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The Genetic and Molecular Basis of Gametogenesis and Maternal Effects in Arabidopsis

English title The Genetic and Molecular Basis of Gametogenesis and Maternal Effects in Arabidopsis
Applicant Grossniklaus Ueli
Number 141245
Funding scheme Project funding (Div. I-III)
Research institution Institut für Pflanzen- und Mikrobiologie Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Embryology, Developmental Biology
Start/End 01.05.2012 - 30.04.2015
Approved amount 930'000.00
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All Disciplines (4)

Discipline
Embryology, Developmental Biology
Genetics
Molecular Biology
Cellular Biology, Cytology

Keywords (6)

gametophyte; genomic imprinting; epigenetics; maternal effects; arabidopsis; fertilization

Lay Summary (English)

Lead
Lay summary
Gametogenesis and the maternal control of embryogenesis have been studied extensively in animal systems at the genetic, molecular, and cellular level. These studies have yielded insight into fundamental concepts and mechanisms involved in the establishment and interpretation of positional information, cell-cell interaction, and signal transduction cascades. In contrast, our knowledge about the genetic and molecular control of these processes in plants is very limited. The simple but highly polar and specialized female gametophyte, which consists of only seven cells belonging to four cell types, make it an ideal system to study the role of positional information and signaling during development. Using Arabidopsis thaliana as a model system, this project focuses on the elucidation of key events during sexual reproduction, namely cell specification, fertilization, and the epigenetic control of seed development with a focus on embryogenesis. We will use a combination of (quantitative) genetic, cell biological, molecular, and computational approaches. The proposed studies will yield insights into fundamental questions: How are cell types specified at the molecular level? Does non-random sister chromatid segregation play a role in differentiation? Are there similarities between distinct signaling cascades? What is the molecular basis of genomic imprinting, which occurs only in mammals and plants? While some of the investigated processes are conserved between animals and plants, others are likely specific, such that the mechanisms can be compared and contrasted to gain new insights into fundamental developmental concepts. Beyond fundamental aspects, however, the proposed studies will contribute to the elucidation of epigenetic mechanisms that transcend plant biology and play a central role in all organisms, including humans, where many diseases have an epigenetic component.
Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Functional analysis of related CrRLK1L receptor-like kinases in pollen tube reception.
Kessler Sharon A, Lindner Heike, Jones Daniel S, Grossniklaus Ueli (2015), Functional analysis of related CrRLK1L receptor-like kinases in pollen tube reception., in EMBO reports, 16(1), 107-15.
Plant germline formation: common concepts and developmental flexibility in sexual and asexual reproduction.
