Elevated air humidity increases UV mediated leaf and DNA damage in pea (Pisum sativum) due to reduced flavonoid content and antioxidant power.
Journal
Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology
ISSN: 1474-9092
Titre abrégé: Photochem Photobiol Sci
Pays: England
ID NLM: 101124451
Informations de publication
Date de publication:
13 Feb 2019
13 Feb 2019
Historique:
pubmed:
28
11
2018
medline:
15
3
2019
entrez:
28
11
2018
Statut:
ppublish
Résumé
Growth in high relative air humidity (RH, >85%) affects plant morphology and causes diminished response to stomatal closing signals. Many greenhouses are prone to high RH conditions, which may negatively affect production and post-harvest quality. UV radiation induces stomatal closure in several species, and facilitates disease control. We hypothesised that UV exposure may trigger stomatal closure in pea plants (Pisum sativum) grown in high RH, thereby restoring stomatal function. The effects of UV exposure were tested on plants grown in moderate (60%) or high (90%) RH. UV exposure occurred at night, according to a disease control protocol. Lower stomatal conductance rates were found in UV-exposed plants, though UV exposure did not improve the rate of response to closing stimuli or desiccation tolerance. UV-exposed plants showed leaf curling, chlorosis, necrosis, and DNA damage measured by the presence of cyclobutane pyrimidine dimers (CPD), all of which were significantly greater in high RH plants. These plants also had lower total flavonoid content than moderate RH plants, and UV-exposed plants had less than controls. Plants exposed to UV had a higher content of cuticular layer uronic compounds than control plants. However, high RH plants had a higher relative amount of cuticular waxes, but decreased proteins and uronic compounds. Plants grown in high RH had reduced foliar antioxidant power compared to moderate RH. These results indicate that high RH plants were more susceptible to UV-induced damage than moderate RH plants due to reduced flavonoid content and oxidative stress defence.
Identifiants
pubmed: 30480699
doi: 10.1039/c8pp00401c
pii: 10.1039/c8pp00401c
doi:
Substances chimiques
Antioxidants
0
Flavonoids
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
387-399Références
M. Heijde and R. Ulm, UV-B photoreceptor-mediated signalling in plants, Trends Plant Sci., 2012, 17, 230–237.
pubmed: 22326562
doi: 10.1016/j.tplants.2012.01.007
G. I. Jenkins, The UV-B photoreceptor UVR8: from structure to physiology, Plant Cell, 2014, 26, 21–37.
T. M. Robson, K. Klem, O. Urban and M. A. K. Jansen, Reinterpreting plant morphological responses to UV-B radiation, Plant, Cell Environ., 2015, 38, 856–866.
doi: 10.1111/pce.12374
M. A. K. Jansen, V. Gaba and B. M. Greenberg, Higher plants and UV-B radiation: balancing damage, repair and acclimation, Trends Plant Sci., 1998, 3, 131–135.
doi: 10.1016/S1360-1385(98)01215-1
J. J. Favory, A. Stec, H. Gruber, L. Rizzini, A. Oravecz, M. Funk, A. Albert, C. Cloix, G. I. Jenkins, E. J. Oakeley, H. K. Seidlitz, F. Nagy and R. Ulm, Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis, EMBO J., 2009, 28, 591–601.
pubmed: 2657586
pmcid: 2657586
doi: 10.1038/emboj.2009.4
R. Yin and R. Ulm, How plants cope with UV-B: from perception to response, Curr. Opin. Plant Biol., 2017, 37, 42–48.
doi: 10.1016/j.pbi.2017.03.013
G. I. Jenkins, J. C. Long, H. K. Wade, M. R. Shenton and T. N. Bibikova, UV and blue light signalling: pathways regulating chalcone synthase gene expression in Arabidopsis, New Phytol., 2001, 151, 121–131.
doi: 10.1046/j.1469-8137.2001.00151.x
S. Nogués, D. J. Allen, J. I. L. Morison and N. R. Baker, Ultraviolet-B radiation effects on water relations, leaf development, and photosynthesis in droughted pea plants, Plant Physiol., 1998, 117, 173–181.
