Skip to main content

Advertisement

SpringerLink
Log in

Contrasting patterns of hormonal and photoprotective isoprenoids in response to stress in Cistus albidus during a Mediterranean winter

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Seasonal accumulation of hormonal and photoprotective isoprenoids, particularly α-tocopherol, carotenoids and abscisic acid, indicate their important role in protecting Cistus albidus plants from environmental stress during a Mediterranean winter. The high diurnal amounts of α-tocopherol and xanthophylls 3 h before maximum light intensity suggest a photoprotective response against the prevailing diurnal changes.

Abstract

The timing to modulate acclimatory/defense responses under changing environmental conditions is one of the most critical points for plant fitness and stress tolerance. Here, we report seasonal and diurnal changes in the contents of isoprenoids originated from the methylerythritol phosphate pathway, including chlorophylls, carotenoids, tocochromanols, and phytohormones (abscisic acid, cytokinins, and gibberellins) in C. albidus during a Mediterranean winter. Plants were subjected not only to typically low winter temperatures but also to drought, as shown by a mean plant water status of 54% during the experimental period. The maximum PSII efficiency, however, remained consistently high (Fv/Fm > 0.8), proving that C. albidus had efficient mechanisms to tolerate combined stress conditions during winter. While seasonal α-tocopherol contents remained high (200–300 µg/g DW) during the experimental period, carotenoid contents increased during winter attaining maximum levels in February (minimum air temperature ≤ 5 °C for 13 days). Following the initial transient increases of bioactive trans-zeatin (about fivefold) during winter, the increased abscisic acid contents proved its important role during abiotic stress tolerance. Diurnal amounts of α-tocopherol and xanthophylls, particularly lutein, zeaxanthin and neoxanthin including the de-epoxidation state, reached maximum levels as early as 2 h after dawn, when solar intensity was 68% lower than the maximum solar radiation at noon. It is concluded that (1) given their proven antioxidant properties, both α-tocopherol and carotenoids seem to play a crucial role protecting the photosynthetic apparatus under severe stress conditions; (2) high seasonal amounts of abscisic acid indicate its important role in abiotic stress tolerance within plant hormones, although under specific environmental conditions, accumulation of bioactive cytokinins appears to be involved to enhance stress tolerance; (3) the concerted diurnal adjustment of α-tocopherol and xanthophylls as early as 3 h before maximum light intensity suggests that plants anticipated the predictable diurnal changes in the environment to protect the photosynthetic apparatus.

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

Abbreviations

2iP:

Isopentenyladenine

DPS:

De-epoxidation state

IPA:

Isopentenyladenosine

MEP:

Methylerythritol phosphate

PC-8:

Plastochromanol-8

RWC:

Relative water content

t-Z:

trans-Zeatin

t-ZR:

trans-Zeatin riboside

VAZ:

Xanthophyll cycle pool

References

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

    CAS  Google Scholar 

  • Bahaji A, Sánchez-López ÁM, De Diego N, Muñoz FJ, Baroja-Fernández E, Li J, Ricarte-Bermejo A, Baslam M, Aranjuelo I, Almagro G, Humplík JF, Novák O, Spíchal L, Doležal K, Pozueta-Romero J (2015) Plastidic phosphoglucose isomerase is an important determinant of starch accumulation in mesophyll cells, growth, photosynthetic capacity, and biosynthesis of plastidic cytokinins in Arabidopsis. PLoS One 10(3):e0119641

    PubMed  PubMed Central  Google Scholar 

  • Barta C, Loreto F (2006) The relationship between the methyl-erythritol phosphate pathway leading to emission of volatile isoprenoids and abscisic acid content in leaves. Plant Physiol 141(4):1676–1683

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bray EA (2002) Abscisic acid regulation of gene expression during water-deficit stress in the era of the Arabidopsis genome. Plant Cell Environ 25(2):153–161

    CAS  PubMed  Google Scholar 

  • Brossa R, Pintó-Marijuan M, Francisco R, López-Carbonell M, Chaves MM, Alegre L (2015) Redox proteomics and physiological responses in Cistus albidus shrubs subjected to long-term summer drought followed by recovery. Planta 241(4):803–822

    CAS  PubMed  Google Scholar 

  • Brunetti C, Ferrini F, Fini A, Tattini M (2014) New evidence for the functional roles of volatile and non-volatile isoprenoids in stressed plants. Agrochimica 58:61–76

