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On the track of transfer cell formation by specialized plant-parasitic nematodes.

Rodiuc N, Vieira P, Banora MY, de Almeida Engler J - Front Plant Sci (2014)

Bottom Line: In both cases, these nematodes are able to remarkably maneuver and reprogram plant host cells.In this review we will discuss the structure, function and formation of these specialized multinucleate cells that act as nutrient transfer cells accumulating and synthesizing components needed for survival and successful offspring of plant-parasitic nematodes.Plant cells with transfer-like functions are also a renowned subject of interest involving still poorly understood molecular and cellular transport processes.

View Article: PubMed Central - PubMed

Affiliation: Laboratório de Interação Molecular Planta-Praga, Embrapa Recursos Genéticos e Biotecnologia, PqEB Brasília, Brasil.

ABSTRACT
Transfer cells are ubiquitous plant cells that play an important role in plant development as well as in responses to biotic and abiotic stresses. They are highly specialized and differentiated cells playing a central role in the acquisition, distribution and exchange of nutrients. Their unique structural traits are characterized by augmented ingrowths of invaginated secondary wall material, unsheathed by an amplified area of plasma membrane enriched in a suite of solute transporters. Similar morphological features can be perceived in vascular root feeding cells induced by sedentary plant-parasitic nematodes, such as root-knot and cyst nematodes, in a wide range of plant hosts. Despite their close phylogenetic relationship, these obligatory biotrophic plant pathogens engage different approaches when reprogramming root cells into giant cells or syncytia, respectively. Both nematode feeding-cells types will serve as the main source of nutrients until the end of the nematode life cycle. In both cases, these nematodes are able to remarkably maneuver and reprogram plant host cells. In this review we will discuss the structure, function and formation of these specialized multinucleate cells that act as nutrient transfer cells accumulating and synthesizing components needed for survival and successful offspring of plant-parasitic nematodes. Plant cells with transfer-like functions are also a renowned subject of interest involving still poorly understood molecular and cellular transport processes.

No MeSH data available.


Related in: MedlinePlus

Anatomy of Meloidogyne incognita-induced giant cells in Arabidopsis thaliana roots. (A) Light microscopy image of sectioned giant cells embedded in a gall and stained with toluidine blue. Cell wall thickenings (black arrows), and a cell wall stub (red arrow) indicating arrest of cytokinesis. (B–D) Ultra-structure of giant cell sections showing cell wall ingrowths (black arrows) along regions predominantly flanking the vascular tissue. Note the xylem elements with thickened cell walls and dense cytoplasm containing numerous organelles including asymmetrically shaped nuclei and small vacuoles. (D) Detailed giant cells showing a PD (green arrow). Asterisk, giant cell; NC, neighboring cells; x, xylem; CW, cell wall; V, vacuole; nu, nucleus. Bars = (A) 25 μm and (B–D) 5 μm.
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Figure 3: Anatomy of Meloidogyne incognita-induced giant cells in Arabidopsis thaliana roots. (A) Light microscopy image of sectioned giant cells embedded in a gall and stained with toluidine blue. Cell wall thickenings (black arrows), and a cell wall stub (red arrow) indicating arrest of cytokinesis. (B–D) Ultra-structure of giant cell sections showing cell wall ingrowths (black arrows) along regions predominantly flanking the vascular tissue. Note the xylem elements with thickened cell walls and dense cytoplasm containing numerous organelles including asymmetrically shaped nuclei and small vacuoles. (D) Detailed giant cells showing a PD (green arrow). Asterisk, giant cell; NC, neighboring cells; x, xylem; CW, cell wall; V, vacuole; nu, nucleus. Bars = (A) 25 μm and (B–D) 5 μm.

Mentions: In the past years there has been extensive data reporting on the anatomy of the sophisticated nematode feeding sites induced by CN and RKN, comprising light, scanning and transmission electron microscopy (e.g., Bird, 1961; Jones and Dropkin, 1976; Wergin and Orion, 1981; Hussey and Mims, 1991; Berg et al., 2008; Sobczak and Golinowski, 2008). Both nematode feeding sites share common features, such as the increase of metabolic activity and cytoplasmic density, the replacement of a large central vacuole by several smaller ones, the large nuclei number of increased size, and the proliferation of organelles including Golgi stacks, mitochondria, plastids, ribosomes, and endoplasmic reticulum (Figure 3; Vieira et al., 2013 and Figure 4: Berg et al., 2008; Sobczak et al., 2011). Concomitant with the structural modifications in a gall or a syncytium, cell walls thicken and finger-like protuberances (ingrowths or cell wall labyrinths) form (Schemes in Figures 1, 3 and 4; Berg et al., 2008; Sobczak et al., 2011; Vieira et al., 2013) with the function to increase the membrane surface area for solute uptake (e.g., Golinowski et al., 1996; Hussey and Grundler, 1998). The cell wall degradation is also observed in syncytia (Scheme in Figures 1B and 2D; de Almeida Engler et al., 1999 and Figures 4A,B; Sobczak et al., 2011). Extensive changes of cell wall architecture in diverse types of TCs encountered in plants may comprise cell wall ingrowths and partial cell wall degradation (Offler et al., 2003) as occurring in syncytia. Increased giant cell wall ingrowths accompanied by intense surrounding vascularization will certainly contribute to the access to nutrient supply by the feeding nematode (Bartlem et al., 2014). Similar intense vascularization around syncytia will certainly enhance nutrient supply to the developing nematode.


