, Volume 249, Issue 5, pp 1583–1598 | Cite as

Responses of olive plants exposed to different irrigation treatments in combination with heat shock: physiological and molecular mechanisms during exposure and recovery

  • Márcia Araújo
  • José Miguel P. Ferreira de Oliveira
  • Conceição Santos
  • José Moutinho-Pereira
  • Carlos Correia
  • Maria Celeste DiasEmail author
Original Article


Main conclusion

A water-deficit period, leading to stomatal control and overexpression of protective proteins (sHSP and DHN), contributes to olive´s tolerance to later imposed stress episodes. Aquaporins modulation is important in olive recovery.

Olive is traditionally cultivated in dry farming or in high water demanding irrigated orchards. The impact of climate change on these orchards remains to unveil, as heat and drought episodes are increasing in the Mediterranean region. To understand how young plants face such stress episodes, olive plants growing in pots were exposed to well-irrigated and non-irrigated treatments. Subsequently, plants from each treatment were either exposed to 40 °C for 2 h or remained under control temperature. After treatments, all plants were allowed to grow under well-irrigated conditions (recovery). Leaves were compared for photosynthesis, relative water content, mineral status, pigments, carbohydrates, cell membrane permeability, lipid peroxidation and expression of the protective proteins’ dehydrin (OeDHN1), heat-shock proteins (OeHSP18.3), and aquaporins (OePIP1.1 and OePIP2.1). Non-irrigation, whilst increasing carbohydrates, reduced some photosynthetic parameters to values below the ones of the well-irrigated plants. However, when both groups of plants were exposed to heat, well-irrigated plants suffered more drastic decreases of net CO2 assimilation rate and chlorophyll b than non-irrigated plants. Overall, OeDHN1 and OeHSP18.3 expression, which was increased in non-irrigated treatment, was potentiated by heat, possibly to counteract the increase of lipid peroxidation and loss of membrane integrity. Plants recovered similarly from both irrigation and temperature treatments, and recovery was associated with increased aquaporin expression in plants exposed to one type of stress (drought or heat). These data represent an important contribution for further understanding how dry-farming olive will cope with drought and heat episodes.


Aquaporins Climate change Dehydrins Drought Heat-shock proteins Photosynthesis 







Heat-shock protein




Non-irrigated plant, NIwith heat shock


Plasma membrane-intrinsic protein


Well-irrigated plant, WIwith heat shock



This work was financed by FCT/MEC through national funds and the co-funding by the FEDER (POCI/01/0145/FEDER/007265), within the PT2020 Partnership Agreement, and COMPETE 2010, within the projects UID/AGR/04033/2013, UID/BIA/04004/2013, UID/MULTI/04378/2013, UID/QUI/00062/2013, and UID/QUI/50006/2013. Institution CITAB, for its financial support through the European Investment Funds by FEDER/COMPETE/POCI—Operational Competitiveness and Internationalization Program, under Project POCI-01-0145-FEDER-006958 and National Funds by FCT—Portuguese Foundation for Science and Technology, under the project UID/AGR/04033/2013. In addition, FCT supported the doctoral fellowship of M Araújo (SFRH/BD/116801/2016), the contract research of MC Dias (SFRH/BPD/100865/2014), and of José Miguel P. Ferreira de Oliveira (SFRH/BPD/74868/2010) through POCH/FSE. The authors would like to thank JCLopes for the English revision of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

425_2019_3109_MOESM1_ESM.docx (14 kb)
Supplementary material 1 (DOCX 14 kb) Supplementary Material S1 Maximum quantum efficiency of photosystem II (Fv/Fm) and non-photochemical quenching (NPQ) measured in leaves of O. europaea after stress exposure and recovery from well-irrigated (WI) and WI with heat shock (WIH), non-irrigated (NI) and NI with heat shock (NIH). Values are mean ± SE (n = 7–10)


