What are tilosomes? An update and new perspectives

Characterization of tilosomes and study of their development revealed that they are similar to the cell wall ingrowths of transfer cells. Roots from Anathallis sclerophylla were used to examine the development, histochemistry and ultrastructure of tilosomes using light, confocal and electron microscopy (both SEM and TEM). Tilosomes initiate as cellulosic papillae in the root elongation zone, increasing the apo/symplast surface throughout the wall-membrane apparatus. Both the development and structure of tilosomes and velamen strips appear similar to the reticulated and flange cell wall ingrowths of Vicia faba transfer cells. We suggest two functional phases for tilosomes: a) in young tissues they increase the symplast connection and thus improve outside-inside transport; and b) in mature tissues they direct solutes to passage cells. Both the physiology and the genetic mechanisms controlling the ontogeny of tilosomes remain obscure.

Keywords:
autofluorescence; callose; cell wall biochemistry; ontogeny; oriented wall deposition; waxes

Authorship

Halisson Rafael Kedrovski ^** Corresponding author: h.r.kedrovski@hotmail.com

Programa de Pós-graduação em Ciências Biológicas (Biologia Vegetal), Departamento de Botânica, Universidade Estadual Paulista “Júlio de Mesquita Filho”, 13506-900, Rio Claro, SP, BrazilUniversidade Estadual Paulista “Júlio de Mesquita Filho”BrazilRio Claro, SP, Brazil Programa de Pós-graduação em Ciências Biológicas (Biologia Vegetal), Departamento de Botânica, Universidade Estadual Paulista “Júlio de Mesquita Filho”, 13506-900, Rio Claro, SP, Brazil

http://orcid.org/0000-0003-1217-860X

Maria das Graças Sajo

http://orcid.org/0000-0003-4642-8769

* Corresponding author: h.r.kedrovski@hotmail.com

SCIMAGO INSTITUTIONS RANKINGS

Figures

Figures (4)

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Figure 1
Tilosome morphology in Anathallis sclerophylla root. A-B Light Microscopy. C-D SEM. E-F TEM. A. Cross section of differentiated roots stained with safrablue, showing “O” thickened endodermis cells (end), cortical cells (co) with pelotons (hy), dead exodermis cells (exd), passage cells of dense cytoplasm (pc), tilosomes (arrowhead) with a thin blue primary wall and the stratified velamen (v). B. Longitudinal section stained with toluidine blue, showing by metachromasy the lignified walls (green) in velamen (v), tilosome (arrowhead) and exodermis (exd); note the cortex cellulosic walls (anil blue) (co) and the difference between the common and the passage cells of exodermis. C-D. Paradermic (C) and cross section (D) showing the tilosomes (arrowhead) adjacent to the exodermis passage cells (pc) and the reticulated and flange patterns of the endovelamen (edv) WIs. E-F. Velamen-exodermis complex showing dead cells in the endovelamen (edv), WIs lumen directed to environment, common exodermis cell (exd) with two layers of secondary wall (s1, s2), vacuolated passage cells (pc) with conspicuous nucleus, mitochondria, ribosomes on an electron-dense matrix and vesicles adjacent to the tonoplast,. Scale bars: 25µm(A), 50 µm(B), 10 µm(C), 3 µm(D), 5 µm(E).

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Figure 2
Macro (A) and micromorphology (B-I) of Anathallis sclerophylla roots. Longitudinal (B-I) sections of the apex, showing the epidermis and cortex (D-F) and the tilosomes (G-I) development. There are three zones in the apex (A-B): 1. Meristematic (mz) (C) with isodiametric protodermis cells (pd), ground meristem (gm) of elliptical cells and procambium (p) of fusiform cells (B-C); 2. Short elongation zone (ez) at the boundary of the root cap (D) with primary walled cells (B); it is characterized by the increase of the cellular volume in the median region of the ground meristem (causing a compression in the exodermis layer (E)), and by the first division of the protodermis originating the endo and epivelamen (edv, epv); 3. Differentiation zone (dz) (D-F), with a second division in the epivelamen, the development of root hairs (rh) and the progressive tissue specialization (A-B). The tilosome (G) begin as small, papillose-like regions in the inner wall of some endovelamen cells laying adjacent the exodermis passage cells. The secondary wall deposition in these cells follow the orientation of the primary WI (G), leading to the tilosomes or velamen stripes formation (H-I). The dotted line indicates the boundary between protoderm and root cap, and the arrows indicate the velamen cell divisions. Scale bars: 120µm (A-B), 50µm (C), 25µm (D-F), 10µm (G-I).