On the track of transfer cell formation by specialized plant-parasitic nematodes.

Rodiuc N, Vieira P, Banora MY, de Almeida Engler J - Front Plant Sci (2014)

Anatomy of Meloidogyne incognita-induced giant cells in Arabidopsis thaliana roots. (A) Light microscopy image of sectioned giant cells embedded in a gall and stained with toluidine blue. Cell wall thickenings (black arrows), and a cell wall stub (red arrow) indicating arrest of cytokinesis. (B–D) Ultra-structure of giant cell sections showing cell wall ingrowths (black arrows) along regions predominantly flanking the vascular tissue. Note the xylem elements with thickened cell walls and dense cytoplasm containing numerous organelles including asymmetrically shaped nuclei and small vacuoles. (D) Detailed giant cells showing a PD (green arrow). Asterisk, giant cell; NC, neighboring cells; x, xylem; CW, cell wall; V, vacuole; nu, nucleus. Bars = (A) 25 μm and (B–D) 5 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4017147&req=5

Figure 3: Anatomy of Meloidogyne incognita-induced giant cells in Arabidopsis thaliana roots. (A) Light microscopy image of sectioned giant cells embedded in a gall and stained with toluidine blue. Cell wall thickenings (black arrows), and a cell wall stub (red arrow) indicating arrest of cytokinesis. (B–D) Ultra-structure of giant cell sections showing cell wall ingrowths (black arrows) along regions predominantly flanking the vascular tissue. Note the xylem elements with thickened cell walls and dense cytoplasm containing numerous organelles including asymmetrically shaped nuclei and small vacuoles. (D) Detailed giant cells showing a PD (green arrow). Asterisk, giant cell; NC, neighboring cells; x, xylem; CW, cell wall; V, vacuole; nu, nucleus. Bars = (A) 25 μm and (B–D) 5 μm.
Mentions: In the past years there has been extensive data reporting on the anatomy of the sophisticated nematode feeding sites induced by CN and RKN, comprising light, scanning and transmission electron microscopy (e.g., Bird, 1961; Jones and Dropkin, 1976; Wergin and Orion, 1981; Hussey and Mims, 1991; Berg et al., 2008; Sobczak and Golinowski, 2008). Both nematode feeding sites share common features, such as the increase of metabolic activity and cytoplasmic density, the replacement of a large central vacuole by several smaller ones, the large nuclei number of increased size, and the proliferation of organelles including Golgi stacks, mitochondria, plastids, ribosomes, and endoplasmic reticulum (Figure 3; Vieira et al., 2013 and Figure 4: Berg et al., 2008; Sobczak et al., 2011). Concomitant with the structural modifications in a gall or a syncytium, cell walls thicken and finger-like protuberances (ingrowths or cell wall labyrinths) form (Schemes in Figures 1, 3 and 4; Berg et al., 2008; Sobczak et al., 2011; Vieira et al., 2013) with the function to increase the membrane surface area for solute uptake (e.g., Golinowski et al., 1996; Hussey and Grundler, 1998). The cell wall degradation is also observed in syncytia (Scheme in Figures 1B and 2D; de Almeida Engler et al., 1999 and Figures 4A,B; Sobczak et al., 2011). Extensive changes of cell wall architecture in diverse types of TCs encountered in plants may comprise cell wall ingrowths and partial cell wall degradation (Offler et al., 2003) as occurring in syncytia. Increased giant cell wall ingrowths accompanied by intense surrounding vascularization will certainly contribute to the access to nutrient supply by the feeding nematode (Bartlem et al., 2014). Similar intense vascularization around syncytia will certainly enhance nutrient supply to the developing nematode.

Bottom Line: In both cases, these nematodes are able to remarkably maneuver and reprogram plant host cells.In this review we will discuss the structure, function and formation of these specialized multinucleate cells that act as nutrient transfer cells accumulating and synthesizing components needed for survival and successful offspring of plant-parasitic nematodes.Plant cells with transfer-like functions are also a renowned subject of interest involving still poorly understood molecular and cellular transport processes.

View Article: PubMed Central - PubMed

Affiliation: Laboratório de Interação Molecular Planta-Praga, Embrapa Recursos Genéticos e Biotecnologia, PqEB Brasília, Brasil.

ABSTRACT
Transfer cells are ubiquitous plant cells that play an important role in plant development as well as in responses to biotic and abiotic stresses. They are highly specialized and differentiated cells playing a central role in the acquisition, distribution and exchange of nutrients. Their unique structural traits are characterized by augmented ingrowths of invaginated secondary wall material, unsheathed by an amplified area of plasma membrane enriched in a suite of solute transporters. Similar morphological features can be perceived in vascular root feeding cells induced by sedentary plant-parasitic nematodes, such as root-knot and cyst nematodes, in a wide range of plant hosts. Despite their close phylogenetic relationship, these obligatory biotrophic plant pathogens engage different approaches when reprogramming root cells into giant cells or syncytia, respectively. Both nematode feeding-cells types will serve as the main source of nutrients until the end of the nematode life cycle. In both cases, these nematodes are able to remarkably maneuver and reprogram plant host cells. In this review we will discuss the structure, function and formation of these specialized multinucleate cells that act as nutrient transfer cells accumulating and synthesizing components needed for survival and successful offspring of plant-parasitic nematodes. Plant cells with transfer-like functions are also a renowned subject of interest involving still poorly understood molecular and cellular transport processes.

No MeSH data available.


Related in: MedlinePlus