  1. Abdallah MB, Methenni K, Nouairi I, Zarrouk M, Youssef NB (2017) Drought priming improves subsequent more severe drought in a drought-sensitive cultivar of olive cv. Chétoui. Sci Hortic 221:43–52. CrossRefGoogle Scholar
  2. Abid M, Ali S, Qi LK, Zahoor R, Tian Z, Jiang D, Snider JL, Dai T (2018) Physiological and biochemical changes during drought and recovery periods at tillering and jointing stages in wheat (Triticum aestivum L.). Sci Rep 8:1–15. CrossRefGoogle Scholar
  3. Araújo M, Santos C, Costa M et al (2016) Plasticity of young Moringa oleifera L. plants to face water deficit and UVB radiation challenges. J Photochem Photobiol B Biol 162:278–285. CrossRefGoogle Scholar
  4. Araújo M, Santos C, Dias MC (2018) Can young olive plants overcome heat shock? In: Alves F, Leal Filho W, Azeiteiro U (eds) Theory and practice of climate adaptation. Springer Int Publishing, New York, pp 193–203CrossRefGoogle Scholar
  5. Assab E, Rampino P, Mita G, Perrotta C (2011) Heat shock response in olive (Olea europaea L.) twigs: identification and analysis of a cDNA coding a class I small heat shock protein. Plant Biosyst 145:419–425. CrossRefGoogle Scholar
  6. Azoulay-Shemer T, Bagheri A, Wang C, Palomares A, Stephan AB, Kunz HH, Schroeder JI (2016) Starch biosynthesis in guard cells but not in mesophyll cells is involved in CO2-induced stomatal closing. Plant Physiol 171:788–798. Google Scholar
  7. Bacelar EA, Correia CM, Moutinho-Pereira JM, Gonçalves BC, Lopes JI, Torres-Pereira JM (2004) Sclerophylly and leaf anatomical traits of five field-grown olive cultivars growing under drought conditions. Tree Physiol 24:233–239. CrossRefGoogle Scholar
  8. Bacelar EA, Santos DL, Moutinho-Pereira JM, Gonçalves BC, Ferreira HF, Correia C (2006) Immediate responses and adaptative strategies of three olive cultivars under contrasting water availability regimes: changes on structure and chemical composition of foliage and oxidative damage. Plant Sci 170:596–605. CrossRefGoogle Scholar
  9. Benlloch-González M, Arquero O, Fournier JM, Barranco D, Benlloch M (2008) K+ starvation inhibits water-stress-induced stomatal closure. J Plant Physiol 165:623–630. CrossRefGoogle Scholar
  10. Biosystems Applied (2008) Guide to performing relative quantitation of gene expression using real-time quantitative PCR. Gene Expr 2009:1–60Google Scholar
  11. Brito C, Dinis L-T, Ferreira H, Moutinho-Pereira J, Correia C (2018) The role of nighttime water balance on Olea europaea plants subjected to contrasting water regimes. J Plant Physiol 226:56–63. CrossRefGoogle Scholar
  12. Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164:1600–1618. CrossRefGoogle Scholar
  13. Chaves MM (1991) Effects of water deficits on carbon assimilation. J Exp Bot 42:1–16. CrossRefGoogle Scholar
  14. Chiappetta A, Muto A, Bruno L, Woloszynska M, Lijsebettens MV, Bitonti MB (2015) A dehydrin gene isolated from feral olive enhances drought tolerance in Arabidopsis transgenic plants. Front Plant Sci 6:1–15. CrossRefGoogle Scholar
  15. Dias MC, Azevedo C, Costa M, Pinto G, Santos C (2014a) Melia azedarach plants show tolerance properties to water shortage treatment: an ecophysiological study. Plant Physiol Biochem 75:123–127. CrossRefGoogle Scholar
  16. Dias MC, Oliveira H, Costa A, Santos C (2014b) Improving elms performance under drought stress: the pretreatment with abscisic acid. Environ Exp Bot 100:64–73. CrossRefGoogle Scholar
  17. Dias MC, Moutinho-Pereira J, Correia C, Monteiro C, Araújo M, Brüggemann W, Santos C (2016) Physiological mechanisms to cope with Cr(VI) toxicity in lettuce: can lettuce be used in Cr phytoremediation? Environ Sci Pollut Res 23:15627–15637. CrossRefGoogle Scholar
  18. Dias MC, Correia S, Serôdio J, Silva AMS, Freitas H, Santos C (2018a) Chlorophyll fluorescence and oxidative stress endpoints to discriminate olive cultivars tolerance to drought and heat episodes. Sci Hortic 231:31–35. CrossRefGoogle Scholar
  19. Dias MC, Pinto DCGA, Correia C, Moutinho-Pereira J, Oliveira H, Freitas H, Silva AMS, Santos C (2018b) UV-B radiation modulates physiology and lipophilic metabolite profile in Olea europaea. J Plant Physiol 222:39–50. CrossRefGoogle Scholar
