Molecular patterning during the development of Phoronopsis harmeri reveals similarities to rhynchonelliform brachiopods

Abstract Background Phoronids, rhynchonelliform and linguliform brachiopods show striking similarities in their embryonic fate maps, in particular in their axis specification and regionalization. However, although brachiopod development has been studied in detail and demonstrated embryonic patterning as a causal factor of the gastrulation mode (protostomy vs deuterostomy), molecular descriptions are still missing in phoronids. To understand whether phoronids display underlying embryonic molecular mechanisms similar to those of brachiopods, here we report the expression patterns of anterior (otx, gsc, six3/6, nk2.1), posterior (cdx, bra) and endomesodermal (foxA, gata4/5/6, twist) markers during the development of the protostomic phoronid Phoronopsis harmeri. Results The transcription factors foxA, gata4/5/6 and cdx show conserved expression in patterning the development and regionalization of the phoronid embryonic gut, with foxA expressed in the presumptive foregut, gata4/5/6 demarcating the midgut and cdx confined to the hindgut. Furthermore, six3/6, usually a well-conserved anterior marker, shows a remarkably dynamic expression, demarcating not only the apical organ and the oral ectoderm, but also clusters of cells of the developing midgut and the anterior mesoderm, similar to what has been reported for brachiopods, bryozoans and some deuterostome Bilateria. Surprisingly, brachyury, a transcription factor often associated with gastrulation movements and mouth and hindgut development, seems not to be involved with these patterning events in phoronids. Conclusions Our description and comparison of gene expression patterns with other studied Bilateria reveals that the timing of axis determination and cell fate distribution of the phoronid shows highest similarity to that of rhynchonelliform brachiopods, which is likely related to their shared protostomic mode of development. Despite these similarities, the phoronid Ph. harmeri also shows particularities in its development, which hint to divergences in the arrangement of gene regulatory networks responsible for germ layer formation and axis specification.

Download Full-text

Molecular patterning during the development of Phoronopsis harmeri reveals similarities to rhynchonelliform brachiopods

10.1101/782839 ◽

2019 ◽

Cited By ~ 1

Author(s):

Carmen Andrikou ◽

Yale J. Passamaneck ◽

Chris J. Lowe ◽

Mark Q. Martindale ◽

Andreas Hejnol

Keyword(s):

Cell Fate ◽

Regulatory Networks ◽

Expression Patterns ◽

Dynamic Expression ◽

Evolutionarily Conserved ◽

Oral Ectoderm ◽

Gene Regulatory ◽

Phoronopsis Harmeri ◽

Evolutionary Lineages ◽

Germ Layer Formation

AbstractBackgroundAnswering the question how conserved patterning systems are across evolutionary lineages requires a broad taxon sampling. Phoronid development has previously been studied using fate mapping and morphogenesis, yet molecular descriptions are missing. Here we report the expression patterns of the evolutionarily conserved anterior (otx, gsc, six3/6, nk2.1), posterior (cdx, bra) and endomesodermal (foxA, gata4/5/6, twist) markers in the phoronid Phoronopsis harmeri.ResultsThe transcription factors foxA, gata4/5/6 and cdx show conserved expression in patterning the development and regionalization of the phoronid embryonic gut, with foxA expressed in the presumptive foregut, gata4/5/6 demarcating the midgut and cdx confined to the hindgut. Surprisingly, brachyury, an evolutionary conserved transcription factor often associated with gastrulation movements and patterning of the mouth and hindgut, seems to be unrelated with gastrulation and mouth patterning in phoronids. Furthermore, six3/6, a well-conserved anterior marker, shows a remarkably dynamic expression, demarcating not only the apical organ and the oral ectoderm, but also clusters of cells of the developing midgut and the anterior mesoderm, similar to what has been reported for brachiopods, bryozoans and some deuterostome Bilateria.ConclusionsOur comparison of gene expression patterns with other studied Bilateria reveals that the timing of axis determination and cell fate distribution of the phoronid shows highest similarities to rhynchonelliform brachiopods. Despite these similarities, the phoronid P. harmeri shows also particularities in its development, which hint to divergences in the arrangement of gene regulatory networks responsible for germ layer formation and axis specification.

Download Full-text

Joint profiling of gene expression and chromatin accessibility of amphioxus development at single cell resolution

10.21203/rs.3.rs-504113/v1 ◽

2021 ◽

Author(s):

Pengcheng Ma ◽

Xingyan Liu ◽

Huimin Liu ◽

Zaoxu Xu ◽

Xiangning Ding ◽

...

