Abstract
Actin plays a critical role in the rhizobium–legume symbiosis. Cytoskeletal rearrangements and changes in actin occur in response to Nod factors secreted by rhizobia during symbiotic interactions with legumes. These cytoskeletal rearrangements are mediated by diverse actin-binding proteins, such as actin depolymerization factors (ADFs). We examined the function of an ADF in the Phaseolus vulgaris–rhizobia symbiotic interaction (PvADFE). PvADFE was preferentially expressed in rhizobia-inoculated roots and nodules. PvADFE promoter activity was associated with root hairs harbouring growing infection threads, cortical cell divisions beneath root hairs, and vascular bundles in mature nodules. Silencing of PvADFE using RNA interference increased the number of infection threads in the transgenic roots, resulting in increased nodule number, nitrogen fixation activity, and average nodule diameter. Conversely, overexpression of PvADFE reduced the nodule number, nitrogen fixation activity, average nodule diameter, as well as NODULE INCEPTION (NIN) and EARLY NODULIN2 (ENOD2) transcript accumulation. Hence, changes in ADFE transcript levels affect rhizobial infection and nodulation, suggesting that ADFE is fine-tuning these processes.
Highlights
Legumes have the ability to establish a symbiotic association with Gram-negative soil bacteria belonging to several genera, including Rhizobium, Bradyrhizobium, Sinorhizobium, and Azorhizobium, commonly called rhizobia [1]
We found that promoter activity PvADFE was detected in the rhizobially infected root hairs and vascular bundles of mature nodules
The predicted tertiary structure of PvADFE is similar to that of Arabidopsis AthADF1 [48], showing three α-helices surrounded by five β-sheets and a putative actin-binding surface (Figure S2B), a feature conserved among actin depolymerization factors (ADFs) that is critical for binding and/or depolymerization of actin filaments [48]
Summary
Legumes have the ability to establish a symbiotic association with Gram-negative soil bacteria belonging to several genera, including Rhizobium, Bradyrhizobium, Sinorhizobium, and Azorhizobium, commonly called rhizobia [1] This mutualistic interaction is initiated by a molecular dialogue in which plant roots exude flavonoids that activate the expression of bacterial genes (nod genes) encoding proteins involved in the synthesis and secretion of lipochitooligosaccharides, called Nod factors (NFs). Silencing of the gene ARP3 causes defects in symbiosome development in Medicago truncatula nodules [24] and L. japonicus mutants in SCARN (encoding suppressor of cAMP receptor defect-nodulation, a protein that binds to the ARP3 complex), present a strong phenotype with reduced root hair growth and aberrant formation and progression of ITs, resulting in uninfected nodules [25] These results add weight to the idea that actin assembly is an important player during the symbiotic interaction. The participation of PvADFE in the common bean symbiosis with Rhizobium tropici by down-regulating or overexpressing PvADFE in transgenic composite plants revealed a role of ADFE likely fine-tuning nodulation
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