Skip to main content

Advertisement

SpringerLink
Log in

Nitrogen alleviates NaCl toxicity in maize seedlings by regulating photosynthetic activity and ROS homeostasis

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Seven-day-old maize seedlings were subjected to NaCl (150 mM) without or with the presence of equimolar concentrations of urea, potassium nitrate or ammonium sulfate (at 60 kg N ha−1) for the subsequent 15 days. The results show that NaCl significantly decreased photosynthetic activity parameters (Hill reaction, Pn, Ci and Gs), shoot fresh and dry weights, chlorophylls, protein, GSH and AsA. The activities of ALA-D, Rubisco, PEP-C, MDH, PPDK, SOD, CAT and APX were significantly inhibited. On the contrary, NaCl significantly elevated MDA, O ∙−2 , H2O2, soluble sugars and proline. The application of the nitrogenous sources mostly ameliorated the photosynthetic activity synchronous with counterbalancing the decreases in growth, protein and pigments. The activities of ALA-D, Rubisco, PEP-C, MDH and PPDK enhanced remarkably with N applied under salinity. Furthermore, enhancements were detected in GSH and AsA contents and SOD, CAT and APX activities, which decreased free radicals, soluble sugars and proline. These effects reveal that maize was vulnerable to NaCl stress; however, N overcame the stress status and ameliorated the plant tolerance to salinity concomitant with repairing photosynthetic activity and maintaining higher antioxidants and ROS homeostasis; urea seemed to be the most efficient. Taken together, these findings conclude that N enhanced the capability of maize to tolerate NaCl via protecting photosynthetic apparatus for normal photochemical functioning and improving antioxidants and ROS homeostasis as effective salt tolerance mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

2,6-DCPIP:

2,6-Dichlorophenolindophenol

3-PGA:

3-Phosphoglyceric acid

ALA:

δ-Aminolevulinate

ALA-D:

δ-Aminolevulinate dehydratase

ANOVA:

Analysis of variance

APX:

Ascorbate peroxidase

AsA:

Ascorbic acid

CAT:

Catalase

CDNB:

1-Chloro-2,4-dinitrobenzene

Ci:

Sub-stomatal CO2 concentration

CP:

Creatine phosphate

CPase:

Creatine phosphokinase

DTT:

Dithiothreitol

Gs:

Stomatal conductance

GSH:

Glutathione

Hibitane:

Chlorohexidine diacetate

LSD:

Least significant differences

MDA:

Malondialdehyde

MDH:

Malate dehydrogenase

Na-tricine:

N-tris hydroxymethyl methyl glycine

O ∙−2 :

Superoxide radical

OAA:

Oxaloacetate

PEP:

Phosphoenolpyruvate

PEP-C:

Phosphoenolpyruvate carboxylase

PGAldDH:

Glyceraldehydes-3-phosphate dehydrogenase

PGK:

Phosphoglycerate kinase

Pn:

Net photosynthetic rate

PPDK:

Pyruvate phosphate dikinase

PVP:

Polyvinyl pyrrolidone

PVPP:

Polyvinyl polypyrrolidone

ROS:

Reactive oxygen species

Ru-1,5-P:

Ribulose-1,5-bisphosphate

Rubisco:

Ru-1,5-P carboxylase/oxygenase

SOD:

Superoxide dismutase

TCA:

Trichloroacetic acid

References

  • Anderson MP, Gronwalds JW (1991) Atrazine resistance in velvetleaf (Abutilon theophrasti) biotype due to enhanced glutathione S-transferase activity. Plant Physiol 96:107–109

    Google Scholar 

  • Ashton AR, Burnell JN, Furbank RT, Jenkins CL, Hatch MD (1990) Enzymes of C4 Photosynthesis. In: Dey PM, Harborne JB (eds) Methods in plant biochemistry. Enzymes of primary metabolism, vol 3. Academic Press, London, pp 39–72

    Chapter  Google Scholar 

  • Badran EG, Abogadallah GM, Nada RM, Nemat Alla MM (2015) Role of glycine in improving the ionic and ROS homeostasis during NaCl stress in wheat. Protoplasma 252:835–844

    Article  CAS  PubMed  Google Scholar 

  • Bates LE, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beer RF Jr, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    Google Scholar 

