Crossing the First Threshold: New Insights into the Influence of the Chemical Structure of Anionic Porphyrins on Plant Cell Wall Interactions and Photodynamic Cell Death Induction

Issawi, Mohammad; Leroy‐Lhez, Stéphanie; Sol, Vincent; Riou, Catherine

doi:10.1021/acs.biochem.9b00107

Cited by 3 publications

(9 citation statements)

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“…According to the phenotypical effects observed in TPPS-treated mycelium under light, it was of interest to localize TPPS inside the cells. In tobacco plant cells, TPPS was also tested at 3.5 µM and it was the most effective porphyrin PS to induce cell death under a short light period of 5 hours and it was proven to mainly localize in the cell wall (Riou et al 2014;Issawi et al 2019). Thus, a similar localization of TPPS was expected in the fungal cells.…”

Section: Tpps Localization Inside Mycelial Cellsmentioning

confidence: 89%

“…Indeed, TPPS with an ammonium counterion could be as an excellent antifungal candidate. Moreover, it was demonstrated that TPPS remains negatively charged in a large array of chemical environments, even under acidic pH and does not aggregate in media, allowing it to diffuse through cell walls and membranes more easily (Leroy-Lhez et al 2019;Issawi et al 2019). Therefore, this PS was thought as an excellent candidate for APDT.…”

Section: Discussionmentioning

confidence: 99%

“…Nevertheless, the Botrytis cell wall composition and its global charge remain controversial. We hypothesized that this neutrality could allow TPPS to cross the fungal cell wall which is completely different from the tobacco cell wall (Cantu et al 2009;Issawi et al 2017Issawi et al , 2019.…”

Section: Tpps Localization Inside Mycelial Cellsmentioning

confidence: 99%

“…With the aim to develop APDT for agriculture applications, TPPS could be a good candidate because of its low toxicity for plants. Moreover, TPPS remains negatively charged in many chemical environments even under acidic pH and does not aggregate in solution, allowing it to easily permeate cells through cell walls and membranes (Leroy-Lhez et al 2019;Issawi et al 2019). Therefore, we hypothesized that TPPS could be a good PS candidate to kill the plant pathogen B. cinerea and be a safe option for grapevine (Vitis vinifera L.) explants.…”

Section: Introductionmentioning

confidence: 99%

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Photodynamic inactivation of Botrytis cinerea for a safe pest management of grapevine

Ambrosini¹,

Issawi²,

Sol³

et al. 2020

Preprint

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Botrytis cinerea is a necrotic fungal plant pathogen responsible for the gray mold disease on more than 200 crops, including grapevine. Due to its genetic plasticity, this fungus presents a strong resistance to a large spectrum of fungicides. Thus, new fighting strategies against B. cinerea are urgently needed. In this context, antimicrobial photodynamic treatment (APDT) was considered. APDT involves the use of a photosensitizer that generates reactive oxygen species upon illumination. Tetra-4-sulfonatophenyl porphyrin tetra-ammonium (TPPS) was tested on B. cinerea; upon light exposure. 1.5 µM TPPS was shown to completely inhibit mycelial growth. A concentration of 12.5 µM TPPS was tested on three genetic background clones from Chardonnay, Merlot and Sauvignon, grown in vitro for 2 months. Treated root apparatus of the three backgrounds was able to increase thiol production as a molecular protection against photoactivated TPPS, leading to a normal phenotype as compared with control plantlets. Finally, two-month-old grapevine leaves were infected with four-day-old mycelium of B. cinerea pre-incubated or not with TPPS. The pre-treated mycelium was unable to infect the isolated leaves of any of the three grapevine varieties after 72 h growth when subjected to a 16 h photoperiod, contrary to untreated mycelium. These results on fungus, plantlets and Botrytis-grapevine leaves, in contact with a very low concentration of TPPS, suggest a strong potential of photo-treatment against Botrytis mycelium for future agricultural practices in vineyard or other cultures.