pubmed: 9576786
pmcid: 35000
doi: 10.1104/pp.117.1.173
A. Gaberščik, M. Vončina, T. Trošt, M. Germ and L. Olof Björn, Growth and production of buckwheat (Fagopyrum esculentum) treated with reduced, ambient, and enhanced UV-B radiation, J. Photochem. Photobiol., B, 2002, 66, 30–36.
doi: 10.1016/S1011-1344(01)00272-X
D. C. Gitz Iii, L. Liu-Gitz, S. J. Britz and J. H. Sullivan, Ultraviolet-B effects on stomatal density, water-use efficiency, and stable carbon isotope discrimination in four glasshouse-grown soybean (Glyicine max) cultivars, Environ. Exp. Bot., 2005, 53, 343–355.
doi: 10.1016/j.envexpbot.2004.04.005
M. A. K. Jansen and R. E. Van Den Noort, Ultraviolet-B radiation induces complex alterations in stomatal behaviour, Physiol. Plant., 2000, 110, 189–194.
doi: 10.1034/j.1399-3054.2000.110207.x
W. Eisinger, T. E. Swartz, R. A. Bogomolni and L. Taiz, The ultraviolet action spectrum for stomatal opening in broad bean, Plant Physiol., 2000, 122, 99–106.
pubmed: 58848
pmcid: 58848
doi: 10.1104/pp.122.1.99
V. E. Tossi, L. Lamattina, G. Jenkins and R. Cassia, UV-B-induced stomatal closure in, Arabidopsis is regulated by the UVR8 photoreceptor in an NO-dependent mechanism, Plant Physiol., 2014, 164(4), 2220–2230.
pubmed: 3982774
pmcid: 3982774
doi: 10.1104/pp.113.231753
L. Vanhaelewyn, E. Prinsen, D. Van Der Straeten and F. Vandenbussche, Hormone-controlled UV-B responses in plants, J. Exp. Bot., 2016, 67, 4469–4482.
pubmed: 27401912
doi: 10.1093/jxb/erw261
H. Bandurska, J. Niedziela and T. Chadzinikolau, Separate and combined responses to water deficit and UV-B radiation, Plant Sci., 2013, 213, 98–105.
pubmed: 24157212
doi: 10.1016/j.plantsci.2013.09.003
V. Alexieva, I. Sergiev, S. Mapelli and E. Karanov, The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat, Plant, Cell Environ., 2001, 24, 1337–1344.
doi: 10.1046/j.1365-3040.2001.00778.x
G. Grammatikopoulos, A. Kyparissis, P. Drilias, Y. Petropoulou and Y. Manetas, Effects of UV-B radiation on cuticle thickness and nutritional value of leaves in two mediterranean evergreen sclerophylls, J. Plant Physiol., 1998, 153, 506–512.
doi: 10.1016/S0176-1617(98)80181-8
D. Steinmüller and M. Tevini, Action of ultraviolet radiation (UV-B) upon cuticular waxes in some crop plants, Planta, 1985, 164, 557–564.
pubmed: 24248232
doi: 10.1007/BF00395975
F. J. Sánchez, M. a. Manzanares, E. F. de Andrés, J. L. Tenorio and L. Ayerbe, Residual transpiration rate, epicuticular wax load and leaf colour of pea plants in drought conditions. Influence on harvest index and canopy temperature, Eur. J. Agron., 2001, 15, 57–70.
doi: 10.1016/S1161-0301(01)00094-6
L. M. Mortensen and H. R. Gislerød, Influence of air humidity and lighting period on growth, vase life and water relations of 14 rose cultivars, Sci. Hortic., 1999, 82, 289–298.
doi: 10.1016/S0304-4238(99)00062-X
S. Torre, T. Fjeld, H. R. Gislerød and R. Moe, Leaf anatomy and stomatal morphology of greenhouse roses grown at moderate or high air humidity, J. Am. Soc. Hortic. Sci., 2003, 128, 598–602.
