Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum - PubMed (original) (raw)

Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum

Jin Xu et al. Plant Physiol. 2010 Nov.

Abstract

Nitric oxide (NO) has been identified as a signal molecule that interplays with reactive oxygen species in response to heavy metal stresses. Roles of NO in regulating cadmium toxicity and iron deficiency have been proposed; however, the function of NO in zinc (Zn) tolerance in plants remains unclear. Here, we investigated NO accumulation and its role in plant Zn tolerance. Zn-induced NO production promoted an increase in reactive oxygen species accumulation in Solanum nigrum roots by modulating the expression and activity of antioxidative enzymes. Subsequently, programmed cell death (PCD) was observed in primary root tips. Inhibiting NO accumulation by 2-phenyl-4,4,5,5-tetramethyl-imidazoline-1-oxyl-3-oxide (a specific NO scavenger) or N(G)-nitro-l-arginine-methyl ester (a NO synthase inhibitor) prevented the increase of superoxide radical and hydrogen peroxide as well as the subsequent cell death in the root tips, supporting the role of NO in Zn-induced PCD in the root tips. Zn-induced NO production affected the length of primary roots, the number of lateral roots, and root hair growth and thereby modulated root system architecture and activity. Investigation of metal contents in Zn-treated roots suggests that NO is required for metal (especially iron) uptake and homeostasis in plants exposed to excess Zn. Taken together, our results indicate that NO production and the subsequent PCD in root tips exposed to excess Zn are favorable for the S. nigrum seedling response to long-term Zn toxicity by modulating root system architecture and subsequent adaptation to Zn stress.

PubMed Disclaimer

Figures

Figure 1.

NO production in S. nigrum roots exposed to Zn2+ or to Zn2+ and Fe2+. Two-week-old S. nigrum seedlings grown in Hoagland solution were treated with 200 or 400 μ

m

ZnCl2 in the presence or absence of 200 μ

m

Fe-EDTA. NO content was determined by the methemoglobin method as described in “Materials and Methods.” Symbols are as follows: black diamonds, control; purple squares, 200 μ

m

ZnCl2; red triangles, 400 μ

m

ZnCl2; green squares, 400 μ

m

ZnCl2 plus 200 μ

m

Fe-EDTA. Asterisks indicate values significantly different from those of the roots treated with 400 μ

m

ZnCl2 alone: * Student’s t test with P < 0.05. FW, Fresh weight.

Figure 2.

ROS production in roots of 2-week-old S. nigrum seedlings grown in Hoagland solution exposed to Zn2+ or to Zn2+ plus PTIO or Zn2+ plus

l

-NAME. A, H2O2 production was measured by the DCFH-DA method. Values are normalized against the levels in untreated controls (2 h) that are given a value of 1. B, O2− production was quantified as described in “Materials and Methods.” Symbols are as follows: black diamonds, control; blue crosses, 0.2 m

m

PTIO; purple squares, 0.5 m

m l

-NAME; red triangles, 400 μ

m

ZnCl2; green squares, 400 μ

m

ZnCl2 plus 0.2 m

m

PTIO; orange diamonds, 400 μ

m

ZnCl2 plus 0.5 m

m l

-NAME. Asterisks indicate values significantly different from those of the roots treated with 400 μ

m

ZnCl2 alone: * Student’s t test with P < 0.05. Images of H2O2 and O2− detection are presented in

Supplemental Figures S6

and

S7

, respectively. FW, Fresh weight; Rel. Fluor., relative fluorescence units.

Figure 3.

Detection of cell death and oxidative damage in the roots of 2-week-old S. nigrum seedlings grown in Hoagland solution treated with 400 μ

m

ZnCl2 (Zn) or 400 μ

m

ZnCl2 plus 0.2 m

m

PTIO (Zn+PTIO) or 400 μ

m

ZnCl2 plus 0.5 m

m l

-NAME (Zn+

l

-NAME). A, Effect of PTIO or

l

-NAME on PM integrity. Roots were excised and then stained with 3 μg mL−1 PI for 1 min as described in “Materials and Methods.” B, MDA content in roots of S. nigrum seedlings. ck, Untreated control; PTIO, 0.2 m

m

PTIO;

l

-NAME, 0.5 m

m l

-NAME; FW, fresh weight.

Figure 4.

