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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

Plasmodesmata localization in Meloidogyne incognita-induced galls and Heterodera schachtii-syncytium in Arabidopsis thaliana roots. (A)In vivo localization of MP17PLRV-GFP (plasmodesmata localization marked by green fluorescence). In an uninfected root; (B) in a gall at early stage after nematode infection; and (C) in a mature gall. (C’) Detail of two adjacent giant cells containing numerous PD (red arrow). (D)In vivo MP17PLRV-GFP localization between two giant cells and connecting NCs. Observations of Figures A–D were made on non- and infected material of Arabidopsis transgenic lines (35S:MP17PLRV-GFP). Non-infected roots, and galls were dissected from roots, embedded in 5% agar and fresh slices were observed using an inverted confocal microscope. (E) Cleared whole-mount gall showing the complex network of PD between giant cells. (E’) Detail of giant cells containing numerous PD (red arrows). (F,G) PD (red arrows point to green fluorescence of PD) in a section of a syncytium flanked by NCs, and (F’) a differential interference contrast image is presented to show syncytium tissue morphology. (G) Double localization of PD (red arrows point to green fluorescence of PD) and callose (white arrows to yellow dots). Green dots hint at open PD whereas yellow dots suggest that solute transport can be blocked by callose in syncytia. UR, uninfected root; n, nematode; NC, neighboring cells; Asterisk, giant cell; S, syncytium. Bars = 50 μm.
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Figure 5: Plasmodesmata localization in Meloidogyne incognita-induced galls and Heterodera schachtii-syncytium in Arabidopsis thaliana roots. (A)In vivo localization of MP17PLRV-GFP (plasmodesmata localization marked by green fluorescence). In an uninfected root; (B) in a gall at early stage after nematode infection; and (C) in a mature gall. (C’) Detail of two adjacent giant cells containing numerous PD (red arrow). (D)In vivo MP17PLRV-GFP localization between two giant cells and connecting NCs. Observations of Figures A–D were made on non- and infected material of Arabidopsis transgenic lines (35S:MP17PLRV-GFP). Non-infected roots, and galls were dissected from roots, embedded in 5% agar and fresh slices were observed using an inverted confocal microscope. (E) Cleared whole-mount gall showing the complex network of PD between giant cells. (E’) Detail of giant cells containing numerous PD (red arrows). (F,G) PD (red arrows point to green fluorescence of PD) in a section of a syncytium flanked by NCs, and (F’) a differential interference contrast image is presented to show syncytium tissue morphology. (G) Double localization of PD (red arrows point to green fluorescence of PD) and callose (white arrows to yellow dots). Green dots hint at open PD whereas yellow dots suggest that solute transport can be blocked by callose in syncytia. UR, uninfected root; n, nematode; NC, neighboring cells; Asterisk, giant cell; S, syncytium. Bars = 50 μm.

Mentions: A significant demand for nutrients from feeding cells is created by nematodes. This is manifested by the development of TC wall labyrinths of wall ingrowths, an idea long sustained as a hallmark of giant cells (Jones and Northcote, 1972a,b; Jones and Gunning, 1976). These wall ingrowths notably increase the surface area of the plasma membrane, assisting the transport of nutrients into or out of the feeding cell, i.e., like symplast–apoplast exchange occurring in plant TCs (Gunning and Pate, 1969; Gunning et al., 1974; Offler et al., 2003). Furthermore, TC wall labyrinths can be observed on the cell walls of neighboring giant cells, indicating that nutrient transport in the apoplast, pooled from outlying cells, can be an important source of giant-cell nutrients. As shown by Berg et al. (2008), walls lying between giant cells are thickened and labyrinth-rich, suggesting that nutrients might also flow between these feeding cells (Jones and Northcote, 1972b; Jones and Gunning, 1976). As well, solutes that are phloem-derived are imported into the giant cells either via plasmodesmata (PD) (symplastically; Figure 3D; Vieira et al., 2013 and Figures 5B–E’; Hofmann et al., 2010; Vieira et al., 2012) or by means of active transport (apoplasmically).


