Experimental Approach Reveals the Role of alx1 in the Evolution of the Echinoderm Larval Skeleton.

Over the course of evolution, the acquisition of novel structures has ultimately led to wide variation in morphology among extant multicellular organisms. Thus, the origins of genetic systems for new morphological structures are a subject of great interest in evolutionary biology. The larval skeleto...

Full description

Bibliographic Details
Main Authors: Hiroyuki Koga, Haruka Fujitani, Yoshiaki Morino, Norio Miyamoto, Jun Tsuchimoto, Tomoko F Shibata, Masafumi Nozawa, Shuji Shigenobu, Atsushi Ogura, Kazunori Tachibana, Masato Kiyomoto, Shonan Amemiya, Hiroshi Wada
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4750990?pdf=render
_version_ 1828413955053191168
author Hiroyuki Koga
Haruka Fujitani
Yoshiaki Morino
Norio Miyamoto
Jun Tsuchimoto
Tomoko F Shibata
Masafumi Nozawa
Shuji Shigenobu
Atsushi Ogura
Kazunori Tachibana
Masato Kiyomoto
Shonan Amemiya
Hiroshi Wada
author_facet Hiroyuki Koga
Haruka Fujitani
Yoshiaki Morino
Norio Miyamoto
Jun Tsuchimoto
Tomoko F Shibata
Masafumi Nozawa
Shuji Shigenobu
Atsushi Ogura
Kazunori Tachibana
Masato Kiyomoto
Shonan Amemiya
Hiroshi Wada
author_sort Hiroyuki Koga
collection DOAJ
description Over the course of evolution, the acquisition of novel structures has ultimately led to wide variation in morphology among extant multicellular organisms. Thus, the origins of genetic systems for new morphological structures are a subject of great interest in evolutionary biology. The larval skeleton is a novel structure acquired in some echinoderm lineages via the activation of the adult skeletogenic machinery. Previously, VEGF signaling was suggested to have played an important role in the acquisition of the larval skeleton. In the present study, we compared expression patterns of Alx genes among echinoderm classes to further explore the factors involved in the acquisition of a larval skeleton. We found that the alx1 gene, originally described as crucial for sea urchin skeletogenesis, may have also played an essential role in the evolution of the larval skeleton. Unlike those echinoderms that have a larval skeleton, we found that alx1 of starfish was barely expressed in early larvae that have no skeleton. When alx1 overexpression was induced via injection of alx1 mRNA into starfish eggs, the expression patterns of certain genes, including those possibly involved in skeletogenesis, were altered. This suggested that a portion of the skeletogenic program was induced solely by alx1. However, we observed no obvious external phenotype or skeleton. We concluded that alx1 was necessary but not sufficient for the acquisition of the larval skeleton, which, in fact, requires several genetic events. Based on these results, we discuss how the larval expression of alx1 contributed to the acquisition of the larval skeleton in the putative ancestral lineage of echinoderms.
first_indexed 2024-12-10T13:18:02Z
format Article
id doaj.art-fbc397cbe37849e692e427dd87dffe4c
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-10T13:18:02Z
publishDate 2016-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-fbc397cbe37849e692e427dd87dffe4c2022-12-22T01:47:27ZengPublic Library of Science (PLoS)PLoS ONE1932-62032016-01-01112e014906710.1371/journal.pone.0149067Experimental Approach Reveals the Role of alx1 in the Evolution of the Echinoderm Larval Skeleton.Hiroyuki KogaHaruka FujitaniYoshiaki MorinoNorio MiyamotoJun TsuchimotoTomoko F ShibataMasafumi NozawaShuji ShigenobuAtsushi OguraKazunori TachibanaMasato KiyomotoShonan AmemiyaHiroshi WadaOver the course of evolution, the acquisition of novel structures has ultimately led to wide variation in morphology among extant multicellular organisms. Thus, the origins of genetic systems for new morphological structures are a subject of great interest in evolutionary biology. The larval skeleton is a novel structure acquired in some echinoderm lineages via the activation of the adult skeletogenic machinery. Previously, VEGF signaling was suggested to have played an important role in the acquisition of the larval skeleton. In the present study, we compared expression patterns of Alx genes among echinoderm classes to further explore the factors involved in the acquisition of a larval skeleton. We found that the alx1 gene, originally described as crucial for sea urchin skeletogenesis, may have also played an essential role in the evolution of the larval skeleton. Unlike those echinoderms that have a larval skeleton, we found that alx1 of starfish was barely expressed in early larvae that have no skeleton. When alx1 overexpression was induced via injection of alx1 mRNA into starfish eggs, the expression patterns of certain genes, including those possibly involved in skeletogenesis, were altered. This suggested that a portion of the skeletogenic program was induced solely by alx1. However, we observed no obvious external phenotype or skeleton. We concluded that alx1 was necessary but not sufficient for the acquisition of the larval skeleton, which, in fact, requires several genetic events. Based on these results, we discuss how the larval expression of alx1 contributed to the acquisition of the larval skeleton in the putative ancestral lineage of echinoderms.http://europepmc.org/articles/PMC4750990?pdf=render
spellingShingle Hiroyuki Koga
Haruka Fujitani
Yoshiaki Morino
Norio Miyamoto
Jun Tsuchimoto
Tomoko F Shibata
Masafumi Nozawa
Shuji Shigenobu
Atsushi Ogura
Kazunori Tachibana
Masato Kiyomoto
Shonan Amemiya
Hiroshi Wada
Experimental Approach Reveals the Role of alx1 in the Evolution of the Echinoderm Larval Skeleton.
PLoS ONE
title Experimental Approach Reveals the Role of alx1 in the Evolution of the Echinoderm Larval Skeleton.
title_full Experimental Approach Reveals the Role of alx1 in the Evolution of the Echinoderm Larval Skeleton.
title_fullStr Experimental Approach Reveals the Role of alx1 in the Evolution of the Echinoderm Larval Skeleton.
title_full_unstemmed Experimental Approach Reveals the Role of alx1 in the Evolution of the Echinoderm Larval Skeleton.
title_short Experimental Approach Reveals the Role of alx1 in the Evolution of the Echinoderm Larval Skeleton.
title_sort experimental approach reveals the role of alx1 in the evolution of the echinoderm larval skeleton
url http://europepmc.org/articles/PMC4750990?pdf=render
work_keys_str_mv AT hiroyukikoga experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT harukafujitani experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT yoshiakimorino experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT noriomiyamoto experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT juntsuchimoto experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT tomokofshibata experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT masafuminozawa experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT shujishigenobu experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT atsushiogura experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT kazunoritachibana experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT masatokiyomoto experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT shonanamemiya experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton
AT hiroshiwada experimentalapproachrevealstheroleofalx1intheevolutionoftheechinodermlarvalskeleton