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RESEARCH ◥ RESULTS: We sequenced the genomes of sev- RESEARCH ARTICLE SUMMARY en nodulating species belonging to the Fagales, Rosales, and Cucurbitales orders and the legume subfamily Caesalpinioideae. We complemented PLANT SCIENCE this dataset by sequencing three genomes of non- nodulating species from the Cucurbitales and from the legume subfamilies Cercidoideae and Phylogenomics reveals multiple losses Papilionoideae. Using a genome-wide phyloge- nomic approach, we found that all legume genes of nitrogen-fixing root nodule symbiosis ◥ with a characterized role ON OUR WEBSITE in NFN symbiosis are con- Maximilian Griesmann, Yue Chang, Xin Liu, Yue Song, Georg Haberer, Read the full article served in nodulating spe- Matthew B. Crook, Benjamin Billault-Penneteau, Dominique Lauressergues, at http://dx.doi. cies with one exception. We Jean Keller, Leandro Imanishi, Yuda Purwana Roswanjaya, Wouter Kohlen, org/10.1126/ observed larger numbers Petar Pujic, Kai Battenberg, Nicole Alloisio, Yuhu Liang, Henk Hilhorst, science.aat1743 of order-specific gene fam- .................................................. Marco G. Salgado, Valerie Hocher, Hassen Gherbi, Sergio Svistoonoff, Jeff J. Doyle, ily expansions that, solely Shixu He, Yan Xu, Shanyun Xu, Jing Qu, Qiang Gao, Xiaodong Fang, Yuan Fu, because of their phylogenetic distribution, may Philippe Normand, Alison M. Berry, Luis G. Wall, Jean-Michel Ané, include genes contributing to multiple gains or Katharina Pawlowski, Xun Xu, Huanming Yang, Manuel Spannagl, Klaus F. X. Mayer, subsequent refinements of the symbiosis. In Gane Ka-Shu Wong, Martin Parniske*, Pierre-Marc Delaux*, Shifeng Cheng* parallel, we discovered signatures of multiple independent loss-of-function events for the gene Downloaded from INTRODUCTION: Access to nutrients such as phyletic NFN clade. However, only 10 of the encoding the indispensable NFN symbiosis nitrogen is required for plant growth. Legumes 28 plant families within this clade contain regulator NODULE INCEPTION (NIN)in10of and nine additional plant families benefit from species engaged in the NFN symbiosis. Even 13 genomes of nonnodulating species within the nitrogen-fixing root nodule (NFN) symbio- within these 10 families, most genera do not the NFN clade. The pattern suggests at least sis, in which roots develop nodules that intra- form this symbiosis. The NFN symbiosis re- eight independent losses of NFN symbiosis. cellularly host nitrogen-fixing bacteria. In this quires the coordinated function of more than http://science.sciencemag.org/ CONCLUSION: We found that multiple inde- mutually beneficial symbiosis, the bacteria con- 30 essential genes. Presence of this symbiosis pendent losses of NFN symbiosis occurred in vert atmospheric nitrogen into ammonium and in related families suggests that a genetic change the four orders of the NFN clade. These results deliver it to the host plant. NFN symbiosis thus in the ancestor of the NFN clade enabled evo- suggest that NFN symbiosis has previously been enables plant survival under nitrogen-limiting lution of NFN symbiosis in this clade. The more common than currently evident and that conditions in terrestrial ecosystems. In agricul- scattered distribution of functional NFN sym- this symbiosis is subject to an underestimated ture, this symbiosis reduces reliance on nitro- biosis across the clade has led to the question adverse selection pressure. gen fertilizer, thus reducing the costs, ecological of whether NFN symbiosis evolved multiple ▪ impact, and fossil fuel consumption attendant times independently in a convergent manner on large-scale application of fertilizers. or was lost multiple times regardless of the number of times it arose. Fossil data have The list of author affiliations is available in the full article online. on July 13, 2018 RATIONALE: Molecular phylogenies show been unable to answer this question. Here *Corresponding author. Email: [email protected] (S.C.); that NFN symbiosis is restricted to four angio- we used molecular evidence to ask how the [email protected] (P.