    Google Scholar 

  • Chaudhary N, Khurana P (2009) Vitamin E biosynthesis genes in rice: molecular characterization, expression profiling and comparative phylogenetic analysis. Plant Sci 177:479–491

    CAS  Google Scholar 

  • Cortleven A, Nitschke S, Klaumünzer M, AbdElgawad H, Asard H, Grimm B, Riefler M, Schmülling T (2014) A novel protective function for cytokinin in the light stress response is mediated by the ARABIDOPSIS HISTIDINE KINASE2 and ARABIDOPSIS HISTIDINE KINASE3 receptors. Plant Physiol 164:1470–1483

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cotado A, Müller M, Morales M, Munné-Bosch S (2018) Linking jasmonates with pigment accumulation and photoprotection in a high-mountain endemic plant, Saxifraga longifolia. Environ Exp Bot 154:56–65

    CAS  Google Scholar 

  • Covington MF, Harmer SL (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol 5:222

    Google Scholar 

  • Covington MF, Maloof J, Straume M, Kay S, Harmer SL (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9:R130

    PubMed  PubMed Central  Google Scholar 

  • Daie J, Campbell WF (1981) Response of tomato plants to stressful temperatures: increase in abscisic acid concentrations. Plant Physiol 67:26–29

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    CAS  PubMed  Google Scholar 

  • Demming-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    Google Scholar 

  • Demming-Adams B, Adams WW III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–27

    Google Scholar 

  • Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W, Gershenzon J (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc Natl Acad Sci USA 102(3):933–938

    CAS  PubMed  Google Scholar 

  • Estévez JM, Cantero A, Reindl A, Reichler S, León P (2001) 1-Deoxy-d-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem 276(25):22901–22909

    PubMed  Google Scholar 

  • Falk J, Munné-Bosch S (2010) Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot 61(6):1549–1566

    CAS  PubMed  Google Scholar 

  • Fernández-Marín B, Hernández A, Garcia-Plazaola JI, Esteban R, Míguez F, Artetxe U, Gómez-Sagasti MT (2017) Photoprotective strategies of Mediterranean plants in relation to morphological traits and natural environmental pressure: a meta-analytical approach. Front Plant Sci 8:1051

    PubMed  PubMed Central  Google Scholar 

  • Finkelstein R (2013) Abscisic acid synthesis and response. The Arabidopsis book. American Society of Plant Biologists, Rockville. https://doi.org/10.1199/tab.0166

    Book  Google Scholar 

  • Flores A, Grau A, Laurich F, Dörffling K (1988) Effect of new terpenoid analogues of abscisic acid on chilling and freezing resistance. J Plant Physiol 132:362–369

    CAS  Google Scholar 

  • Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155(1):93–100

    CAS  PubMed  Google Scholar 

  • Grundy J, Stoker C, Carré IA (2015) Circadian regulation of abiotic stress tolerance in plants. Front Plant Sci 6:648

    PubMed  PubMed Central  Google Scholar 

  • Gruszka J, Pawlak A, Kruk J (2008) Tocochromanols, plastoquinol, and other biological prenyllipids as singlet oxygen quenchers-determination of singlet oxygen quenching rate constants and oxidation products. Free Radic Biol Med 45:920–928

    CAS  PubMed  Google Scholar 

  • Havaux M (1996) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–151

    Google Scholar 

  • Hedden P, Kamiya Y (1997) Gibberellin biosynthesis: enzymes, genes and their regulation. Annu Rev Plant Physiol Plant Mol Biol 48:431–460

    CAS  PubMed  Google Scholar 

  • Hemmerlin A, Harwood JL, Bach TJ (2012) A raison d’être for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Prog Lipid Res 51:95–148

    CAS  PubMed  Google Scholar 

  • Hormaetxe K, Becerril JM, Hernández A, Esteban R, García-Plazaola JI (2008) Plasticity of photoprotective mechanisms of Buxus sempervirens L. leaves in response to extreme temperatures. Plant Biol 9:59–68

    Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    CAS  PubMed  Google Scholar 

  • Hsieh MH, Goodman HM (2005) The Arabidopsis IspH homolog is involved in the plastid non-mevalonate pathway of isoprenoid biosynthesis. Plant Physiol 138:641–653

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, Shi H, Hu Z, Liu A, Amombo E, Chen L, Fu J (2017) ABA is involved in regulation of cold stress response in Bermudagrass. Front Plant Sci 13(8):1613

