Gamete expression of TALE class HD genes activates the diploid sporophyte program in Marchantia polymorpha

Dierschke, Tom; Flores-Sandoval, Eduardo; Rast-Somssich, Madlen I.; Althoff, Felix; Zachgo, Sabine; Bowman, John L.

doi:10.7554/elife.57088

Title: Gamete expression of TALE class HD genes activates the diploid sporophyte program in Marchantia polymorpha

Journal Article · 17 September 2021 · eLife

DOI: https://doi.org/10.7554/elife.57088 · OSTI ID:1904155

^[1]; Flores-Sandoval, Eduardo ^[2]; Rast-Somssich, Madlen I. ^[2]; Althoff, Felix ^[3]; Zachgo, Sabine ^[3];

^[2]

Monash University, Melbourne, VIC (Australia); University of Osnabruck (Germany); OSTI
Monash University, Melbourne, VIC (Australia)
University of Osnabruck (Germany)

Eukaryotic life cycles alternate between haploid and diploid phases and in phylogenetically diverse unicellular eukaryotes, expression of paralogous homeodomain genes in gametes primes the haploid-to-diploid transition. In the unicellular chlorophyte alga Chlamydomonas, KNOX and BELL TALE-homeodomain genes mediate this transition. We demonstrate that in the liverwort Marchantia polymorpha, paternal (sperm) expression of three of five phylogenetically diverse BELL genes, MpBELL234, and maternal (egg) expression of both MpKNOX1 and MpBELL34 mediate the haploid-to-diploid transition. Loss-of-function alleles of MpKNOX1 result in zygotic arrest, whereas a loss of either maternal or paternal MpBELL234 results in variable zygotic and early embryonic arrest. Expression of MpKNOX1 and MpBELL34 during diploid sporophyte development is consistent with a later role for these genes in patterning the sporophyte. These results indicate that the ancestral mechanism to activate diploid gene expression was retained in early diverging land plants and subsequently co-opted during evolution of the diploid sporophyte body.

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Research Organization:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Monash University, Melbourne, VIC (Australia)

Sponsoring Organization:: USDOE Office of Science (SC); Australian Research Council; German Research Foundation (DFG)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1904155

Journal Information:: eLife, Journal Name: eLife Vol. 10; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

References (85)

