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Outline Outline 1/25/2019 Overview of the Nitrogen-Fixing Clade: Examples of Angiosperms The Discovery of a Single Origin with Nitrogen-Fixing Symbioses of Predisposition Ceanothus Trevoa Datisca Douglas E. Soltis and Pamela S. Soltis J. Xiang Parasponia Myrica Comptonia Outline • Introduction – Families with nitrogen-fixing symbiosis via root nodules • Traditional view of relationships Alnus – Cronquist’s system Casuarina Coriaria – Implications for origin of nitrogen-fixing symbiosis • Angiosperms: early DNA sequence data – Nitrogen-fixing clade – Current view of relationships • Hypotheses: gains vs. losses Elaeagnus Shepherdia Purshia Angiosperm Families with Nodular Outline Nitrogen-Fixing Symbioses Prokaryote Angiosperm Family Nodulators/# Genera • Introduction – Families with nitrogen-fixing symbiosis via root nodules Rhizobiaceae Fabaceae 530/730 Cannabaceae 1/11 • Traditional view of relationships (Including ‘Celtidaceae’) – Cronquist’s system Frankia Betulaceae 1/6 Casuarinaceae 4/4 – Implications for origin of nitrogen-fixing symbiosis Elaeagnaceae 3/3 • Angiosperms: early DNA sequence data Myricaceae 2/3 Rhamnaceae 7/55 – Nitrogen-fixing clade Rosaceae 5/100 – Current view of relationships Datiscaeae 1/1 Coriariaceae 1/1 • Hypotheses: gains vs. losses 1 1/25/2019 Major Groups of Angiosperms Angiosperm Phylogeny: Chase et al. (1993) Cronquist (1981) Chloroplast gene Implications of Cronquist’s Classification sequence data (rbcL) suggest a single origin of the • Nitrogen-fixing families distantly related predisposition for • Multiple origins of nodular nitrogen-fixing symbiotic nitrogen symbioses fixation in • Agriculture: ‘easy’ to introduce the trait to non- angiosperms nodulating crops ~30,000 species Soltis et al. (1995) Outline Soltis et al. (1995) • Introduction • “These findings, furthermore, suggest a single – Families with nitrogen-fixing symbiosis via root nodules evolutionary origin of the underlying capacity • Traditional view of relationships for symbiotic nodular nitrogen fixation.” – Cronquist’s system • “…nodulating and non-nodulating members – Implications for origin of nitrogen-fixing symbiosis of this nitrogen-fixing clade should be • Angiosperms: early DNA sequence data examined to ascertain whether recurrent – Nitrogen-fixing clade losses or recurrent gains of nitrogen-fixing – Current view of relationships ability have occurred.” • Hypotheses: gains vs. losses 2 1/25/2019 Celastrales, Oxalidales, Malpighiales Myricaceae Juglandaceae Back to the Future Betulaceae Nitrogen-fixing Ticodendraceae Fagales Casuarinceae Clade: Fagaceae Nothofagaceae Cucurbitaceae Current View Tetramelaceae Begoniaceae Datiscaceae Cucurbitales Coriariaceae Corynocarpaceae Anisophylleaceae ~30,000 species Apodanthaceae Urticaceae Moraceae Cannabaceae Ulmaceae Rosales Dirachmaceae Rhamnaceae Elaeagnaceae Rosaceae Fabaceae Polygalaceae Fabales Surianaceae Quillajaceae Zygophyllaceae Zygophyllales Krameriaceae Malvids Angiosperm Phylogenetic Framework (2018) Outline • Introduction – Families with nitrogen-fixing symbiosis via root nodules • Traditional view of relationships – Cronquist’s system – Implications for origin of nitrogen-fixing symbiosis • Angiosperms: early DNA sequence data – Nitrogen-fixing clade – Current view of relationships • Hypotheses: gains vs. losses APG IV (2016) Modified from Sun et al. (2016) Soltis et al. (1995) • “These findings, furthermore, suggest a single evolutionary origin of the underlying capacity for symbiotic nodular nitrogen fixation.” • “…nodulating and non-nodulating members of this nitrogen-fixing clade should be examined to ascertain whether recurrent losses or recurrent gains of nitrogen-fixing ability have occurred.” 