-M.D.); [email protected] — (M.P.) sperm orders Fabales, Fagales, Cucurbitales, current pattern of plant species with NFN sym- Cite this article as M. Griesmann et al., Science 361, eaat1743 and Rosales—that together form the mono- biosis evolved. (2018). DOI: 10.1126/science.aat1743 Phylogenomics and evolution of NFN symbiosis. Genome sequencing of nodulating and nonnodulating species combined with 27 previously available genomes resulted in a dataset spanning the NFN clade and species outside the NFN clade as an outgroup. Orthogroups were identified and filtered following three phylogenetic patterns.This genome-wide analysis identified two genes involved in NFN symbiosis, NIN and RHIZOBIUM-DIRECTED POLAR GROWTH (RPG), that were lost in most nonnodulating species. The occurrence of multiple losses (red crosses) of NFN symbiosis suggests an adverse selection pressure. Griesmann et al., Science 361, 144 (2018) 13 July 2018 1of1 RESEARCH ◥ that form nodules (referred to here as “nodulating RESEARCH ARTICLE species”) and these do not form a monophyletic group; moreover, within 9 of these 10 families, most genera do not form NFN symbiosis (7). In PLANT SCIENCE addition to this scattered distribution, a further unsolved mystery that surrounds the evolution of NFN symbiosis is its diversity at multiple levels: Phylogenomics reveals multiple Legumes (Fabales) and the nonlegume Parasponia (Rosales) (8) form nodules with rhizobia, whereas species of the actinobacterial genus Frankia in- losses of nitrogen-fixing root fect actinorhizal plants from eight plant families of the orders Fagales, Cucurbitales, and Rosales nodule symbiosis (9). A diversity of infection mechanisms has been described (9), and root nodule structures display Maximilian Griesmann1,2, Yue Chang3,4, Xin Liu3,4, Yue Song3,4, Georg Haberer2, wide variations (5, 7). The most parsimonious Matthew B. Crook5, Benjamin Billault-Penneteau1, Dominique Lauressergues6, hypothesis to explain the restricted and yet Jean Keller6, Leandro Imanishi7, Yuda Purwana Roswanjaya8, Wouter Kohlen8, scattered distribution pattern of such diverse Petar Pujic9, Kai Battenberg10, Nicole Alloisio9, Yuhu Liang3,4, Henk Hilhorst11, NFN symbioses predicted a genetic change in Marco G. Salgado12, Valerie Hocher13, Hassen Gherbi13, Sergio Svistoonoff 13, the ancestor of the NFN clade, a predisposition Jeff J. Doyle14, Shixu He3,4, Yan Xu3,4, Shanyun Xu3,4, Jing Qu3,4, Qiang Gao3,15, event, that enabled the subsequent independent Xiaodong Fang3,15, Yuan Fu3,4, Philippe Normand9, Alison M. Berry10, Luis G. Wall7, evolution of NFN symbiosis specifically and ex- Downloaded from Jean-Michel Ané16,17, Katharina Pawlowski12, Xun Xu3,4, Huanming Yang3,18, clusively in this clade (the multiple-origins hypo- 5 7 10–12 Manuel Spannagl2, Klaus F. X. Mayer2,19, Gane Ka-Shu Wong3,20,21, Martin Parniske1*, thesis), along with a number of losses ( , , ). Recent quantitative phylogenetic modeling studies Pierre-Marc Delaux6*, Shifeng Cheng3,4* supported scenarios with independent gains and switches between the nonnodulating and nod- The root nodule symbiosis of plants with nitrogen-fixing bacteria affects global nitrogen ulating states during the evolution of the NFN cycles and food production but is restricted to a subset of genera within a single clade of 11 13 clade ( , ). However, none of these analyses http://science.sciencemag.org/ flowering plants. To explore the genetic basis for this scattered occurrence, we sequenced provide direct evidence or the molecular causes the genomes of 10 plant species covering the diversity of nodule morphotypes, bacterial of the specific gains and losses that explain the symbionts, and infection strategies. In a genome-wide comparative analysis of a total of distribution of NFN symbiosis in extant genera. 37 plant species, we discovered signatures of multiple independent loss-of-function events Exploring the genetic basis underlying the in the indispensable symbiotic regulator NODULE INCEPTION in 10 of 13 genomes of evolutionary dynamics of the NFN symbiosis in nonnodulating species within this clade. The discovery that multiple independent losses plants will improve our understanding of the di- shaped the present-day distribution of nitrogen-fixing root nodule symbiosis in plants versity of symbiotic associations observed in ex- reveals a phylogenetically wider distribution in evolutionary history and a so-far-underestimated tant taxa and the ecosystems they inhabit and selection pressure against this symbiosis. potentially provide keys to engineer it in crops and to predict the stability of