doi: 10.21273/JASHS.128.4.0598
D. Fanourakis, S. M. P. Carvalho, D. P. F. Almeida and E. Heuvelink, Avoiding high relative air humidity during critical stages of leaf ontogeny is decisive for stomatal functioning, Physiol. Plant., 2011, 142, 274–286.
pubmed: 21457269
doi: 10.1111/j.1399-3054.2011.01475.x
L. E. Arve, M. T. Terfa, H. R. Gislerød, J. E. Olsen and S. Torre, High relative air humidity and continuous light reduce stomata functionality by affecting the ABA regulation in rose leaves, Plant, Cell Environ., 2013, 36, 382–392.
doi: 10.1111/j.1365-3040.2012.02580.x
L. E. Arve, O. M. O. Kruse, K. K. Tanino, J. E. Olsen, C. Futsæther and S. Torre, Growth in continuous high air humidity increases the expression of CYP707A-genes and inhibits stomatal closure, Environ. Exp. Bot., 2015, 115, 11–19.
doi: 10.1016/j.envexpbot.2015.02.004
S. Aliniaeifard and U. van Meeteren, Natural variation in stomatal response to closing stimuli among Arabidopsis thaliana accessions after exposure to low VPD as a tool to recognize the mechanism of disturbed stomatal functioning, J. Exp. Bot., 2014, 65, 6529–6542.
pubmed: 25205580
pmcid: 4246184
doi: 10.1093/jxb/eru370
ISHS Acta Horticulturae 1104: XXIX International Horticultural Congress on Horticulture: Sustaining Lives, Livelihoods and Landscapes (IHC2014): International Symposium on Ornamental Horticulture in the Global Greenhouse, ed. R. A. Criley, 2015.
D. Fanourakis, D. Bouranis, H. Giday, D. R. A. Carvalho, A. Rezaei Nejad and C.-O. Ottosen, Improving stomatal functioning at elevated growth air humidity: a review, J. Plant Physiol., 2016, 207, 51–60.
pubmed: 27792901
doi: 10.1016/j.jplph.2016.10.003
A. R. Nejad and U. van Meeteren, Stomatal response characteristics of Tradescantia virginiana grown at high relative air humidity, Physiol. Plant., 2005, 125, 324–332.
doi: 10.1111/j.1399-3054.2005.00567.x
L. E. Arve, Stomatal functioning and abscisic acid (ABA), regulation in plants developed in different air humidity regimes, 2013 : 29, Norwegian University of Life Sciences, 2013.
S. Aliniaeifard and U. van Meeteren, Can prolonged exposure to low VPD disturb the ABA signalling in stomatal guard cells?, J. Exp. Bot., 2013, 64, 3551–3566.
pubmed: 23956410
pmcid: 3745724
doi: 10.1093/jxb/ert192
L. E. Arve, D. R. A. Carvalho, J. E. Olsen and S. Torre, ABA induces H2O2 production in guard cells, but does not close the stomata on, Vicia faba leaves developed at high air humidity, Plant Signaling Behav., 2014, 9, e29192.
L. E. Arve and S. Torre, Ethylene is involved in high air humidity promoted stomatal opening of tomato (Lycopersicon esculentum) leaves, Funct. Plant Biol., 2015, 42, 376–386.
pubmed: 32480682
doi: 10.1071/FP14247
L. E. Arve, O. M. O. Kruse, K. K. Tanino, J. E. Olsen, C. Futsæther and S. Torre, Daily changes in VPD during leaf development in high air humidity increase the stomatal responsiveness to darkness and dry air, J. Plant Physiol., 2017, 211, 63–69.
pubmed: 28161560
doi: 10.1016/j.jplph.2016.12.011
E. Domínguez, J. Cuartero and A. Heredia, An overview on plant cuticle biomechanics, Plant Sci., 2011, 181, 77–84.
doi: 10.1016/j.plantsci.2011.04.016
L. Schreiber and M. Riederer, Ecophysiology of cuticular transpiration: comparative investigation of cuticular water permeability of plant species from different habitats, Oecologia, 1996, 107, 426–432.