Green algal transcriptomes for phylogenetics and comparative genomics Cooper, Endymion; Delwiche, Charles figshare https://doi.org/10.6084/m9.figshare.1604778	dataset	January 2016
Weitere Beobachtungen über die Eigenschaften der X-Strahlen Röntgen, W. C. Annalen der Physik, Vol. 300, Issue 1 https://doi.org/10.1002/andp.18983000104	journal	January 1898
Molecular genetics of sexual development in the mushroomCoprinus cinereus Kamada, Takashi BioEssays, Vol. 24, Issue 5 https://doi.org/10.1002/bies.10083	journal	April 2002
Untersuchungen �ber die mutagene Wirkung von Maleins�urehydrazid an Sphaerocarpus donnellii Abel, W. O. Chromosoma, Vol. 11, Issue 1 https://doi.org/10.1007/BF00328659	journal	January 1960
Die Umwandlung eines haploiden, genotypisch weiblichen Gametophyten von Sphaerocarpus Donnellii in einen männlichen mit Hilfe von Röntgenstrahlen Lorbeer, Gerhard Planta, Vol. 25, Issue 1 https://doi.org/10.1007/BF01909306	journal	April 1936
The origin of a Land Flora Bower, F. O. Zeitschrift für Induktive Abstammungs- und Vererbungslehre, Vol. 1, Issue 1 https://doi.org/10.1007/BF01990593	journal	December 1908
Identification of the pheromone response element inUstilago maydis Urban, M.; Kahmann, R.; Bölker, M. Molecular and General Genetics MGG, Vol. 251, Issue 1 https://doi.org/10.1007/BF02174341	journal	April 1996
Revelation of ancestral roles of KNOX genes by a functional analysis of Physcomitrella homologues Singer, S. D.; Ashton, N. W. Plant Cell Reports, Vol. 26, Issue 12 https://doi.org/10.1007/s00299-007-0409-5	journal	August 2007
Haploid embryo production in rice and maize induced by PsASGR-BBML transgenes Conner, Joann A.; Podio, Maricel; Ozias-Akins, Peggy Plant Reproduction, Vol. 30, Issue 1 https://doi.org/10.1007/s00497-017-0298-x	journal	February 2017
Comparison of the MpEF1α and CaMV35 promoters for application in Marchantia polymorpha overexpression studies Althoff, Felix; Kopischke, Sarah; Zobell, Oliver Transgenic Research, Vol. 23, Issue 2 https://doi.org/10.1007/s11248-013-9746-z	journal	September 2013
a1 Protein alters the dna binding specificity of α2 repressor Goutte, Caroline; Johnson, Alexander D. Cell, Vol. 52, Issue 6 https://doi.org/10.1016/0092-8674(88)90429-1	journal	March 1988
A two-component regulatory system for self/non-self recognition in Ustilago maydis Gillissen, Bernd; Bergemann, Jörg; Sandmann, Claus Cell, Vol. 68, Issue 4 https://doi.org/10.1016/0092-8674(92)90141-x	journal	February 1992
Early Sexual Origins of Homeoprotein Heterodimerization and Evolution of the Plant KNOX/BELL Family Lee, Jae-Hyeok; Lin, Huawen; Joo, Sunjoo Cell, Vol. 133, Issue 5 https://doi.org/10.1016/j.cell.2008.04.028	journal	May 2008
Analysis of Homeodomain Specificities Allows the Family-wide Prediction of Preferred Recognition Sites Noyes, Marcus B.; Christensen, Ryan G.; Wakabayashi, Atsuya Cell, Vol. 133, Issue 7 https://doi.org/10.1016/j.cell.2008.05.023	journal	June 2008
Variation in Homeodomain DNA Binding Revealed by High-Resolution Analysis of Sequence Preferences Berger, Michael F.; Badis, Gwenael; Gehrke, Andrew R. Cell, Vol. 133, Issue 7 https://doi.org/10.1016/j.cell.2008.05.024	journal	June 2008
Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome Bowman, John L.; Kohchi, Takayuki; Yamato, Katsuyuki T. Cell, Vol. 171, Issue 2 https://doi.org/10.1016/j.cell.2017.09.030	journal	October 2017
Natural Variation in Leaf Morphology Results from Mutation of a Novel KNOX Gene Kimura, Seisuke; Koenig, Daniel; Kang, Julie Current Biology, Vol. 18, Issue 9 https://doi.org/10.1016/j.cub.2008.04.008	journal	May 2008
Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin Montgomery, Sean A.; Tanizawa, Yasuhiro; Galik, Bence Current Biology, Vol. 30, Issue 4 https://doi.org/10.1016/j.cub.2019.12.015	journal	February 2020
To Be Specific or Not: The Critical Relationship Between Hox And TALE Proteins Merabet, Samir; Mann, Richard S. Trends in Genetics, Vol. 32, Issue 6 https://doi.org/10.1016/j.tig.2016.03.004	journal	June 2016
pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation Hellens, Roger P.; Edwards, E. Anne; Leyland, Nicola R. Plant Molecular Biology, Vol. 42, Issue 6, p. 819-832 https://doi.org/10.1023/a:1006496308160	journal	January 2000
A gene complex controlling segmentation in Drosophila Lewis, E. B. Nature, Vol. 276, Issue 5688 https://doi.org/10.1038/276565a0	journal	December 1978
A regulatory hierarchy for cell specialization in yeast Herskowitz, Ira Nature, Vol. 342, Issue 6251 https://doi.org/10.1038/342749a0	journal	December 1989
GLUTAMATE RECEPTOR-LIKE channels are essential for chemotaxis and reproduction in mosses Ortiz-Ramírez, Carlos; Michard, Erwan; Simon, Alexander A. Nature, Vol. 549, Issue 7670 https://doi.org/10.1038/nature23478	journal	July 2017
Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation Hori, Koichi; Maruyama, Fumito; Fujisawa, Takatomo Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4978	journal	May 2014
Conservation of ethylene as a plant hormone over 450 million years of evolution Ju, Chuanli; Van de Poel, Bram; Cooper, Endymion D. Nature Plants, Vol. 1, Issue 1 https://doi.org/10.1038/nplants.2014.4	journal	January 2015
A single homeobox gene triggers phase transition, embryogenesis and asexual reproduction Horst, Nelly A.; Katz, Aviva; Pereman, Idan Nature Plants, Vol. 2, Issue 2 https://doi.org/10.1038/nplants.2015.209	journal	January 2016
Modulating Hox gene functions during animal body patterning Pearson, Joseph C.; Lemons, Derek; McGinnis, William Nature Reviews Genetics, Vol. 6, Issue 12 https://doi.org/10.1038/nrg1726	journal	November 2005
The rapid evolution of reproductive proteins Swanson, Willie J.; Vacquier, Victor D. Nature Reviews Genetics, Vol. 3, Issue 2 https://doi.org/10.1038/nrg733	journal	February 2002
An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages Radhakrishnan, Guru V.; Keller, Jean; Rich, Melanie K. Nature Plants, Vol. 6, Issue 3 https://doi.org/10.1038/s41477-020-0613-7	journal	March 2020
Mechanisms regulating zygotic genome activation Schulz, Katharine N.; Harrison, Melissa M. Nature Reviews Genetics, Vol. 20, Issue 4 https://doi.org/10.1038/s41576-018-0087-x	journal	December 2018
A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds Khanday, Imtiyaz; Skinner, Debra; Yang, Bing Nature, Vol. 565, Issue 7737 https://doi.org/10.1038/s41586-018-0785-8	journal	December 2018
A unique life cycle transition in the red seaweed Pyropia yezoensis depends on apospory Mikami, Koji; Li, Chengze; Irie, Ryunosuke Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0549-5	journal	August 2019
A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins Hackbusch, J.; Richter, K.; Muller, J. Proceedings of the National Academy of Sciences, Vol. 102, Issue 13 https://doi.org/10.1073/pnas.0501181102	journal	March 2005
Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity Smith, Harley M. S.; Boschke, Ilja; Hake, Sarah Proceedings of the National Academy of Sciences, Vol. 99, Issue 14 https://doi.org/10.1073/pnas.092271599	journal	July 2002
Phylotranscriptomic analysis of the origin and early diversification of land plants Wickett, Norman J.; Mirarab, Siavash; Nguyen, Nam Proceedings of the National Academy of Sciences, Vol. 111, Issue 45 https://doi.org/10.1073/pnas.1323926111	journal	October 2014
A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant Conner, Joann A.; Mookkan, Muruganantham; Huo, Heqiang Proceedings of the National Academy of Sciences, Vol. 112, Issue 36 https://doi.org/10.1073/pnas.1505856112	journal	August 2015
Did homeodomain proteins duplicate before the origin of angiosperms, fungi, and metazoa? Bharathan, Geeta; Janssen, Bart-Jan; Kellogg, Elizabeth A. Proceedings of the National Academy of Sciences, Vol. 94, Issue 25 https://doi.org/10.1073/pnas.94.25.13749	journal	December 1997