Schmidt Anja, Schmid Marc W, Grossniklaus Ueli (2015), Plant germline formation: common concepts and developmental flexibility in sexual and asexual reproduction., in Development (Cambridge, England), 142(2), 229-41.
Rcount: simple and flexible RNA-Seq read counting.
Schmid Marc W, Grossniklaus Ueli (2015), Rcount: simple and flexible RNA-Seq read counting., in Bioinformatics (Oxford, England), 31(3), 436-7.
TURAN and EVAN mediate pollen tube reception in Arabidopsis Synergids through protein glycosylation.
Lindner Heike, Kessler Sharon A, Müller Lena M, Shimosato-Asano Hiroko, Boisson-Dernier Aurélien, Grossniklaus Ueli (2015), TURAN and EVAN mediate pollen tube reception in Arabidopsis Synergids through protein glycosylation., in PLoS biology, 13(4), 1002139-1002139.
A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery.
Ngo Quy A, Vogler Hannes, Lituiev Dmytro S, Nestorova Anna, Grossniklaus Ueli (2014), A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery., in Developmental cell, 29(4), 491-500.
Apomictic and sexual germline development differ with respect to cell cycle, transcriptional, hormonal and epigenetic regulation.
Schmidt Anja, Schmid Marc W, Klostermeier Ulrich C, Qi Weihong, Guthörl Daniela, Sailer Christian, Waller Manuel, Rosenstiel Philip, Grossniklaus Ueli (2014), Apomictic and sexual germline development differ with respect to cell cycle, transcriptional, hormonal and epigenetic regulation., in PLoS genetics, 10(7), 1004476-1004476.
Transcriptional silencing by polycomb-group proteins.
Grossniklaus Ueli, Paro Renato (2014), Transcriptional silencing by polycomb-group proteins., in Cold Spring Harbor perspectives in biology, 6(11), 019331-019331.
ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases.
Boisson-Dernier Aurélien, Lituiev Dmytro S, Nestorova Anna, Franck Christina Maria, Thirugnanarajah Sharme, Grossniklaus Ueli (2013), ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases., in PLoS biology, 11(11), 1001719-1001719.
Efficient and rapid isolation of early-stage embryos from Arabidopsis thaliana seeds.
Raissig Michael T, Gagliardini Valeria, Jaenisch Johan, Grossniklaus Ueli, Baroux Célia (2013), Efficient and rapid isolation of early-stage embryos from Arabidopsis thaliana seeds., in Journal of visualized experiments : JoVE, (76), ---.
Genomic imprinting in the Arabidopsis embryo is partly regulated by PRC2.
Raissig Michael T, Bemer Marian, Baroux Célia, Grossniklaus Ueli (2013), Genomic imprinting in the Arabidopsis embryo is partly regulated by PRC2., in PLoS genetics, 9(12), 1003862-1003862.
The Polycomb group protein MEDEA and the DNA methyltransferase MET1 interact to repress autonomous endosperm development in Arabidopsis.
Schmidt Anja, Wöhrmann Heike J P, Raissig Michael T, Arand Julia, Gheyselinck Jacqueline, Gagliardini Valeria, Heichinger Christian, Walter Joern, Grossniklaus Ueli (2013), The Polycomb group protein MEDEA and the DNA methyltransferase MET1 interact to repress autonomous endosperm development in Arabidopsis., in The Plant journal : for cell and molecular biology, 73(5), 776-87.
Transgenerational epigenetic inheritance: how important is it?
Grossniklaus Ueli, Kelly William G, Kelly Bill, Ferguson-Smith Anne C, Pembrey Marcus, Lindquist Susan (2013), Transgenerational epigenetic inheritance: how important is it?, in Nature reviews. Genetics, 14(3), 228-35.
