Abstract
In the Medicago truncatula-Sinorhizobium meliloti symbiosis, chemical signaling initiates rhizobial infection of root nodule tissue, where a large portion of the bacteria are endocytosed into root nodule cells to function in nitrogen-fixing organelles. These intracellular bacteria are subjected to an arsenal of plant-derived nodule-specific cysteine-rich (NCR) peptides, which induce the physiological changes that accompany nitrogen fixation. NCR peptides drive these intracellular bacteria toward terminal differentiation. The bacterial peptidase HrrP was previously shown to degrade host-derived NCR peptides and give the bacterial symbionts greater fitness at the expense of host fitness. The hrrP gene is found in roughly 10% of Sinorhizobium isolates, as it is carried on an accessory plasmid. The objective of the present study is to identify peptidase genes in the core genome of S. meliloti that modulate symbiotic outcome in a manner similar to the accessory hrrP gene. In an overexpression screen of annotated peptidase genes, we identified one such symbiosis-associated peptidase (sap) gene, sapA (SMc00451). When overexpressed, sapA leads to a significant decrease in plant fitness. Its promoter is active in root nodules, with only weak expression evident under free-living conditions. The SapA enzyme can degrade a broad range of NCR peptides in vitro.
Highlights
In the Medicago truncatula-Sinorhizobium meliloti symbiosis, chemical signaling initiates rhizobial infection of root nodule tissue, where a large portion of the bacteria are endocytosed into root nodule cells to function in nitrogen-fixing organelles
In the Sinorhizobium meliloti – Medicago truncatula symbiosis, production of the bacterial EPS succinoglycan enables the development of infection threads within root hairs, allowing the rhizobia to colonize plant tissue[11,12]
Using the online S. meliloti 1021 genome and MEROPS peptidase databases, we identified 131 putative peptidase candidates that could be screened for effects on symbiosis
Summary
In the Medicago truncatula-Sinorhizobium meliloti symbiosis, chemical signaling initiates rhizobial infection of root nodule tissue, where a large portion of the bacteria are endocytosed into root nodule cells to function in nitrogen-fixing organelles. These intracellular bacteria are subjected to an arsenal of plant-derived nodule-specific cysteine-rich (NCR) peptides, which induce the physiological changes that accompany nitrogen fixation. While interkingdom signaling molecules play critical roles during bacterial entry and early nodule development, it has become clear that symbiotic communication is occurring around the time that nitrogen fixation commences This is evidenced by studies in which random pairings of symbiotically competent Medicago hosts and Sinorhizobium strains often give rise to infected nodules that do not fix n itrogen[15,16,17,18]. Considering that an ensemble of cooperating peptidases may make identification difficult by loss-of-function genetic analysis, we employed a plasmid-based overexpression screen focused on gene candidates that most likely encode peptide-hydrolyzing enzymes
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