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First published online September 3, 2004; 10.1104/pp.104.042812

Plant Physiology 136:2722-2733 (2004)
© 2004 American Society of Plant Biologists

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CELL BIOLOGY AND SIGNAL TRANSDUCTION

Cellular and Subcellular Localization of Endogenous Nitric Oxide in Young and Senescent Pea Plants1,2

Francisco J. Corpas*, Juan B. Barroso, Alfonso Carreras, Miguel Quirós, Ana M. León, María C. Romero-Puertas, Francisco J. Esteban, Raquel Valderrama, José M. Palma, Luisa M. Sandalio, Manuel Gómez and Luis A. del Río

Departamento de Bioquímica, Biología Celular y Molecular de Plantas (F.J.C., A.M.L., M.C.R-P., J.M.P., L.M.S., L.A.R.), and Departamento de Agroecología y Protección Vegetal (M.G.), Estación Experimental del Zaidín (EEZ), Consejo Superior de Investigaciones Científicas, E–18080 Granada, Spain; Grupo de Señalización Molecular y Sistemas Antioxidantes en Plantas, Unidad Asociada al Consejo Superior de Investigaciones Científicas (EEZ), Área de Bioquímica y Biología Molecular, Universidad de Jaén, E–23071 Jaen, Spain (J.B.B., A.C., F.J.E., R.V.); and Departamento de Química Inorgánica, Facultad de Ciencias, Universidad de Granada, E–18001 Granada, Spain (M.Q.)

The cellular and subcellular localization of endogenous nitric oxide (NO·) in leaves from young and senescent pea (Pisum sativum) plants was studied. Confocal laser scanning microscopy analysis of pea leaf sections with the fluorescent probe 4,5-diaminofluorescein diacetate revealed that endogenous NO· was mainly present in vascular tissues (xylem and phloem). Green fluorescence spots were also detected in the epidermal cells, palisade and spongy mesophyll cells, and guard cells. In senescent leaves, NO· generation was clearly reduced in the vascular tissues. At the subcellular level, by electron paramagnetic resonance spectroscopy with the spin trap Fe(MGD)2 and fluorometric analysis with 4,5-diaminofluorescein diacetate, NO· was found to be an endogenous metabolite of peroxisomes. The characteristic three-line electron paramagnetic resonance spectrum of NO·, with g = 2.05 and aN = 12.8 G, was detected in peroxisomes. By fluorometry, NO· was also found in these organelles, and the level measured of NO· was linearly dependent on the amount of peroxisomal protein. The enzymatic production of NO· from L-Arg (nitric oxide synthase [NOS]-like activity) was measured by ozone chemiluminiscence. The specific activity of peroxisomal NOS was 4.9 nmol NO· mg–1 protein min–1; was strictly dependent on NADPH, calmodulin, and BH4; and required calcium. In senescent pea leaves, the NOS-like activity of peroxisomes was down-regulated by 72%. It is proposed that peroxisomal NO· could be involved in the process of senescence of pea leaves.

1 This work was supported by the Dirección General de Investigación, Ministry of Education and Science (grant no. PB98–0493–01), the European Union (contract no. HPRN–CT–2000–00094), and Junta de Andalucía (groups CVI 0192 and CVI 0286).

2 This article is dedicated to the loved and esteemed memory of Prof. Dr. Julio López-Gorgé, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, who died of a stroke on June 7, 2004, at the age of 69.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.042812.

* Corresponding author; e-mail javier.corpas{at}eez.csic.es; fax 34–958–129600.

Received March 17, 2004; returned for revision May 27, 2004; accepted May 30, 2004.




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