Skip to main content
SpringerLink
Log in

The hydroperoxide lyase branch of the oxylipin pathway protects against photoinhibition of photosynthesis

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

Abstract

Main conclusion

This study describes a new role for hydroperoxide lyase branch of oxylipin biosynthesis pathway in protecting photosynthetic apparatus under high light conditions.

Lipid-derived signaling molecules, oxylipins, produced by a multi-branch pathway are central in regulation of a wide range of functions. The two most known branches, allene oxide synthase (AOS) and 13-hydroperoxide lyase (HPL) pathways, are best recognized as producers of defense compounds against biotic challenges. In the present work, we examine the role of these two oxylipin branches in plant tolerance to the abiotic stress, namely excessive light. Towards this goal, we have analyzed variable chlorophyll fluorescence parameters of intact leaves of Arabidopsis thaliana genotypes with altered oxylipin profile, followed by examining the impact of exogenous application of selected oxylipins on functional activity of photosynthetic apparatus in intact leaves and isolated thylakoid membranes. Our findings unequivocally bridge the function of oxylipins to photosynthetic processes. Specifically, HPL overexpressing lines display enhanced adaptability in response to high light treatment as evidenced by lower rate constant of photosystem 2 (PS2) photoinhibition and higher rate constant of PS2 recovery after photoinhibition. In addition, exogenous application of linolenic acid, 13-hydroperoxy linolenic acid, 12-oxophytodienoic acid, and methyl jasmonate individually, suppresses photochemical activity of PS2 in intact plants and isolated thylakoid membranes, while application of HPL-branch metabolites—does not. Collectively these data implicate function of HPL branch of oxylipin biosynthesis pathway in guarding PS2 under high light conditions, potentially exerted through tight regulation of free linolenic acid and 13-hydroperoxy linolenic acid levels, as well as competition with production of metabolites by AOS-branch of the oxylipin pathway.

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

Similar content being viewed by others

Abbreviations

PS2:

Photosystem 2

AOS:

Allene oxide synthase

HPL:

Hydroperoxide lyase

LA:

Linolenic acid

13-HPOT:

13-Hydroperoxy-(9Z,11E,15Z)-octadecatrienoic acid

TA:

Traumatic acid

References

  • Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2):163–190. doi:10.1007/s11099-013-0021-6

    Article  CAS  Google Scholar 

  • Attaran E, Major IT, Cruz JA, Rosa BA, Koo AJ, Chen J, Kramer DM, He SY, Howe GA (2014) Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling. Plant Physiol 165(3):1302–1314. doi:10.1104/pp.114.239004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker NR, Oxborough K (2004) Chlorophyll fluorescence as a probe of photosynthetic productivity. In Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Netherlands. doi:10.1007/978-1-4020-3218-9_3

    Google Scholar 

  • Berger S, Benediktyova Z, Matous K, Bonfig K, Mueller MJ, Nedbal L, Roitsch T (2007) Visualization of dynamics of plant–pathogen interaction by novel combination of chlorophyll fluorescence imaging and statistical analysis: differential effects of virulent and avirulent strains of P. syringae and of oxylipins on A. thaliana. J Exp Bot 58(4):797–806. doi:10.1093/jxb/erl208

    Article  CAS  PubMed  Google Scholar 

  • Berry EA, Huang LS, DeRose VJ (1991) Ubiquinol-cytochrome c oxidoreductase of higher plants. Isolation and characterization of the bc1 complex from potato tuber mitochondria. J Biol Chem 266(14):9064–9077

    CAS  PubMed  Google Scholar 

  • Bisignano G, Lagana MG, Trombetta D, Arena S, Nostro A, Uccella N, Mazzanti G, Saija A (2001) In vitro antibacterial activity of some aliphatic aldehydes from Olea europaea L. FEMS Microbiol Lett 198(1):9–13