pubmed: 28307383
doi: 10.1007/BF00333931
T. Shepherd and D. Wynne Griffiths, The effects of stress on plant cuticular waxes, New Phytol., 2006, 171, 469–499.
pubmed: 16866954
doi: 10.1111/j.1469-8137.2006.01826.x
H. Lambers, F. S. Chapin III and T. L. Pons, Plant Physiological Ecology, Springer Science + Business Media, LLC, New York, USA, 2nd edn, 2008.
A. Suthaparan, A. Stensvand, K. A. Solhaug, S. Torre, L. M. Mortensen, D. M. Gadoury, R. C. Seem and H. R. Gislerød, Suppression of powdery mildew (Podosphaera pannosa) in greenhouse roses by brief exposure to supplemental UV-B radiation, Plant Dis., 2012, 96, 1653–1660.
pubmed: 30727454
doi: 10.1094/PDIS-01-12-0094-RE
S. K. Singh, K. R. Reddy, V. R. Reddy and W. Gao, Maize growth and developmental responses to temperature and ultraviolet-B radiation interaction, Photosynthetica, 2014, 52, 262–271.
doi: 10.1007/s11099-014-0029-6
D. Marquenie, A. H. Geeraerd, J. Lammertyn, C. Soontjens, J. F. Van Impe, C. W. Michiels and B. M. Nicolaï, Combinations of pulsed white light and UV-C or mild heat treatment to inactivate conidia of, Botrytis cinerea and, Monilia fructigena, Int. J. Food Microbiol., 2003, 85, 185–196.
P. V. Demkura and C. L. Ballaré, UVR8 mediates UV-B-induced, Arabidopsis defense responses against, Botrytis cinerea by controlling sinapate accumulation, Mol. Plant, 2012, 5, 642–652.
pubmed: 22447155
pmcid: 22447155
doi: 10.1093/mp/sss025
A. Suthaparan, A. Stensvand, K. A. Solhaug, S. Torre, K. H. Telfer, A. K. Ruud, L. M. Mortensen, D. M. Gadoury, R. C. Seem and H. R. Gislerød, Suppression of cucumber powdery mildew by supplemental UV-B radiation in greenhouses can be augmented or reduced by background radiation quality, Plant Dis., 2014, 98, 1349–1357.
pubmed: 30703932
doi: 10.1094/PDIS-03-13-0222-RE
A. Suthaparan, K. A. Solhaug, A. Stensvand and H. R. Gislerød, Determination of UV action spectra affecting the infection process of, Oidium neolycopersici, the cause of tomato powdery mildew, J. Photochem. Photobiol. B, 2016, 156, 41–49.
timeanddate.com, Yearly sun graph for Oslo, https://www.timeanddate.com/sun/norway/oslo, (accessed 04.07.2018, 2018).
Y. Kong, D. Llewellyn and Y. Zheng, Response of growth, yield, and quality of pea shoots to supplemental light-emitting diode lighting during winter greenhouse production, Can. J. Plant Sci., 2018, 98, 732–740.
A. E. S. Green, T. Sawada and E. P. Shettle, The middle ultraviolet reaching the ground, Photochem. Photobiol., 1974, 19, 251–259.
L. Nybakken, R. Horkka and R. Julkunen-Tiitto, Combined enhancements of temperature and UVB influence growth and phenolics in clones of the sexually dimorphic, Salix myrsinifolia, Physiol. Plant., 2012, 145, 551–564.
F. M. Mirabella, in, Internal Reflection Spectroscopy: Theory and Applications, ed. F. M. Mirabella, Marcel Dekker, Inc., New York, 1993, vol. 15, pp. 17–52.