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)

Plasmodesmata localization in Meloidogyne incognita-induced galls and Heterodera schachtii-syncytium in Arabidopsis thaliana roots. (A)In vivo localization of MP17PLRV-GFP (plasmodesmata localization marked by green fluorescence). In an uninfected root; (B) in a gall at early stage after nematode infection; and (C) in a mature gall. (C’) Detail of two adjacent giant cells containing numerous PD (red arrow). (D)In vivo MP17PLRV-GFP localization between two giant cells and connecting NCs. Observations of Figures A–D were made on non- and infected material of Arabidopsis transgenic lines (35S:MP17PLRV-GFP). Non-infected roots, and galls were dissected from roots, embedded in 5% agar and fresh slices were observed using an inverted confocal microscope. (E) Cleared whole-mount gall showing the complex network of PD between giant cells. (E’) Detail of giant cells containing numerous PD (red arrows). (F,G) PD (red arrows point to green fluorescence of PD) in a section of a syncytium flanked by NCs, and (F’) a differential interference contrast image is presented to show syncytium tissue morphology. (G) Double localization of PD (red arrows point to green fluorescence of PD) and callose (white arrows to yellow dots). Green dots hint at open PD whereas yellow dots suggest that solute transport can be blocked by callose in syncytia. UR, uninfected root; n, nematode; NC, neighboring cells; Asterisk, giant cell; S, syncytium. Bars = 50 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Plasmodesmata localization in Meloidogyne incognita-induced galls and Heterodera schachtii-syncytium in Arabidopsis thaliana roots. (A)In vivo localization of MP17PLRV-GFP (plasmodesmata localization marked by green fluorescence). In an uninfected root; (B) in a gall at early stage after nematode infection; and (C) in a mature gall. (C’) Detail of two adjacent giant cells containing numerous PD (red arrow). (D)In vivo MP17PLRV-GFP localization between two giant cells and connecting NCs. Observations of Figures A–D were made on non- and infected material of Arabidopsis transgenic lines (35S:MP17PLRV-GFP). Non-infected roots, and galls were dissected from roots, embedded in 5% agar and fresh slices were observed using an inverted confocal microscope. (E) Cleared whole-mount gall showing the complex network of PD between giant cells. (E’) Detail of giant cells containing numerous PD (red arrows). (F,G) PD (red arrows point to green fluorescence of PD) in a section of a syncytium flanked by NCs, and (F’) a differential interference contrast image is presented to show syncytium tissue morphology. (G) Double localization of PD (red arrows point to green fluorescence of PD) and callose (white arrows to yellow dots). Green dots hint at open PD whereas yellow dots suggest that solute transport can be blocked by callose in syncytia. UR, uninfected root; n, nematode; NC, neighboring cells; Asterisk, giant cell; S, syncytium. Bars = 50 μm.
Mentions: A significant demand for nutrients from feeding cells is created by nematodes. This is manifested by the development of TC wall labyrinths of wall ingrowths, an idea long sustained as a hallmark of giant cells (Jones and Northcote, 1972a,b; Jones and Gunning, 1976). These wall ingrowths notably increase the surface area of the plasma membrane, assisting the transport of nutrients into or out of the feeding cell, i.e., like symplast–apoplast exchange occurring in plant TCs (Gunning and Pate, 1969; Gunning et al., 1974; Offler et al., 2003). Furthermore, TC wall labyrinths can be observed on the cell walls of neighboring giant cells, indicating that nutrient transport in the apoplast, pooled from outlying cells, can be an important source of giant-cell nutrients. As shown by Berg et al. (2008), walls lying between giant cells are thickened and labyrinth-rich, suggesting that nutrients might also flow between these feeding cells (Jones and Northcote, 1972b; Jones and Gunning, 1976). As well, solutes that are phloem-derived are imported into the giant cells either via plasmodesmata (PD) (symplastically; Figure 3D; Vieira et al., 2013 and Figures 5B–E’; Hofmann et al., 2010; Vieira et al., 2012) or by means of active transport (apoplasmically).

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