Skip to main content
Log in

Assessing drought tolerance in field-grown sunflower hybrids by chlorophyll fluorescence kinetics

  • Original Article
  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Drought is one of the most damaging abiotic stress factors commonly experienced by plants, resulting in a significant loss of crop yield worldwide. The aim of the study was to assess drought tolerance of sunflower (Helianthus annuus) hybrids and find out potentially underlying photobiological traits. Experiment was conducted in the agricultural field of Eastern Mediterranean Agricultural Research Institute in Adana. To evaluate the drought tolerance of twenty-six sunflower hybrids polyphasic chlorophyll fluorescence measurements were performed at the three growth stages named as vegetative, head formation and milky seed (stress 1, S1; stress 2, S2; stress 3, S3, respectively). The hybrids were classified from drought tolerant to drought sensitive based on their drought factor index (DFI) values calculated from photosynthetic performance index. 9444 A X 9947 R and 9444 A X 8129 R were determined as the most tolerant hybrids, whereas 2453 A X 8129 R and 7751 A X TT 135 R were determined as the most sensitive hybrids. Severe drought stress (S2) inhibited severely both the donor and the acceptor sides of photosystem II in sensitive hybrids. Photosynthetic structures of drought-tolerant hybrids were less damaged by drought stress, consequently these hybrids could maintain their photosynthetic performances (minor changes in φPo, ψo, δRo, specific and/or phenomenological energy fluxes) approximately control levels under severe drought condition. As a result, results, 9444 A X 9947 R and 9444 A X 8129 R hybrids could be recommended to be used in the breeding programs and further studies as genetic material and to be grown in drought-prone areas.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Askri H, Gharbi F, Rejeb S, Mliki A, Ghorbel A (2018) Differential physiological responses of Tunisian wild grapevines (Vitis vinifera L. subsp. sylvestris) to NaCl salt stress. Braz J Plant Physiol 41:795–804

    Google Scholar 

  • Banks JM (2018) Chlorophyll fluorescence as a tool to identify drought stress in Acer genotypes. Environ Exp Bot 155:118–127

    Article  CAS  Google Scholar 

  • Boureima S, Oukarroum A, Diouf M, Cisse N, Van Damme P (2012) Screening for drought tolerance in mutant germplasm of sesame (Sesamum indicum) probing by chlorophyll a fluorescence. Environ Exp Bot 81:37–43

    Article  CAS  Google Scholar 

  • Brestic M, Zivcak M, Kalaji HM, Carpentier R, Allakhverdiev SI (2012) Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol Biochem 57:93–105

    Article  CAS  PubMed  Google Scholar 

  • Brestic M, Zivcak M, Kunderlikova K, Allakhverdiev SI (2016) High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines. Photosynth Res 130:251–266

    Article  CAS  PubMed  Google Scholar 

  • Ceppi MG, Oukarroum A, Çiçek N, Strasser RJ, Schansker G (2012) The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulphate deficiencies, drought stress and salt stress. Physiol Plant 144:277–288

    Article  CAS  PubMed  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  CAS  Google Scholar 

  • Chen S, Yang J, Zhang M, Strasser RJ, Qiang S (2016) Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise O-J-I-P. Environ Exp Bot 122:126–140

    Article  CAS  Google Scholar 

  • Çiçek N, Arslan Ö, Çulha-Erdal Ş, Eyidoğan F, Ekmekçi Y (2015) Are the photosynthetic performance indexes and the drought factor index satisfactory selection criterion for stress? Fresenius Environ Bull 24:4190–4198

    Google Scholar 

  • Çiçek N, Oukarroum A, Strasser RJ, Schansker G (2018) Salt stress effects on the photosynthetic electron transport chain in two chickpea lines differing in their salt stress tolerance. Photosynth Res 136:291–301

    Article  CAS  PubMed  Google Scholar 

  • Delibaş L (1994) Irrigation. Publication No: 213, Faculty of Agriculture, Trakya University, Tekirdağ, p 199 (in Turkish)

