Evolutionary implications of morphogenesis and molecular patterning of the blind gut in the planarian Schmidtea polychroa

• Published in: Developmental biology Vol. 352; no. 1; pp. 164 - 176
• Main Authors: Martín-Durán, José María, Romero, Rafael
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.04.2011
• Subjects: Animals; anus; Biological Evolution; Body Patterning - genetics; central nervous system; complement; Development; Digestive system; Embryo, Nonmammalian - metabolism; Embryonic Development - genetics; Evolution; Fetal Proteins - genetics; Fetal Proteins - metabolism; Foregut; Gastrointestinal Tract - embryology; GATA Transcription Factors - genetics; GATA Transcription Factors - metabolism; gene deletion; gene expression; Gene Expression Regulation, Developmental; genes; Hindgut; Homeodomain Proteins - genetics; Homeodomain Proteins - metabolism; Membrane Proteins - genetics; Membrane Proteins - metabolism; Midgut; Models, Biological; morphogenesis; Phylogeny; Planarian; Planarians - embryology; Planarians - genetics; Platyhelminthes; T-Box Domain Proteins - genetics; T-Box Domain Proteins - metabolism; Planarian; Midgut; Hindgut; Digestive system; Development; Evolution; Foregut
• ISSN: 0012-1606; 1095-564X
• DOI: 10.1016/j.ydbio.2011.01.032

The formation of a through-gut was a key innovation in the evolution of metazoans. There is still controversy regarding the origin of the anus and how it may have been either gained or lost during evolution in different bilaterian taxa. Thus, the study of groups with a blind gut is of great importance for understanding the evolution of this organ system. Here, we describe the morphogenesis and molecular patterning of the blind gut in the sexual triclad Schmidtea polychroa. We identify and analyze the expression of goosecoid, commonly associated with the foregut, and the GATA, ParaHox and T-box genes, members of which commonly are associated with gut regionalization. We show that GATA456a is expressed in the blind gut of triclads, while GATA456b is localized in dorsal parenchymal cells. Goosecoid is expressed in the central nervous system, and the unique ParaHox gene identified, Xlox, is detected in association with the nervous system. We have not isolated any brachyury gene in the T-box complement of S. polychroa, which consists of one tbx1/10, three tbx2/3 and one tbx20. Furthermore, the absence of genes like brachyury and caudal is also present in other groups of Platyhelminthes. This study suggests that GATA456, in combination with foxA, is a gut-specific patterning mechanism conserved in the triclad S. polychroa, while the conserved gut-associated expression of foregut, midgut and hindgut markers is absent. Based on these data and the deviations in spiral cleavage found in more basal flatworms, we propose that the lack of an anus is an innovation of Platyhelminthes. This may be associated with loss of gut gene expression or even gene loss. ► We describe the embryonic development of the blind gut in the triclad S. polychroa. ► We analyze the expression of through-gut markers during the formation of the gut. ► We find that the foxA/ GATA456 gut-specific patterning mechanism is conserved. ► The gut-associated expression of foregut, midgut and hindgut markers is absent. ► We propose that the lack of an anus is an innovation of Platyhelminthes.