Far-red and Blue Light Synergistically Mitigate Intumescence Injury of Tomato Plants Grown Under Ultraviolet-deficit Light Environment

in HortScience

Intumescence injury is an abiotic-stress-induced physiological disorder associated with abnormal cell enlargement and cell division. The symptom includes blister- or callus-like growths on leaves, which occur on sensitive cultivars of tomato when they are grown under ultraviolet (UV)-deficit light environment, such as light-emitting diodes (LEDs). Previous studies suggest that intumescence can be reduced by increasing far-red (FR) or blue light. In the present study, effects of end-of-day FR (EOD-FR) light and high blue photon flux (PF) ratio during the photoperiod on intumescence injury were examined using ‘Beaufort’ interspecific tomato rootstock seedlings (Solanum lycopersicum × Solanum habrochaites), a cultivar highly susceptible to intumescence injury. Our study showed that EOD-FR light treatment moderately suppressed intumescence injury. Using EOD-FR light treatment, the percent number of leaves exhibiting intumescences was reduced from 62.0–70.7% to 39.4–43.1%. By combining high blue PF ratio (75%) during the photoperiod and EOD-FR light treatment, the percent number of leaves exhibiting intumescences was further suppressed to 5.0%. Furthermore, the combination of high blue PF ratio and EOD-FR light treatment inhibited undesirable stem elongation caused by EOD-FR light treatment. We found that high blue PF ratio during the photoperiod combined with a small dose of EOD-FR lighting (≈1 mmol·m−2·d−1 provided by 5.2 µmol·m−2·s−1 FR PF for 3.3 minutes) could inhibit the problematic intumescence injury of tomato plants grown under LEDs without negatively influencing growth or morphology.

Contributor Notes

This project was funded by USDA NIFA SCRI (award number 2010-51181-21369).

We thank CCS Inc., Orbital Technologies Inc., and Monsanto Co. (De Ruiter Seeds) for generously providing the LED systems and seeds used in our study.

Current affiliation: Department of Horticulture, North Carolina State University, Raleigh, NC.

Corresponding author. E-mail: ckubota@e-mail.arizona.edu.

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Article Figures

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    Intumescence injury on tomato seedlings grown under blue and red light-emitting diodes. (A) Blister-like tumor growths on a leaf. (B) Callus-like tumor growths on stems.

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    Effect of end-of-day far-red (EOD-FR) light dose on (A) percent number of leaves exhibiting intumescences (IMs) per plant (% leaves with IMs), (B) severity of IM injury of first true leaf, and (C) second true leaf [rating scale of 1 to 6: 1 = no IM injury, 2 = IMs covering less than 10% area, 3 = IMs covering 10% to 50% area, 4 = IMs covering 50% to 75% area, showing minor epinasty, 5 = IMs covering 75% to 100% area, showing severe epinasty, 6 = leaf abscission (most severe)] when ‘Beaufort’ tomato rootstock plants were grown under low blue photon flux (PF) (10B-90R%) or high blue PF (75B-25R%) in two experiments (see Table 1). A trend line using a Michaelis–Menten type model was applied in each response to EOD-FR dose under 10B-90R% LEDs (Expt. 2). Means are shown with standard errors (n = 12 or 24).

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    ‘Beaufort’ tomato plants grown under 10B-90R% or 75B-25R% light-emitting diodes without or with varied daily dose of end-of-day far-red (EOD-FR) light treatment (1–76 mmol·m−2·d−1) (16 d after seeding) (Expt. 2).

Article References

  • AhmadM.CashmoreA.R.1997The blue-light receptor cryptochrome 1 shows functional dependence on phytochrome A or phytochrome B in Arabidopsis thalianaPlant J.11421427

    • Search Google Scholar
    • Export Citation
  • BalgeR.J.StruckmeyerB.E.BeckG.E.1969Occurrence, severity and nature of oedema in Pelargonium hortorum AitJ. Amer. Soc. Hort. Sci.94181183

    • Search Google Scholar
    • Export Citation
  • BarreiroR.GuiametJ.J.BeltranoJ.MontaldiE.R.1992Regulation of the photosynthetic capacity of primary bean leaves by the red:far-red ratio and photosynthetic photon flux density of incident lightPhysiol. Plant.8597101

    • Search Google Scholar
    • Export Citation
  • BertramL.LercariB.2000Evidence against the involvement of phytochrome in UVB-induced inhibition of stem growth in green tomato plantsPhotosynth. Res.64107117