    Google Scholar 

  • IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, p 1535

    Google Scholar 

  • Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland R (2009) Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol Plant 2(6):1154–1180

    CAS  PubMed  Google Scholar 

  • Jubany-Marí T, Munné-Bosch S, López-Carbonell M, Alegre L (2009) Hydrogen peroxide is involved in the acclimation of the Mediterranean shrub, Cistus albidus L., to summer drought. J Exp Bot 60(1):107–120

    PubMed  Google Scholar 

  • Kruk J, Szymańska R, Cela J, Munne-Bosch S (2014) Plastochromanol-8: fifty years of research. Phytochemistry 108:9–16

    CAS  PubMed  Google Scholar 

  • Lalk I, Dörffling K (1985) Hardening, abscisic acid, proline and freezing resistance in two winter wheat varieties. Physiol Plant 63:287–292

    CAS  Google Scholar 

  • Lawlor DW (2013) Genetic engineering to improve plant performance under drought: physiological evaluation of achievements, limitations, and possibilities. J Exp Bot 64:83–108

    CAS  PubMed  Google Scholar 

  • Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35(1):53–60

    CAS  PubMed  Google Scholar 

  • Li Y, Walton DC (1990) Violaxanthin is an abscisic acid precursor in water-stressed dark-grown beanleaves. Plant Physiol 92:551–559

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    CAS  Google Scholar 

  • Lichtenthaler HK, Rohmer M, Schwender J (1997) Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plants. Physiol Plant 101:643–652

    CAS  Google Scholar 

  • Liu WZ, Kong DD, Gu XX, Gao HB, Wang JZ, Xia M, Gao Q, Tian LL, Xu ZH, Bao F, Hu Y, Ye NS, Pei ZM, He YK (2013) Cytokinins can act as suppressors of nitric oxide in Arabidopsis. Proc Natl Acad Sci USA 110(4):1548–1553

    CAS  PubMed  Google Scholar 

  • Meier S, Tzfadia O, Vallabhaneni R, Gehring C, Wurtzel ET (2011) A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Syst Biol 5:77

    PubMed  PubMed Central  Google Scholar 

  • Melcher K, Xu Y, Ng LM, Zhou XE, Soon FF, Chinnusamy V, Suino-Powell KM, Kovach A, Tham FS, Cutler SR, Li J, Yong EL, Zhu JK, Xu HE (2010) Identification and mechanism of ABA receptor antagonism. Nat Struct Mol Biol 17(9):1102–1108

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mène-Saffrané L, Jones AD, DellaPenna D (2010) Plastochromanol-8 and tocopherols are essential lipid-soluble antioxidants during seed desiccation and quiescence in Arabidopsis. Proc Natl Acad Sci USA 12(41):17815–17820

    Google Scholar 

  • Morales M, Pintó-Marijuan M, Munné-Bosch S (2016) Seasonal, sex- and plant size-related effects on photoinhibition and photoprotection in the dioecious Mediterranean dwarf palm, Chamaerops humilis. Front Plant Sci 7:1116

    PubMed  PubMed Central  Google Scholar 

  • Müller M, Munné-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectometry. Plant Methods 7:37

    PubMed  PubMed Central  Google Scholar 

  • Munné-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748

    PubMed  Google Scholar 

  • Munne-Bosch S, Alegre L (2000a) Changes in carotenoids, tocopherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus officinalis plants. Planta 210:139–146

    Google Scholar 

  • Munne-Bosch S, Alegre L (2000b) The significance of β-carotene, α-tocopherol and the xanthophyll cycle in the droughted Melissa officinalis plants. Aust J Plant Physiol 27:139–146

    CAS  Google Scholar 

  • Munne-Bosch S, Schwarz K, Alegre L (1999) Enhanced formation of α-tocopherol and highly oxidized abietane diterpenes in water-stressed rosemary plants. Plant Physiol 121:1047–1052

    CAS  PubMed  PubMed Central  Google Scholar 

  • Munné-Bosch S, Weller EW, Alegre L, Müller M, Düchting P, Falk J (2007) α-Tocopherol may influence cellular signaling by modulating jasmonic acid levels in plants. Planta 225:681–691

    PubMed  Google Scholar 

  • Munné-Bosch S, Falara V, Pateraki I, Lopez-Carbonell M, Cela J, Kanellis AK (2009) Physiological and molecular responses of the isoprenoid biosynthetic pathway in a drought-resistant Mediterranean shrub, Cistus creticus exposed to water deficit. J Plant Physiol 166(2):136–145