3 1/25/2019 Historical Perspectives: Historical Perspectives: Swensen (1996); Swensen & Mullin (1997) Swensen (1996); Swensen & Mullin (1997) • Both tree and traits: independent origins Following ‘predisposition’: • Repeated origins more parsimonious than loss • Evidence does not preclude the likelihood that symbiosis evolved via a combination of independent gains and multiple losses • Losses easier than repeated gains • Harder to establish symbioses outside clade • Easier to establish symbioses within clade Historical Perspectives: Werner et al. (2014) Swensen (1996) Actinorhizals ~3500 species Historical Perspectives: Werner et al. (2014): Swensen (1996) Number of Transitions Actinorhizals Transition Best phylogeny s.d. Median Gain of precursor 1.01 0.65 1.01 Loss of precursor 16.71 3.21 19.91 Symbiotic state Vesicle form Gain of fixing 8.15 2.47 6.60 Vesicle septa Loss of fixing 9.93 2.80 10.57 Vesicle location Location of infected cells Gain of stable fixing 24.53 4.79 20.17 Nodule gas diffusion Nodule [hemoglobin] Loss of stable fixing 0.19 4.99 2.02 Nodule roots Mode of infection Combination of gains and losses, deep ‘precursor’ 4 1/25/2019 Rhiz Gains and Losses . Werner et al. (2014): Summary Rosales of Nodulation • Single, cryptic evolutionary innovation Actinorhizals driving symbiotic N2-fixation evolution • Followed by multiple gains and losses of the Fagales symbiosis Multiple Gains • Subsequent emergence of ‘stable fixers’ Cucurbitales • ‘Deep homology’ in symbiotic N2-fixation Rhizobiaceae Fabales Rhiz Li et al. (2015) Gains and Losses . Rosales of Nodulation Multiple gains Actinorhizals Fagales Multiple Gains, Multiple Losses Cucurbitales Rhizobiaceae Fabales ~1000 genera MP, ML Rhiz Outgroups Rhiz Trema Nitrogen Fixing Symbiosis Parasponia Celtis Humulus . no Morus . actinorhizal Boehmeria Pilea rhizobial Zelkova Gains and Losses Ulmus Gains and Losses Rosales Shepherdia Rosales Elaeagnus Hippopha Barbeya R o Dirachma s a R Ceanothus l h e a Trevoa s of Nodulation m of Nodulation Colletia n a Discaria c e Zizyphus a Rhamnus e Photinia Kerria Neilla R Prunus o Actinorhizals Actinorhizals s Dryas a c Cercocarpus e a Cowania e Purshia Rosa Rubus Rhoiptelea Juglans Pterocarya Fagales Carya Fagales Alnus Betula Corylus F Ostrya a g Ticodendron a l Casuarina e Allocasuarina s Myrica Comptonia Trigonobalanus Multiple Gains Quercus Castanea Cucurbitales Fagus Cucurbitales Nothofagus Combretocarpus Cucumis Supported by MP & ML Marah C u Xerosicyos c Coriaria u r b Corynocarpus i t Datisca a l Reconstructions e Begonia s Hillebrandia Octomeles Tetrameles Pisum Tephrosia Glycine Rhizobiaceae Adesmia Rhizobiaceae Single Gain, Sophoria Acosmium Fabales Cladrastis Fabales Albizzia F a Erythrophleum b a c Tachigali F e a Many Losses a Cassia b e Caesalpinia a l Chamaechrista e Senna s Gymnocladus Ceratonia Macrolobium Brownea Bauhinia Cercis Polygala Securidaca Stylobasium Quillaja 5 1/25/2019 Genomic Studies: Repeated Loss Acknowledgments Biosystems Design Program Biological and Environmental Research (BER) Office of Science U.S. Department of Energy (grant #DE-SC0018247) How Many Gains and Losses??? • A single origin followed by losses? • Multiple gains? • ‘Deep homology’ – ‘Predisposition’ enables multiple gains – Allows multiple losses • Better, more deeply sampled phylogeny • Application of new methods that can better trace origins, losses, genotypes, phenotypes • Integration with genomic information Overview of Workshop • HR Kates: Global-Scale Phylogenomics of the Nitrogen-Fixing Clade • S Cheng: Pathway Discovery in Deep Convergence: Big Data in Phylogenomics for Nitrogen-Fixing Root Nodule Symbiosis • L Rutten: Comparative Analysis of Parasponia and Legumes Reveals Insight into the Evolution of Rhizobium LCO Signalling • JM Ané: Evolution by Gene Loss in Plant-Microbe Symbioses • A van Deynze: Nitrogen Fixation in a Landrace of Maize is supported by a Mucilage-Associated Diazotrophic Microbiota • M Kirst: Engineering Nitrogen-Fixing Symbiosis into Poplar 6.
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