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Nitric oxide plays a central role in determining lateral root development in tomato

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Abstract

Nitric oxide (NO) is a bioactive molecule that functions in numerous physiological processes in plants, most of them involving cross-talk with traditional phytohormones. Auxin is the main hormone that regulates root system architecture. In this communication we report that NO promotes lateral root (LR) development, an auxin-dependent process. Application of the NO donor sodium nitroprusside (SNP) to tomato (Lycopersicon esculentum Mill.) seedlings induced LR emergence and elongation in a dose-dependent manner, while primary root (PR) growth was diminished. The effect is specific for NO since the NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (CPTIO) blocked the action of SNP. Depletion of endogenous NO with CPTIO resulted in the complete abolition of LR emergence and a 40% increase in PR length, confirming a physiological role for NO in the regulation of root system growth and development. Detection of endogenous NO by the specific probe 4,5-diaminofluorescein diacetate (DAF-2 DA) revealed that the NO signal was specifically located in LR primordia during all stages of their development. In another set of experiments, SNP was able to promote LR development in auxin-depleted seedlings treated with the auxin transport inhibitor N-1-naphthylphthalamic acid (NPA). Moreover, it was found that LR formation induced by the synthetic auxin 1-naphthylacetic acid (NAA) was prevented by CPTIO in a dose-dependent manner. All together, these results suggest a novel role for NO in the regulation of LR development, probably operating in the auxin signaling transduction pathway.

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Abbreviations

CPTIO :

2-(4-Carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide

DAF-2 DA :

4,5-Diaminofluorescein diacetate

LR :

Lateral root

NAA :

1-Naphthylacetic acid

NO :

Nitric oxide

NPA :

N-1-Naphthylphthalamic acid

PR :

Primary root

SNP :

Sodium nitroprusside

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Acknowledgments

We thank Dr. Gabriela Pagnussat for critical reading and helpful discussions of the manuscript. This work was supported by Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, PICTs 1-6496/99 and 1-9767/00 to L.L.), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 0898/98 to L.L.), Fundación Antorchas and institutional grants from Universidad Nacional de Mar del Plata (UNMdP), Argentina. L.L. is a career research scientist and M.G. a postgraduate fellow from CONICET, Argentina. N.C.-A. is a student fellow from UNMdP, Argentina. N. C.-A. and M.G. contributed equally to this work.

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  1. Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, CC 1245, 7600, Mar del Plata, Argentina

    Natalia Correa-Aragunde, Magdalena Graziano & Lorenzo Lamattina

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  1. Natalia Correa-Aragunde
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  2. Magdalena Graziano
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  3. Lorenzo Lamattina
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Correspondence to Lorenzo Lamattina.

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Correa-Aragunde, N., Graziano, M. & Lamattina, L. Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218, 900–905 (2004). https://doi.org/10.1007/s00425-003-1172-7

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