A novel cis-element enabled bacterial uptake by plant cells
Chloé Cathebras, Xiaoyun Gong, Rosa Elena Andrade, Ksenia Vondenhoff, J. Keller, Pierre‐Marc Delaux, Makoto Hayashi, Maximilian Griesmann, Martin Parniske
Abstract
The root nodule symbiosis of plants with nitrogen-fixing bacteria is phylogenetically restricted to a single clade of flowering plants, which calls for as yet unidentified trait acquisitions and genetic changes in the last common ancestor. Here we discovered-within the promoter of the transcription factor gene Nodule Inception (NIN)-a cis-regulatory element (PACE), exclusively present in members of this clade. PACE was essential for restoring infection threads in nin mutants of the legume Lotus japonicus. PACE sequence variants from root nodule symbiosis-competent species appeared functionally equivalent. Evolutionary loss or mutation of PACE is associated with loss of this symbiosis. During the early stages of nodule development, PACE dictates gene expression in a spatially restricted domain containing cortical cells carrying infection threads. Consistent with its expression domain, PACE-driven NIN expression restored the formation of cortical infection threads, also when engineered into the NIN promoter of tomato. Our data pinpoint PACE as a key evolutionary invention that connected NIN to a pre-existing symbiosis signal transduction cascade that governs the intracellular accommodation of arbuscular mycorrhiza fungi and is conserved throughout land plants. This connection enabled bacterial uptake into plant cells via intracellular support structures such as infection threads, a unique and unifying feature of this symbiosis.