    PubMed  Google Scholar 

  • Nováková M, Motyka V, Dobrev P, Malbeck J, Gaudinová A, Vanková R (2005) Diurnal variation of cytokinin, auxin and abscisic acid levels in tobacco leaves. J Exp Bot 56(421):2877–2883

    PubMed  Google Scholar 

  • Oliván A, Munné-Bosch S (2010) Diurnal patterns of α-tocopherol accumulation in Mediterranean plants. J Arid Environ 74:1572–1576

    Google Scholar 

  • Ozturk T, Ceber ZP, Tükes Kurnaz ML (2015) Projections of climate change in the Mediterranean Basin by using downscaled global climate model outputs. Int J Climatol 35(14):4276–4292

    Google Scholar 

  • Peñuelas J, Munné-Bosch S (2005) Isoprenoids: an evolutionary pool for photoprotection. Trends Plant Sci 10(4):166–169

    PubMed  Google Scholar 

  • Qin F, Kodaira KS, Maruyama K, Mizoi J, Tran LS, Fujita Y et al (2011) SPINDLY, a negative regulator of gibberellic acid signalling, is involved in the plant abiotic stress response. Plant Physiol 157:1900–1913

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104:19631–19636

    CAS  PubMed  Google Scholar 

  • Rivero RM, Shulaev V, Blumwald E (2009) Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol 150:1530–1540

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rivero RM, Gimeno J, van Deynze A, Walia H, Blumwald E (2010) Enhanced cytokinin synthesis in tobacco plants expressing P SARK :IPT prevents the degradation of photosynthetic protein complexes during drought. Plant Cell Physiol 51:1929–1941

    CAS  PubMed  Google Scholar 

  • Schaller GE, Street IH, Kieber JJ (2014) Cytokinin and the cell cycle. Curr Opin Plant Biol 21:7–15

    CAS  PubMed  Google Scholar 

  • Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10(3):296–302

    CAS  PubMed  Google Scholar 

  • Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48

    CAS  PubMed  Google Scholar 

  • Siles L, Müller M, Cela J, Hernández I, Alegre L, Munné-Bosch S (2017) Marked differences in seed dormancy in two populations of the Mediterranean shrub, Cistus albidus L. Plant Ecol Divers 10:231–240

    Google Scholar 

  • Turner NC (1981) Techniques and experimental approaches for the measurement of plant water status. Plant Soil 58:339–366

    Google Scholar 

  • Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    PubMed  Google Scholar 

  • Vranová E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Mol Plant 5(2):318–333

    PubMed  Google Scholar 

  • Vranová E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64:665–700

    PubMed  Google Scholar 

  • Weiss D, Ori N (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 144(3):1240–1246

    CAS  PubMed  PubMed Central  Google Scholar 

  • Werner C, Correia O, Beyschlag W (1999) Two different strategies of Mediterranean macchia plants to avoid photoinhibitory damage by excessive radiation levels during summer drought. Acta Oecol 20:15–23

    Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2009) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Google Scholar 

Download references

Acknowledgements

We are grateful to Serveis Científico-Tècnics of the University of Barcelona for their help in the vitamin E and phytohormone analyses as well as to Serveis de Camps Experimentals (Faculty of Biology) for their technical assistance. This research was supported by the Spanish Government and the Generalitat de Catalunya through the BFU2015-64001P/MINECO/FEDER and the ICREA Academia prize given to SMB.

Author information

Authors and Affiliations

  1. Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, University of Barcelona, Barcelona, Spain

    Marina Pérez-Llorca, Andrea Casadesús, Sergi Munné-Bosch & Maren Müller

  2. Biodiversity Research Institute, Faculty of Biology, University of Barcelona, Barcelona, Spain

    Marina Pérez-Llorca & Sergi Munné-Bosch

Authors
  1. Marina Pérez-Llorca
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Casadesús
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sergi Munné-Bosch
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maren Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maren Müller.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 1146 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pérez-Llorca, M., Casadesús, A., Munné-Bosch, S. et al. Contrasting patterns of hormonal and photoprotective isoprenoids in response to stress in Cistus albidus during a Mediterranean winter. Planta 250, 1409–1422 (2019). https://doi.org/10.1007/s00425-019-03234-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-019-03234-y

Keywords

Search

Navigation