Keyword(s):

Gene Expression ◽

Single Cell ◽

Cell Fate ◽

Regulatory Networks ◽

Functional Divergence ◽

Expression Patterns ◽

Genetic Regulatory Networks ◽

Public Access ◽

Origin And Evolution ◽

Key Species

Abstract Vertebrate evolution was accompanied with two rounds of whole genome duplication followed by functional divergence in terms of regulatory circuits and gene expression patterns. As a basal and slow-evolving chordate species, amphioxus is an ideal paradigm for exploring the origin and evolution of vertebrates. Single cell sequencing has been widely employed to construct the developmental cell atlas of several key species of vertebrates (human, mouse, zebrafish and frog) and tunicate (sea squirts). Here, we performed single-nucleus RNA sequencing (snRNA-seq) and single-cell assay for transposase accessible chromatin sequencing (scATAC-seq) for different stages of amphioxus (covering embryogenesis and adult tissues). With the datasets generated we constructed the developmental tree for amphioxus cell fate commitment and lineage specification, and revealed the underlying key regulators and genetic regulatory networks. The generated data were integrated into an online platform, AmphioxusAtlas, for public access at http://120.79.46.200:81/AmphioxusAtlas.

Download Full-text

Identification of the Q Gene Playing a Role in Spike Morphology Variation in Wheat Mutants and Its Regulatory Network

Frontiers in Plant Science ◽

10.3389/fpls.2021.807731 ◽

2022 ◽

Vol 12 ◽

Author(s):

Jiazi Zhang ◽

Hongchun Xiong ◽

Huijun Guo ◽

Yuting Li ◽

Xiaomei Xie ◽

...

Keyword(s):

Regulatory Network ◽

Molecular Mechanisms ◽

Target Genes ◽

Expression Patterns ◽

Spike Morphology ◽

Regulatory Pathways ◽

Dynamic Expression ◽

Spike Development ◽

Family Gene ◽

Q Gene

The wheat AP2 family gene Q controls domestication traits, including spike morphology and threshability, which are critical for the widespread cultivation and yield improvement of wheat. Although many studies have investigated the molecular mechanisms of the Q gene, its direct target genes, especially those controlling spike morphology, are not clear, and its regulatory pathways are not well established. In this study, we conducted gene mapping of a wheat speltoid spike mutant and found that a new allele of the Q gene with protein truncation played a role in spike morphology variation in the mutant. Dynamic expression levels of the Q gene throughout the spike development process suggested that the transcript abundances of the mutant were decreased at the W6 and W7 scales compared to those of the WT. We identified several mutation sites on the Q gene and showed that mutations in different domains resulted in distinct phenotypes. In addition, we found that the Q gene produced three transcripts via alternative splicing and that they exhibited differential expression patterns in nodes, internodes, flag leaves, and spikes. Finally, we identified several target genes directly downstream of Q, including TaGRF1-2D and TaMGD-6B, and proposed a possible regulatory network. This study uncovered the target genes of Q, and the results can help to clarify the mechanism of wheat spike morphology and thereby improve wheat grain yield.

Download Full-text

Transcription Profiles of Age-at-Maturity-Associated Genes Suggest Cell Fate Commitment Regulation as a Key Factor in the Atlantic Salmon Maturation Process

G3 Genes|Genome|Genetics ◽

10.1534/g3.119.400882 ◽

2019 ◽

Vol 10 (1) ◽

pp. 235-246 ◽

Cited By ~ 3

Author(s):

Johanna Kurko ◽

Paul V. Debes ◽

Andrew H. House ◽

Tutku Aykanat ◽

Jaakko Erkinaro ◽

...