    • Search Google Scholar
    • Export Citation
  • BoardmanN.K.1977Comparative photosynthesis of sun and shade plantsAnnu. Rev. Plant Physiol.28355377

  • BoccalandroH.E.GiordanoC.V.PloschukE.L.PiccoliP.N.BottiniR.CasalJ.J.2012Phototropins but not cryptochromes mediate the blue light-specific promotion of stomatal conductance, while both enhance photosynthesis and transpiration under full sunlightPlant Physiol.15814751484

    • Search Google Scholar
    • Export Citation
  • BlomT.J.TsujitaM.J.RobertsG.L.1995Far-red at end of day and reduced irradiance affect plant height of Easter and Asiatic hybrid liliesHortScience3010091012

    • Search Google Scholar
    • Export Citation
  • CasalJ.J.SánchezR.A.BottoJ.F.1998Modes of action of phytochromesJ. Expt. Bot.49127138

  • ChiaP.-L.KubotaC.2010End-of-day far-red light quality and dose requirements for tomato rootstock hypocotyl elongationHortScience4515011506

    • Search Google Scholar
    • Export Citation
  • ChoryJ.WuD.2001Weaving the complex web of signal transductionPlant Physiol.1257780

  • CosgroveD.1981Rapid suppression of growth by blue light: Occurrence, time course, and general characteristicsPlant Physiol.67584590

  • CraverJ.K.2014The effects of UVB radiation on intumescence development and the characterization of lesions from physiological disorders on ornamental sweet potato (Ipomoea batatas) tomato (Solanum lycopersicum) and interspecific geranium (Pelargonium spp.). Kansas State Univ. Manhattan MS Thesis

  • CraverJ.K.MillerC.T.WilliaK.A.BoyleD.L.2014Characterization and comparison of lesions on ornamental sweetpotato ‘Blackie’, tomato ‘Maxifort’, interspecific geranium ‘Caliente Coral’, and bat-faced cuphea ‘Tiny Mice’J. Amer. Soc. Hort. Sci.139603615

    • Search Google Scholar
    • Export Citation
  • DaleJ.E.MilthorpeF.L.1983General features of the production and growth of leaves p. 151–269. In: J.E. Dale and F.L. Milthorpe (eds.). The growth and functioning of leaves. Cambridge Univ. Press Cambridge MA

  • DecoteauD.R.KasperbauerM.J.DanielsD.D.HuntP.G.1988Plastic mulch color effects on reflected light and tomato plant growthSci. Hort.34169175

    • Search Google Scholar
    • Export Citation
  • Demotes-MainardS.PéronT.CorotA.BerthelootJ.GourrierecJ.L.Pelleschi-TravierS.CrespelL.MorelP.Huché-ThélierL.BoumazaR.VianA.GuérinV.LeducN.SakrS.2016Plant responses to red and far-red lights, applications in horticultureEnviron. Expt. Bot.121421

    • Search Google Scholar
    • Export Citation
  • DoiM.ShigenagaA.EmiT.KinoshitaT.ShimazakiK.2004A transgene encoding a blue-light receptor, phot1, restores blue-light responses in the Arabidopsis phot1 phot2 double mutantJ. Expt. Bot.55517523

    • Search Google Scholar
    • Export Citation
  • DougherT.A.O.BugbeeB.2004Long-term blue light effects on the histology of lettuce and soybean leaves and stemsJ. Amer. Soc. Hort. Sci.129467472

    • Search Google Scholar
    • Export Citation
  • DouglasE.G.1907The formation of intumescences on potato plantsBot. Gaz.43233250

  • EisaH.M.DobrenzA.K.1971Morphological and anatomical aspects of oedema in eggplants (Solanum melongena L.)J. Amer. Soc. Hort. Sci.96766769

    • Search Google Scholar
    • Export Citation
  • FankhauserC.CasalJ.J.2004Phenotypic characterization of a photomorphogenic mutantPlant J.39747760

  • FoltaK.M.SpaldingE.P.2001Opposing roles of phytochrome A and phytochrome B in early cryptochrome-mediated growth inhibitionPlant J.28333340

    • Search Google Scholar
    • Export Citation
  • FranklinK.A.2008Shade avoidanceNew Phytol.179930944

  • HansonH.C.1917Leaf-structure as related to environmentAmer. J. Bot.4533560

  • HectorsK.JacquesE.PrinsenE.GuisezY.VerbelenJ.-P.JansenM.A.K.VissenbergK.2010UV radiation reduces epidermal cell expansion in leaves of Arabidopsis thalianaJ. Expt. Bot.6143394349

