Nitric oxide (NO): a key player in the senescence of Medicago truncatula root nodules

Abstract

SummaryNitric oxide (NO) is a signalling and defence molecule involved in diverse plant developmental processes, as well as in the plant response to pathogens. NO has also been detected at different steps of the symbiosis between legumes and rhizobia. NO is required for an optimal establishment of the Medicago truncatula-Sinorhizobium meliloti symbiotic interaction, but little is known about the role of NO in mature nodules. Here, we investigate the role of NO in the late steps of symbiosis.Genetic and pharmacological approaches were conducted to modulate the NO level inside root nodules, and their effects on nitrogen fixation and root nodule senescence were monitored.An increase in endogenous NO levels led to a decrease in nitrogen fixation and early nodule senescence, characterized by cytological modifications of the nodule structure and the early expression of a specific senescence marker. By contrast, a decrease in NO levels led to a delay in nodule senescence.Together, our results strongly suggest that NO is a signal in developmental as well as stressinduced nodule senescence. In addition, this work demonstrates the pivotal role of the bacterial NO detoxification response in the prevention of early nodule senescence, and hence the maintenance of efficient symbiosis.

An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser‐capture microdissection coupled to RNA sequencing

“…In addition, RNA-seq data revealed activation of some plant senescence marker genes in ZIII (cysteine proteinase genes, MtNAC969 TF; Van de Velde et al, 2006;de Zelicourt et al, 2012). Finally, many bacterial genes specifically controlled by the NO-responsive regulator NnrR (Meilhoc et al, 2010) were upregulated in ZIII, suggesting a local increase in the NO level, recently proposed to trigger nodule senescence (Cam et al, 2012).…”

SYMBIOTIC NODULE SENESCENCE IN LEGUMES: MOLECULAR-GENETIC AND CELLULAR ASPECTS (review)

“…In hmp mutant defective in flavogemoglobin biosynthesis, early senescence was observed with an increased amount of NO indicated in nodule tissues, while the hmp ++ strain with flavogemoglobin overexpression was characterized by slower senescence and decreased amount of NO in nodules. Endogenous NO also caused a premature senescence of nodules (25).…”

“…Recently, using the model legume plant M. truncatula, the regulation of aging in symbiotic nodule by nitrogen monoxide was revealed (25). Bacterial flavogemoglobin has been shown to play an important role in NO control in the nodules.…”

Control of NO level in rhizobium-legume root nodules

“…Indeed a S. meliloti flavohemoglobin (hmp) whose expression is induced both by microaerobic conditions and NO, has been shown to be involved in NO degradation and to be essential in maintaining efficient nitrogen-fixing symbiosis. 14,25 Inoculation of M. truncatula plants with a S. meliloti hmp mutant led to a higher level of NO and early senescence in root nodules, even though plant hemoglobins were still proficient. This drew our attention to the importance of the bacterial protein in controlling NO balance inside nodules.…”

“…This drew our attention to the importance of the bacterial protein in controlling NO balance inside nodules. 14 Another candidate for NO detoxification in denitrifying rhizobia is the respiratory NO reductase (Nor) that catalyzes the reduction of NO into N 2 O (nitrous oxide) in the denitrification process. 26 The S. meliloti enzyme is encoded by norCBQD genes.…”