  20. Dias MC, Santos C, Pinto G, Silva AMS, Silva S (2018c) Titanium dioxide nanoparticles impaired both photochemical and non-photochemical phases of photosynthesis in wheat. Protoplasma. (Epub) Google Scholar
  21. Gollan PJ, Tikkanen M, Aro EM (2015) Photosynthetic light reactions: integral to chloroplast retrograde signalling. Curr Opin Plant Biol 27:180–191. CrossRefGoogle Scholar
  22. Guo W, Chen S, Hussain N, Cong Y, Liang Z, Chen K (2015) Magnesium stress signaling in plant: just a beginning. Plant Signal Behav 10:e992287. CrossRefGoogle Scholar
  23. Halder T, Upadhyaya G, Basak C, Das A, Chakraborty C, Ray S (2018) Dehydrins impart protection against oxidative stress in transgenic tobacco plants. Front Plant Sci 9:1–15. CrossRefGoogle Scholar
  24. Hara M, Kondo M, Kato T (2013) A KS-type dehydrin and its related domains reduce Cu-promoted radical generation and the histidine residues contribute to the radical-reducing activities. J Exp Bot 64:1615–1624. CrossRefGoogle Scholar
  25. Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155. CrossRefGoogle Scholar
  26. 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. CrossRefGoogle Scholar
  27. Irigoyen JJ, Emerich DW, Sanchez-Diaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60. CrossRefGoogle Scholar
  28. Kapilan R, Vaziri M, Zwiazek JJ (2018) Regulation of aquaporins in plants under stress. Biol Res 51:1–11. CrossRefGoogle Scholar
  29. Kumar M, Lee SC, Kim JY, Kim SJ, Aye SS, Kim SR (2014) Over-expression of dehydrin gene, OsDhn1, improves drought and salt stress tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). J Plant Biol 57:383–393. CrossRefGoogle Scholar
  30. Larbi A, Vázquez S, El-Jendoubi H, Msallem M, Abadía J, Abadía A, Morales F (2015) Canopy light heterogeneity drives leaf anatomical, eco-physiological, and photosynthetic changes in olive trees grown in a high-density plantation. Photosynth Res 123:141–155. CrossRefGoogle Scholar
  31. Lawson T, Simkin AJ, Kelly G, Granot D (2014) Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour. New Phytol 203:1064–1081. CrossRefGoogle Scholar
  32. le Provost G, Herrera R, Paiva JA, Chaumeli P, Salin F, Plomion C (2007) A micromethod for high throughput RNA extraction in forest trees. Biol Res 40:291–297. CrossRefGoogle Scholar
  33. Liu C, Li C, Liang D, Ma F, Wang S, Wang P, Wang R (2013) Aquaporin expression in response to water-deficit stress in two Malus species: relationship with physiological status and drought tolerance. Plant Growth Regul 70:187–197. CrossRefGoogle Scholar
  34. Martin-StPaul N, Delzon S, Cochard H (2017) Plant resistance to drought depends on timely stomatal closure. Ecol Lett 20:1437–1447. CrossRefGoogle Scholar
  35. McLoughlin F, Basha E, Fowler ME, Kim M, Bordowitz Katiyar-Agarwal S, Vierling E (2016) Class I and II small heat-shock proteins protect protein translation factors during heat stress. Plant Physiol 172:1221–1236. Google Scholar
  36. Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125. CrossRefGoogle Scholar
  37. Moshelion M, Halperin O, Wallach R, Oren R, Way DA (2015) Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: crop water-use efficiency, growth and yield. Plant Cell Environ 38:1785–1793. CrossRefGoogle Scholar
  38. Nouri MZ, Moumeni A, Komatsu S (2015) Abiotic stresses: insight into gene regulation and protein expression in photosynthetic pathways of plants. Int J Mol Sci 16:20392–20416. CrossRefGoogle Scholar
  39. Osaki M, Shinano T, Tadano T (1991) Redistribution of carbon and nitrogen compounds from the shoot to the harvesting organs during maturation in field crops. Soil Sci Plant Nutr 37:117–128. CrossRefGoogle Scholar
  40. Park C-J, Seo Y-S (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol J 31:323–333. CrossRefGoogle Scholar
  41. Perez-Martin A, Michelazzo C, Torres-Ruiz JM, Flexas J, Fernández JE, Sebastiani L, Diaz-Espejo A (2014) Regulation of photosynthesis and stomatal and mesophyll conductance under water stress and recovery in olive trees: correlation with gene expression of carbonic anhydrase and aquaporins. J Exp Bot 65:3143–3156. CrossRefGoogle Scholar
