A New Role for an Old Enzyme: Nitrate Reductase-mediated Nitric Oxide Generation is Required for Abscisic Acid-induced Stomatal Closure in Arabidopsis Thaliana

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2002 Nov 26

PMID 12446847

Citations 174

Authors

Radhika Desikan

Rachael Griffiths

John Hancock

Steven Neill

Affiliations

Soon will be listed here.

Abstract

The plant hormone abscisic acid (ABA), synthesized in response to water-deficit stress, induces stomatal closure via activation of complex signaling cascades. Recent work has established that nitric oxide (NO) is a key signaling molecule mediating ABA-induced stomatal closure. However, the biosynthetic origin of NO in guard cells has not yet been resolved. Here, we provide pharmacological, physiological, and genetic evidence that NO synthesis in Arabidopsis guard cells is mediated by the enzyme nitrate reductase (NR). Guard cells of wild-type Arabidopsis generate NO in response to treatment with ABA and nitrite, a substrate for NR. Moreover, NR-mediated NO synthesis is required for ABA-induced stomatal closure. However, in the NR double mutant, nia1, nia2 that has diminished NR activity, guard cells do not synthesize NO nor do the stomata close in response to ABA or nitrite, although stomatal opening is still inhibited by ABA. Furthermore, by using the ABA-insensitive (ABI) abi1-1 and abi2-1 mutants, we show that the ABI1 and ABI2 protein phosphatases are downstream of NO in the ABA signal-transduction cascade. These data demonstrate a previously uncharacterized signaling role for NR, that of mediating ABA-induced NO synthesis in Arabidopsis guard cells.

Citing Articles

Improving Soybean Germination and Nodule Development with Nitric Oxide-Releasing Polymeric Nanoparticles.

Preisler A, do Carmo G, da Silva R, Simoes A, Izidoro J, Pieretti J Plants (Basel). 2025; 14(1.

PMID: 39795275 PMC: 11723237. DOI: 10.3390/plants14010017.

A network-based modeling framework reveals the core signal transduction network underlying high carbon dioxide-induced stomatal closure in guard cells.

Gan X, Sengottaiyan P, Park K, Assmann S, Albert R PLoS Biol. 2024; 22(5):e3002592.

PMID: 38691548 PMC: 11090369. DOI: 10.1371/journal.pbio.3002592.

Identification of nitric oxide mediated defense signaling and its microRNA mediated regulation during infection in black pepper.

Asha S, Kattupalli D, Vijayanathan M, Soniya E Physiol Mol Biol Plants. 2024; 30(1):33-47.

PMID: 38435849 PMC: 10901764. DOI: 10.1007/s12298-024-01414-z.

Marker and readout genes for defense priming in Pseudomonas cannabina pv. alisalensis interaction aid understanding systemic immunity in Arabidopsis.

Sistenich A, Furtauer L, Scheele F, Conrath U Sci Rep. 2024; 14(1):3489.

PMID: 38347062 PMC: 10861594. DOI: 10.1038/s41598-024-53982-5.

Nitric oxide in plants: an insight on redox activity and responses toward abiotic stress signaling.

Khator K, Parihar S, Jasik J, Shekhawat G Plant Signal Behav. 2024; 19(1):2298053.

PMID: 38190763 PMC: 10793691. DOI: 10.1080/15592324.2023.2298053.

References

Neill S, Desikan R, Clarke A, Hurst R, Hancock J . Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot. 2002; 53(372):1237-47. View

Meinhard M, Rodriguez P, Grill E . The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta. 2002; 214(5):775-82. DOI: 10.1007/s00425-001-0675-3. View

Garcia-Mata C, Lamattina L . Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol. 2002; 128(3):790-2. PMC: 1540215. DOI: 10.1104/pp.011020. View

Wilkinson J, Crawford N . Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol Gen Genet. 1993; 239(1-2):289-97. DOI: 10.1007/BF00281630. View

Dean J, Harper J . Nitric Oxide and Nitrous Oxide Production by Soybean and Winged Bean during the in Vivo Nitrate Reductase Assay. Plant Physiol. 1986; 82(3):718-23. PMC: 1056196. DOI: 10.1104/pp.82.3.718. View

Schroeder J, Allen G, Hugouvieux V, Kwak J, Waner D . GUARD CELL SIGNAL TRANSDUCTION. Annu Rev Plant Physiol Plant Mol Biol. 2001; 52:627-658. DOI: 10.1146/annurev.arplant.52.1.627. View

Tun N, Holk A, Scherer G . Rapid increase of NO release in plant cell cultures induced by cytokinin. FEBS Lett. 2001; 509(2):174-6. DOI: 10.1016/s0014-5793(01)03164-7. View

Delledonne M, Xia Y, Dixon R, Lamb C . Nitric oxide functions as a signal in plant disease resistance. Nature. 1998; 394(6693):585-8. DOI: 10.1038/29087. View

Pedroso M, Magalhaes J, Durzan D . A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm callus cells and foliar tissues. J Exp Bot. 2000; 51(347):1027-36. DOI: 10.1093/jexbot/51.347.1027. View

10.

Rockel P, Strube F, Rockel A, Wildt J, Kaiser W . Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot. 2001; 53(366):103-10. View

11.

Murata Y, Pei Z, Mori I, Schroeder J . Abscisic acid activation of plasma membrane Ca(2+) channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell. 2001; 13(11):2513-23. PMC: 139468. DOI: 10.1105/tpc.010210. View

12.

Pei Z, Kuchitsu K, Ward J, Schwarz M, Schroeder J . Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell. 1997; 9(3):409-23. PMC: 156927. DOI: 10.1105/tpc.9.3.409. View

13.

Hetherington A . Guard cell signaling. Cell. 2001; 107(6):711-4. DOI: 10.1016/s0092-8674(01)00606-7. View

14.

Meinhard M, Grill E . Hydrogen peroxide is a regulator of ABI1, a protein phosphatase 2C from Arabidopsis. FEBS Lett. 2001; 508(3):443-6. DOI: 10.1016/s0014-5793(01)03106-4. View

15.

Wendehenne D, Pugin A, Klessig D, Durner J . Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci. 2001; 6(4):177-83. DOI: 10.1016/s1360-1385(01)01893-3. View

16.

. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000; 408(6814):796-815. DOI: 10.1038/35048692. View

17.

Neill S, Desikan R, Clarke A, Hancock J . Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 2002; 128(1):13-6. PMC: 1540198. View

18.

Leung J, Merlot S, Giraudat J . The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell. 1997; 9(5):759-71. PMC: 156954. DOI: 10.1105/tpc.9.5.759. View

19.

Sakihama Y, Nakamura S, Yamasaki H . Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organisms. Plant Cell Physiol. 2002; 43(3):290-7. DOI: 10.1093/pcp/pcf034. View

20.

Yamasaki H, Sakihama Y . 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. 2000; 468(1):89-92. DOI: 10.1016/s0014-5793(00)01203-5. View