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Phytoplasma infection in tomato is associated with re-organization of plasma membrane, ER stacks, and actin filaments in sieve elements.

Buxa SV, Degola F, Polizzotto R, De Marco F, Loschi A, Kogel KH, di Toppi LS, van Bel AJ, Musetti R - Front Plant Sci (2015)

Bottom Line: We investigated modifications of the sieve-element ultrastructure induced in tomato plants by 'Candidatus Phytoplasma solani,' the pathogen associated with the stolbur disease.Western blot analysis revealed a decrease of actin and an increase of ER-resident chaperone luminal binding protein (BiP) in midribs of phytoplasma-infected plants.Collectively, the studies provided novel insights into ultrastructural responses of host sieve elements to phloem-restricted prokaryotes.

View Article: PubMed Central - PubMed

Affiliation: Department of Phytopathology and Applied Zoology, Justus Liebig University Giessen, Germany.

ABSTRACT
Phytoplasmas, biotrophic wall-less prokaryotes, only reside in sieve elements of their host plants. The essentials of the intimate interaction between phytoplasmas and their hosts are poorly understood, which calls for research on potential ultrastructural modifications. We investigated modifications of the sieve-element ultrastructure induced in tomato plants by 'Candidatus Phytoplasma solani,' the pathogen associated with the stolbur disease. Phytoplasma infection induces a drastic re-organization of sieve-element substructures including changes in plasma membrane surface and distortion of the sieve-element reticulum. Observations of healthy and stolbur-diseased plants provided evidence for the emergence of structural links between sieve-element plasma membrane and phytoplasmas. One-sided actin aggregates on the phytoplasma surface also inferred a connection between phytoplasma and sieve-element cytoskeleton. Actin filaments displaced from the sieve-element mictoplasm to the surface of the phytoplasmas in infected sieve elements. Western blot analysis revealed a decrease of actin and an increase of ER-resident chaperone luminal binding protein (BiP) in midribs of phytoplasma-infected plants. Collectively, the studies provided novel insights into ultrastructural responses of host sieve elements to phloem-restricted prokaryotes.

No MeSH data available.


Related in: MedlinePlus

(A–F) TEM micrographs of main veins cross-sections of healthy (A,B) and stolbur-diseased tomato leaves (C–F). Arrows point to ER organization, asterisks indicate attachment of phytoplasma cell to sieve-element plasma membrane. In stolbur-diseased samples SER cisternae were frequently intruding into the sieve-element lumen (C–E) and were fragmented into lobes and vesicles (F). CC, companion cell; CW, cell wall; M, mitochondria; P, phytoplasma; PM, plasma membrane; SE, sieve element; SEP, sieve-element plastid. Scale bars (A,B,D) = 200 nm; (C) = 400 nm.
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Figure 5: (A–F) TEM micrographs of main veins cross-sections of healthy (A,B) and stolbur-diseased tomato leaves (C–F). Arrows point to ER organization, asterisks indicate attachment of phytoplasma cell to sieve-element plasma membrane. In stolbur-diseased samples SER cisternae were frequently intruding into the sieve-element lumen (C–E) and were fragmented into lobes and vesicles (F). CC, companion cell; CW, cell wall; M, mitochondria; P, phytoplasma; PM, plasma membrane; SE, sieve element; SEP, sieve-element plastid. Scale bars (A,B,D) = 200 nm; (C) = 400 nm.

Mentions: In total, 60 sections from the 15 embedded blocks have been screened by TEM. TEM images revealed the sieve-element plasma membrane appressed to the cell wall in healthy leaves (Figure 2A). In infected samples, the plasma membrane of the phloem cells (phloem parenchyma cells, companion cells and sieve elements – SEs) was deformed, invaginated or undulating (Figures 2B–H). The membrane of parietal phytoplasmas and the sieve-element plasma membrane appeared in close contact (Figure 2D) via a membrane-bound structure forming a firm connection (Figures 2E–H). The typical pleomorphism and the ribosomes inside the bacterial bodies (Figure 2D) enabled a ready discrimination between phytoplasmas and sieve-element plastids (SEPs) even though size and location were similar (see Figure 5B and Ehlers et al., 2000). The characteristic multiple anchoring of SEPs to the sieve-element plasma membrane (Ehlers et al., 2000) was never observed for phytoplasmas.


