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Benzothiadiazole effect in the compatible tomato-Meloidogyne incognita interaction: changes in giant cell development and priming of two root anionic peroxidases

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Abstract

Main conclusion

BTH application is effective in root-knot nematode-tomato interaction in a way that involves a delay in the formation of nematode feeding site and triggers molecular responses at several levels.

The compatible interaction between root-knot nematodes and their hosts requires the nematode to overcome plant defense systems so that a sophisticated permanent feeding site (giant cells) can be produced within the host roots. It has been suggested that activators of plant defenses may provide a novel management strategy for controlling root-knot nematodes but little is known about the molecular basis by which these elicitors operate. The role of pre-treatment with Benzothiadiazole (BTH), a salicylic acid analog, in inducing resistance against Meloidogyne incognita infection was investigated in tomato roots. A decrease in galling in roots and feeding site numbers was observed following BTH treatment. Histological investigations showed a delay in formation of feeding sites in treated plants. BTH-treated galls had higher H2O2 production, lignin accumulation, and increased peroxidase activity than untreated galls. The expression of two tomato genes, Tap1 and Tap2, coding for anionic peroxidases, was examined by qRT-PCR and in situ hybridization in response to BTH. Tap1 was induced at all infection points, reaching the highest level at 15 dpi. Tap2 expression, although slightly delayed in untreated galls, increased during infection in both treated and untreated galls. The expression of Tap1 and Tap2 was observed in giant cells of untreated roots, whereas the transcripts were localized in both giant cells and in parenchyma cells surrounding the developing feeding sites in treated plants. These results show that BTH applied to tomato plants makes them more resistant to infection by nematodes, which become less effective in overcoming root defense pathway.

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Abbreviations

BABA:

ß-Amino-n-butyric acid

BTH:

Benzothiadiazole

dpi:

Days post inoculation

GC:

Giant cell

INA:

Isonicotinic acid

J2:

Second-stage juveniles

PBS:

Phosphate-buffered saline

POX:

Peroxidase

PR:

Pathogenesis related

RKN:

Root-knot nematode

SA:

Salicylic acid

SAR:

Systemic acquired resistance

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Acknowledgments

We thank Mr. Roberto Lerario (Istituto per la Protezione Sostenibile delle Piante, CNR, Bari, Italy) for technical assistance and Dr. Teresa Bleve-Zacheo for helpful revision of the manuscript. This work was supported with funds provided by the Italian Ministry of Economy and Finance to the National Research Council for the project “Innovazione e Sviluppo del Mezzogiorno-Conoscenze Integrate per Sostenibilità ed Innovazione del Made in Italy Agroalimentare”, Legge n. 191/2009.

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Correspondence to Maria Teresa Melillo.

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M. T. Melillo and P. Veronico contributed equally to the work.

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Melillo, M.T., Leonetti, P. & Veronico, P. Benzothiadiazole effect in the compatible tomato-Meloidogyne incognita interaction: changes in giant cell development and priming of two root anionic peroxidases. Planta 240, 841–854 (2014). https://doi.org/10.1007/s00425-014-2138-7

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