Skip to main content
SpringerLink
Log in

Coordination between xanthophyll cycle and antioxidant system in Sargassum thunbergii (Sargassaceae, Phaeophyta) in response to high light and dehydration stresses

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The differential contribution of the xanthophyll cycle (XC) and the antioxidant system to photoprotect the photosynthetic apparatus of Sargassum thunbergii to high light (HL), dehydration (DY), HL prior to DY (HL-DY), and HL in combination with DY stresses were investigated. Both de-epoxidation state (DPS) and total antioxidant capacity (T-AOC) were upregulated in response to the four kinds of stresses. The de-epoxidation of XC was engaged earlier in response to stress exposure while significant change in antioxidant activities took a relatively long time. Under HL stress, the PSII photoinactivation was significant as suggested by low maximum PSII efficiency together with effective quantum yield and high excitation pressure. Simultaneously, XC-dependent thermal dissipation increased progressively, reaching a high value. The low oxidative stress indicated by low levels of superoxide radical and hydrogen peroxide was accompanied with a low T-AOC. However, DY treated samples exhibited severe oxidative stress and high capacity to detoxify reactive oxygen species, as evidenced by the high T-AOC, oxidized glutathione, and dehydroascorbate. The low activity of XC was reflected by low DPS. These results indicated that XC was more sensitive to HL, while the antioxidant system was more sensitive to DY. When S. thunbergii blades were transferred to DY from HL, the enhancement of antioxidant system activity was greater than that of XC de-epoxidation. There exists coordination between XC and antioxidant system in response to varying environmental factors. In addition, as demonstrated in HL-DY stress, preillumination decreased the degree of photoinhibition and oxidative stress during dehydration, indicating that high light exposure could make the blades more tolerant to dehydration. This observation can be the bases to identify species that have developed with higher competitive abilities in adapting to the intertidal environment.

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

Similar content being viewed by others

References

  • Adams WW, Demmig-Adams B (1994) Carotenoid composition and down regulation of photosystem II in three conifer species during the winter. Physiol Plant 92:451–458

    Article  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50:601–639

    Article  CAS  Google Scholar 

  • Baker CJ, Orlandi EW (1995) Active oxygen in plant pathogenesis. Annu Rev Phytopathol 33:299–321

    Article  CAS  PubMed  Google Scholar 

  • Beck CF (2005) Signaling pathways from the chloroplast to the nucleus. Planta 222:743–756

    Article  CAS  PubMed  Google Scholar 

  • Burritt DJ, Larkindale J, Hurd CL (2002) Antioxidant metabolism in the intertidal red seaweed Stictosiphonia arbuscula following desiccation. Planta 215:829–838

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Li H, Zhang D, Li P, Ma F (2013) The role of anthocyanin in photoprotection and its relationship with the xanthophyll cycle and the antioxidant system in apple peel depends on the light conditions. Physiol Plant 149:354–366

    Article  CAS  PubMed  Google Scholar 

  • Chen LS, Cheng L (2003) Both xanthophyll cycle-dependent thermal dissipation and the antioxidant system are up-regulated in grape (Vitis labrusca L. cv. Concord) leaves in response to N limitation. J Exp Bot 54:2165–2175

    Article  CAS  PubMed  Google Scholar 

  • Chen LS, Li P, Cheng L (2008) Effects of high temperature coupled with high light on the balance between photooxidation and photoprotection in the sun-exposed peel of apple. Planta 228:745–756

    Article  CAS  PubMed  Google Scholar 

  • Collén J, Davison IR (1999) Reactive oxygen metabolism in intertidal Fucus spp. (Phaeophyceae). J Phycol 35:62–69

    Article  Google Scholar 

  • Colombo-Pallotta MF, García-Mendoza E, Ladah LB (2006) Photosynthethic performance, light absorption, and pigment composition of Macrocystis Pyrifera (Laminariales, Phaeophyceae) blades from different depths. J Phycol 42:1225–1234

    Article  CAS  Google Scholar 

  • Contreras-Porcia L, Thomas D, Flores V, Correa JA (2011) Tolerance to oxidative stress induced by desiccation in Porphyra columbina (Bangiales, Rhodophyta). J Exp Bot 62:1815–1829

    Article  CAS  PubMed  Google Scholar 

  • Cruces E, Huovinen P, Gómez I (2013) Interactive effects of UV radiation and enhanced temperature on photosynthesis, phlorotannin induction and antioxidant activities of two sub-Antarctic brown algae. Mar Biol 160:1–13

    Article  CAS  Google Scholar 

  • Dinis TC, Madeira VM, Almeida LM (1994) Action of phenolic derivatives (acetaminophen, salicylate, and 5-aminosalicylate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Arch Biochem Biophys 315:161–169

    Article  CAS  PubMed  Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Marín B, Míguez F, Becerril JM, García-Plazaola JI (2011) Activation of violaxanthin cycle in darkness is a common response to different abiotic stresses: a case study in Pelvetia canaliculata. BMC Plant Biol 11:181

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukuda SY, Yamakawa R, Hirai M, Kashino Y, Koike H, Satoh K (2008) Mechanisms to avoid photoinhibition in a desiccation-tolerant cyanobacterium, Nostoc commune. Plant Cell Physiol 49:488–492

