Abstract
Summary ●Nitrogen‐fixing nodulation occurs in 10 taxonomic lineages, with either rhizobia or Frankia bacteria. To establish such an endosymbiosis, two processes are essential: nodule organogenesis and intracellular bacterial infection. In the legume–rhizobium endosymbiosis, both processes are guarded by the transcription factor NODULE INCEPTION (NIN) and its downstream target genes of the NUCLEAR FACTOR Y (NF‐Y) complex.●It is hypothesized that nodulation has a single evolutionary origin c. 110 Ma, followed by many independent losses. Despite a significant body of knowledge of the legume–rhizobium symbiosis, it remains elusive which signalling modules are shared between nodulating species in different taxonomic clades. We used Parasponia andersonii to investigate the role of NIN and NF‐YA genes in rhizobium nodulation in a nonlegume system.●Consistent with legumes, P. andersonii PanNIN and PanNF‐YA1 are coexpressed in nodules. By analyzing single, double and higher‐order CRISPR‐Cas9 knockout mutants, we show that nodule organogenesis and early symbiotic expression of PanNF‐YA1 are PanNIN‐dependent and that PanNF‐YA1 is specifically required for intracellular rhizobium infection.●This demonstrates that NIN and NF‐YA1 have conserved symbiotic functions. As Parasponia and legumes diverged soon after the birth of the nodulation trait, we argue that NIN and NF‐YA1 represent core transcriptional regulators in this symbiosis.
Highlights
To cope with N limitation, some plant species engage with N2-fixing rhizobium or Frankia bacteria
By creating a series of CRISPR-Cas9 knockout mutants, we provide evidence that PanNIN is essential for nodule initiation in the nonlegume P. andersonii
We show that PanNF-YA1 is required for intracellular rhizobium infection, whereas nodule organogenesis is controlled by a genetically redundant network of NF-YA genes
Summary
Nitrogen (N) is an essential element for plant growth. To cope with N limitation, some plant species engage with N2-fixing rhizobium or Frankia bacteria. Plant species capable of forming N2-fixing nodules all belong to one of the four orders, Fabales, Fagales, Cucurbitales and Rosales, that together form the so-called N-fixing clade (Soltis et al, 1995; Doyle, 2011). Within this clade, nodulation is limited to 10 lineages, of which eight nodulate with Frankia and two with rhizobia (Geurts et al, 2012). The current hypothesis is that this scattered distribution originates from a single evolutionary gain of nodulation in the ancestor to the N2-fixing clade, and subsequent loss of this trait in many descending species (Griesmann et al, 2018; van Velzen et al, 2018, 2019). Such a scenario implies that the nodulation trait in all 10 lineages is based on conserved genetic networks
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