The evaluation of chlorophyll fluorescence activity is a useful tool for rapid and effective assessments of the effect of abiotic factors on the physiology of different crops. In Rubus, this type of measurements describes tolerance to high temperatures, sensitivity to heat and morphological alterations in flowering and chlorophyll content, as a result of plant stress.
OBJECTIVE:
The present research estimated chlorophyll fluorescence and the presence of some phenolic compounds in the leaves of three cultivars of blackberry (Rubus sp.) established in the central region of Colombia, under conditions of open air between 2400 and 2800 masl.
MATERIAL AND METHODS:
This was done through the measurement of chlorophyll a (Junior-PAM II modulated fluorometer), the quantification of phenolic compounds (Folin Ciocalteu), the determination of antioxidant capacity (DPPH and ABTS) and the study of phenolic profiles (UHPLC) in leaves of three blackberry cultivars.
RESULTS:
Cultivars R. alutaceus (0.66), R. glaucus (0.73) and R. alpinus (0.76), presented values lower than the optimum (0.83), for the parameter Fv/Fm. In addition, the direct relationships between the parameters that define the behavior of PSII and the accumulation of different polyphenols were described. Reference was also made to the content of phenolic compounds (ranging from 125 to 150 mg GA g–1 dw), which did not show significant statistical differences. The heat map and principal component analysis show the close relationship between the parameters that characterize the functioning of PSII and the accumulation of phenolic compounds, as a mechanism of adaptation to the adverse conditions of the blackberry cultivars studied.
CONCLUSIONS:
The results reveal that the leaves of the Rubus studied could be a source of functional ingredients for use in the cosmetic, nutraceutical and food industries and epigallocatechin was attributed the greatest responsibility for the antioxidant capacity.
RamakrishnaA, RavishankarGA. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signaling and Behavior. 2011;6(11):1720–31.https://doi.org/10.4161/psb.6.11.17613
2.
ThakurMS, BhattacharyaP, KumarP, PuriS. Improving production of plant secondary metabolites through biotic and abiotic elicitation. Journal of Applied Research on Medicinal and Aromatic Plants. 2019;12:1–2. https://doi.org/10.1016/j.jarmap.2018.11.004
3.
PetersK, BreitsameterL, GerowittB. Impact of climate change on weeds in agriculture: A review. Agric Sustain Dev. 2014;34:707–21. https://doi.org/10.1007/s13593-014-0245-2
4.
OliveiraG, PeñuelasJ. Comparative protective strategies of Cistus albidus and Quercus ilex facing photoinhibitory winter conditions. Environmental and Experimental Botany. 2002;47:281–9. https://doi.org/10.1016/S0098-8472(02)00003-5
5.
ValladaresF, ArandaI, Sánchez-GómezD. Ecología del bosque mediterráneo en un mundo cambiante. In: La luz como factor ecológico y evolutivo para las plantas y su interacción con el agua. Ministerio de Medio Ambiente, EGRAF, S. A., Madrid. 2004.
6.
ArenaC, VitaleL. Photosynthetic adaptive strategies in evergreen and semideciduous species of Mediterranean maquis during winter. In: Najafpour, M.M. Editors. Advances in Photosynthesis –Fundamental Aspects. Croatia. 2012;404-22.
7.
Salamon-AlbertM, CsiszarU, LorinczB. The gas exchange performance of the European blackberry (Rubus fruticosus agg.) and ecological traits for interpreting colonization in forest canopy gaps. Plant Biosystems. 2016;151(4):630–41.https://doi.org/10.1080/11263504.2016.1193067
8.
Casierra-PosadaF, MorenoD. Efecto del estrés por sombra sobre la producción en plantas de limonio (Limonium sp. cv. Bluestream). Revista Colombiana De Ciencias Hortícolas. 2007;1(2):236–45.https://doi.org/10.17584/rcch.2007v1i2.1164
9.
DawoodMG, TaieHAA, NassarRMA, AbdelhamidMT, SchmidhalterU. The changes induced in the physiological, biochemical and anatomical characteristics of Vicia faba by the exogenous application of proline under seawater stress, . South African Journal of Botany. 2014;93:54–63. https://doi.org/10.1016/j.sajb.2014.03.002
10.