    Article  CAS  PubMed  Google Scholar 

  • Blee E, Joyard J (1996) Envelope membranes from spinach chloroplasts are a site of metabolism of fatty acid hydroperoxides. Plant Physiol 110(2):445–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brilli F, Ruuskanen TM, Schnitzhofer R, Muller M, Breitenlechner M, Bittner V, Wohlfahrt G, Loreto F, Hansel A (2011) Detection of plant volatiles after leaf wounding and darkening by proton transfer reaction “time-of-flight” mass spectrometry (PTR-TOF). PLoS One 6(5):e20419. doi:10.1371/journal.pone.0020419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bunker TW, Koetje DS, Stephenson LC, Creelman RA, Mullet JE, Grimes HD (1995) Sink limitation induces the expression of multiple soybean vegetative lipoxygenase mRNAs while the endogenous jasmonic acid level remains low. Plant Cell 7(8):1319–1331. doi:10.1105/tpc.7.8.1319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell DR, Wu CA, Travers SE (2010) Photosynthetic and growth responses of reciprocal hybrids to variation in water and nitrogen availability. Am J Bot 97(6):925–933. doi:10.3732/ajb.0900387

    Article  PubMed  Google Scholar 

  • Chehab EW, Raman G, Walley JW, Perea JV, Banu G, Theg S, Dehesh K (2006) Rice HYDROPEROXIDE LYASES with unique expression patterns generate distinct aldehyde signatures in Arabidopsis. Plant Physiol 141(1):121–134. doi:10.1104/pp.106.078592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chehab EW, Kaspi R, Savchenko T, Rowe H, Negre-Zakharov F, Kliebenstein D, Dehesh K (2008) Distinct roles of jasmonates and aldehydes in plant-defense responses. PLoS One 3(4):e1904. doi:10.1371/journal.pone.0001904

    Article  PubMed  PubMed Central  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381. doi:10.1146/annurev.arplant.48.1.355

    Article  CAS  PubMed  Google Scholar 

  • Creelman RA, Tierney ML, Mullet JE (1992) Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proc Natl Acad Sci USA 89(11):4938–4941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan H, Huang MY, Palacio K, Schuler MA (2005) Variations in CYP74B2 (hydroperoxide lyase) gene expression differentially affect hexenal signaling in the Columbia and Landsberg erecta ecotypes of Arabidopsis. Plant Physiol 139(3):1529–1544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engelberth J, Seidl-Adams I, Schultz JC, Tumlinson JH (2007) Insect elicitors and exposure to green leafy volatiles differentially upregulate major octadecanoids and transcripts of 12-oxo phytodienoic acid reductases in Zea mays. Mol Plant Microbe Interact 20(6):707–716. doi:10.1094/MPMI-20-6-0707

    Article  CAS  PubMed  Google Scholar 

  • Farag MA, Pare PW (2002) C-6-green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61(5):545–554

    Article  CAS  PubMed  Google Scholar 

  • Farmaki T, Sanmartin M, Jimenez P, Paneque M, Sanz C, Vancanneyt G, Leon J, Sanchez-Serrano JJ (2007) Differential distribution of the lipoxygenase pathway enzymes within potato chloroplasts. J Exp Bot 58(3):555–568. doi:10.1093/jxb/erl230

    Article  CAS  PubMed  Google Scholar 

  • Feinbaum RL, Storz G, Ausubel FM (1991) High intensity and blue light regulated expression of chimeric chalcone synthase genes in transgenic Arabidopsis thaliana plants. Mol Gen Genet 226(3):449–456

    Article  CAS  PubMed  Google Scholar 

  • Franceschi VR, Grimes HD (1991) Induction of soybean vegetative storage proteins and anthocyanins by low-level atmospheric methyl jasmonate. Proc Natl Acad Sci USA 88(15):6745–6749. doi:10.1073/pnas.88.15.6745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Froehlich JE, Itoh A, Howe GA (2001) Tomato allene oxide synthase and fatty acid hydroperoxide lyase, two cytochrome P450s involved in oxylipin metabolism, are targeted to different membranes of chloroplast envelope. Plant Physiol 125(1):306–317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genty B, Harbinson J, Cailly A, Rizza F (1996) Fate of excitation at PS II in leaves: the non-photochemical side. University of Sheffield, Department of Molecular Biology and Biotechnolog, Third BBSRC Robert Hill Symposium on Photosynthesis

  • Golbeck JH, Martin IF, Fowler CF (1980) Mechanism of linolenic acid-induced inhibition of photosynthetic electron transport. Plant Physiol 65(4):707–713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graus M, Schnitzler JP, Hansel A, Cojocariu C, Rennenberg H, Wisthaler A, Kreuzwieser J (2004) Transient release of oxygenated volatile organic compounds during light–dark transitions in grey poplar leaves. Plant Physiol 135(4):1967–1975. doi:10.1104/pp.104.043240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamberg M (1988) Biosynthesis of 12-oxo-10,15(Z)-phytodienoic acid: identification of an allene oxide cyclase. Biochem Biophys Res Commun 156(1):543–550