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Figure 3
Ultrastructural details of the protodermis and ground meristem during the tilosomes formation in Anathallis sclerophylla root. The asynchronous WIs deposition (A) in the inner protodermis layer (dp) is noted by small papillae (arrowhead) of fibrillar material in the inner cell wall adjacent to the ground meristem (gm) (A-C). Each papillae is a precursor of the wall system that characterize the reticulate tilosome. In the outer protodermis layers (A), the cells are poorly vacuolated and vesicles/organels rich; they possess flange-like projections (arrows) on the walls, that will give rise to the characteristic velamen strips. The protodermis cells that develop walls ingrowth had increased nuclear region (nu) and few vacuoles in the cytoplasm compared to those which give rise to the cortex in ground meristem. The papillae wall synthesis is closely related to the presence of mitochondria and RER (A-C) and to the increase of cell surface. The ground meristem cells possess large vacuolated (va) and thin walls. The limit between the velamen cell walls and tilosome is not visible. Velamen-exodermis are continuous through the tilosome- exodermis (exo) passage cell; these cells possess many plasmodesmata both before (D-E) and after cell differentiation (F) that can or not be occluded by callose. Scale bars: 5µm(A), 2um(F), 1µm(B, C, D, E).

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Figure 4
Three-dimensional z-stack reconstructions of cross (A-D), and longitudinal (E -L) sections of Anathallis sclerophylla roots stained with calcofluor (A-D) and aniline blue (E-L) fluorophores, in order to demonstrate the wall compositions. Cellulose (A-B) and callose (F, G) shown in blue and lignin in green (C, G, K) are the main walls constituents, although waxes could also be evidenced by autofluorescence when excited by low intensity red light in argon diode (D, H, L). By intense fluorescence, cellulose can be observed in cortical parenchyma (co) and in "O"-thickened cells of exodermis (ex), except for the outer periclinal wall of the passage cells (A-B). Lignin is found in endovelamen (edv), velamen stripes (arrow) (A), tilosomes (arrowhead) (C), "∩"- thickened exodermis cells (C, G), intercellular spaces of outer cortical parenchyma (C), spiral thickenings of internal cortical parenchyma (G), endodermis (en) and vascular cylinder (E, G). Callose occurs in all cell walls, with the highest concentration in the epivelamen (epv) (E-F), in the plasmodesmata around the tilosomes (J) and in the inner layer of the cortical parenchyma including endodermis (F). Waxes (suberin and cutin) occur in a smaller quantity when compared to the fluorescence of other polymers; it is concentrated in the outer layers of the velamen (D, H) but it is diffuse in the tilosomes (D), in the "∩"-thickened exodermis cells, intercellular spaces of the cortical parenchyma, endodermis and phloem (H). Note the occurrence of infections by algae and fungi. Scale bars: 30µm (E-H), 15µm(A-D), 10µm(I-L).

Figure 1 Tilosome morphology in Anathallis sclerophylla root. A-B Light Microscopy. C-D SEM. E-F TEM. A. Cross section of differentiated roots stained with safrablue, showing “O” thickened endodermis cells (end), cortical cells (co) with pelotons (hy), dead exodermis cells (exd), passage cells of dense cytoplasm (pc), tilosomes (arrowhead) with a thin blue primary wall and the stratified velamen (v). B. Longitudinal section stained with toluidine blue, showing by metachromasy the lignified walls (green) in velamen (v), tilosome (arrowhead) and exodermis (exd); note the cortex cellulosic walls (anil blue) (co) and the difference between the common and the passage cells of exodermis. C-D. Paradermic (C) and cross section (D) showing the tilosomes (arrowhead) adjacent to the exodermis passage cells (pc) and the reticulated and flange patterns of the endovelamen (edv) WIs. E-F. Velamen-exodermis complex showing dead cells in the endovelamen (edv), WIs lumen directed to environment, common exodermis cell (exd) with two layers of secondary wall (s1, s2), vacuolated passage cells (pc) with conspicuous nucleus, mitochondria, ribosomes on an electron-dense matrix and vesicles adjacent to the tonoplast,. Scale bars: 25µm(A), 50 µm(B), 10 µm(C), 3 µm(D), 5 µm(E).

