Responses of an adventitious fast‐growing plant to photodynamic stress: comparative study of anionic and cationic porphyrin effect on Arabidopsis thaliana

Abstract

Antimicrobial photodynamic treatment (APDT) based on the use of a photosensitizer to produce reactive oxygen species (ROS) that induce cell death could be envisaged to fight against plant pathogens. For setting this strategy, we want to study how plants themselves respond to photodynamic treatment. In previous work we showed that tomato plantlets were able to resist photoactivated tetra (N-methylpyridyl) porphyrin (CP) or the zinc metalated form (CP-Zn). To enlarge our plant expertise related to exogenous porphyrins treatment and to further defend this approach, we studied how a weed like Arabidopsis thaliana responded to exogenous supply of anionic and cationic porphyrins. Both types of photosensitizers had no negative effect on seed germination and did not hamper the development etiolated Arabidopsis plantlet under dark conditions. Thus, post-emergence effects of porphyrin photoactivation on the development of 14 day-old in vitro Arabidopsis plantlet under light were observed. CP-Zn was the most efficient photosensitizer to kill Arabidopsis plantlets while anionic tetra (4-sulfonatophenyl) porphyrin only delayed their growth and development. Indeed only 7% of plantlets could be rescued after CP-Zn treatment. Furthermore, non-enzymatic and enzymatic defense components involved in detoxification of ROS generated by CP-Zn under illumination were downregulated or stable with the exception of sevenfold increase in proline content. As previously demonstrated in the literature for microbial agents and in the present work for Arabidopsis, CP-Zn was efficient enough to eradicate unwanted vegetation and plant pathogens without at the same time killing plants of agronomic interest such as tomato plantlets.

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

“…The choice of these three varieties was due to their different susceptibility to B. cinerea (Dubos 2002;Fermaud et al 2011). Furthermore, as expected and according to our previous studies (Guillaumot et al 2016;Issawi et al 2018b), TPPS did not induce any phenotypical or biochemical modi cation of the three grapevine plantlets. In addition, this TPPS concentration (12.5 µM) was approximately ten times higher than the minimal concentration inhibiting the mycelium growth (1.5 µM); thus, the strategy presented in this article could work against pathogens without altering plant growth and development.…”

“…In particular, the addition of an ammonium counterion to the sulfate moiety contributed to the inhibition of mycelium growth in the pathogenic fungus Eutypa lata, an ascomycete like B.cinerea. Therefore, taking these results from previous works into account (Fleurat-Lessard et al 2011;Guillaumot et al 2016;Issawi et al 2018b;, we decided to test TPPS, a molecule that presents four external sulfonate groups linked with a tetrapyrrole ring. Indeed, TPPS with an ammonium counterion could be as an excellent antifungal candidate.…”

“…The mixture was centrifuged at 13,000 × g at 4 °C for 20 min. The supernatants were analyzed for their malondialdehyde (MDA) content as described by Hodges (1999) with minor modi cations described in Issawi et al (2018b).…”

“…Coumarins, furocoumarin and phenothiazinium were shown to be active against the plant-infecting fungi Colletrichum acuratum and Aspergillus nidulans (De Menezes et al a, b;2014;Fracarolli et al 2016). Finally, when tested on Citrus sinensis petals and leaves, methylene blue was able to kill the Colletotrichum abscissum fungus and proved to be harmless to plant organs; in addition, this treatment did not induce any secondary resistance (Gonzales et al 2017) Previous research works explored the in vitro phenotypical and molecular responses of Arabidopsis and tomato plantlets to the photodynamic stress induced by an exogenous supply of PS (Guillaumot et al 2016;Issawi et al 2018b). The cationic tetra (N-methylpyridyl) porphyrin, either free base or zinccomplexed, tested at 3.5 µM, in icted harmful effects on both 14-day-old Arabidopsis and tomato plantlets.…”

“…Nevertheless, while Arabidopsis plantlets were killed, tomato plantlets could be rescued after a 14 day-treatment (Guillaumot et al 2016). Surprisingly, the anionic porphyrin tetra-4sulfonatophenylporphyrin tetra-ammonium (TPPS) did not provoke any harmful effect on both plantlets even at concentrations as high as 50 µM (Guillaumot et al 2016;Issawi et al 2018b). With the aim to develop APDT for agriculture applications, TPPS could be a good candidate because of its low toxicity for plants.…”