  • Borella J, Becker R, Lima MC, de Oliveira DS, Braga EJ, de Oliveira AC, do Amarante L (2019) Nitrogen source influences the antioxidative system of soybean plants under hypoxia and re-oxygenation. Sci Agric 76:51–62

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Chaitanya KS, Naithani SC (1994) Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertn. f. New Phytol 126:623–627

    Article  CAS  Google Scholar 

  • Chakraborty K, Bishi SK, Goswami N, Singh AL, Bhaduri D, Zala PV (2019) Salinity-induced changes in seed germination and the expression profile of antioxidant enzymes in peanut as early and late responses in emerging radicles. Acta Physiol Plant 41:134–149

    Article  CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Throne TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–110

    Article  CAS  Google Scholar 

  • Gururani MA, Venkatesh J, Tran LSP (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320

    Article  CAS  PubMed  Google Scholar 

  • Harborne JB (1984) Macromolecules. In: Harborne JB (ed) Phytochemical methods. Chapman and Hall, London, p 243

    Chapter  Google Scholar 

  • Hassan NM, Serag MS, El-Feky FM, Nemat Alla MM (2008) In vitro selection of mung bean and tomato for improving tolerance to NaCl. Ann Appl Biol 152:319–330

    Article  CAS  Google Scholar 

  • Hassan NM, El-Bastawisy ZM, El-Sayed AK, Ebeed HT, Nemat Alla MM (2015) Roles of dehydrin genes in wheat tolerance to drought stress. J Adv Res 6:179–188

    Article  CAS  PubMed  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments. Plant Signal Behav 7:1456–1466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jedmowski C, Ashoub A, Brüggemann W (2013) Reactions of Egyptian landraces of Hordeum vulgare and Sorghum bicolor to drought stress, evaluated by the OJIP fuorescence transient analysis. Acta Physiol Plant 35:345–354

    Article  Google Scholar 

  • Kaya C, Sonmez O, Ashraf M, Polat T, Tuna L, Aydemir S (2015) Exogenous application of nitric oxide and thiourea regulates on growth and some key physiological processes in maize (Zea mays L.) plants under saline stress. Soil Water J S:61–66

    Google Scholar 

  • Keys AJ, Parry MA (1990) Ribulose bisphosphate carboylase/oxygenase and carbonic anhydrase. In: Dey PM, Harborne JB (eds) Methods in plant biochemistry. Enzymes of primary metabolism, vol 3. Academic Press, London, pp 1–14

    Chapter  Google Scholar 

  • Koenigshofer H, Loeppert H (2019) The up-regulation of proline synthesis in the meristematic tissues of wheat seedlings upon short-term exposure to osmotic stress. J Plant Physiol 237:21–29

    Article  CAS  PubMed  Google Scholar 

  • Kong X, Luo Z, Dong H, Li W, Chen Y (2017) Non-uniform salinity in the root zone alleviates salt damage by increasing sodium, water and nutrient transport genes expression in cotton. Sci Rep 7:2879

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumawat RN, Mahla HR (2015) Effect of foliar applied urea and planting pattern on the leaf pigments and yield of cluster bean (Cyamopsis tetragonoloba L.) grown in low rainfall areas of western India. Legum Res 38:96–100

    Article  Google Scholar 

  • Lang Y, Wang M, Xia JB, Zhao QK (2018) Efects of soil drought stress on photosynthetic gas exchange traits and chlorophyll fuorescence in Forsythia suspensa. J For Res 29:45–53

    Article  CAS  Google Scholar 

  • Mauzerall D, Granick S (1956) The occurrence and determination of 5-aminolevulinic acid and porphobilinogen in urea. J Biol Chem 219:435–446

    CAS  PubMed  Google Scholar 

  • Mazumdar P, Lau S, Singh P, Takhtgahi HM, Harikrishna JA (2019) Impact of sea-salt on morpho-physiological and biochemical responses in banana (Musa acuminata cv. Berangan). Physiol Mol Biol Plants 25:713–726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Metzner H, Rau H, Singer H (1965) Untersuchungen zur synchronisierbarkeit einzelner pigment mangel mutanten von Chlorella. Planta 65:186–194

    Article  CAS  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress induced changes in the levels of endogenous ascorbic acid and H2O2 in Vigna seedlings. Plant Physiol 58:166–170

