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Breeding systems and germline development - evolutionary genomic analysis using Arabidopsis relatives

English title Breeding systems and germline development - evolutionary genomic analysis using Arabidopsis relatives
Applicant Shimizu Kentaro
Number 159767
Funding scheme Project funding
Research institution Institut für Evolutionsbiologie und Umweltwissenschaften Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Botany
Start/End 01.06.2015 - 30.11.2018
Approved amount 600'000.00
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All Disciplines (2)

Discipline
Botany
Ecology

Keywords (4)

rapid evolution; breeding system; genome-wide association study; Arabidopsis

Lay Summary (German)

Lead
Das das Fortpflanzungssystem von Pflanzen, Tieren und Pilzen steht im Forschungsfokus verschiedener Bereiche der Biologie, darunter Verhaltensbiologie, Medizin, aber auch Evolutionsbiologie. Dies beruht auf der Tatsache, dass eine Vielzahl von Reproduktionsmerkmalen unter starkem Selektionsdruck stehen.
Lay summary
In Pflanzen wird die Evolution der Autogamie (Selbstbestäubung) als eine der häufigsten evolutionären Veränderungen in Fortpflanzungssytemen erachtet. Dieser Übergang charakterisiert sich durch den Verlust der Selbstinkompatibilität innerhalb einer Art. Die Evolution dieses sogenannten "Selfing-Syndroms" macht sich unter anderem durch kleinere Blüten und ein reduziertes Verhältnis von Pollen zu Ovuli bemerkbar. Interessanterweise können veränderungen genomischer Muster, welche unter anderem eine Reduktion der Genomgröße, im genaueren der Anzahl von Transposons, mit sich führen, beobachtet werden. Wir haben die Evolution der Autogamie auf molekularer Ebene bei nahe verwandten Arten der Modellart Arabidopsis thaliana untersucht. Die Ergebnisse zeigen, dass das Gen SCR (SP11), welches den männlichen Teil der Selbstinkompatibilität darstellt, mutierte, und in seiner Funktion unwirksam wurde. Dies ist mit dem evolutionären Verlust von Selbstinkompatibilität gleichzusetzen, und unterstützt aktuelle Hypothesen zum sexuellen Konflikt. Mit dem großen Fortschritt im "1001 Genome Project", in welchem mehr als 1000 unterschiedliche Ecotypen von Arabidopsis thaliana sequenziert wurden, können mittlerweile genomweite Assoziationsstudien (GWAS) und Genomscans eingesetzt werden, um Merkmale der Selektion  zu quantifizieren. Dies bereitet eine Basis, welche uns ermöglicht, die Evolution von Fortpflanzungsstratiegien auch in anderen, mit Arabidopsis thaliana verwandten, Arten zu studieren.
Direct link to Lay Summary Last update: 19.05.2015

