A novel cis-element enabled bacterial uptake by plant cells

Abstract

The root nodule symbiosis (RNS) of plants with nitrogen-fixing bacteria is phylogenetically restricted to a single clade of flowering plants, which calls for 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 (ITs) in nin mutants of the legume Lotus japonicus. PACE sequence variants from RNS-competent species appeared functionally equivalent. Evolutionary loss or mutation of PACE is associated with loss of this symbiosis. During early stages of nodule development, PACE dictates gene expression in a spatially restricted domain containing cortical cells carrying ITs. Consistent with its expression domain, PACE-driven NIN expression restored the formation of cortical ITs, 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 like ITs, a unique and unifying feature of this symbiosis.

Unravelling molecular mechanisms involved in resistance priming against downy mildew (Plasmopara viticola) in grapevine (Vitis vinifera L.)

“…In contrast to symbiotic interactions, such as nitrogen-fixing symbiosis or arbuscular mycorrhizal symbiosis, wherein molecular mechanisms are largely well conserved 66 , 67 , plant-pathogen interactions are more fluctuant by nature due to their arms race dynamics, and the identification of conserved pathways or responses is more difficult, with some exceptions. Due to the diverse data sources and experimental designs, as well as differing cultivar genetic backgrounds, identifying a common pathway is a challenging task.…”

Conservation of symbiotic signalling across 450 million years of plant evolution

“…The first of the four different cis- regulatory elements bound by phosphorylated CYCLOPS described so far 17–20 was identified in the promoter of NIN from the angiosperm Lotus japonicus . A fusion of this element to a GUS reporter (pCYC-RE:GUS) is activated during infection by rhizobial symbionts forming the root-nodule symbiosis in L. japonicus 17,21 and Medicago truncatula (Figure S1A). We hypothesized that this reporter could be directly activated by phosphorylated CYCLOPS irrespective of the symbiotic context, and not specifically during the root-nodule symbiosis.…”

Comparative phylotranscriptomics reveals a 110 million years-old symbiotic program

“…A role for the common symbiosis pathway in that process can be anticipated given its phylogenetic link with all the plant intracellular symbioses 66 , and the reverse genetic data obtained in diverse RNS-forming species 9 . The gain of a regulatory link between the common symbiosis pathway and the central RNS-regulator NIN at the base of the NFN clade represents one of the events, which have played a role in the transition from the non-NFN-forming to the NFN-forming state 67 . For millions of years, RNS has been maintained in diverse lineages of the Fagales, Fabales, Cucurbitales and Rosales with presumably very high rates of symbiosis loss.…”