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

  • Marina Pérez-Llorca
  • Andrea Casadesús
  • Sergi Munné-Bosch
  • Maren MüllerEmail author
Original Article

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.

Keywords

ABA Carotenoids Cold stress Drought Isoprenoids MEP-pathway Phytohormones Tocopherols 

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

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Supplementary material

425_2019_3234_MOESM1_ESM.pptx (1.1 mb)
Supplementary material 1 (PPTX 1146 kb)

References

  1. 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 311:91–94Google Scholar
  2. 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):e0119641PubMedCentralGoogle Scholar
  3. 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):1676–1683PubMedCentralGoogle Scholar
  4. 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):153–161Google Scholar
  5. 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):803–822Google Scholar
  6. 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 58:61–76Google Scholar
  7. Chaudhary N, Khurana P (2009) Vitamin E biosynthesis genes in rice: molecular characterization, expression profiling and comparative phylogenetic analysis. Plant Sci 177:479–491Google Scholar
  8. 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 164:1470–1483PubMedCentralGoogle Scholar
  9. 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 154:56–65Google Scholar
  10. Covington MF, Harmer SL (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol 5:222Google Scholar
  11. 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:R130PubMedCentralGoogle Scholar
  12. Daie J, Campbell WF (1981) Response of tomato plants to stressful temperatures: increase in abscisic acid concentrations. Plant Physiol 67:26–29PubMedCentralGoogle Scholar
  13. 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 57:779–795Google Scholar
  14. Demming-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24Google Scholar
  15. Demming-Adams B, Adams WW III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–27Google Scholar
  16. 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):933–938Google Scholar
  17. 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):22901–22909Google Scholar
  18. Falk J, Munné-Bosch S (2010) Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot 61(6):1549–1566Google Scholar
  19. 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 8:1051PubMedCentralGoogle Scholar
  20. Finkelstein R (2013) Abscisic acid synthesis and response. The Arabidopsis book. American Society of Plant Biologists, Rockville.  https://doi.org/10.1199/tab.0166 Google Scholar
  21. 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 132:362–369Google Scholar
  22. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155(1):93–100Google Scholar
  23. Grundy J, Stoker C, Carré IA (2015) Circadian regulation of abiotic stress tolerance in plants. Front Plant Sci 6:648PubMedCentralGoogle Scholar
  24. 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 45:920–928Google Scholar
  25. Havaux M (1996) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–151Google Scholar
  26. Hedden P, Kamiya Y (1997) Gibberellin biosynthesis: enzymes, genes and their regulation. Annu Rev Plant Physiol Plant Mol Biol 48:431–460Google Scholar
  27. 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 51:95–148Google Scholar
  28. 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 9:59–68Google Scholar
  29. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684Google Scholar
  30. Hsieh MH, Goodman HM (2005) The Arabidopsis IspH homolog is involved in the plastid non-mevalonate pathway of isoprenoid biosynthesis. Plant Physiol 138:641–653PubMedCentralGoogle Scholar
  31. 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):1613Google Scholar
  32. 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 1535Google Scholar
  33. 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):1154–1180Google Scholar
  34. 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):107–120Google Scholar
  35. Kruk J, Szymańska R, Cela J, Munne-Bosch S (2014) Plastochromanol-8: fifty years of research. Phytochemistry 108:9–16Google Scholar
  36. Lalk I, Dörffling K (1985) Hardening, abscisic acid, proline and freezing resistance in two winter wheat varieties. Physiol Plant 63:287–292Google Scholar
  37. Lawlor DW (2013) Genetic engineering to improve plant performance under drought: physiological evaluation of achievements, limitations, and possibilities. J Exp Bot 64:83–108Google Scholar
  38. Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35(1):53–60Google Scholar
  39. Li Y, Walton DC (1990) Violaxanthin is an abscisic acid precursor in water-stressed dark-grown beanleaves. Plant Physiol 92:551–559PubMedCentralGoogle Scholar
  40. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592Google Scholar
  41. Lichtenthaler HK, Rohmer M, Schwender J (1997) Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plants. Physiol Plant 101:643–652Google Scholar
  42. 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):1548–1553Google Scholar
  43. 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 5:77PubMedCentralGoogle Scholar
  44. 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):1102–1108PubMedCentralGoogle Scholar
  45. 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):17815–17820Google Scholar
  46. 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 7:1116PubMedCentralGoogle Scholar
  47. 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 7:37PubMedCentralGoogle Scholar
  48. Munné-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748Google Scholar
  49. 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 210:139–146Google Scholar
  50. 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 27:139–146Google Scholar
  51. 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 121:1047–1052PubMedCentralGoogle Scholar
  52. 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 225:681–691Google Scholar
  53. 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):136–145Google Scholar
  54. 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):2877–2883Google Scholar
  55. Oliván A, Munné-Bosch S (2010) Diurnal patterns of α-tocopherol accumulation in Mediterranean plants. J Arid Environ 74:1572–1576Google Scholar
  56. 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):4276–4292Google Scholar
  57. Peñuelas J, Munné-Bosch S (2005) Isoprenoids: an evolutionary pool for photoprotection. Trends Plant Sci 10(4):166–169Google Scholar
  58. 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 157:1900–1913PubMedCentralGoogle Scholar
  59. 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 104:19631–19636Google Scholar
  60. Rivero RM, Shulaev V, Blumwald E (2009) Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol 150:1530–1540PubMedCentralGoogle Scholar
  61. 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 51:1929–1941Google Scholar
  62. Schaller GE, Street IH, Kieber JJ (2014) Cytokinin and the cell cycle. Curr Opin Plant Biol 21:7–15Google Scholar
  63. Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10(3):296–302Google Scholar
  64. Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48Google Scholar
  65. 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 10:231–240Google Scholar
  66. Turner NC (1981) Techniques and experimental approaches for the measurement of plant water status. Plant Soil 58:339–366Google Scholar
  67. Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236Google Scholar
  68. Vranová E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Mol Plant 5(2):318–333Google Scholar
  69. Vranová E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64:665–700Google Scholar
  70. Weiss D, Ori N (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 144(3):1240–1246PubMedCentralGoogle Scholar
  71. 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 20:15–23Google Scholar
  72. Zuur AF, Ieno EN, Elphick CS (2009) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of BiologyUniversity of BarcelonaBarcelonaSpain
  2. 2.Biodiversity Research Institute, Faculty of BiologyUniversity of BarcelonaBarcelonaSpain

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