Atypical DNA methylation of genes encoding cysteine-rich peptides in Arabidopsis thaliana.
You Wanhui, Tyczewska Agata, Spencer Matthew, Daxinger Lucia, Schmid Marc W, Grossniklaus Ueli, Simon Stacey A, Meyers Blake C, Matzke Antonius J M, Matzke Marjori (2012), Atypical DNA methylation of genes encoding cysteine-rich peptides in Arabidopsis thaliana., in BMC plant biology, 12, 51-51.
CrRLK1L receptor-like kinases: not just another brick in the wall.
Lindner Heike, Müller Lena Maria, Boisson-Dernier Aurélien, Grossniklaus Ueli (2012), CrRLK1L receptor-like kinases: not just another brick in the wall., in Current opinion in plant biology, 15(6), 659-69.
Dynamic regulation of Polycomb group activity during plant development.
Bemer Marian, Grossniklaus Ueli (2012), Dynamic regulation of Polycomb group activity during plant development., in Current opinion in plant biology, 15(5), 523-9.
Egg cell-secreted EC1 triggers sperm cell activation during double fertilization.
Sprunck Stefanie, Rademacher Svenja, Vogler Frank, Gheyselinck Jacqueline, Grossniklaus Ueli, Dresselhaus Thomas (2012), Egg cell-secreted EC1 triggers sperm cell activation during double fertilization., in Science (New York, N.Y.), 338(6110), 1093-7.
Identification of a DNA methylation-independent imprinting control region at the Arabidopsis MEDEA locus.
Wöhrmann Heike J P, Gagliardini Valeria, Raissig Michael T, Wehrle Wendelin, Arand Julia, Schmidt Anja, Tierling Sascha, Page Damian R, Schöb Hanspeter, Walter Jörn, Grossniklaus Ueli (2012), Identification of a DNA methylation-independent imprinting control region at the Arabidopsis MEDEA locus., in Genes & development, 26(16), 1837-50.
SNP-Ratio Mapping (SRM): identifying lethal alleles and mutations in complex genetic backgrounds by next-generation sequencing.
Lindner Heike, Raissig Michael T, Sailer Christian, Shimosato-Asano Hiroko, Bruggmann Rémy, Grossniklaus Ueli (2012), SNP-Ratio Mapping (SRM): identifying lethal alleles and mutations in complex genetic backgrounds by next-generation sequencing., in Genetics, 191(4), 1381-6.
Tackling drought stress: receptor-like kinases present new approaches.
Marshall Alex, Aalen Reidunn B, Audenaert Dominique, Beeckman Tom, Broadley Martin R, Butenko Melinka A, Caño-Delgado Ana I, de Vries Sacco, Dresselhaus Thomas, Felix Georg, Graham Neil S, Foulkes John, Granier Christine, Greb Thomas, Grossniklaus Ueli, Hammond John P, Heidstra Renze, Hodgman Charlie, Hothorn Michael, Inzé Dirk, Ostergaard Lars, Russinova Eugenia, Simon Rüdiger, Skirycz Aleksandra, Stahl Yvonne (2012), Tackling drought stress: receptor-like kinases present new approaches., in The Plant cell, 24(6), 2262-78.
The Armadillo repeat gene ZAK IXIK promotes Arabidopsis early embryo and endosperm development through a distinctive gametophytic maternal effect.
Ngo Quy A, Baroux Celia, Guthörl Daniela, Mozerov Peter, Collinge Margaret A, Sundaresan Venkatesan, Grossniklaus Ueli (2012), The Armadillo repeat gene ZAK IXIK promotes Arabidopsis early embryo and endosperm development through a distinctive gametophytic maternal effect., in The Plant cell, 24(10), 4026-43.

