Nitric Oxide and Cyclic GMP Are Messengers in the Indole Acetic Acid-Induced Adventitious Rooting Process

Abstract

This report describes part of the signaling pathway and some of the molecules involved in the auxin-induced adventitious root formation in cucumber (Cucumis sativus). Previous results showed that nitric oxide (NO) mediates the auxin response during adventitious root formation (Pagnussat et al., 2002). To determine the order of action of indole acetic acid (IAA) and NO within the signal transduction pathway and to elucidate the target molecules that are downstream of NO action, cucumber hypocotyl cuttings were submitted to a pretreatment leading to endogenous auxin depletion. The auxin depletion treatment provoked a 3-fold reduction of the root number in comparison to the nondepleted explants. The NO-donor sodium nitroprusside was able to promote adventitious rooting in auxin-depleted explants, whereas the specific NO scavenger cPTIO prevented the effect of sodium nitroprusside. The endogenous NO level was monitored in both control and auxin-depleted explants using a NO-specific fluorescent probe. The NO level was 3.5-fold higher in control (nondepleted) explants than in auxin-depleted ones. The exogenous application of IAA restored the NO concentration to the level found in nondepleted explants. Because NO activates the enzyme guanylate cyclase (GC), we analyzed the involvement of the messenger cGMP in the adventitious root development mediated by IAA and NO. The GC inhibitor LY83583 reduced root development induced by IAA and NO, whereas the cell-permeable cGMP derivative 8-Br-cGMP reversed this effect. The endogenous level of cGMP is regulated by both the synthesis via GC and its degradation by the phosphodiesterase activity. When assayed, the phosphodiesterase inhibitor sildenafil citrate was able to induce adventitious rooting in both nondepleted and auxin-depleted explants. Results indicate that NO operates downstream of IAA promoting adventitious root development through the GC-catalyzed synthesis of cGMP.The plant hormone auxin is involved in the regulation of most aspects of plant growth and development, including cell division, elongation, and differentiation. The role of auxins in adventitious rooting is particularly important because the hormone initiates this process-which involves cell division and primordium formation-inducing the dedifferentiation of the cells to form the apical meristem. Although genetic approaches have revealed some discrete aspects of auxin transport, signaling, and response, the understanding of the molecular mechanism of auxin action in the establishment of new root meristems remains preliminary (Doerner, 2000; Berleth and Sachs, 2001).Nitric oxide (NO) is a diffusible multifunctional molecule involved in numerous physiological processes in phylogenetically distant species (Gow and Ischiropoulos, 2001). It was first described in mammals, where it plays variable functions ranging from dilation of blood vessels to neurotransmission and immune response. In comparison with animal studies, relative little is known about NO biological functions in plants. However, the presence of...

Retracted: Nitric oxide enhances plant ultraviolet‐B protection up‐regulating gene expression of the phenylpropanoid biosynthetic pathway

“…Consequently, NO activates signalling pathways, which results in changes of gene expression, through intermediate cellular messengers. Several lines of evidence indicate that cGMP acts downstream of NO signalling (Durner, Wendehenne & Klessig 1998;García-Mata et al 2003;Neill, Desikan & Hancock 2003;Pagnussat, Lanteri & Lamattina 2003). Interestingly, it was recently reported that cGMP is required for the NO-dependent expression of genes involved in the flavonoid biosynthetic pathway (Suita et al 2009).…”

N-3-Oxo-Decanoyl-l-Homoserine-Lactone Activates Auxin-Induced Adventitious Root Formation via Hydrogen Peroxide- and Nitric Oxide-Dependent Cyclic GMP Signaling in Mung Bean

“…cGMP is an intracellular messenger downstream of NO action and is synthesized in response to auxin stimulation (Pagnussat et al, 2003). Consequently, we assessed the potential involvement of cGMP in 3-O-C10-HL-induced adventitious root formation.…”

“…Adventitious roots are derived primarily from plant stems and are essential for plant adaptation to environmental stress; studying the adventitious root formation is also significant for both fundamental and applied plant biology. The phytohormone auxin plays an essential role in stimulating adventitious root formation (Pagnussat et al, 2003(Pagnussat et al, , 2004. Significant progress has been made to elucidate the molecular mechanism of auxin action via the auxin/ indole-3-acetic acid (Aux/IAA) and auxin-response factor (ARF) gene families.…”

“…Significant progress has been made to elucidate the molecular mechanism of auxin action via the auxin/ indole-3-acetic acid (Aux/IAA) and auxin-response factor (ARF) gene families. NO and cyclic GMP (cGMP) mediate auxin-induced root organogenesis (Pagnussat et al, 2003), H 2 O 2 also acts as a signaling molecule in plant adventitious root formation (Li et al, 2007), but the interplay of H 2 O 2 , NO, and cGMP in AHL-mediated root development needs to be fully investigated.…”

“…Accumulated evidence demonstrates that both nitric oxide (NO) and hydrogen peroxide (H 2 O 2 ) are signals to participate in multiple physiological processes, including systemic acquired resistance, the hypersensitive response, leaf senescence, programmed cell death, stomatal closure, root gravitropism, cell wall development, pollen-stigma interaction, and development (Grant and Loake, 2000;Neill et al, 2002;Pagnussat et al, 2003;Hu et al, 2004;Mittler et al, 2004;Schuhegger et al, 2006;Xuan et al, 2008). Adventitious roots are derived primarily from plant stems and are essential for plant adaptation to environmental stress; studying the adventitious root formation is also significant for both fundamental and applied plant biology.…”