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Molecular and Evolutionary Aspects of the Protochordate Digestive System

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Molecular and Evolutionary Aspects of the Protochordate Digestive System Cell and Tissue Research (2019) 377:309–320 https://doi.org/10.1007/s00441-019-03035-5 REVIEW Molecular and evolutionary aspects of the protochordate digestive system Satoshi Nakayama1 & Toshio Sekiguchi2 & Michio Ogasawara1 Received: 29 November 2018 /Accepted: 12 April 2019 /Published online: 2 May 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract The digestive system is a functional unit consisting of an endodermal tubular structure (alimentary canal) and accessory organs that function in nutrition processing in most triploblastic animals. Various morphologies and apparatuses are formed depending on the phylogenetical relationship and food habits of the specific species. Nutrition processing and morphogenesis of the alimentary canal and accessory organs have both been investigated in vertebrates, mainly humans and mammals. When attempting to understand the evolutionary processes that led to the vertebrate digestive system, however, it is useful to examine other chordates, specifically protochordates, which share fundamental functional and morphogenetic molecules with vertebrates, which also possess non- duplicated genomes. In protochordates, basic anatomical and physiological studies have mainly described the characteristic traits of suspension feeders. Recent progress in genome sequencing has allowed researchers to comprehensively detail protochordate genes and has compared the genetic backgrounds among chordate nutrition processing and alimentary canal/accessory organ systems based on genomic information. Gene expression analyses have revealed spatiotemporal gene expression profiles in protochordate alimentary canals. Additionally, to investigate the basis of morphological diversity in the chordate alimentary canal and accessory organs, evolutionary developmental research has examined developmental transcription factors related to morpho- genesis and anterior-posterior pattering of the alimentary canal and accessory organs. In this review, we summarize the current knowledge of molecules involved in nutrition processing and the development of the alimentary canal and accessory organs with innate immune and endocrine roles in protochordates and we explore the molecular basis for understanding the evolution of the chordate digestive system. Keywords Digestive system . Lancelets . Tunicates . Gene expression . Evolution Introduction upon habitat (aquatic, amphibious, or terrestrial) and food habits (carnivorous, herbivorous, or omnivorous) (Fig. 1). The digestive system is a functional unit. The digestive system Alimentary canals with accessory organs, however, have shared functionally performs nutrition processing and morphologically functional sequential processing stages for nutrition processing, consists of an epithelial tubular structure (alimentary canal) and including ingestion, digestion, absorption and elimination that accessory organs in most triploblastic animals, which are het- occur from the mouth to the anus (Reece et al. 2011). erotrophic organisms (Ruppert et al. 2003; Schmidt-Rhaesa Developmentally, the alimentary canal and accessory organs 2007). The morphology of the alimentary canal and accessory are formed as endodermal derivatives (Schmidt-Rhaesa 2007). organs varies greatly among triploblastic animals depending Generally, the endoderm is specified into three regions (foregut, midgut and hindgut). Each region is subdivided into several digestive compartments, such as the pharynx, esophagus, stom- ach and intestine, with the addition of accessory organs includ- * Michio Ogasawara [email protected] ing the pancreas and liver, that exhibit various shapes in each animal group. Although the nomenclature for each digestive 1 The Graduate School of Science, Chiba University, 1-33 Yayoi-cho, compartment is based on the homologous structure in closely Inage-ku, Chiba 263-8522, Japan related animals, occasionally, a specific name is used in a cer- 2 The Noto Marine Laboratory, Division of Marine Environmental tain animal group and some traits are given the same name in Studies, Institute of Nature and Environmental Technology, spite of the fact that their shape is greatly divergent and unclear Kanazawa University, Hosu-gun, Ishikawa 927-0553, Japan 310 Cell Tissue Res (2019) 377:309–320 Fig. 1 Phylogenic relationships of chordates and their habitat, food habit canal and accessory organs are developmentally divided into three and morphology of the alimentary canal and accessory organs. Chordates regions (foregut, midgut and hindgut). The morphology of the consist of lancelets, tunicates and vertebrates. Lancelets and tunicates are alimentary canal and accessory organs varies depending