Collaboration

Group / person Country
Types of collaboration
Ives Barral, Institut für Biochemie, ETHZ, Zürich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Research Infrastructure
Markus Aebi, Institut für Mikrobiologie ETHZ, Zürich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Jörn Walther, Universität des Saarlandes, Saarbrücken Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Ralph Panstruga, Max-Planck-Institut für Pflanzenzüchtungsforschung, Köln Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Lucia Colombo, Università degli Studii di Milano Italy (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Philip Rosenstiel, Christian-Albrechts-Universität zu Kiel Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Research Infrastructure
Martin Kater, Università degli Studii di Milano Italy (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Wilhelm Gruissem, Institut für Pflanzenwissenschaften, ETHZ, Zürich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Daniel Grimanelli, Université de Montpellier France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Stefanie Sprunck, Universität Regensburg Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Karl Schmid, Universität Hohenheim Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Seminar, University of Sydney Individual talk Signaling during plant reproduction 01.04.2015 Sydney, Australia Grossniklaus Ueli;
Seminar, Universitá degli Studi di Milano Individual talk Control of fertilization and interspecific hybridization 01.04.2015 Mailand, Italy Grossniklaus Ueli;
G60 Understanding the Genome III Talk given at a conference Biased chromatid segregation: A key mechanism during plant gametophyte development? 20.03.2015 Chexbres, Switzerland Schmid Roger; Grossniklaus Ueli;
Seminar, Centro de Investigatión Cientifica de Yucatán Talk given at a conference Mechanisms and evolution of genomic imprinting in plants 01.02.2015 Merida, Mexico Grossniklaus Ueli;
Keystone Symposium “Plant Receptor Kinases” From Molecules to Environment” Talk given at a conference Mechanisms of CrRLK1L function in Arabidopsis 01.02.2015 Taos, NM, United States of America Grossniklaus Ueli;
International Symposium on “Pollination and Fertilization” Talk given at a conference A calcium dialogue regulates male-female interactions during pollen tube reception 01.10.2014 Tai'an, China Grossniklaus Ueli;
7th International PhD School in Plant Development Talk given at a conference Back to the rhizoids of plant sexual development 10.09.2014 Retzbach, Germany Rövekamp Moritz; Grossniklaus Ueli;
7th International PhD School in Plant Development Poster Back to the rhizoids of plant sexual development 10.09.2014 Retzbach, Germany Rövekamp Moritz; Grossniklaus Ueli;
Symposium “Cellular Memory, Reprogramming and Systems Biology” Talk given at a conference Function of Polycomb proteins in plants 01.09.2014 Basel, Switzerland Grossniklaus Ueli;
23rd International Congress of Sexual Plant Reproduction Poster Back to the rhizoids of plant sexual development 13.07.2014 Porto, Portugal Rövekamp Moritz; Grossniklaus Ueli;
23rd Congress on Sexual Plant Reproduction Talk given at a conference Glycosylation plays an important role in male-female interactions during fertilization 01.07.2014 Porto, Portugal Grossniklaus Ueli;
Course "Advanced Techniques in Plant Science" Talk given at a conference Gametophyte development and double fertilization 01.07.2014 Cold Spring Harbor, United States of America Grossniklaus Ueli;
FESP/EPSO Congress “Plant Biology Europe” Talk given at a conference Molecular mechanisms underlying fertilization 01.06.2014 Dublin, Ireland Grossniklaus Ueli;
Seminar, Gregor Mendel Institute Individual talk With whom to have sex and with who not: mechanisms of recognition during fertilization 01.05.2014 Wien, Austria Grossniklaus Ueli;
Interdisciplinary Workshop “A Dynamic Architecture of Life?”, Accademia Nazionale dei Lincei Talk given at a conference Epigenetic regulation during plant development 01.05.2014 Rom, Italy Grossniklaus Ueli;
Workshop “Frontiers in Biology and Medicine” Talk given at a conference Sex, parental conflict and infanticide: genomic imprinting in plants and mammals 01.02.2014 Bangalore, India Grossniklaus Ueli;
Seminar, Indian Institute of Technology - Madras Individual talk Molecular mechanisms underlying pollen tube reception and crossing barriers 01.02.2014 Chennai, India Grossniklaus Ueli;
Seminar, The Institute of Mathematical Sciences Individual talk Theoretical and experimental studies on cell specification in the female gametophyte 01.02.2014 Chennai, India Grossniklaus Ueli;
