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High-salinity activates photoprotective mechanisms in Quercus suber via accumulation of carbohydrates and involvement of non-enzymatic and enzymatic antioxidant pathways

Abstract

Cork oak (Quercus suber), native to Mediterranean areas, is a plant of ecological and economical relevance, nevertheless, the effects of soil salinization on this species are currently unknown. We have investigated the physiological and biochemical impact of a high-salinity episode on young cork oak (Q. suber) plants. Besides the control (plants only irrigated with water), two experimental groups (irrigated once with a 300 mM NaCl solution) were analysed, one assessed at 24 h and the other at 6 days. Pigments (chlorophylls and carotenoids) were found increased at 24 h, but decreased at day 6 in salinity conditions. Sugars (glucose, sucrose, starch but not fructose) increased with stress (24 h and 6 days). Salinity conditions impaired photosystem II (PSII) photochemistry, mostly associated with decrease in Fv/Fm and chlorophyll content (6 days). While hydrogen peroxide levels did not increase above control levels, lipid peroxidation increased, suggesting oxidative damage. In salinity conditions, superoxide dismutase and ascorbate peroxidase showed higher activity in the 24 h timepoint, whereas catalase activity increased at 24 h and 6 days. These observations reveal adaptations of Q. suber to high salinity, nevertheless, the decreased photosynthetic activity and oxidative damages observed suggest that additional studies are required to assess Q. suber adaptation to diverse salinity conditions. Moreover, these data provide more information for future programs of conservation and management of salinity areas in the Mediterranean region, and selection of salinity tolerant species.

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References

  1. Acosta-Motos J, Ortuño M, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco M, Hernandez J (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7:18. https://doi.org/10.3390/agronomy7010018

    CAS  Article  Google Scholar 

  2. Akbari M, Katam R, Husain R, Farajpour M, Mazzuca S, Mahna N (2020) Sodium chloride induced stress responses of antioxidative activities in leaves and roots of pistachio rootstock. Biomolecules 10:189. https://doi.org/10.3390/biom10020189

    CAS  Article  PubMed Central  Google Scholar 

  3. Almeida T, Pinto G, Correia B, Santos C, Gonçalves S (2013) QsMYB1 expression is modulated in response to heat and drought stresses and during plant recovery in Quercus suber. Plant Physiol Biochem 73:274–281. https://doi.org/10.1016/j.plaphy.2013.10.007

    CAS  Article  PubMed  Google Scholar 

  4. Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190. https://doi.org/10.1007/s11099-013-0021-6

    CAS  Article  Google Scholar 

  5. Berger E, Frör O, Schäfer RB (2019) Salinity impacts on river ecosystem processes: a critical mini-review. Philos Trans R Soc Lond B Biol Sci 374:20180010. https://doi.org/10.1098/rstb.2018.0010

    CAS  Article  Google Scholar 

  6. Camilo-Alves CSP, Vaz M, Da Clara MIE, Ribeiro NMA (2017) Chronic cork oak decline and water status: new insights. New For 48:753–772. https://doi.org/10.1007/s11056-017-9595-3

    Article  Google Scholar 

  7. Cha-um S, Kirdmanee C (2010) Effects of water stress induced by sodium chloride and mannitol on proline accumulation, photosynthetic abilities and growth characters of eucalyptus (Eucalyptus camaldulensis Dehnh.). New For 40:349–360. https://doi.org/10.1007/s11056-010-9204-1

    Article  Google Scholar 

  8. Cho Y-H, Yoo S-D (2011) Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PLoS Genet 7:e1001263. https://doi.org/10.1371/journal.pgen.1001263

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Costa A, Barbosa I, Roussado C, Graça J, Spiecker H (2016) Climate response of cork growth in the Mediterranean oak (Quercus suber L.) woodlands of southwestern Portugal. Dendrochronologia 38:72–81. https://doi.org/10.1016/j.dendro.2016.03.007