A role for heterodimerization in nuclear localization of a homeodomain protein Spit, Anthony; Hyland, Robert H.; Mellor, E. Jane C. Proceedings of the National Academy of Sciences, Vol. 95, Issue 11 https://doi.org/10.1073/pnas.95.11.6228	journal	May 1998
MRBAYES: Bayesian inference of phylogenetic trees Huelsenbeck, J. P.; Ronquist, F. Bioinformatics, Vol. 17, Issue 8 https://doi.org/10.1093/bioinformatics/17.8.754	journal	August 2001
A siphonous macroalgal genome suggests convergent functions of homeobox genes in algae and land plants Arimoto, Asuka; Nishitsuji, Koki; Higa, Yoshimi DNA Research, Vol. 26, Issue 2 https://doi.org/10.1093/dnares/dsz002	journal	March 2019
The Amount of RNA Editing Sites in Liverwort Organellar Genes Is Correlated with GC Content and Nuclear PPR Protein Diversity Dong, Shanshan; Zhao, Chaoxian; Zhang, Shouzhou Genome Biology and Evolution, Vol. 11, Issue 11 https://doi.org/10.1093/gbe/evz232	journal	October 2019
A simple and rapid method for the preparation of plant genomic DNA for PCR analysis Edwards, K.; Johnstone, C.; Thompson, C. Nucleic Acids Research, Vol. 19, Issue 6 https://doi.org/10.1093/nar/19.6.1349	journal	January 1991
Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals Burglin, T. R. Nucleic Acids Research, Vol. 25, Issue 21 https://doi.org/10.1093/nar/25.21.4173	journal	November 1997
Agrobacterium-Mediated Transformation of the Haploid Liverwort Marchantia polymorpha L., an Emerging Model for Plant Biology Ishizaki, Kimitsune; Chiyoda, Shota; Yamato, Katsuyuki T. Plant and Cell Physiology, Vol. 49, Issue 7 https://doi.org/10.1093/pcp/pcn085	journal	June 2008
CRISPR/Cas9-Mediated Targeted Mutagenesis in the Liverwort Marchantia polymorpha L. Sugano, Shigeo S.; Shirakawa, Makoto; Takagi, Junpei Plant and Cell Physiology, Vol. 55, Issue 3 https://doi.org/10.1093/pcp/pcu014	journal	February 2014
A Brief History of Marchantia from Greece to Genomics Bowman, John L. Plant and Cell Physiology, Vol. 57, Issue 2 https://doi.org/10.1093/pcp/pcv044	journal	March 2015
Efficient and Inducible Use of Artificial MicroRNAs in Marchantia polymorpha Flores-Sandoval, Eduardo; Dierschke, Tom; Fisher, Tom J. Plant and Cell Physiology, Vol. 57, Issue 2 https://doi.org/10.1093/pcp/pcv068	journal	May 2015
The Naming of Names: Guidelines for Gene Nomenclature in Marchantia Bowman, John L.; Araki, Takashi; Arteaga-Vazquez, Mario A. Plant and Cell Physiology, Vol. 57, Issue 2 https://doi.org/10.1093/pcp/pcv193	journal	December 2015
Transcriptional Framework of Male Gametogenesis in the Liverwort Marchantia polymorpha L. Higo, Asuka; Niwa, Masaki; Yamato, Katsuyuki T. Plant and Cell Physiology, Vol. 57, Issue 2 https://doi.org/10.1093/pcp/pcw005	journal	February 2016
Reproductive Induction is a Far-Red High Irradiance Response that is Mediated by Phytochrome and PHYTOCHROME INTERACTING FACTOR in Marchantia polymorpha Inoue, Keisuke; Nishihama, Ryuichi; Araki, Takashi Plant and Cell Physiology, Vol. 60, Issue 5 https://doi.org/10.1093/pcp/pcz029	journal	February 2019
The combination of dissimilar alleles of the A alpha and A beta gene complexes, whose proteins contain homeo domain motifs, determines sexual development in the mushroom Coprinus cinereus. Kües, U.; Richardson, W. V.; Tymon, A. M. Genes & Development, Vol. 6, Issue 4 https://doi.org/10.1101/gad.6.4.568	journal	April 1992
Ectopic expression of a Chlamydomonas mt+-specific homeodomain protein in mt- gametes initiates zygote development without gamete fusion Zhao, H. Genes & Development, Vol. 15, Issue 20 https://doi.org/10.1101/gad.919501	journal	October 2001
WebLogo: A Sequence Logo Generator Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc Genome Research, Vol. 14, Issue 6, p. 1188-1190 https://doi.org/10.1101/gr.849004	journal	May 2004