Seminar University of Wageningen Individual talk The epigenetic regulator MEDEA 10.12.2013 Wageningen, Netherlands Bemer Marian;
Plant Science Center Symposium "Plants in a Changing Climate" Poster EVAN and TURAN Regulate Pollen Tube Reception and Male Gametophyte Development 08.11.2013 Zurich, Switzerland Lindner Heike; Grossniklaus Ueli; Müller Lena;
SEB Workshop "Regulation of Fertilization and Early Seed Development" Talk given at a conference Molecular basis of pollen tube reception and fertilization 01.09.2013 Bath, Great Britain and Northern Ireland Grossniklaus Ueli;
NESCent Imprinting Working Group Talk given at a conference Mechanisms and evolution of genomic imprinting in plants 01.09.2013 Raleigh, United States of America Grossniklaus Ueli;
Seminar, Cornell University Individual talk Molecular control of fertilization and interspecific hybridization 01.09.2013 Ithaca, United States of America Grossniklaus Ueli;
FASEB Meeting "Mechanisms of Plant Development" Poster EVAN and TURAN Regulate Pollen Tube Reception and Male Gametophyte Development 11.08.2013 Saxtons River, VE, United States of America Grossniklaus Ueli; Lindner Heike; Müller Lena;
Annual Meeting of the Society for Experimental Biology Poster A role for the epigenetic regulator MEDEA outside the Arabidopsis seed 02.07.2013 Valencia, Spain Bemer Marian; Grossniklaus Ueli;
Gordon Research Conference "Developmental Biology" Talk given at a conference Cell specification during sprorogenesis and gametogenesis in plants 01.07.2013 Lucca, Italy Grossniklaus Ueli;
Seminar, Vlaams Instituut voor Biotechnologie Individual talk Molecular basis of pollen tube reception and fertilization 01.05.2013 Gent, Belgium Grossniklaus Ueli;
ALW Meeting on Experimental Plant Sciences Talk given at a conference Regulation of fertiization and interspecific hybridization 01.04.2013 Lunteren, Netherlands Grossniklaus Ueli;
55th Annual Maize Genetics Conference Talk given at a conference Maternal control of paternal genome activation 01.03.2013 St. Charles, IL, United States of America Grossniklaus Ueli;
35th Annual Meeting of the Molecular Biology Society of Japan Talk given at a conference Gametogenesis and genomic imprinting in plants 01.12.2012 Fukuoka, Japan Grossniklaus Ueli;
4th NIBB-MPIPZ-TLL Symposium ”Arabidopsis and Emerging Model Systems” Talk given at a conference Molecular control of double fertilization 01.11.2012 Okazaki, Japan Grossniklaus Ueli;
EMBO Plant Biology Lectures Talk given at a conference Epigenetic regulation of seed development 01.10.2012 Buenos Aires, Argentina Grossniklaus Ueli;
EMBO Symposium "Germline - Immortality through Totipotency" Talk given at a conference Sporogenesis and gametogenesis in plants 01.10.2012 Heidelberg, Germany Grossniklaus Ueli;
XV Latin America Congress of Genetics (ALAG) Talk given at a conference Sex, parental conflict and infanticide: genomic imprinting in plants 01.10.2012 Rosario, Argentina Grossniklaus Ueli;
Jahresversammlung der Gesellschaft fur Genetik Deutschland Talk given at a conference Mechanisms of Polycomb Regulations during Seed Development 01.09.2012 Essen, Germany Grossniklaus Ueli;
5th International Ph.D. School in Plant Development Talk given at a conference Control of intra- and interspecific pollen tube reception 01.09.2012 Pontiagano, Italy Grossniklaus Ueli;
Seminar, Plant Science Center Umea Individual talk Molecular basis of fertilization and interspecific crossing barriers 01.09.2012 Umea, Sweden Grossniklaus Ueli;
8th Trinational Arabidopsis Meeting Talk given at a conference Molecular regulation of pollen tube reception 01.09.2012 Lausanne, Switzerland Grossniklaus Ueli;
4th EED Annual Meeting Talk given at a conference Molecular networks controling megasporogenesis in Arabidopsis 15.07.2012 Lisbon, Portugal Grossniklaus Ueli;
3rd COST/Hapreci Meeting Talk given at a conference Theoretical and experimental approaches to study embryo sac development 01.07.2012 Porto, Portugal Grossniklaus Ueli;
77th Cold Spring Harbor Symposium on Quantitative Biology “The Biology of Plants” Poster Genomic imprinting in the Arabidopsis embryo is partly regulated by PRC2 27.05.2012 Cold Spring Harbor, NY, United States of America Bemer Marian; Grossniklaus Ueli; Raissig Michael Thomas;
3rd EMBO Conference on Plant Molecular Biology Talk given at a conference Molecular Control of Fertilization 01.05.2012 Matera, Italy Grossniklaus Ueli;
77th Cold Spring Harbor Symposium on Quantitative Biology "The Biology of Plants" Talk given at a conference Maternal control of early plant embryogenesis 01.05.2012 Cold Spring Harbor, NY, United States of America Grossniklaus Ueli;


