Mapping the landscape of transcription factor promoter activity during vegetative development in Marchantia

Transcription factors (TFs) are essential for the regulation of gene expression and cell fate determination. Characterising the transcriptional activity of TF genes in space and time is a critical step towards understanding complex biological systems. The vegetative gametophyte meristems of bryophytes share some characteristics with the shoot-apical meristems of flowering plants. However, the identity and expression profiles of TFs associated with gametophyte organization are largely unknown. With only ∼450 TF genes, Marchantia polymorpha is an outstanding model system for plant systems biology. We have generated a near-complete collection of promoter elements derived from Marchantia TF genes. We experimentally tested in planta reporter fusions for all the TF promoters in the collection and systematically analysed expression patterns in Marchantia gemmae. This allowed us to build a map of precise expression domains and identify a unique set of TFs expressed in the stem-cell zone, providing new insight into the dynamic regulation of the gametophytic meristem and its evolution. In addition, we provide an online database of expression patterns for all promoters in the collection. We expect that the promoter elements characterised here will be useful for cell-type specific expression, synthetic biology applications, and functional genomics.

[1]  Jia-Wei Wang,et al.  The maturation and aging trajectory of Marchantia polymorpha at single-cell resolution. , 2023, Developmental cell.

[2]  P. Benfey,et al.  GRAS transcription factors regulate cell division planes in moss overriding the default rule , 2023, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Ying Wang,et al.  A conserved module in the formation of moss midribs and seed plant axillary meristems , 2022, Science advances.

[4]  K. Yamato,et al.  The renaissance and enlightenment of Marchantia as a model system , 2022, The Plant cell.

[5]  Hongkui Zeng.  What is a cell type and how to define it? , 2022, Cell.

[6]  Y. Hirakawa,et al.  Evolution of meristem zonation by CLE gene duplication in land plants , 2022, Nature Plants.

[7]  C. J. Harrison,et al.  How was apical growth regulated in the ancestral land plant? Insights from the development of non-seed plants , 2022, Plant physiology.

[8]  K. Yamato,et al.  MarpolBase Expression: A Web-Based, Comprehensive Platform for Visualization and Analysis of Transcriptomes in the Liverwort Marchantia polymorpha , 2022, bioRxiv.

[9]  J. E. Moreno,et al.  Liverwort oil bodies: diversity, biochemistry, and molecular cell biology of the earliest secretory structure of land plants. , 2022, Journal of experimental botany.

[10]  T. Kohchi,et al.  Diminished Auxin Signaling Triggers Cellular Reprogramming by Inducing a Regeneration Factor in the Liverwort Marchantia polymorpha. , 2022, Plant & cell physiology.

[11]  J. Bowman,et al.  Gamete expression of TALE class HD genes activates the diploid sporophyte program in Marchantia polymorpha , 2021, eLife.

[12]  T. Kohchi,et al.  Major components of the KARRIKIN INSENSITIVE2-dependent signaling pathway are conserved in the liverwort Marchantia polymorpha. , 2021, The Plant cell.

[13]  S. Giacomello,et al.  A new era for plant science: spatial single-cell transcriptomics. , 2021, Current opinion in plant biology.

[14]  Y. Saeys,et al.  Advances and Opportunities of Single-Cell Transcriptomics for Plant Research. , 2021, Annual review of plant biology.

[15]  K. Yamato,et al.  Development and Molecular Genetics of Marchantia polymorpha. , 2021, Annual review of plant biology.

[16]  J. Kyozuka,et al.  Fundamental mechanisms of the stem cell regulation in land plants: lesson from shoot apical cells in bryophytes , 2021, Plant Molecular Biology.

[17]  M. Arif,et al.  PpGRAS12 acts as a positive regulator of meristem formation in Physcomitrium patens , 2021, Plant Molecular Biology.

[18]  J. Bowman,et al.  On the Evolutionary Origins of Land Plant Auxin Biology. , 2021, Cold Spring Harbor perspectives in biology.

[19]  K. Yamato,et al.  Fungal-Type Terpene Synthases In Marchantia Polymorpha Are Involved In Sesquiterpene Biosynthesis In Oil Body Cells. , 2021, Plant & cell physiology.

[20]  J. E. Moreno,et al.  Molecular mechanisms involved in functional macroevolution of plant transcription factors. , 2020, The New phytologist.