  42. Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882. CrossRefGoogle Scholar
  43. Pou A, Medrano H, Flexas J, Tyerman SD (2013) A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and re-watering. Plant, Cell Environ 36:828–843. CrossRefGoogle Scholar
  44. Ramos AF, Santos FL (2010) Yield and olive oil characteristics of a low-density orchard (cv. Cordovil) subjected to different irrigation regimes. Agric Water Manag 97:363–373. CrossRefGoogle Scholar
  45. Ré MD, Gonzalez C, Escobar MR et al (2016) Small heat shock proteins and the postharvest chilling tolerance of tomato fruit. Physiol Plant 159:148–160. CrossRefGoogle Scholar
  46. Reddy KS, Sekhar KM, Reddy AR (2017) Genotypic variation in tolerance to drought stress is highly coordinated with hydraulic conductivity-photosynthesis interplay and aquaporin expression in field-grown mulberry (Morus spp.). Tree Physiol 37:926–937. CrossRefGoogle Scholar
  47. Rozen S, Skaletsky H (1999) Primer3 on the WWW for general users and for biologist programmers. In: Misener S, Krawetz SA (eds) Methods in molecular biology, vol 132: bioinformatics methods and protocols. Humana Press, Totowa, pp 365–386CrossRefGoogle Scholar
  48. Sato R, Ito H, Tanaka A (2015) Chlorophyll b degradation by chlorophyll b reductase under high-light conditions. Photosynth Res 126:249–259. CrossRefGoogle Scholar
  49. Secchi F, Lovisolo C, Schubert A (2007) Expression of OePIP2.1 aquaporin gene and water relations of Olea europaea twigs during drought stress and recovery. Ann Appl Biol 150:163–167. CrossRefGoogle Scholar
  50. 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. CrossRefGoogle Scholar
  51. Sofo A (2011) Drought stress tolerance and photoprotection in two varieties of olive tree. Acta Agric Scand Sect B Soil Plant Sci 61:711–720. Google Scholar
  52. Tamburino R, Vitale M, Ruggiero A, Sassi M, Sannino L, Arena S, Costa A, Batelli G, Zambrano N, Scaloni A, Grillo S, Scotti N (2017) Chloroplast proteome response to drought stress and recovery in tomato (Solanum lycopersicum L.). BMC Plant Biol 17:1–14. CrossRefGoogle Scholar
  53. Torres-Ruiz JM, Diaz-Espejo A, Morales-Sillero A, Martín-Palomo MJ, Mayr S, Beikircher B, Fernández JE (2013) Shoot hydraulic characteristics, plant water status and stomatal response in olive trees under different soil water conditions. Plant Soil 373:77–87. CrossRefGoogle Scholar
  54. Tripepi M, Pöhlschroder M, Bitonti MB (2011) Diversity of dehydrins in Oleae europaea plants exposed to stress. Open Plant Sci J 5:9–13. CrossRefGoogle Scholar
  55. von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387. CrossRefGoogle Scholar
  56. Wang Y, Jensen CR, Liu F (2017) Nutritional responses to soil drying and rewetting cycles under partial root-zone drying irrigation. Agric Water Manag 179:254–259. CrossRefGoogle Scholar
  57. Yaneff A, Vitali V, Amodeo G (2015) PIP1 aquaporins: intrinsic water channels or PIP2 aquaporin modulators? FEBS Lett 589:3508–3515. CrossRefGoogle Scholar
  58. Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12:1047–1064. CrossRefGoogle Scholar
  59. Zhu X, Chen J, Qiu K, Kuai B (2017) Phytohormone and light regulation of chlorophyll degradation. Front Plant Sci 8:1–8. Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Life Science, Centre for Functional Ecology (CFE)University of CoimbraCoimbraPortugal
  2. 2.Integrated Biology and Biotechnology Laboratory, Department of Biology, Faculty of SciencesUniversity of PortoPortoPortugal
  3. 3.Center for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB)University of Trás-os-Montes and Alto DouroVila RealPortugal
  4. 4.LAQV, REQUIMTE, Laboratory of Applied Chemistry, Department of Chemical Sciences, Faculty of PharmacyUniversity of PortoPortoPortugal
  5. 5.LAQV, REQUIMTE, Faculty of SciencesUniversity of PortoPortoPortugal
  6. 6.QOPNA and Department of ChemistryUniversity of AveiroAveiroPortugal

Personalised recommendations