Year: 2022
Type: article
Abstract: Hox and ParaHox transcription factors are important for specifying cell fates along the primary body axes during the development of most animals. Within Cnidaria, much of the research on Hox/ParaHox genes has focused on Anthozoa (anemones and corals) and Hydrozoa (hydroids) and has concentrated on the evolution and function of cnidarian Hox genes in relation to their bilaterian counterparts. Here we analyze together the full complement of Hox and ParaHox genes from species representing all four medusozoan classes (Staurozoa, Cubozoa, Hydrozoa, and Scyphozoa) and both anthozoan classes (Octocorallia and Hexacorallia). Our results show that Hox genes involved in patterning the directive axes of anthozoan polyps are absent in the stem leading to Medusozoa. For the first time, we show spatial and temporal expression patterns of Hox and ParaHox genes in the upside-down jellyfish Cassiopea xamachana (Scyphozoa), which are consistent with diversification of medusozoan Hox genes both from anthozoans and within medusozoa. Despite unprecedented taxon sampling, our phylogenetic analyses, like previous studies, are characterized by a lack of clear homology between most cnidarian and bilaterian Hox and Hox-related genes. Unlike previous studies, we propose the hypothesis that the cnidarian-bilaterian ancestor possessed a remarkably large Hox complement and that extensive loss of Hox genes was experienced by both cnidarian and bilaterian lineages.
Source: Genome Biology and Evolution
DOI: 10.1093/gbe/evac172
Institution: University of Florida
Language: English
Subfield: Paleontology
Field: Earth and Planetary Sciences
Domain: Physical Sciences
Open Access status: gold
Estimated APC paid: $2,714
Awards: Dimensions: Collaborative Research: Life at extremes: Linking the phylogenetic and genomic diversity of ctenophores to ecophysiological adaptations in the deep sea, THE EVOLUTION OF CELL-CELL ADHESION AND THE ASSEMBLY OF EPITHELIAL TISSUES WERE INTIMATELY COUPLED TO THE EVOLUTION OF COMPLEX MULTICELLULARITY. EPITHELIA HAVE ESSENTIAL ROLES FROM ACTING AS AN ENVIRONMENTAL BARRIER AND PARTITIONING ORGANISMS INTO DISCRETE COMPARTMENTS TO COORDINATING MORPHOGENESIS DURING DEVELOPMENT. WE PROPOSE TO EXPLORE THE EARLY EVOLUTION OF EPITHELIA - STRUCTURES THAT WE PREDICT WOULD BE ADVANTAGEOUS IN COMPLEX LIFE FORMS ANYWHERE TO UNDERSTAND INNOVATIONS IN THE ANIMAL STEM-LINEAGE THAT CONTRIBUTED TO THE EVOLUTION OF ANIMAL BODY PLANS. DEFINING FEATURES OF EPITHELIA ARE THE ADHESION MODULES THAT TETHER CELLS TO EACH OTHER ENABLE FOLDING AND BENDING OF SHEETS AND TUBES OF CELLS DEFINE APICAL/BASAL POLARITY AND SPECIFY GENE EXPRESSION. OUR FOCUS IS ON THE CADHERIN/CATENIN MODULE (CCM) WHICH FORMS THE MOLECULAR FOUNDATION OF ADHERENS JUNCTIONS IN ALL STUDIED BILATERIAN TISSUES AND IS HYPOTHESIZED TO HAVE EVOLVED IN CONCERT WITH ANIMAL MULTICELLULARITY. FORMATION OF THESE JUNCTIONS APPEARS TO BE THE EARLIEST EVENT IN EPITHELIAL MORPHOGENESIS AND IT SERVES AS A SPATIAL LANDMARK FOR FORMATION OF OTHER TYPES OF CELL-CELL JUNCTIONS. EXPERIMENTAL DISRUPTION OF THE CCM PERTURBS EPITHELIAL DEVELOPMENT INTEGRITY AND POLARITY. OUR OBJECTIVE IS TO EXAMINE HOW AN ANCIENT ACTINMYOSIN SCAFFOLD COMMON TO ALL EUKARYOTES WAS RECRUITED BY THE MORE RECENTLY EVOLVED CCM