Advertisement

An Overview of Methods in Plant Nitric Oxide (NO) Research: Why Do We Always Need to Use Multiple Methods?

  • Hideo YamasakiEmail author
  • Naoko S. Watanabe
  • Yasuko Sakihama
  • Michael F. Cohen
Part of the Methods in Molecular Biology book series (MIMB, volume 1424)

Abstract

The free radical nitric oxide (NO) is a universal signaling molecule among living organisms. To investigate versatile functions of NO in plants it is essential to analyze biologically produced NO with an appropriate method. Owing to the uniqueness of NO, plant researchers may encounter difficulties in applying methods that have been developed for mammalian study. Based on our experience, we present here a practical guide to NO measurement fitted to plant biology.

Key words

Chemiluminescence detection cPTIO DAF Electrochemical detection Nitric oxide RNS ROS RSS 

Notes

Acknowledgements

Due to space limitations we were not able to cite many brilliant works on plant NO research that have applied the methods described in this chapter. Please refer to other chapters for such investigations. We thank Dr. Jon Fukuto for his valuable comments on this chapter. This work was supported by the grants to H.Y. from the Japanese Ministry of Education, Science, Culture and Sports.

References

  1. 1.
    Yamasaki H (2005) The NO world for plants: achieving balance in an open system. Plant Cell Environ 28:78–84CrossRefGoogle Scholar
  2. 2.
    Mur LAJ, Mandon J, Persijn S et al (2013) Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5:1–17CrossRefGoogle Scholar
  3. 3.
    Yamasaki H, Itoh RD, Bouchard JN et al (2011) Nitric oxide synthase-like activities in plants. In: Foyer CH, Zhang H (eds) Nitrogen metabolism in plants in the post-genomic era, vol 42, Annual Plant Reviews. Blackwell Publishing Ltd, West Sussex, pp 103–125Google Scholar
  4. 4.
    Leshem YY (2000) Nitric oxide in plants: occurrence, function and use. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  5. 5.
    Yamasaki H (2004) Nitric oxide research in plant biology: its past and future. In: Magalhaes JR, Singh RP, Passos LP (eds) Nitric oxide signaling in higher plants. Focus on plant molecular biology. Studium Press, Houston, pp 1–23Google Scholar
  6. 6.
    Yamasaki H, Cohen MF (2006) NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends Plant Sci 11:522–524CrossRefPubMedGoogle Scholar
  7. 7.
    Koppenol WH, Traynham JG (1996) Say NO to nitric oxide: nomenclature for nitrogen- and oxygen-containing compounds. Methods Enzymol 268:3–7CrossRefPubMedGoogle Scholar
  8. 8.
    Yamasaki H, Watanabe NS, Fukuto J et al (2014) Nitrite-dependent nitric oxide production pathway: diversity of NO production systems. In: Tsukahara H, Kaneko K (eds) Studies on pediatric disorders. Springer, New York, pp 35–54CrossRefGoogle Scholar
  9. 9.
    Yamasaki H (2000) Nitrite-dependent nitric oxide production pathway: implications for involvement of active nitrogen species in photoinhibition in vivo. Philos Trans R Soc Lond B Biol Sci 355:1477–1488CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Yamasaki H, Sakihama Y, Takahashi S (1999) An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci 4:128–129CrossRefPubMedGoogle Scholar
  11. 11.
    Hughes MN (1999) Relationships between nitric oxide, nitroxyl ion, nitrosonium cation and peroxynitrite. Biochim Biophys Acta 1411:263–272CrossRefPubMedGoogle Scholar
  12. 12.
    Rogstam A, Larsson JT, Kjelgaard P et al (2007) Mechanisms of adaptation to nitrosative stress in Bacillus subtilis. J Bacteriol 189:3063–3071CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Bates JN, Baker MT, Guerra R et al (1991) Nitric oxide generation from nitroprusside by vascular tissue: evidence that reduction of the nitroprusside anion and cyanide loss are required. Biochem Pharmacol 42:S157–S165CrossRefPubMedGoogle Scholar
