The symbiotic role of the actin filament cytoskeleton

Genre, Andrea; Timmers, Ton

doi:10.1111/nph.15506

Cited by 5 publications

(4 citation statements)

References 20 publications

(20 reference statements)

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“…In soybean nodules, cytoskeletal arrays differ between uninfected and infected nodule cells and between developing and mature nodule cells ( 59 ). Continued reorganization of actin cytoskeleton is associated with rhizobium release from infection threads and symbiosome development ( 60 , 61 ). Notably, the key symbiotic phenotype associated with the inactivation of T3SS in incompatible Sinorhizobium strains is the shift from uninfected pseudonodules to well-infected nodules ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency

et al. 2021

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The interkingdom coevolution innovated the rhizobium-legume symbiosis. The application of this nitrogen-fixing system in sustainable agriculture is usually impeded by incompatible interactions between partners. However, the progressive evolution of rhizobium-legume compatibility remains elusive. In this work, deletions of rhcV encoding a structural component of the type three secretion system allow related Sinorhizobium strains to nodulate a previously incompatible soybean cultivar (Glycine max). These rhcV mutants show low to medium to high symbiotic efficiency on the same cultivated soybean while being indistinguishable on wild soybean plants (Glycine soja). The dual pantranscriptomics reveals nodule-specific activation of core symbiosis genes of Sinorhizobium and Glycine genes associated with genome duplication events along the chronogram. Unexpectedly, symbiotic efficiency is in line with lineage-dependent transcriptional profiles of core pathways which predate the diversification of Fabaceae and Sinorhizobium. This is supported by further physiological and biochemical experiments. Particularly, low-efficiency nodules show disordered antioxidant activity and low-energy status, which restrict nitrogen fixation activity. Collectively, the ancient core pathways play a crucial role in optimizing the function of later-evolved mutualistic arsenals in the rhizobium-legume coevolution. IMPORTANCE Significant roles of complex extracellular microbiota in environmental adaptation of eukaryotes in ever-changing circumstances have been revealed. Given the intracellular infection ability, facultative endosymbionts can be considered pioneers within complex extracellular microbiota and are ideal organisms for understanding the early stage of interkingdom adaptation. This work reveals that the later innovation of key symbiotic arsenals and the lineage-specific network rewiring in ancient core pathways, predating the divergence of legumes and rhizobia, underline the progressive evolution of rhizobium-legume compatibility. This insight not only is significant for improving the application benefits of rhizobial inoculants in sustainable agriculture but also advances our general understanding of the interkingdom coevolution which is theoretically explored by all host-microbiota interactions.

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Section: Resultsmentioning

confidence: 99%

Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency

et al. 2021

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“…Besides non-beneficial plant–pathogen interactions, MTs also function in beneficial symbiosis processes between plants and symbiotic microorganisms [ 205 ]. Active cytoskeletal rearrangements are required at different stages of nodule development, from root-hair curling for entrapment of rhizobia to infection thread growth [ 206 , 207 , 208 ]. Endoplasmic MTs appear to support infection thread growth, infection droplet formation, and bacterial release into the host cytoplasm in nodules of legume species, whereas irregular cortical MT arrangements provide a possibility for isodiametric cell growth that allows a notable increase in cell size for hosting numerous symbiosomes [ 209 ].…”

Section: Mts In Biotic Stress Responsesmentioning

confidence: 99%

Microtubule Regulation in Plants: From Morphological Development to Stress Adaptation

Hsiao

Huang

2023

Biomolecules

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Microtubules (MTs) are essential elements of the eukaryotic cytoskeleton and are critical for various cell functions. During cell division, plant MTs form highly ordered structures, and cortical MTs guide the cell wall cellulose patterns and thus control cell size and shape. Both are important for morphological development and for adjusting plant growth and plasticity under environmental challenges for stress adaptation. Various MT regulators control the dynamics and organization of MTs in diverse cellular processes and response to developmental and environmental cues. This article summarizes the recent progress in plant MT studies from morphological development to stress responses, discusses the latest techniques applied, and encourages more research into plant MT regulation.

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“…It has been clearly demonstrated that active cytoskeleton rearrangements are required at different stages of nodule development ( Timmers, 2008 ; Genre and Timmers, 2019 ; Tsyganov et al, 2019 ). Symbiotic nodules can be subdivided into two main types: indeterminate and determinate ( Hirsch, 1992 ).…”

Section: Introductionmentioning

confidence: 99%

Tubulin Cytoskeleton Organization in Cells of Determinate Nodules

et al. 2022

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Plant cell differentiation is based on rearrangements of the tubulin cytoskeleton; this is also true for symbiotic nodules. Nevertheless, although for indeterminate nodules (with a long-lasting meristem) the organization of microtubules during nodule development has been studied for various species, for determinate ones (with limited meristem activity) such studies are rare. Here, we investigated bacteroid morphology and dynamics of the tubulin cytoskeleton in determinate nodules of four legume species: Glycine max, Glycine soja, Phaseolus vulgaris, and Lotus japonicus. The most pronounced differentiation of bacteroids was observed in G. soja nodules. In meristematic cells in incipient nodules of all analyzed species, the organization of both cortical and endoplasmic microtubules was similar to that described for meristematic cells of indeterminate nodules. In young infected cells in developing nodules of all four species, cortical microtubules formed irregular patterns (microtubules were criss-crossed) and endoplasmic ones were associated with infection threads and infection droplets. Surprisingly, in uninfected cells the patterns of cortical microtubules differed in nodules of G. max and G. soja on the one hand, and P. vulgaris and L. japonicus on the other. The first two species exhibited irregular patterns, while the remaining two exhibited regular ones (microtubules were oriented transversely to the longitudinal axis of cell) that are typical for uninfected cells of indeterminate nodules. In contrast to indeterminate nodules, in mature determinate nodules of all four studied species, cortical microtubules formed a regular pattern in infected cells. Thus, our analysis revealed common patterns of tubulin cytoskeleton in the determinate nodules of four legume species, and species-specific differences were associated with the organization of cortical microtubules in uninfected cells. When compared with indeterminate nodules, the most pronounced differences were associated with the organization of cortical microtubules in nitrogen-fixing infected cells. The revealed differences indicated a possible transition during evolution of infected cells from anisotropic growth in determinate nodules to isodiametric growth in indeterminate nodules. It can be assumed that this transition provided an evolutionary advantage to those legume species with indeterminate nodules, enabling them to host symbiosomes in their infected cells more efficiently.

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The symbiotic role of the actin filament cytoskeleton

Abstract: This article is a Commentary on Zhang et al., 221: 1049–1059.

Cited by 5 publications

References 20 publications

Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency

Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency

Microtubule Regulation in Plants: From Morphological Development to Stress Adaptation

Tubulin Cytoskeleton Organization in Cells of Determinate Nodules

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