Abstract
Nitrate and ammonium are the main sources through which plants obtain nitrogen from the soil. Nevertheless, several plant species exhibit symptoms of toxicity when grown with ammonium, including reduced root growth. As nitrite derived from nitrate is the primary pathway for nitric oxide (NO) synthesis, environments containing ammonium as the sole nitrogen source have lower concentrations of this signaling molecule. Application of NO can enhance plant tolerance to stresses. In our study, the effect of NO application on seedlings of two tree species from the Atlantic Forest with different nitrogen utilization strategies and contrasting tolerances to ammonium was evaluated. The tolerant species Cariniana estrellensis did not show a significant difference in root growth under nitrate or ammonium. However, the non-tolerant species Cecropia pachystachya showed low growth when supplied with ammonium. Malondialdehyde did not accumulate in both species, suggesting that ammonium toxicity is not related to oxidative stress. As expected, C. pachystachya roots exhibited higher concentration of NO when grown with nitrate but C. estrellensis displayed higher endogenous concentration of NO when supplied with ammonium, suggesting a predominance of NO synthesis through oxidative pathways. NO application increased root growth in C. pachystachya seedlings grown in ammonium but had no effect on C. estrellensis. Together, these results suggest that greater tolerance to ammonium may be related to higher concentrations of NO and its modulating role in anti-stress responses. Further investigation with a broader range of species is necessary to identify the mechanisms underlying ammonium tolerance and NO production.
References
Astier J, Gross I, Durner J (2018) Nitric oxide production in plants: an update. J Exp Bot 69(14):3401–3411. https://doi.org/10.1093/jxb/erx420
Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159(6):567–584. https://doi.org/10.1078/0176-1617-0774
Camejo G, Wallin B, Enojärvi M (1998) Analysis of oxidation and antioxidants using microtiter plates. Free radic antioxid. https://doi.org/10.1385/0-89603-472-0:377
Costa-Broseta Á, Castillo M, León J (2020) Nitrite reductase 1 is a target of nitric oxide-mediated post-translational modifications and controls nitrogen flux and growth in Arabidopsis. Int J Mol Sci 21(19):7270. https://doi.org/10.3390/ijms21197270
da Silva RC, Rondina ABL, Zangaro W, Oliveira HC (2021) Inorganic nitrogen sources alter the root morphology of neotropical tree seedlings from different successional groups. Trees 35:875–887. https://doi.org/10.1007/s00468-021-02087-x
Da-Silva CJ, Shimoia EP, Posso DA, Cardoso AA, Batz TA, Oliveira ACB, do Amarante L (2021) Nitrate nutrition increases foliar levels of nitric oxide and waterlogging tolerance in soybean. Acta Physiol Plant 43:1–12. https://doi.org/10.1007/s11738-021-03291-5
Debiasi TV, Calzavara AK, da Silva LM et al (2019) Nitrogen metabolism of neotropical tree seedlings with contrasting ecological characteristics. Acta Physiol Plant 41:1–11. https://doi.org/10.1007/s11738-019-2923-9
Debiasi TV, Calzavara AK, Sodek L, Oliveira HC (2021) Nitrogen use plasticity in response to light intensity in neotropical tree species of distinct functional groups. Physiol Plant 172(4):2226–2237. https://doi.org/10.1111/ppl.13470
Di DW, Sun L, Zhang X, Li G, Kronzucker HJ, Shi W (2018) Involvement of auxin in the regulation of ammonium tolerance in rice (Oryza sativa L.). Plant Soil 432:373–387. https://doi.org/10.1007/s11104-018-3813-4