    Article  CAS  PubMed  Google Scholar 

  • Heiden AC, Kobel K, Langebartels C, Schuh-Thomas G, Wildt J (2003) Emissions of oxygenated volatile organic compounds from plants—part I: emissions from lipoxygenase activity. J Atmos Chem 45(2):143–172. doi:10.1023/A:1024069605420

    Article  CAS  Google Scholar 

  • Heraud P, Beardall J (2000) Changes in chlorophyll fluorescence during exposure of Dunaliella tertiolecta to UV radiation indicate a dynamic interaction between damage and repair processes. Photosynth Res 63(2):123–134. doi:10.1023/A:1006319802047

    Article  CAS  PubMed  Google Scholar 

  • Holzinger R, Sandoval-Soto L, Rottenberger S, Crutzen PJ, Kesselmeier J (2000) Emissions of volatile organic compounds from Quercus ilex L. measured by proton transfer reaction mass spectrometry under different environmental conditions. J Geophys Res-Atmos 105(D16):20573–20579. doi:10.1029/2000jd900296

    Article  CAS  Google Scholar 

  • Ivanov AB, Iarin A, Grechkin AN, Tarchevski IA (2001) Effect of 12-hydroxy-9(Z)-dodecenoic acid on growth and cell division in pea roots. Tsitologiia 43(2):166–171

    CAS  PubMed  Google Scholar 

  • Kallenbach M, Gilardoni PA, Allmann S, Baldwin IT, Bonaventure G (2011) C12 derivatives of the hydroperoxide lyase pathway are produced by product recycling through lipoxygenase-2 in Nicotiana attenuata leaves. N Phytol 191(4):1054–1068. doi:10.1111/j.1469-8137.2011.03767.x

    Article  CAS  Google Scholar 

  • Korneev DJ (2002) Information potentialities of the chlorophyll fluorescence induction method. Alterpress, Kiev

    Google Scholar 

  • Labuz J, Sztatelman O, Banas AK, Gabrys H (2012) The expression of phototropins in Arabidopsis leaves: developmental and light regulation. J Exp Bot 63(4):1763–1771. doi:10.1093/jxb/ers061

    Article  CAS  PubMed  Google Scholar 

  • Li C, Schilmiller AL, Liu G, Lee GI, Jayanty S, Sageman C, Vrebalov J, Giovannoni JJ, Yagi K, Kobayashi Y, Howe GA (2005) Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17(3):971–986. doi:10.1105/tpc.104.029108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lichtenthaller HK, Wellburn AR (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382

    Article  Google Scholar 

  • Loreto F, Barta C, Brilli F, Nogues I (2006) On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant Cell Environ 29(9):1820–1828. doi:10.1111/j.1365-3040.2006.01561.x

    Article  CAS  PubMed  Google Scholar 

  • Matsui K, Sugimoto K, Mano J, Ozawa R, Takabayashi J (2012) Differential metabolisms of green leaf volatiles in injured and intact parts of a wounded leaf meet distinct ecophysiological requirements. PLoS One 7(4):e36433. doi:10.1371/journal.pone.0036433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McConn M, Browse J (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8(3):403–416. doi:10.1105/tpc.8.3.403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylides C, Haring MA, Schuurink RC (2008) The Arabidopsis her1 mutant implicates GABA in E-2-hexenal responsiveness. Plant J 53(2):197–213. doi:10.1111/j.1365-313X.2007.03323.x

    Article  CAS  PubMed  Google Scholar 

  • Mita G, Quarta A, Fasano P, De Paolis A, Di Sansebastiano GP, Perrotta C, Iannacone R, Belfield E, Hughes R, Tsesmetzis N, Casey R, Santino A (2005) Molecular cloning and characterization of an almond 9-hydroperoxide lyase, a new CYP74 targeted to lipid bodies. J Exp Bot 56(419):2321–2333. doi:10.1093/jxb/eri225

    Article  CAS  PubMed  Google Scholar 

  • Miyake C, Asada K (1994) Ferredoxin-dependent photoreduction of the monodehydroascorbate radical in spinach thylakoids. Plant Cell Physiol 35(4):539–549