Figure 2 Macro (A) and micromorphology (B-I) of Anathallis sclerophylla roots. Longitudinal (B-I) sections of the apex, showing the epidermis and cortex (D-F) and the tilosomes (G-I) development. There are three zones in the apex (A-B): 1. Meristematic (mz) (C) with isodiametric protodermis cells (pd), ground meristem (gm) of elliptical cells and procambium (p) of fusiform cells (B-C); 2. Short elongation zone (ez) at the boundary of the root cap (D) with primary walled cells (B); it is characterized by the increase of the cellular volume in the median region of the ground meristem (causing a compression in the exodermis layer (E)), and by the first division of the protodermis originating the endo and epivelamen (edv, epv); 3. Differentiation zone (dz) (D-F), with a second division in the epivelamen, the development of root hairs (rh) and the progressive tissue specialization (A-B). The tilosome (G) begin as small, papillose-like regions in the inner wall of some endovelamen cells laying adjacent the exodermis passage cells. The secondary wall deposition in these cells follow the orientation of the primary WI (G), leading to the tilosomes or velamen stripes formation (H-I). The dotted line indicates the boundary between protoderm and root cap, and the arrows indicate the velamen cell divisions. Scale bars: 120µm (A-B), 50µm (C), 25µm (D-F), 10µm (G-I).

Figure 3 Ultrastructural details of the protodermis and ground meristem during the tilosomes formation in Anathallis sclerophylla root. The asynchronous WIs deposition (A) in the inner protodermis layer (dp) is noted by small papillae (arrowhead) of fibrillar material in the inner cell wall adjacent to the ground meristem (gm) (A-C). Each papillae is a precursor of the wall system that characterize the reticulate tilosome. In the outer protodermis layers (A), the cells are poorly vacuolated and vesicles/organels rich; they possess flange-like projections (arrows) on the walls, that will give rise to the characteristic velamen strips. The protodermis cells that develop walls ingrowth had increased nuclear region (nu) and few vacuoles in the cytoplasm compared to those which give rise to the cortex in ground meristem. The papillae wall synthesis is closely related to the presence of mitochondria and RER (A-C) and to the increase of cell surface. The ground meristem cells possess large vacuolated (va) and thin walls. The limit between the velamen cell walls and tilosome is not visible. Velamen-exodermis are continuous through the tilosome- exodermis (exo) passage cell; these cells possess many plasmodesmata both before (D-E) and after cell differentiation (F) that can or not be occluded by callose. Scale bars: 5µm(A), 2um(F), 1µm(B, C, D, E).

Figure 4 Three-dimensional z-stack reconstructions of cross (A-D), and longitudinal (E -L) sections of Anathallis sclerophylla roots stained with calcofluor (A-D) and aniline blue (E-L) fluorophores, in order to demonstrate the wall compositions. Cellulose (A-B) and callose (F, G) shown in blue and lignin in green (C, G, K) are the main walls constituents, although waxes could also be evidenced by autofluorescence when excited by low intensity red light in argon diode (D, H, L). By intense fluorescence, cellulose can be observed in cortical parenchyma (co) and in "O"-thickened cells of exodermis (ex), except for the outer periclinal wall of the passage cells (A-B). Lignin is found in endovelamen (edv), velamen stripes (arrow) (A), tilosomes (arrowhead) (C), "∩"- thickened exodermis cells (C, G), intercellular spaces of outer cortical parenchyma (C), spiral thickenings of internal cortical parenchyma (G), endodermis (en) and vascular cylinder (E, G). Callose occurs in all cell walls, with the highest concentration in the epivelamen (epv) (E-F), in the plasmodesmata around the tilosomes (J) and in the inner layer of the cortical parenchyma including endodermis (F). Waxes (suberin and cutin) occur in a smaller quantity when compared to the fluorescence of other polymers; it is concentrated in the outer layers of the velamen (D, H) but it is diffuse in the tilosomes (D), in the "∩"-thickened exodermis cells, intercellular spaces of the cortical parenchyma, endodermis and phloem (H). Note the occurrence of infections by algae and fungi. Scale bars: 30µm (E-H), 15µm(A-D), 10µm(I-L).

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