    • Search Google Scholar
    • Export Citation
  • HendricksS.B.BorthwickH.A.1967The function of phytochrome in regulation of plant growthProc. Natl. Acad. Sci. USA5821252130

  • HendricksS.B.ButlerW.L.SiegelmanH.W.1962A reversible photoreaction regulating plant growthJ. Phys. Chem.6625502555

  • HernándezR.KubotaC.2016Physiological responses of cucumber seedlings under different blue and red photon flux ratios using LEDsEnviron. Expt. Bot.1216674

    • Search Google Scholar
    • Export Citation
  • HogewoningS.W.TrouwborstG.MaljaarsH.PoorterH.van IeperenW.HarbinsonJ.2010Blue light dose-responses of leaf photosynthesis, morphology, and chemical composition of Cucumis sativus grown under different combinations of red and blue lightJ. Expt. Bot.6131073117

    • Search Google Scholar
    • Export Citation
  • JaedickeK.LichtenthälerA.L.MeybergR.ZeidlerM.HughesJ.2012A phytochrome–phototropin light signaling complex at the plasma membraneProc. Natl. Acad. Sci. USA1091223112236

    • Search Google Scholar
    • Export Citation
  • JansenM.A.K.CoffeyA.M.PrinsenE.2012UV-B induced morphogenesis-Four players or a quartet?Plant Signal. Behav.711851187

  • KasperbauerM.J.PeasleeD.E.1973Morphology and photosynthetic efficiency of tobacco leaves that received end-of-day red and far red light during developmentPlant Physiol.52440442

    • Search Google Scholar
    • Export Citation
  • KigelJ.CosgroveD.J.1991Photoinhibition of stem elongation by blue and red lightPlant Physiol.9510491056

  • LakeJ.A.FieldK.J.DaveyM.P.BeerlingD.J.LomaxB.H.2009Metabolomic and physiological responses reveal multi-phasic acclimation of Arabidopsis thaliana to chronic UV radiationPlant Cell Environ.3213771389

    • Search Google Scholar
    • Export Citation
  • LangS.P.E. StruckmeyerB.TibbittsT.W.1983Morphology and anatomy of intumescence development on tomato plantsJ. Amer. Soc. Hort. Sci.108266271

    • Search Google Scholar
    • Export Citation
  • LangS.P.TibbittsT.W.1983Factors controlling intumescence development on tomato plantsJ. Amer. Soc. Hort. Sci.1089398

  • La RueC.D.1933Intumescences on poplar leaves. I. Structure and developmentAmer. J. Bot.20117

  • LiuX.CohenJ.D.GardnerG.2011Low-fluence red light increases the transport and biosynthesis of auxinPlant Physiol.157891904

  • MancinelliA.L.1994The physiology of phytochrome action p. 235–269. In: R.E. Kendrick and G.H.M. Kronenberg (eds.). Photomorphogenesis in plants. 2nd ed. Kluwer Academic Publishers Dordrecht The Netherlands

  • MancinelliA.L.BorthwickH.A.HendricksS.B.1966Phytochrome action in tomato seed germinationBot. Gaz.12715

  • MassaG.D.KimH.-H.WheelerR.M.MitchellC.A.2008Plant productivity in response to LED lightingHortScience4719511956

  • MetwallyA.W.BeckG.E.StruckmeyerB.E.1970The role of water and cultural practices on oedema of Pelargonium hortorum AitJ. Amer. Soc. Hort. Sci.95808813

    • Search Google Scholar
    • Export Citation
  • MorrowR.C.1987Environmental factors regulating intumescence development (oedema) in tomatoes. Univ. Wisconsin Madison PhD Diss

  • MorrowR.C.TibbittsT.W.1988Evidence for involvement of phytochrome in tumor development on plantsPlant Physiol.8811101114

  • NanyaK.IshigamiY.HikosakaS.GotoE.2012Effects of blue and red light on stem elongation and flowering of tomato seedlingsActa Hort.956261266

    • Search Google Scholar
    • Export Citation
  • NeffM.M.ChoryJ.1998Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis developmentPlant Physiol.1182735

    • Search Google Scholar
    • Export Citation
  • O’CarriganA.BablaM.WangF.LiuX.MakM.ThomasR.BellottiB.ChenZ.-H.2014Analysis of gas exchange, stomatal behaviour and micronutrients uncovers dynamic response and adaptation of tomato plants to monochromatic light treatmentsPlant Physiol. Biochem.82105115