    Article  CAS  Google Scholar 

  • Montillet JL, Cacas JL, Garnier L, Montane MH, Douki T, Bessoule JJ, Polkowska-Kowalczyk L, Maciejewska U, Agnel JP, Vial A, Triantaphylides C (2004) The upstream oxylipin profile of Arabidopsis thaliana: a tool to scan for oxidative stresses. Plant J 40(3):439–451. doi:10.1111/j.1365-313X.2004.02223.x

    Article  CAS  PubMed  Google Scholar 

  • Nabity PD, Zavala JA, DeLucia EH (2013) Herbivore induction of jasmonic acid and chemical defences reduce photosynthesis in Nicotiana attenuata. J Exp Bot 64(2):685–694. doi:10.1093/jxb/ers364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nemchenko A, Kunze S, Feussner I, Kolomiets M (2006) Duplicate maize 13-lipoxygenase genes are differentially regulated by circadian rhythm, cold stress, wounding, pathogen infection, and hormonal treatments. J Exp Bot 57(14):3767–3779. doi:10.1093/jxb/erl137

    Article  CAS  PubMed  Google Scholar 

  • Nilsson AK, Fahlberg P, Johansson ON, Hamberg M, Andersson MX, Ellerstrom M (2016) The activity of HYDROPEROXIDE LYASE 1 regulates accumulation of galactolipids containing 12-oxo-phytodienoic acid in Arabidopsis. J Exp Bot 67(17):5133–5144. doi:10.1093/jxb/erw278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noordermeer MA, Van Dijken AJ, Smeekens SC, Veldink GA, Vliegenthart JF (2000) Characterization of three cloned and expressed 13-hydroperoxide lyase isoenzymes from alfalfa with unusual N-terminal sequences and different enzyme kinetics. Eur J Biochem 267(9):2473–2482

    Article  CAS  PubMed  Google Scholar 

  • Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31(1):1–12

    Article  PubMed  Google Scholar 

  • Perez AG, Sanz C, Olias R, Olias JM (1999) Lipoxygenase and hydroperoxide lyase activities in ripening strawberry fruits. J Agric Food Chem 47(1):249–253

    Article  CAS  PubMed  Google Scholar 

  • Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Ann Rev Plant Physiol 35:15–44

    Article  CAS  Google Scholar 

  • Savchenko T, Dehesh K (2013) Insect herbivores selectively mute GLV production in plants. Plant Signal Behav 8(5):e24136. doi:10.4161/psb.24136

    Article  PubMed  PubMed Central  Google Scholar 

  • Savchenko T, Dehesh K (2014) Drought stress modulates oxylipin signature by eliciting 12-OPDA as a potent regulator of stomatal aperture. Plant Signal Behav 9(4):e28304. doi:10.4161/psb.28304

    Article  PubMed Central  Google Scholar 

  • Savchenko T, Pearse IS, Ignatia L, Karban R, Dehesh K (2013) Insect herbivores selectively suppress the HPL branch of the oxylipin pathway in host plants. Plant J 73(4):653–662. doi:10.1111/tpj.12064

    Article  CAS  PubMed  Google Scholar 

  • Savchenko T, Kolla VA, Wang CQ, Nasafi Z, Hicks DR, Phadungchob B, Chehab WE, Brandizzi F, Froehlich J, Dehesh K (2014a) Functional convergence of oxylipin and abscisic acid pathways controls stomatal closure in response to drought. Plant Physiol 164(3):1151–1160. doi:10.1104/pp.113.234310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savchenko TV, Zastrijnaja OM, Klimov VV (2014b) Oxylipins and plant abiotic stress resistance. Biochem Biokhimiia 79(4):362–375. doi:10.1134/S0006297914040051

    Article  CAS  Google Scholar 

  • Scala A, Mirabella R, Mugo C, Matsui K, Haring MA, Schuurink RC (2013) E-2-hexenal promotes susceptibility to Pseudomonas syringae by activating jasmonic acid pathways in Arabidopsis. Front Plant Sci 4:74. doi:10.3389/fpls.2013.00074

    Article  PubMed  PubMed Central  Google Scholar 

  • Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97(19):10625–10630. doi:10.1073/pnas.190264497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takamura H, Gardner HW (1996) Oxygenation of (3Z)-alkenal to (2E)-4-hydroxy-2-alkenal in soybean seed (Glycine max L.). Biochim Biophys Acta 1303(2):83–91