Keyword(s):

Atlantic Salmon ◽

Cell Fate ◽

Molecular Mechanisms ◽

Genome Wide Association Study ◽

Expression Patterns ◽

Hippo Signaling ◽

Age At Maturity ◽

Specific Expression ◽

Hpg Axis ◽

Tissue Specific

Despite recent taxonomic diversification in studies linking genotype with phenotype, follow-up studies aimed at understanding the molecular processes of such genotype-phenotype associations remain rare. The age at which an individual reaches sexual maturity is an important fitness trait in many wild species. However, the molecular mechanisms regulating maturation timing processes remain obscure. A recent genome-wide association study in Atlantic salmon (Salmo salar) identified large-effect age-at-maturity-associated chromosomal regions including genes vgll3, akap11 and six6, which have roles in adipogenesis, spermatogenesis and the hypothalamic-pituitary-gonadal (HPG) axis, respectively. Here, we determine expression patterns of these genes during salmon development and their potential molecular partners and pathways. Using Nanostring transcription profiling technology, we show development- and tissue-specific mRNA expression patterns for vgll3, akap11 and six6. Correlated expression levels of vgll3 and akap11, which have adjacent chromosomal location, suggests they may have shared regulation. Further, vgll3 correlating with arhgap6 and yap1, and akap11 with lats1 and yap1 suggests that Vgll3 and Akap11 take part in actin cytoskeleton regulation. Tissue-specific expression results indicate that vgll3 and akap11 paralogs have sex-dependent expression patterns in gonads. Moreover, six6 correlating with slc38a6 and rtn1, and Hippo signaling genes suggests that Six6 could have a broader role in the HPG neuroendrocrine and cell fate commitment regulation, respectively. We conclude that Vgll3, Akap11 and Six6 may influence Atlantic salmon maturation timing via affecting adipogenesis and gametogenesis by regulating cell fate commitment and the HPG axis. These results may help to unravel general molecular mechanisms behind maturation.

Download Full-text

Integration of mRNA and miRNA Analysis Reveals the Molecular Mechanism Underlying Salt and Alkali Stress Tolerance in Tobacco

International Journal of Molecular Sciences ◽

10.3390/ijms20102391 ◽

2019 ◽

Vol 20 (10) ◽

pp. 2391 ◽

Cited By ~ 3

Author(s):

Jiayang Xu ◽

Qiansi Chen ◽

Pingping Liu ◽

Wei Jia ◽

Zheng Chen ◽

...

Keyword(s):

Salinity Stress ◽

Regulatory Networks ◽

Molecular Mechanisms ◽

Crop Yields ◽

Antioxidant Activities ◽

Expression Patterns ◽

Differentially Expressed ◽

Alkali Stress ◽

Rna Seq ◽

Alkali Tolerance

Salinity is one of the most severe forms of abiotic stress and affects crop yields worldwide. Plants respond to salinity stress via a sophisticated mechanism at the physiological, transcriptional and metabolic levels. However, the molecular regulatory networks involved in salt and alkali tolerance have not yet been elucidated. We developed an RNA-seq technique to perform mRNA and small RNA (sRNA) sequencing of plants under salt (NaCl) and alkali (NaHCO3) stress in tobacco. Overall, 8064 differentially expressed genes (DEGs) and 33 differentially expressed microRNAs (DE miRNAs) were identified in response to salt and alkali stress. A total of 1578 overlapping DEGs, which exhibit the same expression patterns and are involved in ion channel, aquaporin (AQP) and antioxidant activities, were identified. Furthermore, genes involved in several biological processes, such as “photosynthesis” and “starch and sucrose metabolism,” were specifically enriched under NaHCO3 treatment. We also identified 15 and 22 miRNAs that were differentially expressed in response to NaCl and NaHCO3, respectively. Analysis of inverse correlations between miRNAs and target mRNAs revealed 26 mRNA-miRNA interactions under NaCl treatment and 139 mRNA-miRNA interactions under NaHCO3 treatment. This study provides new insights into the molecular mechanisms underlying the response of tobacco to salinity stress.

Download Full-text

Unique expression patterns of multiple key genes associated with the evolution of mammalian flight

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2013.3133 ◽

2014 ◽

Vol 281 (1783) ◽

pp. 20133133 ◽

Cited By ~ 20

Author(s):

Zhe Wang ◽

Mengyao Dai ◽

Yao Wang ◽

Kimberly L. Cooper ◽

Tengteng Zhu ◽

...