    • Search Google Scholar
    • Export Citation
  • OhgishiM.SajiK.OkadaK.SakaiT.2004Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in ArabidopsisProc. Natl. Acad. Sci. USA10122232228

    • Search Google Scholar
    • Export Citation
  • PeerW.A.MurphyA.S.2007Flavonoids and auxin transport: Modulators or regulators?Trends Plant Sci.12556563

  • PetitteJ.M.OrmrodD.P.1986Factors affecting intumescence development on potato leavesHortScience21493495

  • PinkardE.GillW.MohammedC.2006Physiology and anatomy of lenticel-like structures on leaves of Eucalyptus nitens and Eucalyptus globulus seedlingsTree Physiol.26989999

    • Search Google Scholar
    • Export Citation
  • RangarajanA.TibbittsT.W.1994Exposure with far-red radiation for control of oedema injury on ‘Yale’ ivy geraniumHortScience293840

  • RickC.M.1973Potential genetic resources in tomato species: Clues from observations in native habitats p. 255–269. In: A.M. Srb (ed.). Genes enzymes and populations. Plenum New York NY

  • RudN.A.2009Environmental factors influencing the physiological disorders of edema on ivy geranium (Pelargonium peltatum) and intumescences on tomato (Solanum lycopersicum). Kansas State Univ. Manhattan MS Thesis

  • SagerJ.C.SmithW.O.EdwardsJ.L.CyrK.L.1988Photosynthetic efficiency and phytochrome photoequilibria determination using spectral dataTrans. Amer. Soc. Agr. Eng.3118821889

    • Search Google Scholar
    • Export Citation
  • SavvidesA.FanourakisD.van IeperenW.2012Co-ordination of hydraulic and stomatal conductances across light qualities in cucumber leavesJ. Expt. Bot.6311351143

    • Search Google Scholar
    • Export Citation
  • ShinkleJ.R.JonesR.L.1988Inhibition of stem elongation in Cucumis seedlings by blue light requires calciumPlant Physiol.86960966

  • SiegelmanH.W.TurnerB.C.HendricksS.B.1966The chromophore of phytochromePlant Physiol.4112891292

  • SimsD.A.PearcyR.W.1992Response of leaf anatomy and photosynthetic capacity in Alocasia macrorrhiza (Araceae) to a transfer from low to high lightAmer. J. Bot.79449455

    • Search Google Scholar
    • Export Citation
  • SmithH.1994Sensing the light environment: The functions of the phytochrome family p. 377–416. In: R.E. Kendrick and G.M.H. Kronenberg (eds.). Photomorphogenesis in plants. 2nd ed. Kluwer Academic Publishers Dordrecht The Netherlands

  • Van VolkenburghE.ClelandR.E.WatanabeM.1990Light-stimulated cell expansion in bean (Phaseolus vulgaris L.) leaves. II. Quantity and quality of light requiredPlanta1827780

    • Search Google Scholar
    • Export Citation
  • WarnockS.J.1991Natural habitats of Lycopersicon speciesHortScience26466471

  • WarringtonI.J.1980Humidity-induced gall formation on Eucalyptus speciesAust. For. Res.10185189

  • WetzsteinH.Y.FrettJ.J.1984Light and scanning electron microscopy of intumescences on tissue-cultured, sweetpotato leavesJ. Amer. Soc. Hort. Sci.109280283

    • Search Google Scholar
    • Export Citation
  • WhitelamG.C.JohnsonE.PengJ.CarolP.AndersonM.L.CowlJ.S.HarberdN.P.1993Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white lightPlant Cell5757768

    • Search Google Scholar
    • Export Citation
  • WollaegerH.M.RunkleE.S.2014Growth of impatiens, petunia, salvia, and tomato seedlings under blue, green, and red light-emitting diodesHortScience49734740

    • Search Google Scholar
    • Export Citation
  • ZenkM.H.M.MüllerG.1963In vivo destruction of exogenously applied indolyl-3-acetic acid as influenced by naturally occurring phenolic acidsNature200761763

    • Search Google Scholar
    • Export Citation
  • Zuk-GolaszewskaK.UpadhyayaM.K.GolaszewskiJ.2003The effect of UV-B radiation on plant growth and developmentPlant Soil Environ.49135140

    • Search Google Scholar
    • Export Citation

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