Congruence between PM H+-ATPase and NADPH oxidase during root growth: a necessary probability
- 46 Downloads
Plasma membrane (PM) H+-ATPase and NADPH oxidase (NOX) are two key enzymes responsible for cell wall relaxation during elongation growth through apoplastic acidification and production of ˙OH radical via O2˙−, respectively. Our experiments revealed a putative feed-forward loop between these enzymes in growing roots of Vigna radiata (L.) Wilczek seedlings. Thus, NOX activity was found to be dependent on proton gradient generated across PM by H+-ATPase as evident from pharmacological experiments using carbonyl cyanide m-chlorophenylhydrazone (CCCP; protonophore) and sodium ortho-vanadate (PM H+-ATPase inhibitor). Conversely, H+-ATPase activity retarded in response to different ROS scavengers [CuCl2, N, N’ –dimethylthiourea (DMTU) and catalase] and NOX inhibitors [ZnCl2 and diphenyleneiodonium (DPI)], while H2O2 promoted PM H+-ATPase activity at lower concentrations. Repressing effects of Ca+2 antagonists (La+3 and EGTA) on the activity of both the enzymes indicate its possible mediation. Since, unlike animal NOX, the plant versions do not possess proton channel activity, harmonized functioning of PM H+-ATPase and NOX appears to be justified. Plasma membrane NADPH oxidase and H+-ATPase are functionally synchronized and they work cooperatively to maintain the membrane electrical balance while mediating plant cell growth through wall relaxation.
KeywordsCalcium NADPH oxidase (NOX) Plasma membrane (PM) H+-ATPase Proton gradient Root growth ROS
One of the authors (AM) gratefully recognizes financial support for the present investigation from University Grants Commission (UGC), New Delhi, India, as BSR Fellowship [vide letter F. No. 25-1/2014-15(BSR)/220/2009/(BSR)].
RKK envisaged the study. AM and RKK designed the work. AM performed the experiments. AM and RKK wrote the article.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no competing interests.
- Beffagna N, Buffoli B, Busi C (2005) Modulation of reactive oxygen species production during osmotic stress in Arabidopsis thaliana cultured cells: involvement of the plasma membrane Ca+2-ATPase and H+-ATPase. Plant Cell Physiol 46(8):1326–1339. https://doi.org/10.1093/pcp/pci142 CrossRefPubMedGoogle Scholar
- Carter C, Healy R, O’Tool NM, Saqlan Naqvi SM, Ren G, Park S, Beattie GA, Horner HT, Thornburg RW (2007) Tobacco nectarines express a novel NADPH oxidase implicated in the defense of floral reproductive tissues against microorganisms. Plant Physiol 143(1):389–399. https://doi.org/10.1104/pp.106.089326 CrossRefPubMedPubMedCentralGoogle Scholar
- Fluhr R (2009) Reactive oxygen-generating NADPH oxidases in plants. In: Rio LA, Puppo a (eds) reactive oxygen species in plant signalling. Springer-Verlag, Berlin, pp 1–23. https://doi.org/10.1007/978-3-642-00390-5_1
- Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422(6930):442–446. https://doi.org/10.1038/nature01485 CrossRefPubMedGoogle Scholar
- Hejl AM, Koster KL (2004) Juglone disrupts root plasma membrane H+-ATPase activity and impairs water uptake, root respiration, and growth in soybean (Glycine max) and corn (Zea mays). J Chem Ecol 30(2):453–471. https://doi.org/10.1023/B:JOEC.0000017988.20530.d5 CrossRefPubMedGoogle Scholar
- Janicka-Russak M (2011) Plant plasma membrane H+-ATPases in adaptation of plants to abiotic stresses. In: Shanker A (ed) Abiotic stress response in plants—physiological, biochemical and genetic perspectives. InTech, pp 197–218. https://doi.org/10.5772/24121
- Kurusu T, Kuchitsu K, Tada Y (2015) Plant signalling networks involving Ca+2 and Rboh/Nox-mediated ROS production under salinity stress. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00427
- Li J, Chen G, Wang X, Zhang Y, Jia H, Bi Y (2011) Glucose-6-phosphate dehydrogenase-dependent hydrogen peroxide production is involved in the regulation of plasma membrane H+-ATPase and Na+/H+ antiporter protein in salt-stressed callus from Carex moorcroftii. Physiol Plant 141(3):239–250. https://doi.org/10.1111/j.1399-3054.2010.01429.x CrossRefPubMedGoogle Scholar
- Ogasawara Y, Kaya H, Hiraoka G, Yumoto F, Kimura S, Kadota Y, Hishinuma H, Senzaki E, Yamagoe S, Nagata K, Nara M, Suzuki K, Tanokura M, Kuchitsu K (2008) Synergistic activation of Arabidopsis NADPH oxidase AtrbohD by ca+2 and phosphorylation. J Biol Chem 283(14):8885–8892. https://doi.org/10.1074/jbc.M708106200 CrossRefPubMedGoogle Scholar
- Ramsey IS, Ruchti E, Kaczmarek JS, Clapham DE (2009) Hv1 proton channels are required for high-level NADPH oxidase-dependent superoxide production during the phagocyte respiratory burst. Proc Natl Acad Sci 106(18):7642–7647. https://doi.org/10.1073/pnas.0902761106 CrossRefPubMedPubMedCentralGoogle Scholar
- Schopfer P, Plachy C, Frahry G (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberllin and abscisic acid. Plant Physiol 125:1591–1602CrossRefPubMedPubMedCentralGoogle Scholar
- Singh KL, Chaudhuri A, Kar RK (2014) Superoxide and its metabolism during germination and axis growth of Vigna radiata (L.) Wilczek seeds. Plant Signal Behav. https://doi.org/10.4161/psb.29278
- Taiz L, Zeiger E, Møller IM, Murphy A (2015) Plant physiology and development. Sinauer, SunderlandGoogle Scholar
- Voronkov AS, Andreev IM, Timofeeva GV, Kovaleva LV (2010) Electrogenic activity of plasma membrane H+-ATPase in germinating male gametophyte of Petunia and its stimulation by exogenous auxin: mediatory role of calcium and reactive oxygen species. Russ J Plant Physiol 57(3):401–407. https://doi.org/10.1134/S102144371003012X CrossRefGoogle Scholar
- Wu J, Kurten EL, Monshausen G, Hummel GM, Gilroy S, Baldwin IT (2007) NaRALF, a peptide signal essential for the root hair tip apoplastic pH in Nicotiana attenuata, is required for root hair development and plant growth in native soils. Plant J 52(5):877–890. https://doi.org/10.1111/j.1365-313X.2007.03289.x CrossRefPubMedGoogle Scholar