Communication with the public

Communication Title Media Place Year
Talks/events/exhibitions “Fabrics of Life”, Design Workshop on “Big Data”, Central Saint Martins College of Art and Design International 2014
Talks/events/exhibitions Grüne Gentechnologie und eine nachhaltige Landwirtschaft, Sommerakademie der Studienstiftung Italian-speaking Switzerland German-speaking Switzerland 2014
Media relations: print media, online media Beitrag der Grünen Gentechnik zu einer nachhaltigen Schweizer Landwirtschaft Presskonferenz FoGeFo, Bundeshaus German-speaking Switzerland Western Switzerland 2013
Talks/events/exhibitions Epigenetik und die Vererbung erworbener Eigenschaften, Kantonsschule Wettingen German-speaking Switzerland 2013
Talks/events/exhibitions Epigenetik: eine Wiederbelebung des Lamarckismus?, Kantonsschule Kusnacht German-speaking Switzerland 2013
Talks/events/exhibitions Grüne Gentechnologie und Nachhaltigkeit, Schweizer Studienstiftung German-speaking Switzerland 2013
Talks/events/exhibitions Epigenetik Symposium, Berlin-Brandenburgische Akademie der Wissenschaften, Berlin, Deutschland International 2012

Awards

Title Year
M.T.M. Willemse Poster Award 2014 23rd International Congress of Sexual Plant Reproduction, Porto, Portugal 2014

Associated projects

Number Title Start Funding scheme
137058 Plant Reproductive Isolation: from Mechanisms to Evolution 01.01.2012 ProDoc
150838 Lightsheet Fluorescence Microscopy 01.12.2013 R'EQUIP
160336 The Genetic and Molecular Basis of Gametogenesis and Maternal Effects in Arabidopsis 01.05.2015 Project funding (Div. I-III)
164086 Imaging of Deep-Lying Tissues with Enhanced Resolution and Sensitivity to Study Plant Development 01.12.2015 R'EQUIP
126006 The genetic and molecular basis of gametogenesis and maternal effects in arabidopsis 01.04.2009 Project funding (Div. I-III)

Abstract

Gametogenesis and the maternal control of embryogenesis have been studied extensively in animal systems at the genetic, molecular, and cellular level. These studies have yielded insight into fundamental concepts and mechanism involved in the establishment and interpretation of positional information, cell-cell interaction, and signal transduction cascades. In contrast, our knowledge about genetic and molecular control of these processes in plants is very limited. The simple but highly polar and specialized female gametophyte, which consists of only seven cells belonging to four cell types, make it an ideal system to study the role of positional information and signaling during development. Using Arabidopsis thaliana as a model system, this proposal focuses on the elucidation of key events during sexual reproduction, namely cell specification, fertilization, and the epigenetic control of seed development with a focus on embryogenesis. We will use a combination of (quantitative) genetic, cell biological, molecular, and computational approaches. Many of the methods are established in the laboratory and rely on standard genetic and molecular biology protocols. Others need special adaptations and have been optimized for the study of the elusive and inaccessible female gametophyte. However, also novel experimental approaches will be established and adapted to our system, such as (i) methods to investigate sister chromatid segregation, (ii) network analyses of cell type-specific transcriptomes; (iii) novel cloning approaches using next generation sequencing technology, (iv) genome-wide association studies to identify modifier loci, and (v) the development of genetic and transgenic tools to investigate embryogenesis uninfluenced by the endosperm. The experiments described in this proposal will shed light on fundamental aspects of plant development, such as the role of positional information, cell-cell interactions, signal transduction, and epigenetic gene regulation in development. Thus, they span numerous fields of developmental biology and will yield novel insights into developmental control mechanisms that transcend plant biology. For example, epigenetic mechanisms play an important role in growth and development. While the role of epigenetic gene regulation in cancer and disease has only become apparent over the last years, plant researchers have studied epigenetic phenomena for decades and have contributed much to our understanding of the underlying molecular mechanisms.
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