Characterization of cell death in primary roots of Zn-treated S. nigrum seedlings. DAPI and TUNEL staining was done in primary root cells of 2-week-old S. nigrum seedlings grown in Hoagland solution treated with 400 μ

m

ZnCl2 (Zn) or 400 μ

m

ZnCl2 plus 0.2 m

m

PTIO (Zn+PTIO) or 400 μ

m

ZnCl2 plus 0.5 m

m l

-NAME (Zn+

l

-NAME). Insets show closeup observations of chromatin condensation. ck, Untreated control; PTIO, 0.2 m

m

PTIO;

l

-NAME, 0.5 m

m l

-NAME.

Figure 5.

Effect of PTIO or

l

-NAME on primary root growth (A) and number of lateral roots (B) of the S. nigrum roots treated with 400 μ

m

ZnCl2. Asterisks indicate values significantly different from those of the roots treated with Zn alone: * Student’s t test with P < 0.05. PTIO, 0.2 m

m

PTIO;

l

-NAME, 0.5 m

m l

-NAME; Zn, 400 μ

m

ZnCl2; Zn+PTIO, 400 μ

m

ZnCl2 plus 0.2 m

m

PTIO; Zn+

l

-NAME, 400 μ

m

ZnCl2 plus 0.5 m

m l

-NAME.

Figure 6.

Effect of PTIO or

l

-NAME on Zn accumulation in S. nigrum roots. A, Two-week-old S. nigrum seedlings grown in Hoagland solution were treated with Zn2+ or Zn2+ plus PTIO or Zn2+ plus

l

-NAME for 4 d. Visualization of Zn accumulation in S. nigrum roots was detected with the Zinquin fluorescent probe. The treated roots were stained with 25 μ

m

Zinquin (Sigma) for 1 h as described in “Materials and Methods.” Images were obtained by confocal microscopy. B, Zn content in the roots was measured by ICP-MS right after treatment. Asterisks indicate values significantly different from those of the roots treated with Zn alone: * Student’s t test with P < 0.05. ck, Untreated control; PTIO, 0.2 m

m

PTIO;

l

-NAME, 0.5 m

m l

-NAME; Zn, 400 μ

m

ZnCl2; Zn+PTIO, 400 μ

m

ZnCl2 plus 0.2 m

m

PTIO; Zn+

l

-NAME, 400 μ

m

ZnCl2 plus 0.5 m

m l

-NAME; DW, dry weight.

Figure 7.

Effect of PTIO or

l

-NAME on metal contents of Zn-treated S. nigrum roots. Two-week-old S. nigrum seedlings grown in Hoagland solution were treated with Zn2+ or Zn2+ plus PTIO or Zn2+ plus

l

-NAME. Metal contents in the roots were measured by ICP-MS right after treatment. Asterisks indicate values significantly different from those of the roots treated with Zn alone: * Student’s t test with P < 0.05. ck, Untreated control; PTIO, 0.2 m

m

PTIO;

l

-NAME, 0.5 m

m l

-NAME; Zn, 400 μ

m

ZnCl2; Zn+PTIO, 400 μ

m

ZnCl2 plus 0.2 m

m

PTIO; Zn+

l

-NAME, 400 μ

m

ZnCl2 plus 0.5 m

m l

-NAME; DW, dry weight.

Figure 8.

Ferric-chelate reductase activity regulated by NO during Zn toxicity. Two-week-old S. nigrum seedlings grown in Hoagland solution were treated with 400 μ

m

ZnCl2 in the presence or absence of 0.2 m

m

PTIO or 0.5 m

m l

-NAME for 4 d. A, Visualization of ferric-chelate reductase activity. B, Root ferric-chelate reductase activity in response to PTIO or

l

-NAME. Asterisks indicate values significantly different from those of the roots treated with Zn alone: * Student’s t test with P < 0.05. ck, Untreated control; PTIO, 0.2 m

m

PTIO;

l

-NAME, 0.5 m

m l

-NAME; Zn, 400 μ

m

ZnCl2; Zn+PTIO, 400 μ

m

ZnCl2 plus 0.2 m

m

PTIO; Zn+

l

-NAME, 400 μ

m

ZnCl2 plus 0.5 m

m l

-NAME.

Figure 9.

NO plays an important role in Zn tolerance in the hyperaccumulator S. nigrum. LR, Lateral root; PR, primary root.