on their collectively called Bprotochordates^. The habitats of chordates are diverse phylogenetic relationship and food habit. esp, esophagus; hc, hepatic (aquatic, amphibious, or terrestrial) and therefore their food habits are also cecum; ph, pharynx; st, stomach divergent (carnivorous, herbivorous, or omnivorous). The alimentary homology (e.g., the stomach). Therefore, morphologies and of vertebrate traits is progressing (Dehal et al. 2002;Putnam nomenclature of the alimentary canal and accessory organs et al. 2008;Brozovicetal.2018). can be confusing and the evolution of digestive systems among In this review, we summarize the current knowledge of animal groups should be examined with care, particularly protochordate digestive systems in view of recently accumulat- among different taxa. ed protochordate genomic information, as this information in- To investigate the evolution of digestive systems, knowledge creases our understanding of vertebrate digestive system evo- of phylogenetically varied animals is useful; however, among lution. We first present current anatomical, histlogical and phys- the deuterostomes, studies of the digestive system have been iological knowledge as fundamental information. Then, we ex- mostly carried out in mammals. Therefore, descriptions of the amine the recent state of genome-wide research from molecular digestive system in general biology textbooks are typically fo- and evolutionary perspectives, with a special focus on the di- cused on vertebrates, while descriptions of the digestive system gestive system genes related to the nutrition processing and of other animals are limited. This biased knowledge limits the morphogenesis of the alimentary canal and accessory organs evolutionary understanding of the digestive system (Reece et al. (i.e., differentiation marker genes and developmental transcrip- 2011). Thus, further study in invertebrates provides us with new tion factor genes). We also describe the spatiotemporal expres- insight into the evolution of this organ system. sion patterns of digestive and absorptive differentiation marker Protochordates (lancelets and tunicates) are invertebrate genes and developmental transcription factor genes in chordates that are closely related phylogenetically to vertebrates protochordates. Finally, we discuss the evolution of the chor- (Dehal et al. 2002; Putnam et al. 2008). Molecular phyloge- date digestive system based on the current knowledge of gene netics studies demonstrate that tunicates are a sister group of expression profiles in protochordates. vertebrates and lancelets (also called amphioxus), with the tu- nicates and the vertebrates, constitute the phylum Chordata (Putnam et al. 2008). Protochordates with non-duplicated ge- Anatomical and histological features nomes that arose prior to the whole genome duplication in the of the protochordate alimentary canal vertebrate lineage have been emerging as a key animal group and accessory organs for evolutionary research on the origin of vertebrates. Additionally, the number of protochordate species whose ge- Lancelets and tunicates are marine chordates and they capture nomes have been sequenced has increased in recent years. food particles in seawater through the pharynx as suspension Thus, genome-wide and molecular research on the evolution feeders (Satoh 2009)(Fig.1). The morphology of the Cell Tissue Res (2019) 377:309–320 311 alimentary canal and accessory organs of protochordates varies analyses: (1) Appendicularia, (2) Thaliacea + among protochordate species; however, the sequence of diges- Phlebobranchia + Aplousobranchia and (3) Stolidobranchia tive compartments of the alimentary canal along the anterior- (Kocot et al. 2018;Delsucetal.2018). In this section, we posterior axis (mouth, pharynx, esophagus, stomach/chamber, focus on appendicularians, thaliaceans and ascidians intestine and anus) is sharedinprotochordates(Fig.1). (phlebobranchs, aplousobranchs and stolidobranchs). Appendicularians, known as free-swimming tunicates and Lancelets possess a straight alimentary canal the sister group of all other tunicates, possess a different sus- pension feeding mode compared with that of other tunicates Lancelets, which are fish-like marine chordates, possess an that use a unique mucus net called a Bhouse.^ They do not alimentary canal that exhibits morphologically less diversity need to filter food particles in the pharynx and they possess among species. The alimentary canal extends linearly with only a single pair of gill pores instead of numerous gill slits in several digestive compartments along the anterior-posterior the pharynx (Brena et al. 2003; Burighel et al. 2005; Onuma body axis (Kaji et al. 2013). The pharynx is the domain re- et al. 2017). The endostyle is generally formed on the ventral sponsible for filtering food particles suspended in seawater
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