    Article  PubMed  Google Scholar 

  • Taki N, Sasaki-Sekimoto Y, Obayashi T, Kikuta A, Kobayashi K, Ainai T, Yagi K, Sakurai N, Suzuki H, Masuda T, Takamiya K, Shibata D, Kobayashi Y, Ohta H (2005) 12-oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol 139(3):1268–1283. doi:10.1104/pp.105.067058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong X, Qi J, Zhu X, Mao B, Zeng L, Wang B, Li Q, Zhou G, Xu X, Lou Y, He Z (2012) The rice hydroperoxide lyase OsHPL3 functions in defense responses by modulating the oxylipin pathway. Plant J 71(5):763–775. doi:10.1111/j.1365-313X.2012.05027.x

    Article  CAS  PubMed  Google Scholar 

  • Ueda J, Kato J, Yamane H, Takahashi N (1981) Inhibitory effect of methyl jasmonate and its related-compounds on kinetin-induced retardation of oat leaf senescence. Physiol Plant 52(2):305–309. doi:10.1111/j.1399-3054.1981.tb08511.x

    Article  CAS  Google Scholar 

  • Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castanera P, Sanchez-Serrano JJ (2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc Natl Acad Sci USA 98(14):8139–8144. doi:10.1073/pnas.141079498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vass I (2012) Molecular mechanisms of photodamage in the photosystem II complex. Bba-Bioenerg 1817(1):209–217. doi:10.1016/j.bbabio.2011.04.014

    Article  CAS  Google Scholar 

  • Warden JT, Csatorday K (1987) On the mechanism of linolenic acid inhibition in photosystem II. Biochim Biophys Acta 890(2):215–223

    Article  CAS  PubMed  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111(6):1021–1058. doi:10.1093/aob/mct067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weidhase RA, Kramell HM, Lehmann J, Liebisch HW, Lerbs W, Parthier B (1987) Methyljasmonate-induced changes in the polypeptide pattern of senescing barley leaf segments. Plant Sci 51(2–3):177–186. doi:10.1016/0168-9452(87)90191-9

    Article  CAS  Google Scholar 

  • Wierstra I, Kloppstech K (2000) Differential effects of methyl jasmonate on the expression of the early light-inducible proteins and other light-regulated genes in barley. Plant Physiol 124(2):833–844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan A, Pan JB, An LZ, Gan YB, Feng HY (2012) The responses of trichome mutants to enhanced ultraviolet-B radiation in Arabidopsis thaliana. J Photochem Photobiol B 113:29–35. doi:10.1016/j.jphotobiol.2012.04.011

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman DC, Coudron CA (1979) Identification of traumatin, a wound hormone, as 12-oxo-trans-10-dodecenoic acid. Plant Physiol 63(3):536–541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Grant 16-14-10155 from the Russian Science Foundation. The results presented in Figs. 1a, 4 and 5 were obtained with support from the Grant 15-04-01551 from the Russian Foundation for Basic Research.

Author information

Authors and Affiliations

  1. Institute of Basic Biological Problems, RAS, Institutskaya st., 2, Pushchino, 142290, Moscow Region, Russia

    Tatyana Savchenko, Denis Yanykin, Andrew Khorobrykh, Vasily Terentyev & Vyacheslav Klimov

  2. All-Russian Research Institute of Phytopathology, Institute st., 5, Odintsovo District, B. Vyazyomy, 143050, Moscow Region, Russia

    Tatyana Savchenko & Denis Yanykin

  3. Institute for Integrative Genome Biology, and Department of Botany and Plant Sciences, University of California, Riverside, CA, 92521, USA

    Katayoon Dehesh

Authors
  1. Tatyana Savchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Denis Yanykin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrew Khorobrykh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vasily Terentyev
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vyacheslav Klimov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Katayoon Dehesh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tatyana Savchenko.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Savchenko, T., Yanykin, D., Khorobrykh, A. et al. The hydroperoxide lyase branch of the oxylipin pathway protects against photoinhibition of photosynthesis. Planta 245, 1179–1192 (2017). https://doi.org/10.1007/s00425-017-2674-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2674-z

Keywords

Search

Navigation