do Carmo GC, Iastrenski LF, Debiasi TV et al (2021) Nanoencapsulation improves the protective effects of a nitric oxide donor on drought-stressed Heliocarpus popayanensis seedlings. Ecotox Environ Saf 225:112713. https://doi.org/10.1016/j.ecoenv.2021.112713
Esteban R, Ariz I, Cruz C, Moran JF (2016) Review: mechanisms of ammonium toxicity and the quest for tolerance. Plant Sei 248:92–101. https://doi.org/10.1016/j.plantsci.2016.04.008
Frungillo L, Skelly MJ, Loake GJ, Spoel SH, Salgado I (2014) S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway. Nat Commun 5(1):5401. https://doi.org/10.1038/ncomms6401
Garbin ML, Dillenburg LR (2008) Effects of different nitrogen sources on growth, chlorophyll concentration, nitrate reductase activity and carbon and nitrogen distribution in Araucaria angustifolia. Braz J Plant Physiol 20:295–303. https://doi.org/10.1590/S1677-04202008000400005
Hachiya T, Sakakibara H (2017) Interactions between nitrate and ammonium in their uptake, allocation, assimilation, and signaling in plants. J Exp Bot 68(10):2501–2512. https://doi.org/10.1093/jxb/erw449
Hessini K, Hamed KB, Gandour M, Mejri M, Abdelly C, Cruz C (2013) Ammonium nutrition in the halophyte Spartina alterniflora under salt stress: evidence for a priming effect of ammonium? Plant Soil 370:163–173. https://doi.org/10.1007/s11104-013-1616-1
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ - Calif Agric Exp Stn 347(2):32
Kolbert ZS et al (2019) A forty year journey: the generation and roles of NO in plants. Nitric Oxide 93:53–70. https://doi.org/10.1016/j.niox.2019.09.006
Kong L, Zhang Y, Zhang B, Li H, Wan Z, Si J, Feng B (2022) Does energy cost constitute the primary cause of ammonium toxicity in plants? Planta 256(3):62. https://doi.org/10.1007/s00425-022-03971-7
Kronzucker HJ, Siddiqi MY, Glass AD (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385(6611):59–61. https://doi.org/10.1038/385059a0
Kumar P, Pathak S (2018) Nitric oxide: a key driver of signaling in plants. MOJ Eco Environ Sci 3(3):145–148. https://doi.org/10.15406/mojes.2018.03.00079
Lobit P, López-Pérez L, Cárdenas-Navarro R, Castellanos-Morales VC, Ruiz-Corro R (2007) Effect of ammonium/nitrate ratio on growth and development of avocado plants under hydroponic conditions. Can J Plant Sci 87(1):99–103. https://doi.org/10.4141/P06-02
Lopes-Oliveira PJ, Gomes DG, Pelegrino MT et al (2019) Effects of nitric oxide-releasing nanoparticles on neotropical tree seedlings submitted to acclimation under full sun in the nursery. Sci Rep 9(1):1–10. https://doi.org/10.1038/s41598-019-54030-3
Melo PM, Silva LS, Ribeiro I, Seabra AR, Carvalho HG (2011) Glutamine synthetase is a molecular target of nitric oxide in root nodules of Medicago truncatula and is regulated by tyrosine nitration. Plant Physiol 157(3):1505–1517. https://doi.org/10.1104/pp.111.186056
Meng Y, Jing H, Huang J, Shen R, Zhu X (2022) The role of nitric oxide signaling in plant responses to cadmium stress. Int J Mol Sci 23(13):6901. https://doi.org/10.3390/ijms23136901
Moro CF, Gaspar M, da Silva FR, Pattathil S, Hahn MG, Salgado I, Braga MR (2017) S-nitrosoglutathione promotes cell wall remodelling, alters the transcriptional profile and induces root hair formation in the hairless root hair defective 6 (rhd6) mutant of Arabidopsis thaliana. New Phytol 213(4):1771–1786. https://doi.org/10.1111/nph.14309
Oliveira HC, Freschi L, Sodek L (2013a) Nitrogen metabolism and translocation in soybean plants subjected to root oxygen deficiency. Plant Physiol Biochem 66:141–149. https://doi.org/10.1016/j.plaphy.2013.02.015