TO COORDINATE CELL INTERACTIONS NECESSARY FOR MULTICELLULARITY AND TISSUE DIVERSITY. IMPORTANTLY THIS MULTI-FUNCTIONAL MODULE IS PRESENT IN ALL ANIMAL LINEAGES AND POTENTIALLY SATISFIES ALL REQUIREMENTS FOR MULTICELLULAR ADHESION AND MORPHOGENESIS - CADHERINS ENABLE ADHESION BETWEEN CELLS AND CATENINS BIND TO THE ACTIN SCAFFOLD TO ORGANIZE MULTICELLULAR ARCHITECTURE AND CAN SIGNAL TO THE NUCLEUS TO CHANGE GENE EXPRESSION. WE HAVE A DETAILED MECHANISTIC UNDERSTANDING OF THE COMPONENT PARTS AND FUNCTION OF THIS ADHESION MODULE IN BILATERIAN ANIMALS BUT THE EARLY EVOLUTION OF THIS MODULE IS FAR LESS CLEAR. OUR APPROACH IS TO EXAMINE THE FUNCTION OF CCM PROTEINS IN KEY NON-BILATERIAN ANIMAL LINEAGES INCLUDING CNIDARIANS CTENOPHORES AND SPONGES. LITTLE IS KNOWN ABOUT HOW THEY FUNCTION IN THESE ORGANISMS NOR HOW THEY EVOLVED TO TAKE ON NOVEL ROLES TO ENABLE MULTICELLULAR COMPLEXITY. WHAT IS THE MINIMAL SET OF ADHESION PROTEINS NECESSARY FOR THE COORDINATION OF CELL-CELL ADHESION AND LINKAGE TO THE ACTIN CYTOSKELETON AND ARE BASIC FUNCTIONS OF THIS SET SHARED BY ALL ANIMALS? THE CCM IS A LIKELY CANDIDATE AND WE WILL TEST THIS HYPOTHESIS BY OBSERVING CCM PROTEINS IN CELLS AND TISSUES OF NON-BILATERIAN METAZOANS DURING MORPHOGENESIS BY EXAMINING PHYSICAL INTERACTIONS BETWEEN THESE PUTATIVE EPITHELIAL PROTEINS WITH COMPARATIVE BIOCHEMISTRY AND USING FUNCTIONAL GENETICS TO DELETE AND REPLACE GENES PUTATIVELY INVOLVED IN TISSUE MORPHOGENESIS AND CELL-CELL ADHESION. OTHER POTENTIAL CADHERIN-RELATED PROTEINS SIGNALING AND ACTIN-BINDING PROTEINS WILL BE IDENTIFIED USING BIOINFORMATIC DISSECTION OF GENOMES. RESULTS WILL BE INTEGRATED WITH KNOWN PROPERTIES OF THE CADHERIN-CATENIN ADHESION MODULE IN BILATERIANS. OUR EXPERIMENTAL APPROACH IS UNUSUALLY COMPREHENSIVE AND INTERDISCIPLINARY FOR BROAD COMPARATIVE STUDIES AND INVOLVES A DIVERSE TEAM TO TACKLE THIS PROBLEM THAT COMPRISES EVOLUTIONARY-DEVELOPMENTAL BIOLOGISTS (LOWE/MARTINDALE) AN EVOLUTIONARY-CELL BIOLOGIST (NICHOLS) AND A BIOCHEMIST/STRUCTURAL BIOLOGIST (WEIS). THE CAPACITY TO DEVELOP ROBUST TISSUES THAT PROVIDE A PHYSICAL AND CHEMICAL BARRIER TO THE OUTSIDE ENVIRONMENT AND FACILITATE TISSUE SPECIALIZATION IS A BASIC CHARACTERISTIC OF COMPLEX LIFE. THE WORK OUTLINED IN THIS PROPOSAL ADDRESSES FUNDAMENTAL QUESTIONS ABOUT THE ASSEMBLY OF A KEY CELLULAR INNOVATION EARLY IN ANIMAL EVOLUTION EPITHELIA ARE AT THE CORE OF HYPOTHESES OF THE EVOLUTION OF MULTICELLULARITY AND ANIMAL BODY-PLAN COMPLEXITY AND THEREFORE CENTRAL TO THE NASA EXOBIOLOGY MISSION OF UNDERSTANDING ADVANCED LIFE., ANIMALS CAN BE DIVIDED INTO TWO BROAD CLADES BASED ON THEIR BODY PLANS. OVER 99% OF EXTANT ANIMALS BELONG TO A SINGLE CLADE OF COMPLEX BILATERALLY SYMMETRICAL ANIMALS CALLED THE BILATERIA AND 4 REMAINING EARLY EMERGING CLADES ARE CALLED NON-BILATERIANS. THE EVOLUTION OF COMPLEX ANIMALS REMAINS AN ENDURING UNSOLVED QUESTION IN BIOLOGY UNLIKELY TO BE SOLVED BY THEORIES INVOKING ENVIRONMENTAL CHANGES IN EARTH'S HISTORY AND ITS RESOLUTION IS CRITICAL TO UNDERSTANDING THE EXISTENCE OF COMPLEX LIFE IN THE UNIVERSE. THE DEVELOPMENTAL ORIGINS OF BILATERALITY NOR INCREASES IN GENOMIC COMPLEXITY CANNOT BE THE DEFINITIVE EVENT THAT DROVE THE DRAMATICALLY SUCCESSFUL RADIATION OF COMPLEX ANIMALS BECAUSE THESE TRAITS PREDATED THE ORIGIN OF BILATERIA. RATHER