[21]  Masaki Shimamura,et al.  Morphology of gemmae, an overlooked taxonomic trait in the genus Marchantia L. (Marchantiaceae) , 2020, The Bryologist.

[22]  T. Kohchi,et al.  The liverwort oil body is formed by redirection of the secretory pathway , 2020, Nature Communications.

[23]  Evolutionary Origins , 2020, The Anatomy of Grief.

[24]  T. Kohchi,et al.  Induction of Multichotomous Branching by CLAVATA Peptide in Marchantia polymorpha , 2020, Current Biology.

[25]  K. Ishizaki,et al.  Gemma cup and gemma development in Marchantia polymorpha. , 2020, The New phytologist.

[26]  T. Kohchi,et al.  Design principles of a minimal auxin response system , 2020, Nature Plants.

[27]  T. Kohchi,et al.  Deep evolutionary origin of gamete-directed zygote activation by KNOX/BELL transcription factors in green plants , 2020, bioRxiv.

[28]  T. Kohchi,et al.  Positional cues regulate dorsal organ formation in the liverwort Marchantia polymorpha , 2020, Journal of Plant Research.

[29]  N. Patron,et al.  Systematic tools for reprogramming plant gene expression in a simple model, Marchantia polymorpha. , 2020, ACS synthetic biology.

[30]  J. Bowman,et al.  Oil Body Formation in Marchantia polymorpha Is Controlled by MpC1HDZ and Serves as a Defense against Arthropod Herbivores , 2020, Current Biology.

[31]  C. Delwiche,et al.  Reconstructing trait evolution in plant evo–devo studies , 2019, Current Biology.

[32]  K. Yamato,et al.  Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin , 2019, Current Biology.

[33]  J. Franco-Zorrilla,et al.  Jasmonate-Related MYC Transcription Factors Are Functionally Conserved in Marchantia polymorpha , 2019, Plant Cell.

[34]  T. Kohchi,et al.  Cytokinin Signaling is Essential for Organ Formation in Marchantia polymorpha. , 2019, Plant & cell physiology.

[35]  T. Kohchi,et al.  Control of proliferation in the haploid meristem by CLE peptide signaling in Marchantia polymorpha , 2019, PLoS genetics.

[36]  K. Yamato,et al.  A cis‐acting bidirectional transcription switch controls sexual dimorphism in the liverwort , 2019, The EMBO journal.

[37]  K. Torii,et al.  Stem cells within the shoot apical meristem: identity, arrangement and communication , 2018, Cellular and Molecular Life Sciences.

[38]  K. Torii,et al.  Stem cells within the shoot apical meristem: identity, arrangement and communication , 2018, Cellular and Molecular Life Sciences.

[39]  J. Bowman,et al.  UVR8-mediated induction of flavonoid biosynthesis for UVB tolerance is conserved between the liverwort Marchantia polymorpha and flowering plants. , 2018, The Plant journal : for cell and molecular biology.

[40]  L. Dolan,et al.  Negative regulation of conserved RSL class I bHLH 1 transcription factors evolved independently among land 2 plants , 2022 .

[41]  M. Scanlon,et al.  CLAVATA Was a Genetic Novelty for the Morphological Innovation of 3D Growth in Land Plants , 2018, Current Biology.

[42]  Anthony West,et al.  Loop Assembly: a simple and open system for recursive fabrication of DNA circuits , 2018, bioRxiv.

[43]  Jill E. M. Harrison,et al.  The origin and early evolution of vascular plant shoots and leaves , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  M. Elowitz,et al.  Challenges and emerging directions in single-cell analysis , 2017, Genome Biology.

[45]  N. Cunniffe,et al.  Regional Growth Rate Differences Specified by Apical Notch Activities Regulate Liverwort Thallus Shape , 2017, Current Biology.

[46]  J. Haseloff,et al.  MarpoDB: An Open Registry for Marchantia Polymorpha Genetic Parts , 2017, Plant & cell physiology.

[47]  J. Bowman,et al.  Class III HD-Zip activity coordinates leaf development in Physcomitrella patens. , 2016, Developmental biology.

[48]  Roland Eils,et al.  Complex heatmaps reveal patterns and correlations in multidimensional genomic data , 2016, Bioinform..

[49]  Shin-Han Shiu,et al.  Evolution of Gene Duplication in Plants1[OPEN] , 2016, Plant Physiology.