S. Dudonne, X. Vitrac, P. Coutiere, M. Woillez and J. M. Merillon, Comparative study of antioxidant properties and total phenolic content of 30 plant extracts of industrial interest using DPPH, ABTS, FRAP, SOD, and ORAC assays, J. Agric. Food Chem., 2009, 57, 1768–1774.
pubmed: 19199445
doi: 10.1021/jf803011r
A. Szydłowska-Czerniak, I. Bartkowiak-Broda, I. Karlović, G. Karlovits and E. Szłyk, Antioxidant capacity, total phenolics, glucosinolates and colour parameters of rapeseed cultivars, Food Chem., 2011, 127, 556–563.
pubmed: 23140700
doi: 10.1016/j.foodchem.2011.01.040
G. Clarke, K. N. Ting, C. Wiart and J. Fry, High Correlation of 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging, ferric reducing activity potential and total phenolics content indicates redundancy in use of all three assays to screen for antioxidant activity of extracts of plants from the Malaysian rainforest, Antioxidants, 2013, 2, 1–10.
pubmed: 26787618
pmcid: 4665400
doi: 10.3390/antiox2010001
K. Maxwell and G. N. Johnson, Chlorophyll fluorescence—a practical guide, J. Exp. Bot., 2000, 51, 659–668.
pubmed: 10938857
pmcid: 10938857
doi: 10.1093/jexbot/51.345.659
E. N. Dubis, A. T. Dubis and J. W. Morzycki, Comparative analysis of plant cuticular waxes using HATR FT-IR reflection technique, J. Mol. Struct, 1999, 511–512, 173–179.
B. Ribeiro da Luz, Attenuated total reflectance spectroscopy of plant leaves: a tool for ecological and botanical studies, New Phytol., 2006, 172, 305–318.
M. Bağcıoğlu, B. Zimmermann and A. Kohler, A multiscale vibrational spectroscopic approach for identification and biochemical characterization of pollen, PLoS One, 2015, 10, e0137899.
A. B. Britt, Repair of DNA damage induced by solar UV, Photosynth. Res., 2004, 81, 105–112.
S. Li, M. Paulsson and L. O. Björn, Temperature-dependent formation and photorepair of DNA damage induced by UV-B radiation in suspension-cultured tobacco cells, J. Photochem. Photobiol., B, 2002, 66, 67–72.
doi: 10.1016/S1011-1344(01)00277-9
L. M. Mortensen, C. O. Ottosen and H. R. Gislerød, Effects of air humidity and K : Ca ratio on growth, morphology, flowering and keeping quality of pot roses, Sci. Hortic., 2001, 90, 131–141.
doi: 10.1016/S0304-4238(00)00251-X
G. J. Hoffman, S. L. Rawlins, M. J. Garber and E. M. Cullen, Water relations and growth of cotton as influenced by salinity and relative humidity, Agron. J., 1971, 63, 822–826.
doi: 10.2134/agronj1971.00021962006300060002x
L. M. Mortensen and H. R. Gislerød, Effects of air humidity and supplementary lighting on foliage plants, Sci. Hortic., 1990, 44, 301–308.
doi: 10.1016/0304-4238(90)90130-7
J. Ren, W. R. Dai, Z. Y. Xuan, Y. N. Yao, H. Korpelainen and C. Y. Li, The effect of drought and enhanced UV-B radiation on the growth and physiological traits of two contrasting poplar species, For. Ecol. Manage., 2007, 239, 112–119.
doi: 10.1016/j.foreco.2006.11.014
J. H. Bassman, G. E. Edwards and R. Robberecht, Long-term exposure to enhanced UV-B radiation is not detrimental to growth and photosynthesis in Douglas-fir, New Phytol., 2002, 154, 107–120.
doi: 10.1046/j.1469-8137.2002.00354.x
A. G. Roro, S. A. F. Dukker, T. I. Melby, K. A. Solhaug, S. Torre and J. E. Olsen, UV-B-induced inhibition of stem elongation and leaf expansion in pea depends on modulation of gibberellin metabolism and intact gibberellin signalling, J. Plant Growth Regul., 2017, 1–11, DOI: 10.1007/s00344-017-9671-0.