Similar articles

• Depressing time: Waiting, melancholia, and the psychoanalytic practice of care.
  Salisbury L, Baraitser L. Salisbury L, et al. In: Kirtsoglou E, Simpson B, editors. The Time of Anthropology: Studies of Contemporary Chronopolitics. Abingdon: Routledge; 2020. Chapter 5. In: Kirtsoglou E, Simpson B, editors. The Time of Anthropology: Studies of Contemporary Chronopolitics. Abingdon: Routledge; 2020. Chapter 5. PMID: 36137063 Free Books & Documents. Review.
• Zinc induces distinct changes in the metabolism of reactive oxygen and nitrogen species (ROS and RNS) in the roots of two Brassica species with different sensitivity to zinc stress.
  Feigl G, Lehotai N, Molnár Á, Ördög A, Rodríguez-Ruiz M, Palma JM, Corpas FJ, Erdei L, Kolbert Z. Feigl G, et al. Ann Bot. 2015 Sep;116(4):613-25. doi: 10.1093/aob/mcu246. Epub 2014 Dec 22. Ann Bot. 2015. PMID: 25538112 Free PMC article.
• Antioxidants for female subfertility.
  Showell MG, Mackenzie-Proctor R, Jordan V, Hart RJ. Showell MG, et al. Cochrane Database Syst Rev. 2020 Aug 27;8(8):CD007807. doi: 10.1002/14651858.CD007807.pub4. Cochrane Database Syst Rev. 2020. PMID: 32851663 Free PMC article.
• Sphingolipids modulate redox signalling during human sperm capacitation.
  Serafini S, O'Flaherty C. Serafini S, et al. Hum Reprod. 2024 Dec 10:deae268. doi: 10.1093/humrep/deae268. Online ahead of print. Hum Reprod. 2024. PMID: 39658334
• Antioxidants for female subfertility.
  Showell MG, Mackenzie-Proctor R, Jordan V, Hart RJ. Showell MG, et al. Cochrane Database Syst Rev. 2017 Jul 28;7(7):CD007807. doi: 10.1002/14651858.CD007807.pub3. Cochrane Database Syst Rev. 2017. PMID: 28752910 Free PMC article. Updated. Review.

Cited by

• Crops' response to the emergent air pollutants.
  Shrestha RK, Shi D, Obaid H, Elsayed NS, Xie D, Ni J, Ni C. Shrestha RK, et al. Planta. 2022 Sep 12;256(4):80. doi: 10.1007/s00425-022-03993-1. Planta. 2022. PMID: 36097229 Review.
• Nitrate reductase-mediated nitric oxide production is involved in copper tolerance in shoots of hulless barley.
  Hu Y, You J, Liang X. Hu Y, et al. Plant Cell Rep. 2015 Mar;34(3):367-79. doi: 10.1007/s00299-014-1715-3. Epub 2014 Dec 2. Plant Cell Rep. 2015. PMID: 25447636
• Aminolevulinic acid and nitric oxide regulate oxidative defense and secondary metabolisms in canola (Brassica napus L.) under drought stress.
  Akram NA, Iqbal M, Muhammad A, Ashraf M, Al-Qurainy F, Shafiq S. Akram NA, et al. Protoplasma. 2018 Jan;255(1):163-174. doi: 10.1007/s00709-017-1140-x. Epub 2017 Jul 12. Protoplasma. 2018. PMID: 28699026
• Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions.
  Shen J, Xing T, Yuan H, Liu Z, Jin Z, Zhang L, Pei Y. Shen J, et al. PLoS One. 2013 Oct 23;8(10):e77047. doi: 10.1371/journal.pone.0077047. eCollection 2013. PLoS One. 2013. PMID: 24194857 Free PMC article.
• Zinc Hyperaccumulation in Plants: A Review.
  Balafrej H, Bogusz D, Triqui ZA, Guedira A, Bendaou N, Smouni A, Fahr M. Balafrej H, et al. Plants (Basel). 2020 Apr 29;9(5):562. doi: 10.3390/plants9050562. Plants (Basel). 2020. PMID: 32365483 Free PMC article. Review.

References

1. 1. Barclay KD, McKersie BD. (1994) Peroxidation reactions in plant membranes: effects of free fatty acids. Lipids 29: 877–883 - PubMed
2. 1. Behboodi BS, Samadi L. (2004) Detection of apoptotic bodies and oligonucleosomal DNA fragments in cadmium-treated root apical cells of Allium cepa Linnaeus. Plant Sci 167: 411–416
3. 1. Ben Amor N, Ben Hamed K, Debez A, Grignonb C, Abdelly C. (2005) Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity. Plant Sci 168: 889–899
4. 1. Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D. (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149: 1302–1315 - PMC - PubMed
5. 1. Bi X, Feng X, Yang Y, Qiu G, Li G, Li F, Liu T, Fu Z, Jin Z. (2006) Environmental contamination of heavy metals from zinc smelting areas in Hezhang County, western Guizhou, China. Environ Int 32: 883–890 - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources

• Full Text Sources

  • PubMed Central
  • Silverchair Information Systems