  14. 14.
    Liu XP, Liu QH, Gupta E et al (2005) Quantitative measurements of NO reaction kinetics with a Clark-type electrode. Nitric Oxide 13:68–77CrossRefPubMedGoogle Scholar
  15. 15.
    Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468:89–92CrossRefPubMedGoogle Scholar
  16. 16.
    Sakihama Y, Cohen MF, Grace SC et al (2002) Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177:67–80CrossRefPubMedGoogle Scholar
  17. 17.
    Cohen MF, Mazzola M, Yamasaki H (2006) Nitric oxide research in agriculture: bridging the plant and bacterial realms. In: Rai K, Takabe T (eds) Abiotic stress tolerance in plants. Springer, Dordrecht, pp 71–90CrossRefGoogle Scholar
  18. 18.
    Takahashi S, Tamashiro A, Sakihama Y et al (2002) High-susceptibility of photosynthesis to photoinhibition in the tropical plant Ficus microcarpa L. f. cv. Golden Leaves. BMC Plant Biol 2:1–8CrossRefGoogle Scholar
  19. 19.
    Mur LAJ, Mandon J, Cristescu SM et al (2011) Methods of nitric oxide detection in plants: a commentary. Plant Sci 181:509–519CrossRefPubMedGoogle Scholar
  20. 20.
    Mur LAJ, Santosa IE, Laarhoven LJJ et al (2005) Laser photoacoustic detection allows in planta detection of nitric oxide in tobacco following challenge with avirulent and virulent Pseudomonas syringae pathovars. Plant Physiol 138:1247–1258CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Conrath U, Amoroso G, Kohle H et al (2004) Non-invasive online detection of nitric oxide from plants and some other organisms by mass spectrometry. Plant J 38:1015–1022CrossRefPubMedGoogle Scholar
  22. 22.
    Rockel P, Strube F, Rockel A et al (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110CrossRefPubMedGoogle Scholar
  23. 23.
    Hossain KK, Itoh RD, Yoshimura G et al (2010) Effects of nitric oxide scavengers on thermoinhibition of seed germination in Arabidopsis thaliana. Russ J Plant Physiol 57:222–232CrossRefGoogle Scholar
  24. 24.
    Wink DA, Grisham MB, Mitchell JB et al (1996) Direct and indirect effects of nitric oxide in chemical reactions relevant to biology. Methods Enzymol 268:12–31CrossRefPubMedGoogle Scholar
  25. 25.
    Akaike T, Maeda H (1996) Quantitation of nitric oxide using 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl 3-oxide (PTIO). Methods Enzymol 268:211–221CrossRefPubMedGoogle Scholar
  26. 26.
    Malinski T, Mesaros S, Tomboulian P (1996) Nitric oxide measurement using electrochemical methods. Methods Enzymol 268:58–69CrossRefPubMedGoogle Scholar
  27. 27.
    Sakihama Y, Nakamura S, Yamasaki H (2002) Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organisms. Plant Cell Physiol 43:290–297CrossRefPubMedGoogle Scholar
  28. 28.
    Griess P (1879) Bemerkungen zu der Abhandlung der HH. Weselsky und Benedikt. Ueber einige Azoverbindungen. Ber Dtsch Chem Ges 12:426–428CrossRefGoogle Scholar
  29. 29.
    Stuehr DJ, Marletta MA (1985) Mammalian nitrate biosynthesis: mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. PNAS 82:7738–7742CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Vitecek J, Reinohl V, Jones RL (2008) Measuring NO production by plant tissues and suspension cultured cells. Mol Plant 1:270–284CrossRefPubMedGoogle Scholar
  31. 31.
    Hunter RA, Storm WL, Coneski PN et al (2013) Inaccuracies of nitric oxide measurement methods in biological media. Anal Chem 85:1957–1963CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517–529CrossRefPubMedGoogle Scholar
  33. 33.
    Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21CrossRefPubMedGoogle Scholar
  34. 34.
    Mallick N, Rai LC, Mohn FH et al (1999) Studies on nitric oxide (NO) formation by the green alga Scenedesmus obliquus and the diazotrophic cyanobacterium Anabaena doliolum. Chemosphere 39:1601–1610CrossRefPubMedGoogle Scholar
  35. 35.
    Maxwell K, Johnson GN (2000) Chlorophyll fluorescence - a practical guide. J Exp Bot 51:659–668CrossRefPubMedGoogle Scholar
  36. 36.
    Gilmore AM, Yamasaki H (1998) 9-aminoacridine and dibucaine exhibit competitive interactions and complicated inhibitory effects that interfere with measurements of Δ pH and xanthophyll cycle-dependent photosystem II energy dissipation. Photosynth Res 57:159–174CrossRefGoogle Scholar
  37. 37.
    Gurung S, Cohen MF, Yamasaki H (2014) Azide-dependent nitric oxide emission from the water fern Azolla pinnata. Russ J Plant Physiol 61:543–547CrossRefGoogle Scholar
  38. 38.
    Gupta KJ, Igamberdiev AU (2013) Recommendations of using at least two different methods for measuring NO. Front Plant Sci 4:1–4CrossRefGoogle Scholar
  39. 39.
    Arita NO, Cohen MF, Tokuda G et al (2007) Fluorometric detection of nitric oxide with diaminofluoresceins (DAFs): applications and limitations for plant NO research. In: Lamattina L, Polacco J (eds) Nitric oxide in plant growth, development and stress physiology. Springer, Würzburg, pp 269–280CrossRefGoogle Scholar
  40. 40.
    Az-ma T, Fujii K, Yuge O (1994) Reaction between imidazolineoxil N-oxide (carboxy-PTIO) and nitric oxide released from cultured endothelial cells: quantitative measurement of nitric oxide by ESR spectrometry. Life Sci 54:185–190CrossRefGoogle Scholar
  41. 41.
    Lichtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43:379–393CrossRefGoogle Scholar
  42. 42.
    Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237CrossRefGoogle Scholar
  43. 43.
    Takahashi S, Nakamura T, Sakamizu M et al (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol 45:251–255CrossRefPubMedGoogle Scholar
  44. 44.
    Hossain KK, Nakamura T, Yamasaki H (2011) Effect of nitric oxide on leaf non-photochemical quenching of fluorescence under heat-stress conditions. Russ J Plant Physiol 58:629–633CrossRefGoogle Scholar
  45. 45.
    Planchet E, Kaiser WM (2006) Nitric oxide (NO) detection by DAF fluorescence and chemiluminescence: a comparison using abiotic and biotic NO sources. J Exp Bot 57:3043–3055CrossRefPubMedGoogle Scholar
  46. 46.
    Singh RJ, Hogg N, Joseph J et al (1996) Mechanism of nitric oxide release from S-nitrosothiols. J Biol Chem 271:18596–18603CrossRefPubMedGoogle Scholar
  47. 47.
    Planchet E, Gupta KJ, Sonoda M et al (2005) Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J 41:732–743CrossRefPubMedGoogle Scholar
  48. 48.
    Ono K, Akaike T, Sawa T et al (2014) Redox chemistry and chemical biology of H2S, hydropersulfides, and derived species: Implications of their possible biological activity and utility. Free Radic Biol Med 77:82–94CrossRefPubMedGoogle Scholar
  49. 49.
    Gruhlke MCH, Slusarenko AJ (2012) The biology of reactive sulfur species (RSS). Plant Physiol Biochem 59:98–107CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Hideo Yamasaki
    • 1
    Email author
  • Naoko S. Watanabe
    • 1
  • Yasuko Sakihama
    • 2
  • Michael F. Cohen
    • 3
    • 4
  1. 1.Faculty of ScienceUniversity of the RyukyusNishiharaJapan
  2. 2.Research Faculty of AgricultureHokkaido UniversitySapporoJapan
  3. 3.Department of BiologySonoma State UniversityRohnert ParkUSA
  4. 4.Biological Systems UnitOkinawa Institute of Science and TechnologyKunigami-gunJapan

Personalised recommendations