Responsible applicant and co-applicants

Employees

Publications

Publication
Fine‐scale empirical data on niche divergence and homeolog expression patterns in an allopolyploid and its diploid progenitor species
Akiyama Reiko, Sun Jianqiang, Hatakeyama Masaomi, Lischer Heidi E. L., Briskine Roman V., Hay Angela, Gan Xiangchao, Tsiantis Miltos, Kudoh Hiroshi, Kanaoka Masahiro M., Sese Jun, Shimizu Kentaro K., Shimizu‐Inatsugi Rie (2020), Fine‐scale empirical data on niche divergence and homeolog expression patterns in an allopolyploid and its diploid progenitor species, in New Phytologist, epub-nph.17101.
Adaptive reduction of male gamete number in the selfing plant Arabidopsis thaliana
Tsuchimatsu Takashi, Kakui Hiroyuki, Yamazaki Misako, Marona Cindy, Tsutsui Hiroki, Hedhly Afif, Meng Dazhe, Sato Yutaka, Städler Thomas, Grossniklaus Ueli, Kanaoka Masahiro M., Lenhard Michael, Nordborg Magnus, Shimizu Kentaro K. (2020), Adaptive reduction of male gamete number in the selfing plant Arabidopsis thaliana, in Nature Communications, 11(1), 2885-2885.
Pollen Grain Counting Using a Cell Counter
Kakui Hiroyuki, Yamazaki Misako, Hamaya Naoto-Benjamin, Shimizu Kentaro K. (2020), Pollen Grain Counting Using a Cell Counter, in Geitmann Anja (ed.), Springer US, New York, NY, 1-11.
Molecular basis of flowering under natural long-day conditions in Arabidopsis
Song Young Hun, Kubota Akane, Kwon Michael S., Covington Michael F., Lee Nayoung, Taagen Ella R., Laboy Cintrón Dianne, Hwang Dae Yeon, Akiyama Reiko, Hodge Sarah K., Huang He, Nguyen Nhu H., Nusinow Dmitri A., Millar Andrew J., Shimizu Kentaro K., Imaizumi Takato (2018), Molecular basis of flowering under natural long-day conditions in Arabidopsis, in Nature Plants, 4(10), 824-835.
Agrobacterium-mediated floral dip transformation of the model polyploid species Arabidopsis kamchatica
Yew Chow-Lih, Kakui Hiroyuki, Shimizu Kentaro K. (2018), Agrobacterium-mediated floral dip transformation of the model polyploid species Arabidopsis kamchatica, in Journal of Plant Research, 131(2), 349-358.
Homeolog expression quantification methods for allopolyploids
Kuo Tony, Hatakeyama Masaomi, Tameshige Toshiaki, Shimizu Kentaro K., Sese Jun (2018), Homeolog expression quantification methods for allopolyploids, in -, 1.
Patterns of polymorphism and selection in the subgenomes of the allopolyploid Arabidopsis kamchatica
Paape Timothy, Briskine Roman V., Halstead-Nussloch Gwyneth, Lischer Heidi E. L., Shimizu-Inatsugi Rie, Hatakeyama Masaomi, Tanaka Kenta, Nishiyama Tomoaki, Sabirov Renat, Sese Jun, Shimizu Kentaro K. (2018), Patterns of polymorphism and selection in the subgenomes of the allopolyploid Arabidopsis kamchatica, in Nature Communications, 9(1), 3909-3909.
Positional bias in variant calls against draft reference assemblies
Briskine Roman V., Shimizu Kentaro K. (2017), Positional bias in variant calls against draft reference assemblies, in BMC Genomics, 18(1), 263-263.
Reference-guided de novo assembly approach improves genome reconstruction for related species
Lischer Heidi E. L., Shimizu Kentaro K. (2017), Reference-guided de novo assembly approach improves genome reconstruction for related species, in BMC Bioinformatics, 18(1), 474-474.
Genomics meets remote sensing in global change studies: monitoring and predicting phenology, evolution and biodiversity
Yamasaki Eri, Altermatt Florian, Cavender-Bares Jeannine, Schuman Meredith C, Zuppinger-Dingley Debra, Garonna Irene, Schneider Fabian D, Guillén-Escribà Carla, van Moorsel Sofia J, Hahl Terhi, Schmid Bernhard, Schaepman-Strub Gabriela, Schaepman Michael E, Shimizu Kentaro K (2017), Genomics meets remote sensing in global change studies: monitoring and predicting phenology, evolution and biodiversity, in Current Opinion in Environmental Sustainability, 29, 177-186.
Genome assembly and annotation of Arabidopsis halleri , a model for heavy metal hyperaccumulation and evolutionary ecology
Briskine Roman V., Paape Timothy, Shimizu-Inatsugi Rie, Nishiyama Tomoaki, Akama Satoru, Sese Jun, Shimizu Kentaro K. (2017), Genome assembly and annotation of Arabidopsis halleri , a model for heavy metal hyperaccumulation and evolutionary ecology, in Molecular Ecology Resources, 17(5), 1025-1036.
