Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses

Abstract

SignificanceFixed 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.

Mutant analysis in the nonlegume Parasponia andersonii identifies NIN and NF‐YA1 transcription factors as a core genetic network in nitrogen‐fixing nodule symbioses

“…Furthermore, it was shown that, in L. japonicus , ectopic expression of LjNF‐YA1 results in lateral roots with malformed tips (Soyano et al ., ; Sorin et al ., ) We observed a mild, though consistent, decrease in lateral roots formed in plantlets containing a mutation in Pannf‐ya1 . This supports the findings that NF‐YA1 orthologous genes have a nonsymbiotic function in root development, and may explain why NF‐YA1 is not pseudogenized in species that have lost the nodulation trait (Soyano et al ., ; Griesmann et al ., ; van Velzen et al ., ). As the P. andersonii nf‐ya1 knockout mutants are not affected in the symbiosis with arbuscular mycorrhiza, it suggests that NF‐YA1 symbiotic functioning is exclusively required to allow entry of symbiotic bacteria.…”

“…Protein sequences of L. japonicus (Lj3.0, Lotus Base (REF; Mun et al ., ); Sato et al ., ), Glycine max (Wm82.a2.v1; Sato et al ., ; Schmutz et al ., ), Phaseolus vulgaris (Pvulgaris v.2.1; Schmutz et al ., ), Morus notabilis (Genbank ATGF00000000.1; He et al ., ), Prunus persica (Ppersica v.2.1; International Peach Genome Initiative et al ., ) Fragaria vesca (Fvesca v.1.1; Shulaev et al ., ) were retrieved from P hytozome 12 (http://phytozome.jgi.doe.gov/), unless stated otherwise. Casuarina glauca and Datisca glomerata assemblies were downloaded and set up as custom B last database in Geneious 8.1.9 (Griesmann et al ., ; van Velzen et al ., ). Sequences from diploid Peanut Arachis duranensis were retrieved from NCBI (Bertioli et al ., ).…”

“…All experiments were done using P. andersonii WU1.14 (van Velzen et al, 2018;Wardhani et al, 2019). Plants were maintained as described previously Wardhani et al, 2019).…”

“…We aimed to use Parasponia to investigate the extent to which NIN and NF‐YA transcriptional regulators have conserved functions in root nodule formation. Previous studies have shown that NIN and NF‐YA1 are transcriptionally induced in Parasponia andersonii nodules (van Velzen et al ., ). By creating a series of CRISPR‐Cas9 knockout mutants, we provide evidence that PanNIN is essential for nodule initiation in the nonlegume P. andersonii .…”

“…NIN belongs to a small family of NIN-Like proteins (NLPs), of which, in Arabidopsis thaliana, several members are involved in nitrate signalling (Schauser et al, 2005;Castaings et al, 2009;Konishi & Yanagisawa, 2013). Orthologues of NIN are found across eudicots, but within the N-fixation clade functional copies of this gene have been repeatedly lost from the genomes of nonnodulating species (Griesmann et al, 2018;van Velzen et al, 2018). This suggests that within the N 2 -fixation clade, NIN predominantly performs a nodulation-specific function.…”