    Article  Google Scholar 

  10. Daliakopoulos IN, Tsanis IK, Koutroulis A, Kourgialas NN, Varouchakis AE, Karatzas GP, Ritsema CJ (2016) The threat of soil salinity: a European scale review. Sci Total Environ 573:727–739. https://doi.org/10.1016/j.scitotenv.2016.08.177

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Dias MC, Mariz-Ponte N, Santos C (2019) Lead induces oxidative stress in Pisum sativum plants and changes the levels of phytohormones with antioxidant role. Plant Physiol Biochem 137:121–129. DOI:https://doi.org/10.1016/j.plaphy.2019.02.005

    CAS  Article  PubMed  Google Scholar 

  12. Dias MC, Pinto DCGA, Freitas H, Santos C, Silva AMS (2020) The antioxidant system in Olea europaea to enhanced UV-B radiation also depends on flavonoids and secoiridoids. Phytochemistry 170:12199. https://doi.org/10.1016/j.phytochem.2019.112199

    CAS  Article  Google Scholar 

  13. Dong S, Zhang J, Beckles DM (2018) A pivotal role for starch in the reconfiguration of 14 C-partitioning and allocation in Arabidopsis thaliana under short-term abiotic stress. Sci Rep 8:9314. https://doi.org/10.1038/s41598-018-27610-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Fusaro L, Mereu S, Brunetti C, Di Ferdinando M, Ferrini F, Manes F, Salvatori E, Marzuoli R, Gerosa G, Tattini M (2014) Photosynthetic performance and biochemical adjustments in two co-occurring Mediterranean evergreens, Quercus ilex and Arbutus unedo, differing in salt-exclusion ability. Funct Plant Biol 41:391–200. https://doi.org/10.1071/FP13241

    CAS  Article  PubMed  Google Scholar 

  15. Hasanuzzaman M, Nahar K, Rahman A, Anee TI, Alam MU, Bhuiyan TF, Oku H, Fujita M (2017) Approaches to enhance salt stress tolerance in wheat, wheat improvement, management and utilization. In: Wanyera R, Owuoche J, IntechOpen. https://doi.org/10.5772/67247

  16. Hernández JA (2019) Salinity tolerance in plants: trends and perspectives. Int J Mol Sci 20:2408. https://doi.org/10.3390/ijms20102408

    Article  PubMed Central  Google Scholar 

  17. Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611. https://doi.org/10.1007/s004250050524

    CAS  Article  Google Scholar 

  18. Jalali P, Navabpour S, Yamchi A, Soltanloo H, Bagherikia (2020) Differential responses of antioxidant system and expression profile of some genes of two rice genotypes in response to salinity stress. Biologia 75:785–793. https://doi.org/10.2478/s11756-019-00393-x

    CAS  Article  Google Scholar 

  19. Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20:586–594. https://doi.org/10.1016/j.tplants.2015.06.008

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Katuwal K, Xiao B, Jespersen D (2020) Physiological responses and tolerance mechanisms of seashore paspalum and centipedegrass exposed to osmotic and iso-osmotic salt stresses. J Plant Physiol 248:153154. https://doi.org/10.1016/j.jplph.2020.153154

    CAS  Article  PubMed  Google Scholar 

  21. Khan AL, Muneer S, Kim Y, Al-Rawahi A, Al-Harrasi A (2019) Silicon and salinity: crosstalk in crop-mediated stress tolerance mechanisms. Front Plant Sci 10:1429. https://doi.org/10.3389/fpls.2019.01429

    Article  PubMed  PubMed Central  Google Scholar 

  22. Kharusi L, Yahyai R, Yaish MW (2019) Antioxidant response to salinity in salt-tolerant and salt-susceptible cultivars of date palm. Agriculture 9:8. https://doi.org/10.3390/agriculture9010008

    CAS  Article  Google Scholar 

  23. Khedr AHA (2003) Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. J Exp Bot 54:2553–2562. https://doi.org/10.1093/jxb/erg277