Duplicated pollen–pistil recognition loci control intraspecific unilateral incompatibility in Brassica rapa
Takada Yoshinobu, Murase Kohji, Shimosato-Asano Hiroko, Sato Takahiro, Nakanishi Honoka, Suwabe Keita, Shimizu Kentaro K., Lim Yong Pyo, Takayama Seiji, Suzuki Go, Watanabe Masao (2017), Duplicated pollen–pistil recognition loci control intraspecific unilateral incompatibility in Brassica rapa, in Nature Plants, 3(7), 17096-17096.
The population genomic signature of environmental association and gene flow in an ecologically divergent tree species Metrosideros polymorpha (Myrtaceae)
Izuno Ayako, Kitayama Kanehiro, Onoda Yusuke, Tsujii Yuki, Hatakeyama Masaomi, Nagano Atsushi J., Honjo Mie N., Shimizu-Inatsugi Rie, Kudoh Hiroshi, Shimizu Kentaro K., Isagi Yuji (2017), The population genomic signature of environmental association and gene flow in an ecologically divergent tree species Metrosideros polymorpha (Myrtaceae), in Molecular Ecology, 26(6), 1515-1532.
Cost-Effective Discovery of Nucleotide Polymorphisms in Populations of an Allopolyploid Species Using Pool-Seq
Hirao Akira S., Onda Yoshihiko, Shimizu-Inatsugi Rie, Sese Jun, K. Shimizu Kentaro, Kenta Tanaka (2017), Cost-Effective Discovery of Nucleotide Polymorphisms in Populations of an Allopolyploid Species Using Pool-Seq, in American Journal of Molecular Biology, 07(04), 1031-1046.
Conserved but Attenuated Parental Gene Expression in Allopolyploids: Constitutive Zinc Hyperaccumulation in the Allotetraploid Arabidopsis kamchatica
Paape Timothy, Hatakeyama Masaomi, Shimizu-Inatsugi Rie, Cereghetti Teo, Onda Yoshihiko, Kenta Tanaka, Sese Jun, Shimizu Kentaro K. (2016), Conserved but Attenuated Parental Gene Expression in Allopolyploids: Constitutive Zinc Hyperaccumulation in the Allotetraploid Arabidopsis kamchatica, in Molecular Biology and Evolution, 33(11), 2781-2800.
Genome sequencing of Metrosideros polymorpha (Myrtaceae), a dominant species in various habitats in the Hawaiian Islands with remarkable phenotypic variations
Izuno Ayako, Hatakeyama Masaomi, Nishiyama Tomoaki, Tamaki Ichiro, Shimizu-Inatsugi Rie, Sasaki Ryuta, Shimizu Kentaro K., Isagi Yuji (2016), Genome sequencing of Metrosideros polymorpha (Myrtaceae), a dominant species in various habitats in the Hawaiian Islands with remarkable phenotypic variations, in Journal of Plant Research, (4), 727-736.
Plant adaptive radiation mediated by polyploid plasticity in transcriptomes
Shimizu-Inatsugi Rie, Terada Aika, Hirose Kyosuke, Kudoh Hiroshi, Sese Jun, Shimizu Kentaro K. (2016), Plant adaptive radiation mediated by polyploid plasticity in transcriptomes, in Molecular Ecology, 26(1), 193-207.
Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism
Novikova Polina Yu, Hohmann Nora, Nizhynska Viktoria, Tsuchimatsu Takashi, Ali Jamshaid, Muir Graham, Guggisberg Alessia, Paape Tim, Schmid Karl, Fedorenko Olga M, Holm Svante, Säll Torbjörn, Schlötterer Christian, Marhold Karol, Widmer Alex, Sese Jun, Shimizu Kentaro K, Weigel Detlef, Krämer Ute, Koch Marcus A, Nordborg Magnus (2016), Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism, in Nature Genetics, (9), 1077-1082.
The Cardamine hirsuta genome offers insight into the evolution of morphological diversity
Gan Xiangchao, Hay Angela, Kwantes Michiel, Haberer Georg, Hallab Asis, Ioio Raffaele Dello, Hofhuis Hugo, Pieper Bjorn, Cartolano Maria, Neumann Ulla, Nikolov Lachezar A., Song Baoxing, Hajheidari Mohsen, Briskine Roman, Kougioumoutzi Evangelia, Vlad Daniela, Broholm Suvi, Hein Jotun, Meksem Khalid, Lightfoot David, Shimizu Kentaro K., Shimizu-Inatsugi Rie, Imprialou Martha, Kudrna David, et al. (2016), The Cardamine hirsuta genome offers insight into the evolution of morphological diversity, in Nature Plants, (11), 16167-16167.
Evolution of selfing: recurrent patterns in molecular adaptation
Shimizu Kentaro, Tsuchimatsu Takashi (2015), Evolution of selfing: recurrent patterns in molecular adaptation, in Annual Reviews, 46, 593-622.