KelloggAA, BranamanTJ, JonesNM, LittleC, SwansonJ. Morphological studies of developing Rubus prickles suggest that they are modified glandular trichomes. Botany. 2011;89:217–26. https://doi.org/10.1139/b11-008
11.
NicotraAB, AtkinOK, BonserSP, DavidsonAM, FinneganEJ, MathesiusU, et al. Plant phenotypic plasticity in a changing climate. Trends in Plant Science. 2010;15(12):684–92.https://doi.org/10.1016/j.tplants.2010.09.008
12.
CrogeCP, CuquelFLL, PintroP, BiasiLA, DeBona C. Compounds of Blackberries Produced in Different Climates. HortSci. 2019;54(12):2209–13.https://doi.org/10.21273/HORTSCI14377-19
13.
GambiniJ, López-GruesoR, Olaso-GonzálezG, InglésM, AbdelazidK, El AlamiM, Bonet-CostaV, BorrásC, ViñaJ. Resveratrol: Distribución, propiedades y perspectivas. Revista Española de Geriatría y gerontología. 2013;48(2):79–88.https://doi.org/10.1016/j.regg.2012.04.007
14.
CoelhoGC, RachwalMFG, DedecekRA, CurcioGR, NietscheK, SchenkelEP. Effect of light intensity on methylxanthine contents of Ilex paraguariensis A. St Hil Biochem Syst Ecol. 2007;35:75–80.
15.
ChenY, GuoQ, LiuL, LiaoL, ZhuZ. Influence of fertilization and drought stress on the growth and production of secondary metabolites in Prunella vulgaris L. J Med Plant Res. 2011;5(9):1749–55.
16.
Petinatti PavariniD, Petinatti PavariniS, NiehuesM, Peporine LopesN. Exogenous influences on plant secondary metabolite levels. Animal Feed Science and Technology. 2012;176(1-4):5–16.https://doi.org/10.1016/j.anifeedsci.2012.07.002
17.
Moreno-MedinaBL, Casierra-PosadaF, CutlerJ. Phytochemical Composition and Potential Use of Rubus Species. Gesunde Pflanzen. 2018;70(1):1–10.https://doi.org/10.1007/s10343-018-0416-1
18.
García-ParraM, StechaunerR, RoaDF, Ortiz GonzálezD, RamírezJ, Plazas LeguizamónN, ColmenaresR. Chlorophyll fluorescence and its relationship with physiological stress in Chenopodium quinoa Willd. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 2020;48(4):1742–55.https://doi.org/10.15835/nbha48412059
19.
Molina-BravoR, ArellanoC, SosondkiB, FernandezF. A protocol to assess heat tolerance in a segregating population of raspberry using chlorophyll fluorescence. Scientia Horticulturae. 2011;130:524–30. https://doi.org/10.1016/j.scienta.2011.07.022
20.
GotameTP, AndersenL, PetersenKK, PedersenHL, OttoesenCO, GrahamJ. Chlorophyll fluorescence and flowering behaviour of annual-fruiting raspberry cultivars under elevated temperature regimes. Eur J Hortic Sci. 2013;78:193–202.
21.
BradishCM, BushakraJM, DossettM, BassilNV, FinnCE, FernandezGE. Genotyping and phenotyping heat tolerance in black raspberry(Rubus occidentalis L.). Acta Hortic. 2016;1127:321–4. https://doi.org/10.17660/ActaHortic.2016.1127.50
22.
Peña-OlmosJ, Casierra-PosadaF. Chlorophyll Fluorescence in Partially Defoliated Grape Plants (Vitis vinifera L. cv. Chardonnay). Rev Fac Nac Agron Medellín. 2013;66(1):6881–9.
23.
WaterhouseL. Determination of total phenolics. In: Wrolstad, R.E. (Ed.), Handbook of Food Analytical Chemistry. John Wiley and Sons, New Jersey, 2001;463-70.
KuskoskiE, AsueroA, TroncosoA, FilhoJ, FettR. Aplicación de diversos métodos químicos para determinar actividad antioxidante en pulpa de frutos. Ciênc Tecnol Aliment. 2005;25(4):726–32.https://doi.org/10.1590/S0101-20612005000400016
26.
