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Recurrent patterns in molecular adaptation and speciation: evolutionary genomic analysis using Arabidopsis relatives

Applicant Shimizu Kentaro
Number 140917
Funding scheme Project funding
Research institution Institut für Pflanzen- und Mikrobiologie Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Botany
Start/End 01.06.2012 - 31.05.2015
Approved amount 502'000.00
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All Disciplines (2)

Discipline
Botany
Ecology

Keywords (5)

evolution; climate change; mating system; genome-wide association study; adaptation

Lay Summary (English)

Lead
Lay summary

A central question in biology is the molecular basis of biodiversity. Rapid advances in next-generation sequencing are providing novel tools for addressing key ecological and evolutionary questions in integrated biological sciences. However, the study of adaptive molecular variation has been largely limited to model species. Therefore, general patterns in molecular adaptation and speciation remain unclear, but their discovery is essential to enable understanding and prediction of biological responses to naturally and artificially changing environments. Studying adaptive evolution that occurred many times in parallel is an appropriate approach to investigating recurring patterns. We focus on the evolution of self-compatibility, which has been considered to be one of the most frequent evolutionary shifts in flowering plants and has been a major focus in evolutionary biology since Darwin’s research. It is noteworthy that plant sexual reproduction may be particularly vulnerable to the effects of natural and artificial environmental changes, through evolutionary and plastic responses. A broad impact of this proposal to the society would be to reinforce our previous key research finding that climate change, including glacial cycles, may induce rapid—and possibly irreversible—evolution.

Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Bacterial diversity and composition in the fluid of pitcher plants of the genus Nepenthes
Takeuchi Yayoi, Chaffron Samuel, Salcher Michaela M., Shimizu-Inatsugi Rie, Kobayashi Masaki J., Diway Bibian, von Mering Christian, Pernthaler Jakob, Shimizu Kentaro K. (2015), Bacterial diversity and composition in the fluid of pitcher plants of the genus Nepenthes, in Systematic and Applied Microbiology, 38(5), 330-339.
Evolution of the Selfing Syndrome in Arabis alpina (Brassicaceae).
Tedder Andrew, Carleial Samuel, Gołębiewska Martyna, Kappel Christian, Shimizu Kentaro K, Stift Marc (2015), Evolution of the Selfing Syndrome in Arabis alpina (Brassicaceae)., in PloS one, 10(6), 0126618-0126618.
Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae).
Tedder Andrew, Helling Matthias, Pannell John R, Shimizu-Inatsugi Rie, Kawagoe Tetsuhiro, van Campen Julia, Sese Jun, Shimizu Kentaro K (2015), Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae)., in Annals of botany, 115(5), 763-76.
Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia
Kubo Ken-ichi, Paape Timothy, Hatakeyama Masaomi, Entani Tetsuyuki, Takara Akie, Kajihara Kie, Tsukahara Mai, Shimizu-Inatsugi Rie, Shimizu Kentaro K (corresponding author), Takayama Seiji (corresponding author) (2015), Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia, in Nature Plants, 1(1), 14005.
Genome-wide quantification of homeolog expression ratio revealed nonstochastic gene regulation in synthetic allopolyploid Arabidopsis.
Akama Satoru, Shimizu-Inatsugi Rie, Shimizu Kentaro K, Sese Jun (2014), Genome-wide quantification of homeolog expression ratio revealed nonstochastic gene regulation in synthetic allopolyploid Arabidopsis., in Nucleic acids research, 42(6), 46-46.
Multiple hybridization events in Cardamine (Brassicaceae) during the last 150 years: revisiting a textbook example of neoallopolyploidy.
Zozomová-Lihová Judita, Krak Karol, Mandáková Terezie, Shimizu Kentaro K, Spaniel Stanislav, Vít Petr, Lysak Martin A (2014), Multiple hybridization events in Cardamine (Brassicaceae) during the last 150 years: revisiting a textbook example of neoallopolyploidy., in Annals of botany, 113(5), 817-30.
Effects of pollen availability and the mutation bias on the fixation of mutations disabling the male specificity of self-incompatibility
Tsuchimatsu Takashi, Shimizu Kentaro K. (2013), Effects of pollen availability and the mutation bias on the fixation of mutations disabling the male specificity of self-incompatibility, in Journal of Evolutionary Biology, 1.
The More the Merrier: Recent Hybridization and Polyploidy in Cardamine
Mandakova Terezie, Kovarik Ales, Zozomova-Lihova Judita, Shimizu-Inatsugi Rie, Shimizu Kentaro K., Mummenhoff Klaus, Marhold Karol, Lysak Martin A. (2013), The More the Merrier: Recent Hybridization and Polyploidy in Cardamine, in PLANT CELL, 25(9), 3280-3295.
Chapter 12 Overview: the evolution of genes responsible for adaptation
Shimizu Kentaro K (2012), Chapter 12 Overview: the evolution of genes responsible for adaptation, in Morinaga Shinichi, Kudoh Hiroshi (ed.), Kyoritsu, Tokyo, Japan, Tokyo, 189-196.
Chapter 16: Genome duplication - speciation and ecogenomics of polyploid species
Shimizu-Inatsugi Rie, Shimizu Kentaro K (2012), Chapter 16: Genome duplication - speciation and ecogenomics of polyploid species, in Morinaga Shinichi, Kudoh Hiroshi (ed.), Kyoritsu, Tokyo, Japan, Tokyo, 246-262.
Recent Loss of Self-Incompatibility by Degradation of the Male Component in Allotetraploid Arabidopsis kamchatica.
Tsuchimatsu Takashi, Kaiser Pascal, Yew Chow-Lih, Bachelier Julien B, Shimizu Kentaro K (2012), Recent Loss of Self-Incompatibility by Degradation of the Male Component in Allotetraploid Arabidopsis kamchatica., in PLoS genetics, 8(7), 1002838-1002838.