this trait over long itrogen is one of the main requirements survival under nitrogen-limiting conditions. In evolutionary times. Here we used a genome-wide on July 13, 2018 for plant growth. Members of the legume agriculture, this independence from chemical comparison including genomic and phylogenomic family (Fabaceae, order Fabales) and of nitrogen fertilizer reduces costs and fossil fuel methods (14) to address the long-standing con- N nine additional plant families benefit from consumption imposed by the Haber-Bosch pro- undrum of the evolution of NFN symbiosis and symbiosis with nitrogen-fixing bacteria, cess (2). Since the discovery of the NFN symbi- identify the underlying genetic players (15, 16). either phylogenetically diverse rhizobia or species osis, with rhizobia in 1888 and with Frankia in of the genus Frankia, which are hosted inside 1895 (3, 4),
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    A Homeotic Mutation Changes Legume Nodule Ontogeny into Actinorhizal-type Ontogeny. Item Type Article Authors Shen, Defeng; Xiao, Ting Ting; Velzen, Robin van; Kulikova, Olga; Gong, Xiaoyun; Geurts, Rene; Pawlowski, Katharina; Bisseling, Ton Citation Shen, D., Xiao, T. T., Velzen, R. van, Kulikova, O., Gong, X., Geurts, R., … Bisseling, T. (2020). A Homeotic Mutation Changes Legume Nodule Ontogeny into Actinorhizal-type Ontogeny. The Plant Cell, tpc.00739.2019. doi:10.1105/tpc.19.00739 Eprint version Post-print DOI 10.1105/tpc.19.00739 Publisher American Society of Plant Biologists (ASPB) Journal The Plant cell Rights Archived with thanks to The Plant cell Download date 27/09/2021 18:01:31 Link to Item http://hdl.handle.net/10754/662517 Plant Cell Advance Publication. Published on April 10, 2020, doi:10.1105/tpc.19.00739 RESEARCH ARTICLE A Homeotic Mutation Changes Legume Nodule Ontogeny into Actinorhizal-type Ontogeny Defeng Shen,a,1,2 Ting Ting Xiao,a,1,3 Robin van Velzen,a,b Olga Kulikova,a Xiaoyun Gong,c,4 René Geurts,a Katharina Pawlowski,c and Ton Bisselinga,5 aLaboratory of Molecular Biology, Wageningen University, Graduate School Experimental Plant Sciences, 6708 PB Wageningen, The Netherlands. bBiosystematics Group, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands. cDepartment of Ecology, Environment and Plant Sciences, Stockholm University, 106 91 Stockholm, Sweden. 1These authors contributed equally to this work. 2Present address: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany. 3Present address: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Sciences and Engineering (BESE), Thuwal, 23955-6900, Saudi Arabia.
  • Vol. 2 Cover. Fruits & Seeds

    Vol. 2 Cover. Fruits & Seeds

    Fruits and Seeds of United States Department of Genera in the Subfamily Agriculture Agricultural Faboideae (Fabaceae) Research Service Technical Bulletin Number 1890 Volume II December 2003 United States Department of Agriculture Fruits and Seeds of Agricultural Research Genera in the Subfamily Service Technical Bulletin Faboideae (Fabaceae) Number 1890 Volume II Joseph H. Kirkbride, Jr., Charles R. Gunn, and Anna L. Weitzman Fruits of A, Centrolobium paraense E.L.R. Tulasne. B, Laburnum anagyroides F.K. Medikus. C, Adesmia boronoides J.D. Hooker. D, Hippocrepis comosa, C. Linnaeus. E, Campylotropis macrocarpa (A.A. von Bunge) A. Rehder. F, Mucuna urens (C. Linnaeus) F.K. Medikus. G, Phaseolus polystachios (C. Linnaeus) N.L. Britton, E.E. Stern, & F. Poggenburg. H, Medicago orbicularis (C. Linnaeus) B. Bartalini. I, Riedeliella graciliflora H.A.T. Harms. J, Medicago arabica (C. Linnaeus) W. Hudson. Kirkbride is a research botanist, U.S. Department of Agriculture, Agricultural Research Service, Systematic Botany and Mycology Laboratory, BARC West Room 304, Building 011A, Beltsville, MD, 20705-2350 (email = [email protected]). Gunn is a botanist (retired) from Brevard, NC (email = [email protected]). Weitzman is a botanist with the Smithsonian Institution, Department of Botany, Washington, DC. Contents Volume I Procedures .................................................................................................................................................................................... 3 Fruit morphology .........................................................................................................................................................................