    CAS  Article  PubMed  Google Scholar 

  24. Kim HN, Jin HY, Kwak MJ, Khaine I, You HN, Lee TY, Ahn TH, Woo SY (2017) Why does Quercus suber species decline in Mediterranean areas? J Asia-Pac Biodivers 10:337–341. https://doi.org/10.1016/j.japb.2017.05.004

    Article  Google Scholar 

  25. Kurtz CM, Savage JA, Huang I-Y, Cavender-Bares J (2013) Consequences of salinity and freezing stress for two populations of Quercus virginiana Mill. (Fagaceae) grown in a common garden 1. J Torrey Bot Soc 140:145–156. https://doi.org/10.3159/TORREY-D-12-00060.1

    Article  Google Scholar 

  26. Ma Y, Dias MC, Freitas H (2020) Drought and salinity stress responses and microbe-induced tolerance in plants. https://doi.org/10.3389/fpls.2020.591911

    Article  PubMed  PubMed Central  Google Scholar 

  27. Magalhães AP, Verde N, Reis F, Martins I, Costa D, Lino-Neto T, Castro PH, Tavares RM, Azevedo H (2016) RNA-Seq and gene network analysis uncover activation of an ABA-dependent signalosome during the cork oak root response to drought. Front Plant Sci 6:1–17. https://doi.org/10.3389/fpls.2015.01195

    Article  Google Scholar 

  28. Mousavi S, Regni L, Bocchini M, Mariotti R, Cultrera NGM, Mancuso S, Googlani J, Chakerolhosseini MR, Guerrero C, Albertini E, Baldoni L, Proietti P (2019) Physiological, epigenetic and genetic regulation in some olive cultivars under salt stress. Sci Rep 9:1093

    Article  Google Scholar 

  29. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1038/s41598-018-37496-5

    CAS  Article  Google Scholar 

  30. Natali L, Vangelisti A, Guidi L, Remorini D, Cotrozzi L, Lorenzini G, Nali C, Pellegrini C, Trivellini C, Vernieri P, Landi M, Cavallini A, Giordani T (2018) How Quercus ilex L. saplings face combined salt and ozone stress: a transcriptome analysis. BMC Genom 19:87. https://doi.org/10.1186/s12864-018-5260-2

    CAS  Article  Google Scholar 

  31. Peguero-Pina JJ, Sancho-Knapik D, Morales F, Flexas J, Gil-Pelegrín E (2009) Differential photosynthetic performance and photoprotection mechanisms of three Mediterranean evergreen oaks under severe drought stress. Funct Plant Biol 36:453. https://doi.org/10.1071/FP08297

    Article  PubMed  Google Scholar 

  32. Rahman A, Nahar K, Mahmud JA, Hasanuzzaman M, Hossain MS, Fujita M (2017) Salt stress tolerance in rice: emerging role of exogenous phytoprotectants. In: Jinquan L (ed), Advances in international rice eesearch, IntechOpen. https://doi.org/10.5772/67098

  33. Riadh K, Wided M, Hans-Werner K, Chedly A (2010) Responses of halophytes to environmental stresses with special emphasis to salinity. Ad Bot Res. https://doi.org/10.1016/S0065-2296(10)53004-0

    Article  Google Scholar 

  34. Sedas A, González Y, Winter K, Lopez OR (2019) Seedling responses to salinity of 26 Neotropical tree species. AoB PLANTS 11plz062. https://doi.org/10.1093/aobpla/plz062

    Article  PubMed  PubMed Central  Google Scholar 

  35. Shin YK, Bhandari SR, Cho MC, Lee JG (2020) Evaluation of chlorophyll fluorescence parameters and proline content in tomato seedlings grown under different salt stress conditions. Hortic Environ Biotechnol 61:433–443. https://doi.org/10.1007/s13580-020-00231-z

    CAS  Article  Google Scholar 

  36. Sims DA, Gamon JA (2002) Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sens Environ 81:337–354. https://doi.org/10.1016/S0034-4257(02)00010-X

