A Sinorhizobium meliloti-specific N-acyl homoserine lactone quorum-sensing signal increases nodule numbers in Medicago truncatula independent of autoregulation

Abstract

N-acyl homoserine lactones (AHLs) act as quorum sensing signals that regulate cell-density dependent behaviors in many gram-negative bacteria, in particular those important for plant-microbe interactions. AHLs can also be recognized by plants, and this may influence their interactions with bacteria. Here we tested whether the exposure to AHLs affects the nodule-forming symbiosis between legume hosts and rhizobia. We treated roots of the model legume, Medicago truncatula, with a range of AHLs either from its specific symbiont, Sinorhizobium meliloti, or from the potential pathogens, Pseudomonas aeruginosa and Agrobacterium vitis. We found increased numbers of nodules formed on root systems treated with the S. meliloti-specific AHL, 3-oxo-C14-homoserine lactone, at a concentration of 1 μM, while the other AHLs did not result in significant changes to nodule numbers. We did not find any evidence for altered nodule invasion by the rhizobia. Quantification of flavonoids that could act as nod gene inducers in S. meliloti did not show any correlation with increased nodule numbers. The effects of AHLs were specific for an increase in nodule numbers, but not lateral root numbers or root length. Increased nodule numbers following 3-oxo-C14-homoserine lactone treatment were under control of autoregulation of nodulation and were still observed in the autoregulation mutant, sunn4 (super numeric nodules4). However, increases in nodule numbers by 3-oxo-C14-homoserine lactone were not found in the ethylene-insensitive sickle mutant. A comparison between M. truncatula with M. sativa (alfalfa) and Trifolium repens (white clover) showed that the observed effects of AHLs on nodule numbers were specific to M. truncatula, despite M. sativa nodulating with the same symbiont. We conclude that plant perception of the S. meliloti-specific 3-oxo-C14-homoserine lactone influences nodule numbers in M. truncatula via an ethylene-dependent, but autoregulation-independent mechanism.

Effect of the plant flavonoid luteolin on Ensifer meliloti 3001 phenotypic responses

“…In fact, data obtained in this work suggest that the effect of the host flavonoid on the rhizobium depends on nutritional conditions. Indeed, in Pseudomonas aeruginosa, the flavanone naringenin reduces AHL production (Vandeputte et al 2011), AHL production has been shown to be related to nodule number control in Medicago truncatula (Veliz-vallejos et al 2014), and the mutant of sinI gene (encoding the AHL synthase) has delayed nodule formation (Gao et al 2003).…”

“…AHLs in turn trigger specific responses in the host to positively influence nodule numbers (Veliz-Vallejos et al 2014). E. meliloti, a Gram-negative nitrogen-fixing proteobacterium that is distributed worldwide in temperate soils both in free-living and symbiotic form, is considered a model bacterium for legume-rhizobium symbiosis (McIntosh et al 2009).…”

Defining plant growth promoting rhizobacteria molecular and biochemical networks in beneficial plant-microbe interactions

“…Joseph and Phillips (2003) observed a significant increase of stomatal conductance and transpiration in Phaseolus vulgaris L. (bean) when 10 nM AHL was applied to the roots (Joseph and Phillips 2003). In the legume M. truncatula, an increase in nodule number was found when S. meliloti-specific 3-oxo-C14-HL was applied to the roots (Veliz-Vallejos et al 2014). Specific plant responses were demonstrated in the landmark work by Mathesius et al (2003), who generated thorough protein expression data from M. truncatula exposed to AHL from its symbiont S. meliloti (3-oxo-C16:1-HL) and from the plant pathogen P. aeruginosa (3-oxo-C12-HL).…”

Effective Colonization of Spinach Root Surface by Rhizobium

“…Yuan et al (2015) described how organic acids from banana roots exudates could attract a beneficial strain of Bacillus amyloliquefaciens and promote its biofilm formation. Veliz-Vallejos et al (2014) observed an increase in nodule number in Medicago truncatula under the impact of 3-oxo-C14-HSL, an N-acyl-homoserine lactone (the major group of quorum-sensing signal molecules in gram-negative bacteria) produced by Ensifer meliloti. Xie et al (2014) described the effects of different concentrations of spermidine and implicated a promotion of tobacco plant growth with an optimum concentration of exogenous spermidine.…”