    Article  CAS  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA-Gen Subj 990:87–92

    Article  CAS  Google Scholar 

  • Grace SC, Logan BA (1996) Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. Plant Physiol 112:1631–1640

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212

    Article  CAS  PubMed  Google Scholar 

  • Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci U S A 96:8762–8767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kampfenkel K, Vanmontagu M, Inze D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225:165–167

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Gupta V, Trivedi N, Kumari P, Bijo AJ, Reddy CRK, Jha B (2011) Desiccation induced oxidative stress and its biochemical responses in intertidal red alga Gracilaria corticata (Gracilariales, Rhodophyta). Environ Exp Bot 72:194–201

    Article  CAS  Google Scholar 

  • Li XM, Zhang QS, Tang YZ, Liu HL, Li XL (2014) Highly efficient photoprotective responses to high light stress in Sargassum thunbergii germlings, a representative brown macroalga of intertidal zone. J Sea Res 85:491–498

  • Liu YF, Qi MF, Li TL (2012) Photosynthesis, photoinhibition, and antioxidant system in tomato leaves stressed by low night temperature and their subsequent recovery. Plant Sci 196:8–17

    Article  CAS  PubMed  Google Scholar 

  • Logan BA, Demmig-Adams B, Adams WW, Grace SC (1998) Antioxidants and xanthophyll cycle-dependent energy dissipation in Cucurbita pepo L. and Vinca major L. acclimated to four growth PPFDs in the field. J Exp Bot 49:1869–1879

    Article  CAS  Google Scholar 

  • Logan BA, Kornyeyev D, Hardison J, Holaday AS (2006) The role of antioxidant enzymes in photoprotection. Photosynth Res 88:119–132

    Article  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • May MJ, Vernoux T, Leaver C, Van Montagu M, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667

    CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–67

    Article  CAS  PubMed  Google Scholar 

  • Neill SO, Gould KS, Kilmartin PA, Mitchell KA, Markham KR (2002) Antioxidant capacities of green and cyanic leaves in the sun species, Quintinia serrata. Funct Plant Biol 29:1437–1443

    Article  CAS  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Biol 50:333–359

    Article  CAS  Google Scholar 

  • Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keep active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Patterson BD, Macrae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–92

    Article  CAS  PubMed  Google Scholar 

  • Rautenberger R, Wiencke C, Bischof K (2013) Acclimation to UV radiation and antioxidative defence in the endemic Antarctic brown macroalga Desmarestia anceps along a depth gradient. Polar Biol 36:1779–1789

    Article  Google Scholar 

  • Roháček K (2010) Method for resolution and quantification of components of the non-photochemical quenching (qN). Photosynth Res 105:101–113

    Article  PubMed  Google Scholar 

  • Roháček K, Bertrand M, Moreau B, Jacquette B, Caplat C, Morant-Manceau A, Schoefs B (2014) Relaxation of the non-photochemical chlorophyll fluorescence quenching in diatoms: kinetics, components and mechanisms. Phil Trans R Soc B 369:20130241

    Article  PubMed  PubMed Central  Google Scholar 

  • Stamenković M, Bischof K, Hanelt D (2014) Xanthophyll cycle pool size and composition in several Cosmarium strains (Zygnematophyceae, Streptophyta) are related to their geographic distribution patterns. Protist 165:14–30

    Article  PubMed  Google Scholar 

  • Tausz M, Šircelj H, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? J Exp Bot 55:1955–1962

    Article  CAS  PubMed  Google Scholar 

  • Yu YQ, Zhang QS, Tang YZ, Li XM, Liu HL, Li LX (2013) Diurnal changes of photosynthetic quantum yield in the intertidal macroalga Sargassum thunbergii under simulated tidal emersion conditions. J Sea Res 80:50–57

    Article  Google Scholar 

  • Zhang QS, Li W, Liu S, Pan JH (2009) Size-dependence of reproductive allocation of Sargassum thunbergii (Sargassaceae, Phaeophyta) in Bohai Bay, China. Aquat Bot 91:194–198

    Article  Google Scholar 

  • Zhu JJ, Zhang JL, Liu HC, Cao KF (2009) Photosynthesis, non-photochemical pathways and activities of antioxidant enzymes in a resilient evergreen oak under different climatic conditions from a valley-savanna in Southwest China. Physiol Plant 135:62–72

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the National Natural Science Foundation of China No. 41376154. Special thanks go to Dr. Shikai Liu from Fish Molecular Genetics and Biotechnology Laboratory of Auburn University for his great help in proofreading the manuscript.

Author information

Authors and Affiliations

  1. Ocean School, Yantai University, Yantai, 264005, People’s Republic of China

    Guo Ning Nan, Quan Sheng Zhang, Zi Tong Sheng & Di Zhang

Authors
  1. Guo Ning Nan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Quan Sheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zi Tong Sheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Di Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Quan Sheng Zhang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nan, G.N., Zhang, Q.S., Sheng, Z.T. et al. Coordination between xanthophyll cycle and antioxidant system in Sargassum thunbergii (Sargassaceae, Phaeophyta) in response to high light and dehydration stresses. J Appl Phycol 28, 2587–2596 (2016). https://doi.org/10.1007/s10811-016-0791-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-016-0791-x

Keywords

Search

Navigation