[50]  J. Bowman.  A Brief History of Marchantia from Greece to Genomics. , 2016, Plant & cell physiology.

[51]  Masaki Shimamura.  Marchantia polymorpha: Taxonomy, Phylogeny and Morphology of a Model System. , 2016, Plant & cell physiology.

[52]  K. Yamato,et al.  Molecular Genetic Tools and Techniques for Marchantia polymorpha Research. , 2016, Plant & cell physiology.

[53]  T. Kohchi,et al.  RSL Class I Genes Controlled the Development of Epidermal Structures in the Common Ancestor of Land Plants , 2016, Current Biology.

[54]  Joachim Wittbrodt,et al.  MEPD: medaka expression pattern database, genes and more , 2015, Nucleic Acids Res..

[55]  Christian Rogers,et al.  Standards for plant synthetic biology: a common syntax for exchange of DNA parts. , 2015, The New phytologist.

[56]  T. Kohchi,et al.  Comparison of the MpEF1α and CaMV35 promoters for application in Marchantia polymorpha overexpression studies , 2014, Transgenic Research.

[57]  J. Gómez-Skarmeta,et al.  A mobile insulator system to detect and disrupt cis-regulatory landscapes in vertebrates , 2014, Genome research.

[58]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[59]  Jim Haseloff,et al.  Integrated genetic and computation methods for in planta cytometry , 2012, Nature Methods.

[60]  Steven M. Gallo,et al.  REDfly v3.0: toward a comprehensive database of transcriptional regulatory elements in Drosophila , 2010, Nucleic Acids Res..

[61]  T. Nishiyama,et al.  Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development , 2008, Evolution & development.

[62]  L. Dolan,et al.  Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomitrella patens. , 2007, Journal of experimental botany.

[63]  J. Glazebrook,et al.  Transformation of agrobacterium using the freeze-thaw method. , 2006, CSH protocols.

[64]  Inna Dubchak,et al.  VISTA Enhancer Browser—a database of tissue-specific human enhancers , 2006, Nucleic Acids Res..

[65]  K. Sakakibara,et al.  KNOX homeobox genes potentially have similar function in both diploid unicellular and multicellular meristems, but not in haploid meristems , 2005, Evolution & development.

[66]  Eve Chiapello.  Evolution and co‐optation , 2004 .

[67]  R. Simon,et al.  The DORNROSCHEN/ENHANCER OF SHOOT REGENERATION1 gene of Arabidopsis acts in the control of meristem ccll fate and lateral organ development. , 2003, The Plant cell.

[68]  Andreas Wagner,et al.  Genetic redundancy caused by gene duplications and its evolution in networks of transcriptional regulators , 1996, Biological Cybernetics.

[69]  B. Galatis,et al.  On the fine structure of differentiating mucilage papillae of Marchantia , 1977 .

[70]  Morton W. Miller,et al.  Relation between Extrapolation Number and Apical Cell Number in Gemmae of Marchantia polymorpha L. , 1966, Nature.

[71]  U. Grenander.  Some Direct Estimates of the Mode , 1965 .

[72]  Morton W. Miller,et al.  A Relationship between Extrapolation Number and Cellular Kinetics in Apical Cells of Gemmae of Marchantia polymorpha L. , 1965 .

[73]  F. Bower.  The origin of a Land Flora , 1908, Zeitschrift für induktive Abstammungs- und Vererbungslehre.

[74]  J. Bowman.  The liverwort Marchantia polymorpha, a model for all ages. , 2022, Current topics in developmental biology.

[75]  Nicola J Patron,et al.  Phytobricks: Manual and Automated Assembly of Constructs for Engineering Plants. , 2020, Methods in molecular biology.

[76]  J. Bowman,et al.  Evolution and co-option of developmental regulatory networks in early land plants. , 2019, Current topics in developmental biology.

[77]  S. Henikoff,et al.  The INTACT method for cell type–specific gene expression and chromatin profiling in Arabidopsis thaliana , 2011, Nature Protocols.

[78]  M. Timmermans,et al.  Genetic and epigenetic regulation of stem cell homeostasis in plants. , 2008, Cold Spring Harbor symposia on quantitative biology.

[79]  J. Rousseau.  Action des hétéro-auxines sur les chapeaux du Marchantia potimorpha L. , 1953 .