Abstract
The dichotomy between smooth and striated myocytes is fundamental for bilaterian musculature, but its evolutionary origin is unsolved. In particular, interrelationships of visceral smooth muscles remain unclear. Absent in fly and nematode, they have not yet been characterized molecularly outside vertebrates. Here, we characterize expression profile, ultrastructure, contractility and innervation of the musculature in the marine annelid Platynereis dumerilii and identify smooth muscles around the midgut, hindgut and heart that resemble their vertebrate counterparts in molecular fingerprint, contraction speed and nervous control. Our data suggest that both visceral smooth and somatic striated myocytes were present in the protostome-deuterostome ancestor and that smooth myocytes later co-opted the striated contractile module repeatedly - for example, in vertebrate heart evolution. During these smooth-to-striated myocyte conversions, the core regulatory complex of transcription factors conveying myocyte identity remained unchanged, reflecting a general principle in cell type evolution.
Highlights
Musculature is composed of myocytes that are specialized for active contraction (SchmidtRhaesa, 2007)
The conservation of molecular signatures for both smooth and striated myocytes indicates that a dual musculature already existed in bilaterian ancestors: a fast striated somatic musculature, under strict nervous control; and a slow smooth visceral musculature around the midgut and hindgut, able to undergo automatic peristalsis due to self-excitable myocytes directly coupled by gap junctions
A core regulatory complexes’ (CoRCs) composed of NK3, FoxF and GATA4/5/6 together with Myocyte Enhancer Factor-2 (Mef2) and Myocardin activated the smooth contractile effectors SM-myosin heavy chains (MHC), SM-MRLC and calponin (Figure 7—figure supplement 1)
Summary
Musculature is composed of myocytes that are specialized for active contraction (SchmidtRhaesa, 2007). In vertebrates, striated myocytes are found in voluntary skeletal muscles, and at the anterior and posterior extremities of the digestive tract (anterior esophagus muscles and external anal sphincter), and in the muscular layer of the heart; smooth myocytes are found in involuntary visceral musculature that ensures slow, long-range deformation of internal organs. This includes the posterior esophagus and the rest of the gut, and blood vessels, and most of the urogenital system. In the nematode Caenorhabditis, somatic muscles are striated, while the short intestine and rectum visceral myocytes are only one sarcomere-long and hard to classify (Corsi et al, 2000; White, 1988)
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