A Glycosyltransferase from Nicotiana alata Pollen Mediates Synthesis of a Linear (1,5)-α-L-Arabinan When Expressed in Arabidopsis Lampugnani, Edwin R.; Ho, Yin Ying; Moller, Isabel E. Plant Physiology, Vol. 170, Issue 4 https://doi.org/10.1104/pp.15.02005	journal	February 2016
The Arabidopsis BELL1 and KNOX TALE Homeodomain Proteins Interact through a Domain Conserved between Plants and Animals Bellaoui, Mohammed; Pidkowich, Mark S.; Samach, Alon The Plant Cell, Vol. 13, Issue 11 https://doi.org/10.1105/tpc.010161	journal	November 2001
Cell-Fate Switch of Synergid to Egg Cell in Arabidopsis eostre Mutant Embryo Sacs Arises from Misexpression of the BEL1-Like Homeodomain Gene BLH1 Pagnussat, Gabriela Carolina; Yu, Hee-Ju; Sundaresan, Venkatesan The Plant Cell, Vol. 19, Issue 11 https://doi.org/10.1105/tpc.107.054890	journal	November 2007
KNOXLost theOX: TheArabidopsis KNATMGene Defines a Novel Class of KNOX Transcriptional Regulators Missing the Homeodomain Magnani, Enrico; Hake, Sarah The Plant Cell, Vol. 20, Issue 4 https://doi.org/10.1105/tpc.108.058495	journal	April 2008
Gsp1 Triggers the Sexual Developmental Program Including Inheritance of Chloroplast DNA and Mitochondrial DNA in Chlamydomonas reinhardtii Nishimura, Yoshiki; Shikanai, Toshiharu; Nakamura, Soichi The Plant Cell, Vol. 24, Issue 6 https://doi.org/10.1105/tpc.112.097865	journal	June 2012
Horsetails Are Ancient Polyploids: Evidence from Equisetum giganteum Vanneste, Kevin; Sterck, Lieven; Myburg, Alexander Andrew The Plant Cell, Vol. 27, Issue 6 https://doi.org/10.1105/tpc.15.00157	journal	May 2015
Detection of protein–protein interactions in plants using bimolecular fluorescence complementation Bracha‐Drori, Keren; Shichrur, Keren; Katz, Aviva The Plant Journal, Vol. 40, Issue 3 https://doi.org/10.1111/j.1365-313X.2004.02206.x	journal	August 2004
KNOX homeobox genes potentially have similar function in both diploid unicellular and multicellular meristems, but not in haploid meristems Sano, Ryosuke; Juarez, Cristina M.; Hass, Barbara Evolution and Development, Vol. 7, Issue 1 https://doi.org/10.1111/j.1525-142X.2005.05008.x	journal	January 2005
Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes Derelle, Romain; Lopez, Philippe; Guyader, Hervé Le Evolution & Development, Vol. 9, Issue 3 https://doi.org/10.1111/j.1525-142X.2007.00153.x	journal	May 2007
Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development Sakakibara, Keiko; Nishiyama, Tomoaki; Deguchi, Hironori Evolution & Development, Vol. 10, Issue 5 https://doi.org/10.1111/j.1525-142X.2008.00271.x	journal	September 2008
The Revised Classification of Eukaryotes Adl, Sina M.; Simpson, Alastair G. B.; Lane, Christopher E. Journal of Eukaryotic Microbiology, Vol. 59, Issue 5 https://doi.org/10.1111/j.1550-7408.2012.00644.x	journal	September 2012
Cytokinin‐induced promotion of root meristem size in the fernAzollasupports a shoot‐like origin of euphyllophyte roots Vries, Jan; Fischer, Angela Melanie; Roettger, Mayo New Phytologist, Vol. 209, Issue 2 https://doi.org/10.1111/nph.13630	journal	September 2015
Nonreciprocal complementation of KNOX gene function in land plants Frangedakis, Eftychios; Saint‐Marcoux, Denis; Moody, Laura A. New Phytologist, Vol. 216, Issue 2 https://doi.org/10.1111/nph.14318	journal	November 2016
Characterisation of evolutionarily conserved key players affecting eukaryotic flagellar motility and fertility using a moss model Meyberg, Rabea; Perroud, Pierre‐François; Haas, Fabian B. New Phytologist, Vol. 227, Issue 2 https://doi.org/10.1111/nph.16486	journal	April 2020
Homeodomain-like DNA binding proteins control the haploid-to-diploid transition in Dictyostelium Hedgethorne, Katy; Eustermann, Sebastian; Yang, Ji-Chun Science Advances, Vol. 3, Issue 9 https://doi.org/10.1126/sciadv.1602937	journal	September 2017
Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology Huelsenbeck, J. P. Science, Vol. 294, Issue 5550 https://doi.org/10.1126/science.1065889	journal	December 2001
