), duplicated
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