Keyword(s):

Regulatory Networks ◽

Molecular Mechanisms ◽

Expression Patterns ◽

Genetic Changes ◽

Multiple Gene ◽

Membrane Growth ◽

Complex Integration ◽

Key Genes ◽

Bat Wing

Bats are the only mammals capable of true flight. Critical adaptations for flight include a pair of dramatically elongated hands with broad wing membranes. To study the molecular mechanisms of bat wing evolution, we perform genomewide mRNA sequencing and in situ hybridization for embryonic bat limbs. We identify seven key genes that display unique expression patterns in embryonic bat wings and feet, compared with mouse fore- and hindlimbs. The expression of all 5′HoxD genes ( Hoxd9–13 ) and Tbx3 , six known crucial transcription factors for limb and digit development, is extremely high and prolonged in the elongating wing area. The expression of Fam5c , a tumour suppressor, in bat limbs is bat-specific and significantly high in all short digit regions (the thumb and foot digits). These results suggest multiple genetic changes occurred independently during the evolution of bat wings to elongate the hand digits, promote membrane growth and keep other digits short. Our findings also indicate that the evolution of limb morphology depends on the complex integration of multiple gene regulatory networks and biological processes that control digit formation and identity, chondrogenesis, and interdigital regression or retention.

Download Full-text

MON-719 The Cellular and Molecular Landscape of Hypothalamic Patterning and Differentiation

Journal of the Endocrine Society ◽

10.1210/jendso/bvaa046.1237 ◽

2020 ◽

Vol 4 (Supplement_1) ◽

Author(s):

Thomas Kim

Keyword(s):

Cell Fate ◽

Regulatory Networks ◽

Large Scale ◽

Molecular Mechanisms ◽

Brain Atlas ◽

Specific Gene ◽

Cell Fate Specification ◽

Human Hypothalamus ◽

Fate Specification ◽

Time Points

Abstract The hypothalamus is a central regulator of physiological homeostasis. During development, multiple transcription factors coordinate the patterning and specification of hypothalamic nuclei. However, the molecular mechanisms controlling hypothalamic patterning and cell fate specification are poorly understood. To identify genes that control these processes, we have used single-cell RNA sequencing (scRNA-Seq) to profile mouse hypothalamic gene expression across multiple developmental time points. We have further utilised scRNA-Seq to phenotype mutations in genes that play major roles in early hypothalamic patterning. To first understand hypothalamic development, hypothalami were collected at both embryonic (E10-E16, E18) and postnatal (PN4, PN8, PN14, PN45) time points. At early stages, when the bulk of hypothalamic patterning occurs (E11-E13), we observe a clear separation between mitotic progenitors and postmitotic neural precursor cells. We likewise observed clean segregation among cells expressing regional hypothalamic markers identified in previous large-scale analysis of hypothalamic development. This analysis reveals new region-specific markers and identifies candidate genes for selectively regulating patterning and cell fate specification in individual hypothalamic regions. With our rich dataset of developing mouse hypothalamus, we integrated our dataset with the Allen Brain Atlas in situ data, publicly available adult hypothalamic scRNA-Seq dataset to understand hierarchy of hypothalamic cell differentiation, as well as re-defining cell types of the hypothalamus. We next used scRNA-Seq to phenotype multiple mutant lines, including a line that has been extensively characterised as a proof of concept (Ctnnb1 overexpression), and lines that have not been characterised (Nkx2.1, Nkx2.2, Dlx1/2 deletion). We show that this approach can rapidly and comprehensively characterize mutants that have altered hypothalamic patterning, and in doing so, have identified multiple genes that simultaneously repress posterior hypothalamic identity while promoting prethalamic identity. This result supports a modified columnar model of organization for the diencephalon, where prethalamus and hypothalamus are situated in adjacent dorsal and ventral domains of the anterior diencephalon. These data serve as a resource for further studies of hypothalamic development and dysfunction, and able to delineate transcriptional regulatory networks of hypothalamic formation. Lastly, using our mouse hypothalamus as a guideline, we are comparing dataset of developing chicken, zebrafish and human hypothalamus, to identify evolutionarily conserved and divergent region-specific gene regulatory networks. We aim to use this knowledge and information of key molecular pathways of human hypothalamic development and produce human hypothalamus organoids.

Download Full-text

Molecular Logic of Hypothalamus Development

Journal of the Endocrine Society ◽

10.1210/jendso/bvab048.1037 ◽

2021 ◽

Vol 5 (Supplement_1) ◽

pp. A507-A507

Author(s):

Thomas Kim

Keyword(s):

Transcription Factors ◽

Cell Fate ◽

Regulatory Networks ◽

Molecular Mechanisms ◽

Developmental Time ◽

Specific Gene ◽

Molecular Logic ◽

Hypothalamic Nuclei ◽

Physiological Homeostasis ◽

Mutant Lines

Download Full-text

The seasonal development dynamics of the yak hair cycle transcriptome

10.21203/rs.2.10952/v1 ◽

2019 ◽

Author(s):

Pengjia Bao ◽

Jiayu Luo ◽

Yanbin Liu ◽

Min Chu ◽

Qingmiao Ren ◽

...