Collaboration

Group / person Country
Types of collaboration
Prof. Martin Lysak, Masaryk University Czech Republic (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Prof. Jun Sese, Tokyo Institute of Technology Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
Dr. Kenta Tanaka, Tsukuba University Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
Prof. Seiji Takayama, NAIST Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
Prof. Michael Purugganan, New York University United States of America (North America)
- in-depth/constructive exchanges on approaches, methods or results
Prof. Magnus Nordborg, Gregor Mendel Institute Austria (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Prof. Hiroshi Kudoh, Center for Ecological Research, Kyoto University Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
Prof. Alex Widmer, ETHZ Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Prof. Rolf Holderegger, WSL Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Prof. Michael Lenhard, Potsdam University Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Prof. Karol Marhold, Slovakian Academy of Sciences Slovakia (Europe)
- in-depth/constructive exchanges on approaches, methods or results

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Graduate University for Advanced Studies Individual talk Recurrent patterns in speciation by genome duplication and in the evolution of selfing 02.06.2015 Hayama, Japan Shimizu Kentaro;
International Symposium of Correlative Gene System Talk given at a conference Transcriptome and environmental responses of polyploid species studied by a new bioinformatic workflow HomeoRoq 28.05.2015 Nara, Japan Shimizu Kentaro;
Kyoto–Zurich Plant Workshop “Analyzing Plants in Complex Environments” Talk given at a conference Adaptation of allopolyploid species to new habitats 23.12.2014 Kyoto, Japan Shimizu Kentaro;
Kyoto–Zurich Plant Workshop “Analyzing Plants in Complex Environments” Talk given at a conference Ecological genomics of the polyploid Arabidopsis kamchatica and tropical trees 22.12.2014 Kyoto, Japan Shimizu Kentaro;
5th NIBB-MPIPZ-TLL Symposium, Horizons in Plant Biology Talk given at a conference Breeding systems of diploid and polyploidy Arabidopsis relatives 24.11.2014 Cologne, Germany Shimizu Kentaro;
Phenology Symposium, URPP Global Change and Biodiversity Talk given at a conference Phenology: from molecular biology and genomics to ecology and geography 24.10.2014 Zürich, Switzerland Shimizu Kentaro;
23rd International Conference on Sexual Plant Reproduction Talk given at a conference Evolutionary and genetic basis of reduced pollen number in the predominantly selfing species Arabidopsis thaliana 16.07.2014 Porto, Portugal Shimizu Kentaro;
14th HFSP Awardees Meeting Talk given at a conference Network merging analysis of duplicate genome function in recently hybridized species in Switzerland 08.07.2014 Lugano, Switzerland Shimizu Kentaro;
Evolution 2014 Talk given at a conference Male-driven evolution of self-compatibility in diploid and polyploid Arabidopsis 22.06.2014 Raleigh, United States of America Shimizu Kentaro;
Society for Molecular Biology and Evolution Talk given at a conference Non-stochastic homeolog-specific gene regulation and the evolution of self-compatibility in the allopolyploid Arabidopsis kamchatica 10.06.2014 Puerto Rico, Puerto Rico Shimizu Kentaro;
International symposium of Adaptomics "Genome-enabled approaches towards molecular functions in ecology and evolution" Talk given at a conference Transcriptome and the evolution of self-compatibility of Arabidopsis kamchatica, the allopolyploid derived from A. lyrata and A. halleri 31.03.2014 Bad-Neuenahr, Germany Shimizu Kentaro;
Workshop on a basic plant science Talk given at a conference Evolution of selfing in Arabidopsis 21.03.2014 Toyama, Japan Shimizu Kentaro;
Japan Society for Plant Physiologists Talk given at a conference The evolution of selfing in Arabidopsis: integrating molecular genetics and evolutionary biology 19.03.2014 Toyama, Japan Shimizu Kentaro;
Ecology Society Talk given at a conference Discovery of androdioecy in an Arabidopsis relative Cardamine amara 18.03.2014 Hiroshima, Japan Shimizu Kentaro;
Disease, immunity and ancient DNA: How interdisciplinary research reveals the evolution of human health and environmental adaptation Talk given at a conference Evolutionary genomics of mating systems 17.02.2014 Zürich, Switzerland Shimizu Kentaro;
Illumina Day, Advances in Genome Science Talk given at a conference Nonstochastic gene regulation in synthetic allopolyploid Arabidopsis kamchatica studied by HomeoRoq 11.02.2014 Zürich, Switzerland Shimizu Kentaro;
Swiss Plant Science Web Talk given at a conference Genome-wide quantification of homeolog expression ratio revealed non-stochastic gene regulation in synthetic allopolyploid Arabidopsis kamchatica 29.01.2014 Meringen, Switzerland Shimizu Kentaro;