    Google Scholar 

  • Ekmekçi Y, Bohms A, Thomson JA, Mundree SG (2005) Photochemical and antioxidant responses in the leaves of Xerophyta viscosa Baker and Digitaria sanguinalis L. under water deficit. Z Naturforschung C 60:435–443

    Article  Google Scholar 

  • FAOSTAT (2018) Food and Agriculture Organization of the United Nation (FAO) statistical databases. http://www.fao.org. Accessed 15 Dec 2018

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212

    Article  Google Scholar 

  • Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fracasso A, Trindade L, Amaducci S (2016) Drought tolerance strategies highlighted by two Sorghum bicolor races in a dry-down experiment. J Plant Physiol 190:1–14

    Article  CAS  PubMed  Google Scholar 

  • Goltsev V, Zaharieva I, Chernev P, Kouzmanova M, Kalaji HM, Yordanov I, Krasteva V, Alexandrov V, Stefanov D, Allakhverdiev SI, Strasser RJ (2012) Drought-induced modifications of photosynthetic electron transport in intact leaves: analysis and use of neural networks as a tool for a rapid non-invasive estimation. Biochim Biophys Acta 1817:1490–1498

    Article  CAS  PubMed  Google Scholar 

  • Goltsev VN, Kalaji HM, Paunov M, Baba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol 63:869–893

    Article  CAS  Google Scholar 

  • Hermans C, Smeyers M, Rodriguez RM, Eyletters M, Strasser RJ, Delhaye JP (2003) Quality assessment of urban trees: a comparative study of physiological characterisation, airborne imaging and on site fluorescence monitoring by the OJIP-test. J Plant Physiol 160:81–90

    Article  CAS  PubMed  Google Scholar 

  • Hussain M, Farooq S, Hasan W, Ul-Allahd S, Tanveere M, Farooq M, Nawaz A (2018) Drought stress in sunflower: physiological effects and its management through breeding and agronomic alternatives. Agric Water Manag 201:152–166

    Article  Google Scholar 

  • Jedmowski C, Ashoub A, Momtaz O, Brüggemann W (2015) Impact of drought, heat, and their combination on chlorophyll fluorescence and yield of wild barley (Hordeum spontaneum). J Bot. https://doi.org/10.1155/2015/120868

    Article  Google Scholar 

  • Kalaji HM, Govindjee Bosa K, Koscielniak J, Zuk-Golaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ Exp Bot 73:64–72

    Article  CAS  Google Scholar 

  • Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dąbrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli D, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serôdio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Lukasik I, Goltsev V, Ladle RJ (2016a) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102

    Article  CAS  Google Scholar 

  • Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L, Goltsev V, Guidi L, Jajoo A, Li P, Losciale P, Mishra VK, Misra AN, Nebauer SG, Pancaldi S, Penella C, Pollastrini M, Suresh K, Tambussi E, Yanniccari M, Zivcak M, Cetner MD, Samborska IA, Stirbet A, Olsovska K, Kunderlikova K, Shelonzek H, Szymon Rusinowski S, Baba W (2016b) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res 132:13–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalaji HM, Rackova L, Paganova V, Swoczyna T, Rusinowski S, Sitko K (2018a) Can chlorophyll-a fluorescence parameters be used as bio-indicators to distinguish between drought and salinity stress in Tilia cordata Mill? Environ Exp Bot 152:149–157. https://doi.org/10.1016/j.envexpbot.2017.11.001

    Article  CAS  Google Scholar 

  • Kalaji HM, Rastogi A, Zivcak M, Brestic M, Daszkowska-Golec A, Sitko K, Alsharafa KY, Lotfi R, Stypinski P, Samborska IA, Cetner MD (2018b) Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors. Photosynthetica 56:953–961

    Article  CAS  Google Scholar 

  • Kan X, Ren J, Chen T, Cui M, Li C, Zhou R, Zhang Y, Liu H, Deng D, Yin Z (2017) Effects of salinity on photosynthesis in maize probed by prompt fluorescence, delayed fluorescence and P700 signals. Environ Exp Bot 140:56–64