TakedaF, GlennDM, TworkoskiT. Rotating cross-arm trellis technology for blackberry production. Journal of Berry Research. 2013;3(1):5–40.https://doi.org/10.3233/JBR-130044
RenteriaJ, AtkinsonR, CrespoC, GardenerM, GrosholzE. Challenges for the management of the invasive blackberry (Rubus niveus) in the restoration of the Scalesia forest in the Galapagos Islands. Invasive Plant Science and Management. 2021;14(1):20–8.https://doi.org/10.1017/in2021.5
29.
Meléndez-JaramilloE, Cantú-AyalaC, Sánchez-ReyesC, Sandoval-BecerraFM. Herrera-Fernández BAltitudinal and seasonal distribution of butterflies (Lepidoptera, Papilionoidea) in Cerro Bufa El Diente, Tamaulipas, Mexico. ZooKeys. 2019;900:31–68. https://doi.org/10.3897/zookeys900.36978
30.
VásquezD, PalominosF, MartínezS. Visible-Light Photocatalytic Degradation of Aniline Blue by Stainless-Steel Foam Coated with TiO2 Grafted with Anthocyanins from a Maqui-Blackberry System. Catalysts. 2020;10(11):1245.https://doi.org/10.3390/catal10111245
31.
Casierra-PosadaF. Fotoinhibición: Respuesta fisiológica de los vegetales al estrés por exceso de luz. Revista Colombiana de Ciencias Hortícolas. 2007;1(1):114–23.
32.
BarbatoR, BergoE, SzabòI, DallaF, GiacomettiG. Ultraviolet B exposure of whole leaves of barley a2ffects structure and functional organization of photosystem II. J Biol Chem. 2000;275(15):10976–82.https://doi.org/10.1074/jbc.275.15.10976
ParkashV, SinghS. A review on potential plant-based water stress indicators for vegetable crops. Sustainability. 2020;12(10):3945.https://doi.org/10.3390/su12103945
35.
MurchieEH, LawsonT. Chlorophyll fluorescence analysis: A guide to good practice and understanding some new applications. J Exp Bot. 2013;64(13):3983–98.https://doi.org/10.1093/jxb/ert208
36.
Demmig-AdamsB. AdamsWW. Photoprotection in an ecological context: The remarkable complexity of thermal energy dissipation. New Phytologist. 2006;172(1):11–21.https://doi.org/10.1111/j.1469-8137.2006.01835.x
37.
CarpenedoAS, Machado AraujoM, Almeri TabaldiL, Benítez LeónE, Zavistanovicz ThairiniC, Manzoni BarbosaF, Pasquetti BerghettiA, Santos de LimaM. ¿El sombreamiento es capaz de potenciar el crecimiento de plantas de Myrocarpus frondosus en el campo? . Bosque (Valdivia). 2020;41(2):93–102.https://dx.doi.org/10.4067/S0717-92002020000200093
38.
Peña-OlmosJ, Casierra-PosadaF. Eficiencia fotoquímica del fotosistema II en plantas de brócoli (Brassica oleracea var Italica) afectadas por exceso de hierro. ORINOQUIA. 2013;17(1):15–22.
39.
Casierra-PosadaF, Aguilar-AvendañoO. Respuestas fisiológicas y morfológicas de plantas de mora (Rubus s) sometidas a estrés por viento inducido. Revista Colombiana De Ciencias Hortícolas. 2011;2(1):43–53.https://doi.org/10.17584/rcch.2008v2i1.1172
40.
DietzelL, GläßerC, LiebersM, HiekelS, CourtoisF, CzarneckiO, ChlickeH, ZuboY, BörnerT, MayerK, GrimmB, PfannschmidtT. Identification of early nuclear target genes of plastidial redox signals that trigger the long-term response of Arabidopsis to light quality shifts. Molecular Plant. 2015;8(8):1237–52.https://doi.org/10.1016/j.mol2015.03.004
41.
Alvarado-SanabriaO, Garces-VaronG, Restrepo-DiazH. Effect of two nocturnal temperatures on chlorophyll fluorescence parameters of flag leaves and panicle characteristics in seven rice (Oryza sativa L. ) genotypes. Pak J Bot. 2021;53(1):97–103.http://dx.doi.org/10.30848/PJB2021-1(32)
42.
HuangE, ZhangS, Fang CaoH. Evidence for leaf fold to remedy the deficiency of physiological photoprotection for photosystem II. Huang Photosynthetic Research. 2012;110:185–91. https://doi.org/10.1007/s11120-011-9717-2
43.