Plant & Animal Genome XXII Talk given at a conference Ecological Transcriptome with Meteorological Data: Synchronous Flowering of Dipterocarps in Tropical Forests Triggered By Drought 12.01.2014 San Diego, United States of America Shimizu Kentaro;
The 36th Annual Meeting of the Molecular Biology Society of Japan Talk given at a conference General patterns in the evolution of selfing: combining molecular genetics and computer simulation 04.12.2013 Kobe, Japan Shimizu Kentaro;
Mini-symposium Mating system transitions and their implications for evolution Talk given at a conference Emergent androdioecy in Swiss populations of Cardamine amara (Brassicaceae) 10.10.2013 Konstanz, Germany Tedder Andrew;
Mini-symposium Mating system transitions and their implications for evolution Talk given at a conference Recurrent patterns in the evolution of self-compatibility in diploid and polyploid Arabidopsis 10.10.2013 Konstanz, Germany Shimizu Kentaro;
Current Opinion conference "Plant genome and evolution" Talk given at a conference Genome-wide quantification of homeolog expression ratio revealed non-stochastic gene regulation in synthetic allopolyploid Arabidopsis 09.09.2013 Amsterdam, Netherlands Shimizu Kentaro;
Retreat of URPP Evolution in Action Talk given at a conference Polyploid speciation and breeding systems in Arabidopsis relatives 09.07.2013 Switzerland, Switzerland Shimizu Kentaro;
Evolution meeting Talk given at a conference Genome-wide quantification of homeolog expression ratio in allopolyploid Arabidopsis revealed non-stochastic gene regulation 23.06.2013 Snowbird, Utah, United States of America Shimizu Kentaro;
Gregor Mendel Instiute Individual talk Ecological genomics and transcriptomics of polyploid Arabidopsis relatives and of tropical trees 10.06.2013 Wienna, Austria Shimizu Kentaro;
Arabis meeting, WSL Talk given at a conference Mating system variation and sporophytic self-incompatibility in European Arabis alpina 17.04.2013 Birmensdorf, Switzerland Tedder Andrew;
Symposium on Arabidopsis natural accessions and related species, The 54th Annual Meeting of the Japanese Society of Plant Physiologists Talk given at a conference Recurrent patterns in the adaptation and speciation in Arabidopsis relatives 22.03.2013 Okyama, Japan Shimizu Kentaro;
The pre-SOL2012 Symposium in Plant Evolutionary Biology: “Spencer Barrett et al. in Zurich” Talk given at a conference Evolution of selfing in diploid and polyploid Arabidopsis 31.01.2013 Zurich, Switzerland, Switzerland Shimizu Kentaro;
SWISSPLANT'13 meeting Talk given at a conference Ecological transcriptome in natura: flowering genes of the perennial Arabidopsis halleri and the tropical tree Shorea beccariana 31.01.2013 Switzerland, Switzerland Shimizu Kentaro;
The 35th Annual Meeting of the Molecular Biology Society of Japan, Fukuoka, Japan Talk given at a conference Recurrent patterns in the evolution of selfing and polyploid speciation in Arabidopsis relatives 11.12.2012 Fukuoka, Japan, Japan Shimizu Kentaro;
Human Frontier Science Program Luncheon seminar at the 35th Annual Meeting of the Molecular Biology Society of Japan Talk given at a conference Polyploid speciation and adaptive evolution studied by next-generation sequencing 11.12.2012 Fukuoka, Japan, Japan Shimizu Kentaro;
International symposium "Arabidopsis and Emerging Model Systems" Talk given at a conference Polyploid model species of Arabidopsis and Cardamine: recurrent patterns in the evolution of selfing and polyploid speciation 19.11.2012 Okazaki, Japan, Japan Shimizu Kentaro;
International Symposium on the Mechanisms of Sexual Reproduction in Animals and Plants, Joint Meeting of the 2nd Allo-authentication Meeting and the 5th Egg-Coat Meeting (MCBEEC) Talk given at a conference Recurrent patterns in the evolution of plant breeding systems 14.11.2012 Japan, Japan Shimizu Kentaro;
The 13th Swiss-Japanese-Conference on Biotechnology and Bioprocess Engineering 2012 Talk given at a conference Next-generation sequencing for evolutionary genomics of model and non-model species 04.11.2012 Walzenhausen, Switzerland, Switzerland Shimizu Kentaro;
5th URPP Systems Biology and Functional Genomics Meeting, Brunnen Talk given at a conference Evolutionary and ecological genomics for Arabidopsis relatives and non-model species 14.09.2012 Brunnen, Switzerland, Switzerland Shimizu Kentaro;
Evolution 2012 Talk given at a conference Recurrent patterns in the evolution of predominant selfing in Arabidopsis relatives 08.07.2012 Ottawa, Canada, Canada Shimizu Kentaro;
Joining Forces Symposium: Next Generation Sequencing Talk given at a conference Ecological transcriptome and SNP analysis: from model to non-model species 22.06.2012 ETHZ, Zurich, Switzerland, Switzerland Shimizu Kentaro;