EMBRYOLOGICAL AND MOLECULAR STUDIES IN BILATERIANS AND NON-BILATERIANS INDICATE THAT THE CRITICAL DEVELOPMENTAL CONSTRAINT TO BILATERIAN RADIATION WAS A SHIFT IN THE SITE OF GASTRULATION FROM ONE EMBRYONIC POLE IN PRE-BILATERIANS (E.G. CTENOPHORES AND CNIDARIANS) TO THE OPPOSITE POLE IN VIRTUALLY ALL OF BILATERIA. GASTRULATION WAS CRUCIAL FOR EVOLUTIONARY RADIATION OF ANIMALS BECAUSE IT IS DURING THIS PROCESS THAT EMBRYOS ACQUIRE CELLULAR AND MORPHOLOGICAL COMPLEXITY DURING ONTOGENY. GASTRULATION REQUIRES COMPLEX MOLECULAR INTERACTIONS BETWEEN CELLS FROM DIFFERENT EMBRYONIC REGIONS LEADING TO ACTIVATION OF SPATIALLY RESTRICTED GENE REGULATORY NETWORKS (GRN). THESE GRNS IN TURN INDUCE ORGANIZED TISSUES WITH DISTINCT DIFFERENTIATED CELL TYPES THAT HAVE BEEN CRUCIAL FOR THE SUCCESS OF BILATERIA. IN MOST ANIMALS THE LOCALIZED SIGNAL FOR ASYMMETRIC ACTIVATION OF GRNS THAT INDUCE GASTRULATION CAN BE TRACED BACK TO THE ANIMAL-VEGETAL (AV) AXIS A POLARITY ESTABLISHED IN THE OVUM DURING OOGENESIS. WE PROPOSE THAT A SHIFT IN THE SITE OF ACTIVATION OF A SUBSET OF MOLECULAR SIGNALING PATHWAYS FROM THE ANIMAL TO THE VEGETAL POLE TRIGGERED AN AXIAL REORGANIZATION THAT RELIEVED THE DEVELOPMENTAL CONSTRAINT OF GENERATING MULTIPLE GERM LAYER CELL TYPES FROM THE SAME SPATIAL LOCATION (ANIMAL POLE) THAT DROVE BODY PLAN EVOLUTION OF BILATERIA. OUR GOAL IS TO EXPERIMENTALLY RECONSTRUCT THE MECHANISM FOR THIS AXIS REORGANIZATION IN EMBRYOS OF THREE PHYLOGENETICALLY PIVOTAL EXPERIMENTAL SYSTEMS. OUR CENTRAL HYPOTHESIS IS THAT CRITICAL UPSTREAM REGULATORS OF CELL SIGNALING PATHWAYS FOCUSED AT THE ANIMAL POLE OF PRE-BILATERIANS LED TO GASTRULATION AT THAT POLE AND THAT A SHIFT OF A SUBSET OF THESE REGULATORS TO THE VEGETAL POLE LED TO GASTRULATION AT THAT POLE IN BILATERIA. THE CENTRAL OBJECTIVES OF THIS PROPOSAL ARE TO: 1) TO IDENTIFY AND FUNCTIONALLY CHARACTERIZE NOVEL MEDIATORS OF ANIMALVEGETAL AXIS POLARITY IN NON-BILATERIANS 2) TO IDENTIFY GENES THAT ARE DIRECTLY ACTIVATED OR REPRESSED BY BETA-CATENIN IN SEA URCHINS NEMATOSTELLA AND MNEMIOPSIS TO DETERMINE THE UNDERLYING CIS-REGULATORY MECHANISMS 3) TO EXPERIMENTALLY RE-ENGINEER THE PRIMARY EGG AXIS AND GASTRULATION SITE BY MANIPULATING THE SPATIAL ACTIVATION OF SIGNALING PATHWAYS. OUR RESEARCH WILL COMBINE EMBRYO MANIPULATION WITH MODULATION OF GENE EXPRESSION USING MRNA INJECTION MORPHOLINOS TRANSGENESIS AND CRISPR/CAS9 IN SEA URCHINS (BILATERIA) AND TWO PREBILATERIANS (CNIDARIANS AND CTENOPHORES). WE WILL ALSO USE CO- IMMUNOPRECIPITATION TO IDENTIFY UPSTREAM REGULATORS OF THESE SIGNALING PATHWAYS AND CELL SORTING TO IDENTIFY NOVEL MODIFICATIONS OF GRNS IN EMBRYOS WITH RE-ENGINEERED PRIMARY EGG AXES. WE AIM TO EXPERIMENTALLY DISSECT THE CELLULAR AND MOLECULAR CONSTRAINTS TO RAPID ANIMAL BODY PLAN DIVERSIFICATION WHICH DIRECTLY ADDRESSES THE GOALS OF SECTION 3.14.IV OF THE 2015 ASTROBIOLOGY ROADMAP ASSOCIATED WITH THE EVOLUTION OF ADVANCED LIFE THE ORIGIN AND EARLY EVOLUTION OF THOSE BIOLOGICAL FACTORS THAT ARE ESSENTIAL TO MULTICELLULAR LIFE SUCH AS DEVELOPMENTAL PROGRAMS INTERCELLULAR SIGNALING PROGRAMMED CELL DEATH THE CYTOSKELETON CELLULAR ADHESION CONTROL AND DIFFERENTIATION IN THE CONTEXT OF THE ORIGIN OF ADVANCED LIFE., A functional analysis of the evolution of metazoan cell polarity
OpenAlex ID: W4311182010