BresticM, ZivcakM. PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: Protocols and applications.In: Molecular stress physiology of plants, (Ed.): Rout, G.R. and Das, A.B. Springer, New Delhi, India. 2013.
44.
RitchieG Chlorophyll fluorescence: What is it and what do the numbers mean? In: Riley, L.E., Dumroese, R.K., Landis, T.D., tech. coords. 2006;34-42.
45.
MoraesDP, Lozano-SánchezJ, MachadoML, VizzottoML, LazzarettiM, Leyva-JimenezF, et al. Characterization of a new blackberry cultivar BRS Xingu: Chemical composition, phenolic compounds, and antioxidant capacity in vitro and in vivo. Food Chem. 2020;322:126783. https://doi.org/10.1016/j.foodchem.2020.126783
46.
WuY, ZhangC, HuangZ, LyuL, LiJ, LiW, WuW. The color difference of rubus fruits is closely related to the composition of flavonoids including anthocyanins. LWT. 2020;149:111825. https://doi.org/10.1016/j.lwt.2021.111825
47.
ZorziM, GaiF, MedanaC, AigottiR, MorelloS, PeirettiPG. Bioactive compounds and antioxidant capacity of small berries. Foods. 2020;9(5):2304–8158.https://doi.org/10.3390/foods9050623
BurchardP, BilgerW, WeissenböckG. Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultravioletinduced chlorophyll fluorescence measurements, Plant Cell Environ. 2008;23(12):1373–80. https://doi.org/10.1046/j.1365-3040.2000.00633.x
50.
RozemaJ, BjörnLO, BornmanJF, GaberscikA, HäderDP, TrostT, et al. The role of UV-B radiation in aquatic and terrestrial ecosystems–an experimental and functional analysis of the evolution of UV-absorbing compounds. J Photochem Photobiol B. 2002;66(1):2–12.https://doi.org/10.1016/S1011-1344(01)00269-X
51.
BidelLPR, MeyerS, GoulasY, CadotY. Responses of epidermal phenolic compounds to light acclimation: In vivo qualitative and quantitative assessment using chlorophyll fluorescence excitation spectra in leaves of three woody species. Journal of Photochemistry and Photobiology B: Biology. 2007;88(2-3):63–79.https://doi.org/10.1016/j.jphotobiol.2007.06.002
52.
Gouveia-FigueiraS. Castilho P. Phenolic screening by HPLC–DAD–ESI/MSn and antioxidant capacity of leaves, flowers and berries
of Rubus grandifolius Lowe.. Industrial Crops and Products. 2015;73:28–40. https://doi.org/10.1016/j.indcro2015.03.022
53.
KarasD, UlrichováJ, ValentováK. Galloylation of polyphenols alters their biological activity. Food and Chemical Toxicology. 2017;105:223–40. https://doi.org/10.1016/j.fct.2017.04.021
54.
SmithG, MarkhamK. Tautomerism of flavonol glucosides: Relevance to plant UV protection and flower colour. Chemistry. 1998;118(2):99–105.https://doi.org/10.1016/s1010-6030(98)00354-2
55.
CuongDM, KwonSJ, NguyenBN, ChunSW, KimJK, ParkSU. Effect of salinity stress on phenylpropanoid genes expression and related gene expression in wheat sprout. Agronomy. 2020;10(3):390.https://doi.org/10.3390/agronomy10030390
56.
ZhouP, LiQ, LiuG, XuN, YangY, ZengW. Integrated analysis of transcriptomic and metabolomic data reveals critical metabolic pathways involved in polyphenol biosynthesis in Nicotiana tabacum under chilling stress. Funct Plant Biol. 2018;46(1):30–43.https://doi.org/10.1071/FP18099
57.
KytidouK, ArtolaM, OverkleeftH, AertsM. Plant glycosides and glycosidases: A treasure-trove for therapeutics. Frontiers in Plant Science. 2020;11:357. https://doi.org/10.3389/fpls.2020.00357
58.
ŠamecD, KaralijaE, ŠolaI, VujčićV, Salopek-SondiB. The role of polyphenols in abiotic stress response: The influence of molecular structure. Plants. 2021;10(1):118.https://doi.org/10.3390/plants10010118