    Article  CAS  Google Scholar 

  • Kaya Y, Balkan Nalcaiyi AS, Culha Erdal Ş, Arslan Ö, Cicek N, Pekcan V, Yilmaz Mİ, Evci G, Ekmekci Y (2016) Evaluation of male inbred lines of sunflower (Helianthus annuus L.) for resistance to drought via chlorophyll fluorescence. Turk J Field Crops 21:162–173

    Article  Google Scholar 

  • Lu C, Zhang J (1999) Effect of water stress on photosystem II photochemistry and its thermostability in wheat plants. J Exp Bot 336:1199–1206

    Article  Google Scholar 

  • Naumann JC, Young DR, Anderson JE (2008) Leaf chlorophyll fluorescence, reflectance, and physiological response to freshwater and saltwater flooding in the evergreen shrub, Myrica cerifera. Environ Exp Bot 63:402–409

    Article  CAS  Google Scholar 

  • Osakabe Y, Osakabe K, Shinozaki K, Tran LSP (2014) Response of plants to water stress. Front Plant Sci 5:1–8. https://doi.org/10.3389/fpls.2014.00086

    Article  Google Scholar 

  • Oukarroum A, Madidi SE, Schansker G, Strasser RJ (2007) Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ Exp Bot 60:438–446

    Article  CAS  Google Scholar 

  • Oukarroum A, Schansker G, Strasser RJ (2009) Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiol Plant 137:188–199

    Article  CAS  PubMed  Google Scholar 

  • Oukarroum A, Bussotti F, Goltsev V, Kalaji HM (2015) Correlation between reactive oxygen species production and photochemistry of photosystems I and II in Lemna gibba L. plants under salt stress. Environ Exp Bot 109:80–88

    Article  CAS  Google Scholar 

  • Oukarroum A, Lebrihi A, El Gharous M, Goltsev V, Strasser RJ (2018) Desiccation-induced changes of photosynthetic transport in Parmelina tiliacea (Hoffm.) Ach. analysed by simultaneous measurements of the kinetics of prompt fluorescence, delayed fluorescence and modulated 820 nm reflection. J Lumin 198:302–308

    Article  CAS  Google Scholar 

  • Öz MT, Turan Ö, Kayıhan C, Eyidoğan F, Ekmekçi Y, Yücel M, Öktem HA (2014) Evaluation of photosynthetic performance of wheat cultivars exposed to boron toxicity by the JIP fluorescence test. Photosynthetica 52:555–563

    Article  CAS  Google Scholar 

  • Pekcan V, Evci G, Yilmaz MI, Balkan Nalcaiyi AS, Çulha Erdal Ş, Cicek N, Ekmekci Y, Kaya Y (2015) Drought effects on yield traits of some sunflower inbred lines. Agric For 61:101–107

    Google Scholar 

  • Pereira WE, de Siqueira DL, Martínez CA, Puiatti M (2000) Gas exchange and chlorophyll fluorescence in four citrus rootstocks under aluminium stress. J Plant Physiol 157:513–520

    Article  CAS  Google Scholar 

  • Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882

    Article  CAS  PubMed  Google Scholar 

  • Psidova E, Zivcak M, Stojnic S, Orlovic S, Gömöry D, Kucerova J, Ditmarova L, Strelcova K, Brestic M, Kalaji HM (2018) Altitude of origin influences the responses of PSII photochemistry to heat waves in European beech (Fagus sylvatica L.). Environ Exp Bot 152:97–106

    Article  CAS  Google Scholar 

  • Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202

    Article  CAS  Google Scholar 

  • Ripoll J, Bertin N, Bidel LPR, Urban L (2016) A user’s view of the parameters derived from the induction curves of maximal chlorophyll a fluorescence: perspectives for analyzing stress. Front Plant Sci 7:1679. https://doi.org/10.3389/fpls.2016.01679

    Article  PubMed  PubMed Central  Google Scholar 

  • Robock A, Vinnikov KY, Srinivasan G, Entin JK, HoIIinger SE, Speranskaya NA, Liu S, Namkhai A (2000) The global soil moisture data bank. Bull Am Meteorol Soc 81:1281–1299