    Article  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxide in spinach chloroplast. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nemat Alla MM, Hassan NM (1998) Efficacy of exogenous GA3 and herbicide safeners in protection of Zea mays from metolachlor toxicity. Plant Physiol Biochem 36:809–815

    Article  Google Scholar 

  • Nemat Alla MM, Hassan NM (2014) Alleviation of isoproturon toxicity to wheat by exogenous application of glutathione. Pestic Biochem Physiol 112:56–62

    Article  CAS  PubMed  Google Scholar 

  • Nemat Alla MM, Badawi AM, Hassan NM, El-Bastawisy ZM, Badran EG (2007) Induction of glutathione and glutathione-associated enzymes in butachlor-tolerant plant species. Am J Plant Physiol 2:195–205

    Article  Google Scholar 

  • Nemat Alla MM, Khedr AA, Serag MM, Abu-Alnaga AZ, Nada RM (2011) Physiological aspects of tolerance in Atriplex halimus L. to NaCl and drought. Acta Physiol Plant 33:547–557

    Article  CAS  Google Scholar 

  • Nemat Alla MM, Abogadallah GM, Badran EG, Nada RM, Hassan NM (2016) Role of CaCl2 in osmoregulation and up-regulation of the salt stress related genes, NHX1 and SOS1 in wheat during NaCl stress. Agrochimica 60:29–42

    Google Scholar 

  • Okuda T, Masuda Y, Yamanaka A, Sagisaka S (1991) Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment. Plant Physiol 97:1265–1267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effect on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  PubMed  Google Scholar 

  • Perreault F, Dionne J, Didur O, Juneau P, Popovic R (2011) Efect of cadmium on photosystem II activity in Chlamydomonas reinhardtii: alteration of O-J-I-P fuorescence transients indicating the change of apparent activation energies within photosystem II. Photosynth Res 107:151–157

    Article  CAS  PubMed  Google Scholar 

  • Perveen S, Iqbal N, Saeed M, Zafar S, Arshad Z (2018) Role of foliar application of sulfur-containing compounds on maize (Zea mays L. var. Malka and hybrid DTC) under salt stress. Braz J Bot 41:805–815

    Article  Google Scholar 

  • Schlüter U, Crawford RM (2001) Long-term anoxia tolerance in leaves of Acorus calamus L. and Iris pseudacorus L. J Exp Bot 52:2213–2225

    Article  PubMed  Google Scholar 

  • Spreitzer RL (1993) Genetic dissection of Rubisco structure and function. Annu Rev Plant Physiol Plant Mol Biol 44:411–434

    Article  CAS  Google Scholar 

  • Sun CQ, Chen FD, Teng NJ, Liu ZL, Fang WM, Hou XL (2010) Interspecifc hybrids between Chrysanthemum grandiforum (Ramat.) Kitamura and C. indicum (L.) Des Moul. and their drought tolerance evaluation. Euphytica 174:51–60

    Article  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  PubMed  Google Scholar 

  • Trebst A (1972) Measurement of Hill reaction and photoreduction. In: Pietro SA (ed) Methods in enzymology. Academic Press, New York, pp 146–165

    Google Scholar 

  • Wu Y, Liao W, Dawuda MM, Hu L, Yu J (2019) 5-Aminolevulinic acid (ALA) biosynthetic and metabolic pathways and its role in higher plants. Plant Growth Regul 87:357–374

    Article  CAS  Google Scholar 

  • Zhang LX, Zheng P, Ruan Z, Tian L, Ashraf M (2015) Nitric oxide accumulation and glycinebetaine metabolism in two osmotically stressed maize cultivars supplied with different nitrogen forms. Biol Plant 59:183–186

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Botany Department, Faculty of Science, Damietta University, PO 34517, Kafr Saad, Egypt

    Mamdouh M. Nemat Alla & Nemat M. Hassan

Authors
  1. Mamdouh M. Nemat Alla
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nemat M. Hassan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mamdouh M. Nemat Alla.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by P. Wojtaszek.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nemat Alla, M.M., Hassan, N.M. Nitrogen alleviates NaCl toxicity in maize seedlings by regulating photosynthetic activity and ROS homeostasis. Acta Physiol Plant 42, 93 (2020). https://doi.org/10.1007/s11738-020-03080-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-020-03080-6

Keywords

Search

Navigation