Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses
| Autor: | M. Eric Schranz, Luuk Rutten, Rimi Repin, J.G.J. Hontelez, Elio Schijlen, Wei Liu, Defeng Shen, Robin van Velzen, Kana Miyata, Luca Santuari, Fengjiao Bu, Arjan van Zeijl, Sandra Smit, Trupti Sharma, Renze Heidstra, Rens Holmer, Yuda Purwana Roswanjaya, Titis A. K. Wardhani, Wouter Kohlen, J. Verver, René Geurts, Menno Schilthuizen, Marijke Hartog, Qingqin Cao, Ton Bisseling, Berivan Gungor, Joelle Jansen, Wei-Cai Yang, Johan van den Hoogen, Maryam Seifi Kalhor, Elena Fedorova |
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| Rok vydání: | 2018 |
| Předmět: |
0106 biological sciences
0301 basic medicine Frankia Plant Developmental Biology Plant Biology Sequence Homology comparative genomics Plant Root Nodulation 01 natural sciences Nod factor Phylogeny Plant Proteins Genetics Multidisciplinary biology copy number variation food and beverages Fabaceae Genomics Biological Sciences Biological Evolution Biosystematiek symbiosis Medicago truncatula Phenotype PNAS Plus Nitrogen fixation Rhizobium Laboratory of Molecular Biology Root Nodules Plant Bioinformatics Evolution Nitrogen Rhizobia BIOS Applied Bioinformatics 03 medical and health sciences Symbiosis Nitrogen Fixation Bioinformatica evolution Laboratorium voor Moleculaire Biologie Amino Acid Sequence Comparative genomics Copy number variation fungi Biological nitrogen fixation biological nitrogen fixation 15. Life on land biology.organism_classification Laboratorium voor Phytopathologie 030104 developmental biology Laboratory of Phytopathology Biosystematics EPS 010606 plant biology & botany |
| Zdroj: | Proceedings of the National Academy of Sciences of the United States of America Proceedings of the National Academy of Sciences of the United States of America 115 (2018) 20 Proceedings of the National Academy of Sciences of the United States of America, 115(20), E4700-E4709 |
| ISSN: | 1091-6490 0027-8424 |
| Popis: | Significance Fixed nitrogen is essential for plant growth. Some plants, such as legumes, can host nitrogen-fixing bacteria within cells in root organs called nodules. Nodules are considered to have evolved in parallel in different lineages, but the genetic changes underlying this evolution remain unknown. Based on gene expression in the nitrogen-fixing nonlegume Parasponia andersonii and the legume Medicago truncatula, we find that nodules in these different lineages may share a single origin. Comparison of the genomes of Parasponia with those of related nonnodulating plants reveals evidence of parallel loss of genes that, in legumes, are essential for nodulation. Taken together, this raises the possibility that nodulation originated only once and was subsequently lost in many descendant lineages. Nodules harboring nitrogen-fixing rhizobia are a well-known trait of legumes, but nodules also occur in other plant lineages, with rhizobia or the actinomycete Frankia as microsymbiont. It is generally assumed that nodulation evolved independently multiple times. However, molecular-genetic support for this hypothesis is lacking, as the genetic changes underlying nodule evolution remain elusive. We conducted genetic and comparative genomics studies by using Parasponia species (Cannabaceae), the only nonlegumes that can establish nitrogen-fixing nodules with rhizobium. Intergeneric crosses between Parasponia andersonii and its nonnodulating relative Trema tomentosa demonstrated that nodule organogenesis, but not intracellular infection, is a dominant genetic trait. Comparative transcriptomics of P. andersonii and the legume Medicago truncatula revealed utilization of at least 290 orthologous symbiosis genes in nodules. Among these are key genes that, in legumes, are essential for nodulation, including NODULE INCEPTION (NIN) and RHIZOBIUM-DIRECTED POLAR GROWTH (RPG). Comparative analysis of genomes from three Parasponia species and related nonnodulating plant species show evidence of parallel loss in nonnodulating species of putative orthologs of NIN, RPG, and NOD FACTOR PERCEPTION. Parallel loss of these symbiosis genes indicates that these nonnodulating lineages lost the potential to nodulate. Taken together, our results challenge the view that nodulation evolved in parallel and raises the possibility that nodulation originated ∼100 Mya in a common ancestor of all nodulating plant species, but was subsequently lost in many descendant lineages. This will have profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants. |
| Databáze: | OpenAIRE |
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