G. Agati and M. Tattini, Multiple functional roles of flavonoids in photoprotection, New Phytol., 2010, 186, 786–793.
pubmed: 20569414
doi: 10.1111/j.1469-8137.2010.03269.x
S. M. Siipola, T. Kotilainen, N. Sipari, L. O. Morales, A. V. Lindfors, T. M. Robson and P. J. Aphalo, Epidermal UV-A absorbance and whole-leaf flavonoid composition in pea respond more to solar blue light than to solar UV radiation, Plant, Cell Environ., 2015, 38, 941–952.
doi: 10.1111/pce.12403
G. Agati, E. Azzarello, S. Pollastri and M. Tattini, Flavonoids as antioxidants in plants: location and functional significance, Plant Sci., 2012, 196, 67–76.
pubmed: 23017900
doi: 10.1016/j.plantsci.2012.07.014
I. F. F. Benzie and J. J. Strain, The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay, Anal. Biochem., 1996, 239, 70–76.
doi: 10.1006/abio.1996.0292
F. Gniwotta, G. Vogg, V. Gartmann, T. L. W. Carver, M. Riederer and R. Jetter, What do microbes encounter at the plant surface? Chemical composition of pea leaf cuticular waxes, Plant Physiol., 2005, 139, 519–530.
pubmed: 16113231
pmcid: 1203400
doi: 10.1104/pp.104.053579
M. Wen, J. Au, F. Gniwotta and R. Jetter, Very-long-chain secondary alcohols and alkanediols in cuticular waxes of, Pisum sativum leaves, Phytochemistry, 2006, 67, 2494–2502.
pubmed: 16997335
doi: 10.1016/j.phytochem.2006.08.016
A. M. Abdulmajeed, S. R. Derby, S. K. Strickland and M. M. Qaderi, Interactive effects of temperature and UVB radiation on methane emissions from different organs of pea plants grown in hydroponic system, J. Photochem. Photobiol., B, 2017, 166, 193–201.
doi: 10.1016/j.jphotobiol.2016.11.019
E. Domínguez, J. A. Heredia-Guerrero and A. Heredia, The biophysical design of plant cuticles: an overview, New Phytol., 2011, 189, 938–949.
pubmed: 21374891
doi: 10.1111/j.1469-8137.2010.03553.x
F. Marga, T. C. Pesacreta and K. H. Hasenstein, Biochemical analysis of elastic and rigid cuticles of, Cirsium horridulum, Planta, 2001, 213, 841–848.
A. R. McLeod, S. C. Fry, G. J. Loake, D. J. Messenger, D. S. Reay, K. A. Smith and B. W. Yun, Ultraviolet radiation drives methane emissions from terrestrial plant pectins, New Phytol., 2008, 180, 124–132.
doi: 10.1111/j.1469-8137.2008.02571.x
L. W. Mapson and F. A. Isherwood, Biological synthesis of ascorbic acid: the conversion of derivatives of D-galacturonic acid into L-ascorbic acid by plant extracts, Biochem. J., 1954, 59, ix–ix.
F. A. Isherwood, Y. T. Chen and L. W. Mapson, Synthesis of L-ascorbic acid in plants and animals, Nature, 1953, 171, 348.
pubmed: 13036892
doi: 10.1038/171348a0
K. Yokawa and F. Baluška, Pectins, ROS homeostasis and UV-B responses in plant roots, Phytochemistry, 2015, 112, 80–83.
pubmed: 25220496
doi: 10.1016/j.phytochem.2014.08.016
T. A. Day and T. C. Vogelmann, Alterations in photosynthesis and pigment distributions in pea leaves following UV-B exposure, Physiol. Plant., 1995, 94, 433–440.
doi: 10.1111/j.1399-3054.1995.tb00950.x
J.-M. He, H. Xu, X.-P. She, X.-G. Song and W.-M. Zhao, The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean, Funct. Plant Biol., 2005, 32, 237–247.
pubmed: 32689127
doi: 10.1071/FP04185