Extracellular ATP and nitric oxide signaling pathways regulate redox-dependent responses associated to root hair growth in etiolated Arabidopsis seedlings

Abstract

Addendum to: Tonón C, Terrile MC, Iglesias MJ, Lamattina L, Casalongué C. Extracellular ATP, nitric oxide and superoxide act coordinately to regulate hypocotyl growth in etiolated Arabidopsis seedlings. J Plant Physiol 2010; 167:540-546; PMID: 19962212; DOI: 10.1016 DOI: 10. /j.jplph.2009. E xtracellular ATP (eATP) and nitric oxide (NO) have emerged as crucial players in plant development, stress responses and cell viability. Glutathione (GSH) is an abundant reducing agent with proposed roles in plant growth, development and stress physiology. In a recent publication, we demonstrated that eATP and NO restore hypocotyl elongation of etiolated Arabidopsis seedlings treated with GSH. Here it is reported that exogenous ATP also restores root hair growth suggesting a role for ATP and NO in the regulation of redox balance associated to specific processes of plant morphogenesis. A tentative model integrating redox-, eATPand NO-signaling pathways during root hair growth in Arabidopsis seedlings is presented. Linking Signaling Pathways to Gain Understanding on the Regulation of Morphological Processes in PlantsThe first living organisms evolved under reducing conditions a long time before the environment became oxidizing due to oxygen produced by photosynthesis. As a consequence, the most fundamental signaling pathways were initially adapted to reducing conditions. Plants, as sessile organisms have taken advantage of the regulatory mechanisms evolved on a changing redox-status and nowadays they are strongly dependent of environmental redox conditions. An efficient redox control together with other signaling mechanisms cooperates to maintain the steady-state redox homeostasis in plant cell. In this scenario, two small signaling molecules such as ATP and NO have a very ancient origin and are involved in cell redox physiology. 1,2 ATP and NO play diverse biological functions in phylogenetically distant species. Intracellular ATP is the major source of energy for cellular reactions. However, ATP also acts as a signaling molecule at the extracellular face of the plasma membrane in animals as well as in plants. 3 NO is an important regulatory molecule in eukaryotes. Several roles have been attributed to extracellular ATP (eATP) and NO in plants, ranging from cell viability to pathogen defence and cell death.2-4 NO production stimulated by eATP was shown in tomato suspension cells, 5 hairy roots of Salvia miltiorrhiza 6 as well as in algae. 7 Reichler et al. 8 showed that the intersection of eATP signaling and NO via the cellular messenger cGMP regulates pollen germination and pollen tube growth in Arabidopsis. Thus, the biochemical and molecular mechanisms underlying eATP and NO signaling pathways in plants have just begun to emerge. Lately, we have described an interconnection between eATP, NO and redox system during hypocotyl elongation in etiolated Arabidopsis seedlings. 9It was demonstrated that a fine-tuning of redox balance and endogenous NO level is associated to eATP action. Therefore, these findings open a new w...

Both the stimulation and inhibition of root hair growth induced by extracellular nucleotides in Arabidopsis are mediated by nitric oxide and reactive oxygen species

“…eATP and NO also appear to regulate redox-dependent effects on root hair initiation . Furthermore, our findings support the model for eATP control of root hair growth proposed by Terrile et al (2010). These recent results are a further indication that there is coordination between eATP, NO and ROS signaling during plant growth and development.…”

Extracellular Nucleotides and Apyrases Regulate Stomatal Aperture in Arabidopsis

“…The induction of these signaling intermediates by eATP in other species is also well established (Kim et al, 2006;Foresi et al, 2007;Wu and Wu, 2008;Clark et al, 2010b;Terrile et al, 2010). Because H 2 O 2 and NO play roles in stomatal closure in response to ABA and stressors (García-Mata and Lamattina, 2001;Desikan et al, 2002Desikan et al, , 2006Kwak et al, 2003;Neill et al, 2008), we tested the effects of applied nucleotides on their production in guard cells.…”

Receptor-Like Activity Evoked by Extracellular ADP in Arabidopsis Root Epidermal Plasma Membrane

“…Extracellular purine nucleotides have been shown to be involved in the regulation of plant cell viability, membrane permeability, immunity, symbiosis, stress responses, and growth (Lew and Dearnaley, 2000;Tang et al, 2003;Chivasa et al, 2005Chivasa et al, , 2009Kim et al, 2006Kim et al, , 2009Roux and Steinebrunner, 2007;Wu et al, 2007;Riewe et al, 2008a;Wu and Wu, 2008;Yi et al, 2008;Demidchik et al, 2009;Govindarajulu et al, 2009;Kim et al, 2009;Clark et al, 2010aClark et al, , 2010bTanaka et al, 2010aTanaka et al, , 2010bTerrile et al, 2010;Tonó n et al, 2010). Purine nucleotide release from plant cells may occur through wounding, exocytosis, or through the activity of plasma membrane (PM) ATP-binding cassette transporters (Thomas et al, 2000;Kim et al, 2006).…”

“…Manipulation of ecto-apyrase levels results in abnormal growth in Arabidopsis (Arabidopsis thaliana), cotton (Gossypium hirsutum), and potato (Solanum tuberosum; Wu et al, 2007;Riewe et al, 2008a;Clark et al, 2010aClark et al, , 2010b while nodulation by Bradyrhizobium japonicum is impaired in ecto-apyrase-deficient soybean (Glycine max; Govindarajulu et al, 2009). Current models suggest that poise of the cell's state between death, stress adaptation, and growth involves signaling governed by the level of extracellular ATP (Chivasa et al, 2005Roux and Steinebrunner, 2007;Wu et al, 2007;Wu and Wu, 2008;Kim et al, 2009;Clark et al, 2010aClark et al, , 2010bTerrile et al, 2010;Tonó n et al, 2010).…”