Knowledge transfer events

Active participation

Title Type of contribution Date Place Persons involved
Scientifica Workshop 30.08.2013 Zürich, Switzerland Shimizu Kentaro;


Self-organised

Title Date Place
Guided tour of the laboratory and research garden for elementary school children 14.04.2015 Institute of Evolutionary Biology and Environmental Studies, UZH, Switzerland
Tour at zoological museum for children of Japanese School 12.11.2014 Zoological Museum, UZH, Switzerland
Guided tour of the laboratory and botanical garden for children of Japanese primary and middle school 09.07.2013 Botanical Garden and Institute, UZH, Switzerland
Guidance of laboratory and botanical garden for children of Japanese primary and middle schools at U 11.06.2012 Botanical Garden and Institute, UZH, Switzerland

Communication with the public

Communication Title Media Place Year
Media relations: print media, online media "Series Visiting laboratories: Prof. Kentaro Shimizu, Evolutionary and Ecological Genomics, UZH National Geographic Web International 2015
Media relations: print media, online media Ausgeklügeltes System St. Galler Tagblatt German-speaking Switzerland 2015
Other activities Guided tour of the laboratory and research garden for elementary school children International 2015
Media relations: print media, online media Petunie umgeht Selbstbefruchtung mit ausgeklugeltem System SDA / Schweizerische Depeschenagentur German-speaking Switzerland 2015
Media relations: print media, online media Sophisticated system prevents self-fertilization in petunias UZH Mediadesk German-speaking Switzerland International 2015
Other activities Tour at zoological museum for children of Japanese School International 2014
Talks/events/exhibitions Scientifica 2013 German-speaking Switzerland 2013
Other activities Guidance of laboratory and botanical garden for children of Japanese primary and middle schools at U International 2012
Other activities Guided tour of the laboratory and botanical garden for children of Japanese primary and middle schoo International 2012

Associated projects

Number Title Start Funding scheme
127155 Adaptive genetic variation and plant adaptation to environmental heterogeneity (AVE) 01.04.2010 Sinergia
135717 Evolution of breeding systems and phenology: evolutionary genomic analysis using Arabidopsis relatives 01.04.2011 Project funding
158542 PSC Discovery Program for Youth 01.04.2015 Agora
159767 Breeding systems and germline development - evolutionary genomic analysis using Arabidopsis relatives 01.06.2015 Project funding

Abstract

A central question in biology is the molecular basis of biodiversity. Rapid advances in next-generation sequencing are providing novel tools for addressing key ecological and evolutionary questions in integrated biological sciences. However, the study of adaptive molecular variation has been largely limited to model species. Therefore, general patterns in molecular adaptation and speciation remain unclear, but their discovery is essential to enable understanding and prediction of biological responses to naturally and artificially changing environments. Studying adaptive evolution that occurred many times in parallel is an appropriate approach to investigating recurring patterns.Since our precursor projects (2008-2011, 2011-2012), we have studied the evolution of selfing in Arabidopsis thaliana, and polyploid speciation of A. kamchatica and Cardamine spp. This proposal represents an extension of these earlier projects, and focuses on the evolution of selfing through loss of self-incompatibility (which is considered one of the most frequent evolutionary shifts in flowering plants) and its relationship to speciation by genome duplication. We address the following questions regarding general patterns in the evolution of selfing.Q1. Were mutations in the same genes responsible for the evolution of selfing in different species? In particular, were mutations in the male component of self-incompatibility spread frequently, as predicted by evolutionary theory?Q2. Which type of mutations (regulatory, amino-acid-changing or loss-of-function) contributed to the evolution of selfing?Q3. Are major- or minor-effect mutations more prevalent?Q4. Are dominant, recessive or co-dominant mutations the most prevalent?Q5. Did the evolution of self-compatibility occur recurrently during a particular geological period (the recent glacial-interglacial cycle)?Q6. Does genome duplication or polyploid speciation affect the processes noted above? More specifically, is the epistatic interaction between duplicated loci relevant in the evolution of self-incompatibility genes and other genes?Based on preliminary results, the research plan is divided into four parts. First, we will conduct functional studies of the evolution of self-compatibility in the allopolyploid A. kamchatica. Second, genome-wide polymorphisms in A. kamchatica will be assayed to assess the evolutionary forces and epistatic interactions underlying self-compatibility and other traits. Third, using these data, we will conduct genome-wide association studies (GWASs) in A. thaliana and A. kamchatica to investigate the coordinated sets of floral traits of selfing species, referred to as “selfing syndrome”. Fourth, we will investigate the evolution of self-compatibility in the autopolyploid species Cardamine amara subsp. austriaca.It is noteworthy that plant sexual reproduction may be particularly vulnerable to the effects of natural and artificial environmental changes, through evolutionary and plastic responses. A broad impact of this proposal to the society would be to reinforce our previous key research finding that climate change, including glacial cycles, may induce rapid-and possibly irreversible-evolution.
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