Oliveira HC, Salgado I, Sodek L (2013b) Involvement of nitrite in the nitrate-mediated modulation of fermentative metabolism and nitric oxide production of soybean roots during hypoxia. Planta 237:255–264. https://doi.org/10.1007/s00425-012-1773-0
Oliveira HC, da Silva LMI, de Freitas LD et al (2017) Nitrogen use strategies of seedlings from neotropical tree species of distinct successional groups. Plant Physiol Biochem 114:119–127. https://doi.org/10.1016/j.plaphy.2017.03.003
Pissolato MD, Silveira NM, Prataviera PJC et al (2020) Enhanced nitric oxide synthesis through nitrate supply improves drought tolerance of sugarcane plants. Front Plant Sci 11:970. https://doi.org/10.3389/fpls.2020.00970
Planas-Portell J, Gallart M, Tiburcio AF, Altabella T (2013) Copper-containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol 13(1):1–13. https://doi.org/10.1186/1471-2229-13-109
Qin C, Yi KK, Wu P (2011) Ammonium affects cell viability to inhibit root growth in Arabidopsis. J Zhejiang Univ Sci B 12(6):477–484. https://doi.org/10.1631/jzus.B1000335
Rosales EP, Iannone MF, Groppa MD, Benavides MP (2011) Nitric oxide inhibits nitrate reductase activity in wheat leaves. Plant Physiol Biochem 49(2):124–130. https://doi.org/10.1016/j.plaphy.2010.10.009
Sasakawa H, Yamamoto Y (1978) Comparison of the uptake of nitrate and ammonium by rice seedlings: influences of light, temperature, oxygen concentration, exogenous sucrose, and metabolic inhibitors. Plant Physiol 62(4):665–669. https://doi.org/10.1104/pp.62.4.665
The SV, Snyder R, Tegeder M (2021) Targeting nitrogen metabolism and transport processes to improve plant nitrogen use efficiency. Front Plant Sci 11:628366. https://doi.org/10.3389/fpls.2020.628366
Wang C, Zhang SH, Li W, Wang PF, Li L (2011) Nitric oxide supplementation alleviates ammonium toxicity in the submerged macrophyte Hydrilla verticillata (Lf) Royle. Ecotoxicol Environ Saf 74(1):67–73. https://doi.org/10.1016/j.ecoenv.2010.07.005
Wany A, Gupta AK, Kumari A et al (2019) Nitrate nutrition influences multiple factors in order to increase energy efficiency under hypoxia in Arabidopsis. Ann Bot 123(4):691–705. https://doi.org/10.1093/aob/mcy202
Zhou X, Joshi S, Khare T, Patil S, Shang J, Kumar V (2021) Nitric oxide, crosstalk with stress regulators and plant abiotic stress tolerance. Plant Cell Rep 40(8):1395–1414. https://doi.org/10.1007/s00299-021-02705-5
Funding
This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (M.G., grant no 2019/15095-3), Conselho Nacional de Desenvolvimento Científico e Tecnológico (H.C.O., 311034/2020-9; R.C.S., 141538/2020-1; W.A.V., 309633/2021-4), Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná (W.A.V., PRONEX grant agreement 014/2017), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (A.C.P., A.M.D., Finance Code 001). Authors thank the core facility CMLP-UEL for the use of the confocal microscope free of charge.
Author information
Authors and Affiliations
Contributions
R.C.S., A.C.P., and A.M.D. performed the experiments. H.C.O., M.G., and W.A.V. designed and supervised the research. All authors contributed to data interpretation, discussion of the results, and article preparation.
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher’s Note
Springer nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Da Silva, R.C., Preisler, A.C., Dionisio, A.M. et al. Does nitric oxide alleviate the effects of ammonium toxicity on root growth of Atlantic forest tree species?. Theor. Exp. Plant Physiol. (2024). https://doi.org/10.1007/s40626-024-00313-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s40626-024-00313-8