Actin Depolymerizing Factor Modulates Rhizobial Infection and Nodule Organogenesis in Common Bean

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.

Structure and Development of the Legume-Rhizobial Symbiotic Interface in Infection Threads

“…L. japonicus mutants 121F-specific p53 inducible RNA ( Ljpir1 ) and nck-associated protein 1 ( Ljnap1 ) [ 76 ], as well as the M. truncatula required for infection thread ( Mtrit–1 ) mutant (ortholog Ljnap1 ) [ 117 ] were characterized by a similar phenotype (disorganization of the actin cytoskeleton, no reorganization of F–actin in response to inoculation, a decrease in the number of microcolonies in curled root hairs) [ 76 , 116 ]. In addition, Actin reorganization is regulated by the activation of the ROP GTPase family [ 118 ], inositol phospholipids [ 119 ], and actin depolymerization factor (PvADFE) in the Phaseolus vulgaris L.-rhizobia symbiosis [ 120 ].…”

Rapid Changes to Endomembrane System of Infected Root Nodule Cells to Adapt to Unusual Lifestyle

“…Zhang et al [67] defined five zones in the infected zone of M. truncatula root nodules with specific rearrangements of actin. The cytoskeletal patterns are mediated by diverse actin-binding proteins such as actin depolymerization factors (ADFs) [68], formin [64][65][66], Phospholipase Dβ [69] and the ARP2/3 complex [70], which nucleates new actin filaments and forms branched actin networks. The manipulation of host cell actin via the ARP2/3 actin nucleating complex is also used as common strategy for the establishment of an intracellular lifestyle by enteropathogenic bacteria in animal cells [71].…”

Research progress on the roles of actin-depolymerizing factor in plant stress responses

“…Conversely, land plants possess an expanded ADF gene family. For example, eleven ADF genes have been identified in Arabidopsis thaliana ( Feng et al., 2006 ; Ruzicka et al., 2007 ), rice ( Oryza sativa ; Feng et al., 2006 ; Huang et al., 2012 ), and tomato ( Solanum lycopersicum ; Khatun et al., 2016 ) each; eight in cucumber ( Cucumis sativus ; Liu et al., 2016 ) and Antarctic hairgrass ( Deschampsia antarctica ; Byun et al., 2021 ) each; nine in common bean ( Phaseolus vulgaris ; Ortega-Ortega et al., 2020 ); ten in pigeon pea ( Cajanus albicans ; Cao et al., 2020 ); thirteen in maize ( Zea mays ; Huang et al., 2020 ); fourteen in poplar ( Populus trichocarpa ; Roy-Zokan et al., 2015 ); eighteen in soybean ( Glycine max ; Sun et al., 2023 ); twenty-five in wheat ( Triticum aestivum ; Xu et al., 2021 ); twenty-seven in banana ( Musa acuminata ; Nan et al., 2017 ); and thirty-seven in upland cotton ( Gossypium hirsutum ; Sun et al., 2021 ). In contrast to single-cell eukaryotes and animals, plants exhibit a multitude of distinct and functionally specialized actin filament systems, alongside a larger actin gene family ( McDowell et al., 1996 ; Zhang et al., 2010 ; Gunning et al., 2015 ).…”

“…These bacteria can form symbiotic nitrogen-fixing nodules with leguminous plants and increase nitrogen fixation in arable fields by as much as 30% ( Mus et al., 2016 ). PvADFE is one of the nine ADF genes found in common bean, primarily expressed in roots and nodules inoculated with Rhizobium tropici ( Ortega-Ortega et al., 2020 ). In addition, PvADFE silencing increases the number and size of nodules and enhances nitrogen fixation activity.…”