Phytoplasma infection in tomato is associated with re-organization of plasma membrane, ER stacks, and actin filaments in sieve elements.

Buxa SV, Degola F, Polizzotto R, De Marco F, Loschi A, Kogel KH, di Toppi LS, van Bel AJ, Musetti R - Front Plant Sci (2015)

(A–F) TEM micrographs of main veins cross-sections of healthy (A,B) and stolbur-diseased tomato leaves (C–F). Arrows point to ER organization, asterisks indicate attachment of phytoplasma cell to sieve-element plasma membrane. In stolbur-diseased samples SER cisternae were frequently intruding into the sieve-element lumen (C–E) and were fragmented into lobes and vesicles (F). CC, companion cell; CW, cell wall; M, mitochondria; P, phytoplasma; PM, plasma membrane; SE, sieve element; SEP, sieve-element plastid. Scale bars (A,B,D) = 200 nm; (C) = 400 nm.
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Related In: Results  -  Collection

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Figure 5: (A–F) TEM micrographs of main veins cross-sections of healthy (A,B) and stolbur-diseased tomato leaves (C–F). Arrows point to ER organization, asterisks indicate attachment of phytoplasma cell to sieve-element plasma membrane. In stolbur-diseased samples SER cisternae were frequently intruding into the sieve-element lumen (C–E) and were fragmented into lobes and vesicles (F). CC, companion cell; CW, cell wall; M, mitochondria; P, phytoplasma; PM, plasma membrane; SE, sieve element; SEP, sieve-element plastid. Scale bars (A,B,D) = 200 nm; (C) = 400 nm.
Mentions: In total, 60 sections from the 15 embedded blocks have been screened by TEM. TEM images revealed the sieve-element plasma membrane appressed to the cell wall in healthy leaves (Figure 2A). In infected samples, the plasma membrane of the phloem cells (phloem parenchyma cells, companion cells and sieve elements – SEs) was deformed, invaginated or undulating (Figures 2B–H). The membrane of parietal phytoplasmas and the sieve-element plasma membrane appeared in close contact (Figure 2D) via a membrane-bound structure forming a firm connection (Figures 2E–H). The typical pleomorphism and the ribosomes inside the bacterial bodies (Figure 2D) enabled a ready discrimination between phytoplasmas and sieve-element plastids (SEPs) even though size and location were similar (see Figure 5B and Ehlers et al., 2000). The characteristic multiple anchoring of SEPs to the sieve-element plasma membrane (Ehlers et al., 2000) was never observed for phytoplasmas.

Bottom Line: We investigated modifications of the sieve-element ultrastructure induced in tomato plants by 'Candidatus Phytoplasma solani,' the pathogen associated with the stolbur disease.Western blot analysis revealed a decrease of actin and an increase of ER-resident chaperone luminal binding protein (BiP) in midribs of phytoplasma-infected plants.Collectively, the studies provided novel insights into ultrastructural responses of host sieve elements to phloem-restricted prokaryotes.

View Article: PubMed Central - PubMed

Affiliation: Department of Phytopathology and Applied Zoology, Justus Liebig University Giessen, Germany.

ABSTRACT
Phytoplasmas, biotrophic wall-less prokaryotes, only reside in sieve elements of their host plants. The essentials of the intimate interaction between phytoplasmas and their hosts are poorly understood, which calls for research on potential ultrastructural modifications. We investigated modifications of the sieve-element ultrastructure induced in tomato plants by 'Candidatus Phytoplasma solani,' the pathogen associated with the stolbur disease. Phytoplasma infection induces a drastic re-organization of sieve-element substructures including changes in plasma membrane surface and distortion of the sieve-element reticulum. Observations of healthy and stolbur-diseased plants provided evidence for the emergence of structural links between sieve-element plasma membrane and phytoplasmas. One-sided actin aggregates on the phytoplasma surface also inferred a connection between phytoplasma and sieve-element cytoskeleton. Actin filaments displaced from the sieve-element mictoplasm to the surface of the phytoplasmas in infected sieve elements. Western blot analysis revealed a decrease of actin and an increase of ER-resident chaperone luminal binding protein (BiP) in midribs of phytoplasma-infected plants. Collectively, the studies provided novel insights into ultrastructural responses of host sieve elements to phloem-restricted prokaryotes.

No MeSH data available.


Related in: MedlinePlus