KNOX2 Genes Regulate the Haploid-to-Diploid Morphological Transition in Land Plants Sakakibara, K.; Ando, S.; Yip, H. K. Science, Vol. 339, Issue 6123 https://doi.org/10.1126/science.1230082	journal	February 2013
Sex-Specific Homeodomain Proteins Sxi1α and Sxi2a Coordinately Regulate Sexual Development in Cryptococcus neoformans Hull, Christina M.; Boily, Marie-Josee; Heitman, Joseph Eukaryotic Cell, Vol. 4, Issue 3 https://doi.org/10.1128/EC.4.3.526-535.2005	journal	March 2005
Transcription of novel genes, including a gene linked to the mating-type locus, induced by Chlamydomonas fertilization Ferris, P. J.; Goodenough, U. W. Molecular and Cellular Biology, Vol. 7, Issue 7 https://doi.org/10.1128/mcb.7.7.2360-2366.1987	journal	July 1987
Evolution in the Cycles of Life Bowman, John L.; Sakakibara, Keiko; Furumizu, Chihiro Annual Review of Genetics, Vol. 50, Issue 1 https://doi.org/10.1146/annurev-genet-120215-035227	journal	November 2016
Flower and Fruit Abortion: Proximate Causes and Ultimate Functions Stephenson, A. G. Annual Review of Ecology and Systematics, Vol. 12, Issue 1 https://doi.org/10.1146/annurev.es.12.110181.001345	journal	November 1981
Morphology supports the setaphyte hypothesis: mosses plus liverworts form a natural group Renzaglia, Karen S.; Villarreal Aguilar, Juan Carlos; Garbary, David J. Bryophyte Diversity and Evolution, Vol. 40, Issue 2 https://doi.org/10.11646/bde.40.2.1	journal	December 2018
Common ancestry of heterodimerizing TALE homeobox transcription factors across Metazoa and Archaeplastida Joo, Sunjoo; Wang, Ming Hsiu; Lui, Gary BMC Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12915-018-0605-5	journal	November 2018
KNOX genes: versatile regulators of plant development and diversity Hay, A.; Tsiantis, M. Development, Vol. 137, Issue 19 https://doi.org/10.1242/dev.030049	journal	September 2010
The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing Keeling, Patrick J.; Burki, Fabien; Wilcox, Heather M. PLoS Biology, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pbio.1001889	journal	June 2014
Antagonistic Roles for KNOX1 and KNOX2 Genes in Patterning the Land Plant Body Plan Following an Ancient Gene Duplication Furumizu, Chihiro; Alvarez, John Paul; Sakakibara, Keiko PLOS Genetics, Vol. 11, Issue 2 https://doi.org/10.1371/journal.pgen.1004980	journal	February 2015
A Simple Auxin Transcriptional Response System Regulates Multiple Morphogenetic Processes in the Liverwort Marchantia polymorpha Flores-Sandoval, Eduardo; Eklund, D. Magnus; Bowman, John L. PLOS Genetics, Vol. 11, Issue 5 https://doi.org/10.1371/journal.pgen.1005207	journal	May 2015
Development of Gateway Binary Vector Series with Four Different Selection Markers for the Liverwort Marchantia polymorpha Ishizaki, Kimitsune; Nishihama, Ryuichi; Ueda, Minoru PLOS ONE, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pone.0138876	journal	September 2015
Efficient CRISPR/Cas9-based genome editing and its application to conditional genetic analysis in Marchantia polymorpha Sugano, Shigeo S.; Nishihama, Ryuichi; Shirakawa, Makoto PLOS ONE, Vol. 13, Issue 10 https://doi.org/10.1371/journal.pone.0205117	journal	October 2018
A cis ‐acting bidirectional transcription switch controls sexual dimorphism in the liverwort Hisanaga, Tetsuya; Okahashi, Keitaro; Yamaoka, Shohei The EMBO Journal, Vol. 38, Issue 6 https://doi.org/10.15252/embj.2018100240	journal	January 2019
A Staining Protocol for Identifying Secondary Compounds in Myrtaceae Retamales, Hernan A.; Scharaschkin, Tanya Applications in Plant Sciences, Vol. 2, Issue 10 https://doi.org/10.3732/apps.1400063	journal	October 2014
Convergent recruitment of TALE homeodomain life cycle regulators to direct sporophyte development in land plants and brown algae Arun, Alok; Coelho, Susana M.; Peters, Akira F. eLife, Vol. 8 https://doi.org/10.7554/eLife.43101	journal	January 2019

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