Keyword(s):

Hormonal Regulation ◽

Regulatory Networks ◽

Molecular Mechanisms ◽

Time Series Data ◽

Expression Profiles ◽

Expression Patterns ◽

Seasonal Development ◽

Series Data ◽

Hair Cycle ◽

Adaptation Mechanism

Abstract Background: Mammalian hair play an important role in mammals' ability to adapt to changing climatic environments. The seasonal circulation of yak hair helps them adapt to high altitude but the regulation mechanisms of the proliferation and differentiation of hair follicle (HF) cells during development are still unknown. Here, using time series data for whole genome expression profiles and hormone contents, we systematically analyzed the mechanism regulating the periodic expression of hair development in the yak and reviewed how different combinations of genetic pathways regulate HF development and cycling. Results: This study used high-throughput RNA sequencing to provide a detailed description of global gene expression in 15 samples from five developmental time points during the yak hair cycle. A total of 11,666 genes were found to be involved in the hair cycle. According to clustering analysis and the morphological features we observed, we found that these 15 samples could be significantly grouped into three phases, which represent different developmental periods in the hair cycle. A total of 2,316 genes were identified in these three consecutive developmental periods and their expression patterns could be divided into 9 clusters; GO annotation and KEGG pathway enrichment were performed on these differentially expressed genes (DEGs), showing that the three periods have distinctive functions in the seasonal hair cycle. The regulatory network of related signaling factors highlighted the interaction and dynamic expression of key DEGs during the seasonal hair cycle. Through co-expression analysis, we revealed a number of modular hub genes highly associated with hormones that may play unique roles in hormonal regulation of events associated with the hair cycle. Conclusions: Our results revealed the molecular mechanisms and developmental regulatory networks of the seasonal hair cycle in the yak and filled a gap in the current research field. The findings will be valuable in further understanding the alpine adaptation mechanism in the yak, which is important in order to make full use of yak hair resources and promote the economic development of pastoral plateau areas. Keywords: Hair cycle, Seasonal development, Transcriptome, Yak

Download Full-text

Comparative analyses of saprotrophy in Salisapilia sapeloensis and diverse plant pathogenic oomycetes reveal lifestyle-specific gene expression

FEMS Microbiology Ecology ◽

10.1093/femsec/fiaa184 ◽

2020 ◽

Vol 96 (11) ◽

Author(s):

Sophie de Vries ◽

Jan de Vries ◽

John M Archibald ◽

Claudio H Slamovits

Keyword(s):

Gene Expression ◽

Regulatory Networks ◽

Plant Pathogens ◽

Molecular Mechanisms ◽

Expression Patterns ◽

Reference Points ◽

Global Perspective ◽

Specific Gene ◽

Gene Regulatory ◽

Specific Array

ABSTRACT Oomycetes include many devastating plant pathogens. Across oomycete diversity, plant-infecting lineages are interspersed by non-pathogenic ones. Unfortunately, our understanding of the evolution of lifestyle switches is hampered by a scarcity of data on the molecular biology of saprotrophic oomycetes, ecologically important primary colonizers of dead tissue that can serve as informative reference points for understanding the evolution of pathogens. Here, we established Salisapilia sapeloensis as a tractable system for the study of saprotrophic oomycetes. We generated multiple transcriptomes from S. sapeloensis and compared them with (i) 22 oomycete genomes and (ii) the transcriptomes of eight pathogenic oomycetes grown under 13 conditions. We obtained a global perspective on gene expression signatures of oomycete lifestyles. Our data reveal that oomycete saprotrophs and pathogens use similar molecular mechanisms for colonization but exhibit distinct expression patterns. We identify a S. sapeloensis-specific array and expression of carbohydrate-active enzymes and putative regulatory differences, highlighted by distinct expression levels of transcription factors. Salisapilia sapeloensis expresses only a small repertoire of candidates for virulence-associated genes. Our analyses suggest lifestyle-specific gene regulatory signatures and that, in addition to variation in gene content, shifts in gene regulatory networks underpin the evolution of oomycete lifestyles.

Download Full-text