    Article  Google Scholar 

  37. Stitt M, Bulpin PV, Ap Rees T (1978) Pathway of starch breakdown in photosynthetic tissues of Pisum sativum. Biochim Biophys Acta Gen Subj 544:200–214. https://doi.org/10.1016/0304-4165(78)90223-4

    CAS  Article  Google Scholar 

  38. Thalmann M, Santelia D (2017) Starch as a determinant of plant fitness under abiotic stress. New Phytol 214:943–951. https://doi.org/10.1111/nph.14491

    CAS  Article  PubMed  Google Scholar 

  39. Thyroff E, Burney O, Mickelbart M, Jacobs D (2019) Unraveling shade tolerance and plasticity of semi-evergreen oaks: insights from maritime forest live oak restoration. Front Plant Sci 10:1526. https://doi.org/10.3389/fpls.2019.01526

    Article  PubMed  PubMed Central  Google Scholar 

  40. Wang N, Qiao W, Liu X, Shi J, Xu Q, Zhou H, Yan G, Huang Q (2017) Relative contribution of Na+/K + homeostasis, photochemical efficiency and antioxidant defense system to differential salt tolerance in cotton (Gossypium hirsutum L.) cultivars. Plant Physiol Biochem 119:121–131. https://doi.org/10.1016/j.plaphy.2017.08.024

    CAS  Article  PubMed  Google Scholar 

  41. Wu G, Zhou Z, Chen P, Tang X, Shao H, Wang H (2014) Comparative ecophysiological study of salt stress for wild and cultivated soybean species from the yellow river delta, China. Sci World J. https://doi.org/10.1155/2014/651745

    Article  PubMed  PubMed Central  Google Scholar 

  42. Zhang M, Fang Y, Ji Y, Jiang Z, Wang L (2013) Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. S Afric J Bot 85:1–9

    Article  Google Scholar 

  43. Zhou B, Wang J, Guo Z, Tan H, Zhu X (2006) A simple colorimetric method for determination of hydrogen peroxide in plant tissues. Plant Growth Regul 49:113–118. https://doi.org/10.1007/s10725-006-9000-2

    CAS  Article  Google Scholar 

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Acknowledgements

This work was supported by FEDER through the Operational Competitiveness Program—COMPETE—within the scope of project “PTDC/AGRGPL/118505/2010 “An integrated approach to identify stress-related regulatory genes in cork oak (SuberStress)”, and from PT national funds (FCT/MCTES, Fundação para a Ciência e a Tecnologia and Ministério da Ciência, Tecnologia e Ensino Superior) through grant UID/QUI/50006/2020; and the projects of the CEF UI0183—UID/BIA/04004/2020 and LAQV-REQUIMTE UIDB/50006/2020. J.M.P. Ferreira de Oliveira (Grant Number SFRH/BPD/74868/2010) and M.C. Dias (Grant Number SFRH/BPD/100865/2014) thank FCT (Fundação para a Ciência e Tecnologia) for funding through program DL 57/2016 – Norma transitória. M.Araújo thanks FCT (Grant Number SFRH/BD/116801/2016). The authors thanks to G. Pinto and J. Amaral for their technical support.

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JMPFO, CS, MMO and MCD designed the experiments; JMPFO and MCD performed the research; JMPFO, MA and MCD analysed the data; JMPFO, CS, MMO, MA and MCD wrote and revised the manuscript.

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Correspondence to Maria Celeste Dias.

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de Oliveira, J.M.P.F., Santos, C., Araújo, M. et al. High-salinity activates photoprotective mechanisms in Quercus suber via accumulation of carbohydrates and involvement of non-enzymatic and enzymatic antioxidant pathways. New Forests (2021). https://doi.org/10.1007/s11056-021-09856-z

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Keywords

  • Carbohydrates
  • Carotenoids
  • Cork oak
  • Mediterranean region
  • Photosynthetic performance
  • Salt stress