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Section: Tpps Localization Inside Mycelial Cellsmentioning

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Section: Tpps Localization Inside Mycelial Cellsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Photodynamic inactivation of Botrytis cinerea for a safe pest management of grapevine

Ambrosini¹,

Issawi²,

Sol³

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…With the aim to develop APDT for agriculture applications, TPPS could be a good candidate because of its low toxicity for plants. Moreover, TPPS remains negatively charged in many chemical environments even under acidic pH and does not aggregate in solution, allowing it to easily permeate cells through cell walls and membranes 29,30 . Therefore, we hypothesized that TPPS could be a good PS candidate to kill the plant pathogen B. cinerea and has potential to be a safe option for grapevine (Vitis vinifera L.) explants.…”

mentioning

confidence: 99%

Photodynamic inactivation of Botrytis cinerea by an anionic porphyrin: an alternative pest management of grapevine

Ambrosini

Issawi

Sol

et al. 2020

Sci Rep

Self Cite

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Botrytis cinerea is a necrotic plant fungus that causes gray mold disease in over 200 crops, including grapevine. Due to its genetic plasticity, this fungus presents strong resistance to many fungicides. Thus, new strategies against B. cinerea are urgently needed. In this context, antimicrobial photodynamic treatment (APDT) was considered. APDT involves the use of a photosensitizer that generates reactive oxygen species upon illumination with white light. Tetra-4-sulfonatophenyl porphyrin tetra-ammonium (TPPS) was tested on B. cinerea using light. 1.5 µM TPPS completely inhibited mycelial growth. TPPS (12.5 µM) was tested on three grapevine clones from Chardonnay, Merlot and Sauvignon, grown in vitro for 2 months. Treated root apparatus of the three backgrounds increased thiol production as a molecular protection against photoactivated TPPS, leading to a normal phenotype as compared with control plantlets. Finally, 2-month-old grapevine leaves were infected with 4-day-old mycelium of B. cinerea pre-incubated or not with TPPS. The pre-treated mycelium was unable to infect the detached leaves of any of the three grapevine varieties after 72 h growth when subjected to a 16 h photoperiod, contrary to untreated mycelium. These results suggest a strong potential of photo-treatment against B. cinerea mycelium for future agricultural practices in vineyard or other cultures.

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The dark side of 5,10,15,20-(tetra-4-sulfonatophenyl)-porphyrin tetra-ammonium (TPPS) on Botrytis cinerea mycelium growth

Ambrosini

Riou

2022

J. Porphyrins Phthalocyanines

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The powerful inhibitory effect of a photoactivated anionic porphyrin (TPPS) on the mycelium growth of a phytopathogenic fungus Botrytis cinerea, was previously demonstrated, suggesting a new agricultural application of photodynamic treatment. In this context, it was also needed to investigate the effect of non-photoactivated TPPS onB. cinerea.Unexpectedly, TPPS tested at 3.5 [Formula: see text]M, induced a delay of the Botrytis cinerea mycelium growth that was later recovered under dark conditions. This delay, compared to the control, was low and suggested that the stress was induced by TPPS. This hypothesis was also confirmed at phenotypical level by Environmental Scanning Electron Microscopy analysis. Further tests at a biochemical level: total proteins, thiols and proline content determinations; and at cellular level, by monitoring cell leakage, gave more evidence for the presence of this stress. Nevertheless, TPPS induced a very short-lived effect on B. cinerea, suggesting that the mycelium was able to induce a rapid defense mechanism that involved medium acidification. A 4-day-old mycelium acidified the culture medium from a pH of 8 to less than 4. This acidic medium thus induced changes in the TPPS chemical structure that became protonated in its inner core. To our knowledge, this is the first paper that reports a dark effect of TPPS on Botrytis cinereamycelium growth that could be rapidly counteracted by the protonation of TPPS leading to its no-longer dark toxicity.

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Crossing the First Threshold: New Insights into the Influence of the Chemical Structure of Anionic Porphyrins on Plant Cell Wall Interactions and Photodynamic Cell Death Induction

Cited by 3 publications

References 44 publications

Photodynamic inactivation of Botrytis cinerea for a safe pest management of grapevine

Photodynamic inactivation of Botrytis cinerea for a safe pest management of grapevine

Photodynamic inactivation of Botrytis cinerea by an anionic porphyrin: an alternative pest management of grapevine

The dark side of 5,10,15,20-(tetra-4-sulfonatophenyl)-porphyrin tetra-ammonium (TPPS) on Botrytis cinerea mycelium growth

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