Datasets

Genome assembly and annotation of Arabidopsis halleri, a model for heavy metal hyperaccumulation and evolutionary ecology

Author Briskine, Roman
Persistent Identifier (PID) 10.5061/ dryad.gn4hh
Repository dryad


Patterns of polymorphism and selection in the subgenomes of the allopolyploid Arabidopsis kamchatica

Author Paape, Tim
Persistent Identifier (PID) 10.5061/dryad.15rs596
Repository dryad


Collaboration

Group / person Country
Types of collaboration
Department of Plant and Microbial Biology, University of Zurich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Artificial Intelligence Research Center (AIST) Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Institute of Marine Geology and Geophysics, Far East Branch, Russian Academy of Sciences Russia (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Advanced Science Research Center, Kanazawa University Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Department of Environmental Systems Science, ETH Zurich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Swiss Institute of Bioinformatics (SIB), Lausanne Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Functional Genomics Center Zurich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Kihara Institute for Biological Research, Yokohama City University Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Kyoto University Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Sugadaira Montane Research Center, University of Tsukuba Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel

Scientific events



Self-organised

Title Date Place
Genomics and modeling 13.07.2018 Yokohama City, Japan
50 years since Ohno’s genome duplication: integration across disciplines and time scales, Society of Molecular Biology and Evolution 10.07.2018 Yokohama, Japan
Polyploidization and Evolution of Sexual Reproduction, the 25th International Congress on Sexual Plant Reproduction 15.06.2018 Gifu, Japan
Plant development and evolution: from molecules to ecosystems 20.02.2018 Zurich, Switzerland
Molecular studies in natura symposium – How plants sense and react in the nature 19.02.2018 Zurich, Switzerland
Plant genomics in LS2 meeting 02.02.2017 Zurich, Switzerland
The Nagoya Protocol on Access and Benefit-Sharing (ABS) and its implications for academic research 20.12.2016 Zurich, Switzerland
Plants in changing environments 01.11.2016 Kyoto, Japan
Genome duplication: integrating comparative genomics, population genetics, and experimentally synthesized polyploids, 17th Annual Meeting of the Society of Evolutionary Studies, Japan 21.08.2015 Tokyo, Japan

Knowledge transfer events

Active participation

Title Type of contribution Date Place Persons involved
Public talk as an awardee of the NISTEP Award (Award for nice step researchers) from the Minister of Education, Culture, Sports, Science and Technology Talk 08.07.2016 Tokyo, Japan Shimizu Kentaro;


Communication with the public

Communication Title Media Place Year
Talks/events/exhibitions Guided tours of the Paleontological Museum of the University of Zurich German-speaking Switzerland International 2018
Talks/events/exhibitions Agora “PSC Discovery Program for the Youth” German-speaking Switzerland 2017
Talks/events/exhibitions Observing the plant epidermis for children of the Japanese School in Uster International 2017
Talks/events/exhibitions Guided tours of the laboratory and the Museum of Anthropology of the University of Zurich International German-speaking Switzerland 2016
Talks/events/exhibitions Lecture at the meeting of NPO for promoting advanced high-school education of mathematics & science International 2015

Awards

Title Year
First Prize for the poster award at the PSC Symposium “Dynamics of Plant Development & Evolution” 2017
NISTEP Award (Award for nice step researchers) from the Minister of Education, Culture, Sports, Science and Technology, Japan 2015

Associated projects

Number Title Start Funding scheme
158542 PSC Discovery Program for Youth 01.04.2015 Agora
182318 Evolutionary functional genomics of selfing and polyploid speciation 01.12.2018 Project funding
171682 PSC Creative Camps for Youth 01.04.2017 Agora
140917 Recurrent patterns in molecular adaptation and speciation: evolutionary genomic analysis using Arabidopsis relatives 01.06.2012 Project funding

Abstract

The breeding system of plants, animals and fungi is a major selective force on various reproductive traits. This fact makes it a highly interesting study object for diverse disciplines, such as behavioral biology, breeding science or medical science as well as evolutionary biology. In plants, the evolution of autogamy or self-fertilization is considered a very frequent evolutionary transition of breeding systems. The establishment of autogamy is typically characterized by the loss of self-incompatibility, accompanied by small floral size and a reduced pollen to ovule ratio. Interestingly, the evolutionary shift to autogamy causes changes in genomic patterns, including a reduction in genome size, more exactly in the number of transposable elements. We have studied the molecular basis of the evolution of self-compatibility using relatives to the model species Arabidopsis thaliana. We discovered the disruption of the gene SCR/SP11, which is the male self-incompatibility locus, which was responsible for the evolutionary loss of self-incompatibility. Furthermore, we identified that this loss-of function in SCR is a recurrent pattern. These findings support the hypothesis of sexual conflict. With the advance of the 1001 genome project of Arabidopsis thaliana, in which more than 1000 different ecotypes were sequenced, genome-wide association studies (GWAS) and genome scans became feasible approaches to study selection on quantitative traits. We propose the use of GWAS of study the evolution of breeding systems in Arabidopsis relatives.
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