    Article  Google Scholar 

  • Schansker G, Toth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta 1706:250–261

    Article  CAS  PubMed  Google Scholar 

  • Seiler GJ, Qi LL, Marek LF (2017) Utilization of sunflower crop wild relatives for cultivated sunflower improvement. Crop Sci 57:1083–1101

    Article  Google Scholar 

  • Sperdouli I, Moustakas M (2012) Differential response of photosystem II photochemistry in young and mature leaves of Arabidopsis thaliana to the onset of drought stress. Acta Physiol Plant 34:1267–1276

    Article  CAS  Google Scholar 

  • Sperdouli I, Moustakas M (2014) Leaf developmental stage modulates metabolite accumulation and photosynthesis contributing to acclimation of Arabidopsis thaliana to water deficit. J Plant Res 127:481–489

    Article  CAS  PubMed  Google Scholar 

  • Stirbet A, Lazár D, Kromdijk J, Govindjee (2018) Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica 56:86–104

    Article  CAS  Google Scholar 

  • Strasser RJ (1978) The grouping model of plant photosynthesis. In: Akoyunoglou G, Argyroudi-Akoyunoglou JH (eds) Chloroplast development. Elsevier Biomedical Press, North-Holland, pp 513–538

    Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring ast fluorescence transients to address environmental questions: the JIP test. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer Academic, Dordrecht, pp 977–980

    Google Scholar 

  • Strasser BJ, Dau H, Heinze I, Senger H (1999) Comparison of light induced and cell cycle dependent changes in the photosynthetic apparatus: a fluorescence induction study on the green alga Scenedesmus obliquus. Photosynth Res 60:217–227

    Article  CAS  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor & Francis, London, pp 443–480

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326

    Article  CAS  PubMed  Google Scholar 

  • Strauss AJ, Krüger GHJ, Strasser RJ, Van Heerden PDR (2006) Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient O–J–I–P. Environ Exp Bot 56:147–157

    Article  CAS  Google Scholar 

  • Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of stress impact on plants’ vitality: applications in detecting and evaluating the beneficial role of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza: state of the art. Genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, Springer, Berlin, pp 679–703

    Chapter  Google Scholar 

  • Umar M, Siddiqui ZS (2018) Physiological performance of sunflower genotypes under combined salt and drought stress environment. Acta Bot Croat 77:36–44

    Article  CAS  Google Scholar 

  • Yusuf MD, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee Sarin NB (2010) Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochim Biophys Acta 1797:1428–1438

    Article  CAS  PubMed  Google Scholar 

  • Zivcak M, Brestic M, Olsovska K, Slamka P (2008) Performance index as a sensitive indicator of water stress in Triticum aestivum L. Plant Soil Environ 54:133–139

    Article  Google Scholar 

  • Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji MH, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546

    Article  CAS  PubMed  Google Scholar 

  • Zivcak M, Brestic M, Kunderlikova K, Olsovska K, Allakhverdiev SI (2015) Effect of photosystem I inactivation on chlorophyll a fluorescence induction in wheat leaves: does activity of photosystem I play any role in OJIP rise? J Photochem Photobiol B 152:318–324

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Scientific and Technological Research Council of Turkey (TUBITAK, Project Number: 1001- 113O926).

Author information

Authors and Affiliations

Authors

Contributions

VP and YK designed the study and ANÇ and VŞ carried out the field experiment. ÖA, ŞÇE and ASBN performed the chlorophyll fluorescence measurements. NÇ and YE analyzed the data and wrote the manuscript. We attest to the fact that all authors listed on the title page have contributed significantly to the work, have read the manuscript, attest to the validity and legitimacy of the data and its interpretation and agree to its submission to Brazilian Journal of Botany.

Corresponding author

Correspondence to Yasemin Ekmekçi.

Additional information

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

Çiçek, N., Pekcan, V., Arslan, Ö. et al. Assessing drought tolerance in field-grown sunflower hybrids by chlorophyll fluorescence kinetics. Braz. J. Bot 42, 249–260 (2019). https://doi.org/10.1007/s40415-019-00534-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-019-00534-1

Keywords

Navigation