Chlorophyll fluorescence and other physiological parameters as indicators of waterlogging and shadow stress in lulo (Solanum quitoense var. septentrionale) seedlings

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Alefsi David Sánchez-Reinoso
Yulieth Jiménez-Pulido
Jean Paul Martínez-Pérez
Carlos Salvador Pinilla
Gerhard Fischer


Climate change has resulted in an increasing frequency of the phenomenon “La Niña,” generating prolonged periods of waterlogging and low light. The objective of the present study was to evaluate the effects of two abiotic stresses: shading (65%) and waterlogging, and their interaction on fluorescence parameters of chlorophyll a in lulo (Solanum quitoense var. septentrionale) seedlings. A completely randomized design with a factorial arrangement was implemented. The first factor consisted of two levels of light (with and without shading). The second factor were four levels of duration of the waterlogging period (0, 3, 6 and 9 days), for a total of 8 treatments with three replicates. The response variables were recorded at 6, 12 and 18 days after the application of the waterlogging treatments began. Measurements of relative water content (RWC), electrolyte leakage, chlorophyll content and chlorophyll a fluorescence were recorded. The lulo plants appeared to be more susceptible to waterlogging than to shading, with a lower RWC when waterlogged 6 and 9 days, presenting damage at the level of photosystem II from day 3, causing a decrease in the chlorophyll content. The plants flooded under shading had a greater tolerance to this factor than those cultivated in full light. The techniques of quantification of the chlorophyll a fluorescence, especially the maximum quantum efficiency of the PSII, the effective photochemical quantum yield of PS II and the photochemical quenching were useful tools that characterized the lulo seedlings under stress conditions.


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Aldana, F., P. García, and G. Fischer. 2014. Effect of waterlogging stress on the growth, development and symptomatology of cape gooseberry (Physalis peruviana L.) plants. Rev. Acad. Colomb. Cienc. Ex. Fis. Nat. 38(149), 393-400. Doi: 10.18257/raccefyn.114

Andrade, C., K. Dázio, M. Santos, D. Silva, and J. Donizeti. 2018. Hydrogen peroxide promotes the tolerance of soybeans to waterlogging. Sci. Hortic. 232, 40-45. Doi: 10.1016/j.scienta.2017.12.048

Anjum, S.A., X.Y. Xie, L.C. Wang, M.F. Saleem, C. Man, and W. Lei. 2011. Morphological, physiological and biochemical responses of plants to drought stress. Afr. J. Agr. Res. 6(9), 2026-2032.

Ardila, G., G. Fischer, and J.C. García. 2015. La poda de tallos y racimos florales afecta la producción de frutos de lulo (Solanum quitoense var. septentrionale). Rev. Colomb. Cienc. Hortic. 9(1), 24-37. Doi: 10.17584/rcch.2015v9i1.3743

Ashraf, M. 2012. Waterlogging stress in plants: A review. Afr. J. Agr. Res. 7(13), 1976-1981. Doi: 10.5897/AJARX11.084

Bailey-Serres J. and L. Voesenek. 2008. Flooding stress: acclimations and genetic diversity. Annu. Rev. Plant Biol. 59, 313-339. Doi: 10.1146/annurev.arplant.59.032607.092752

Bansal, R., S. Sharma, K. Tripathi, C. Gayacharan, and A. Kumar. 2019. Waterlogging tolerance in black gram [Vigna mungo (L.) Hepper] is associated with chlorophyll content and membrane integrity. Ind. J. Biochem. Biophys. 56, 81-85.

Baracaldo. A., R. Carvajal, A. Romero, A. Prieto, F. García, G. Fischer, and D. Miranda. 2014. El anegamiento afecta el crecimiento y producción de biomasa en tomate chonto (Solanum lycopersicum L.), cultivado bajo sombrío. Rev. Colomb. Cienc. Hortic. 8(1), 92-102. Doi: 10.17584/rcch.2014v8i1.2803

Bonnet, J.G. and J.F. Cárdenas. 2012. Lulo (Solanum quitoense Lam.). pp. 604-621. In: Fischer, G. (ed.) Manual para el cultivo de frutales en el trópico. Ed. Produmedios, Bogota.

Cardona, W.A., L.G. Bautista, N. Flórez-Velasco, and G. Fischer. 2016. Desarrollo de la biomasa y raíz en plantas de lulo (Solanum quitoense var. septentrionale) en respuesta al sombrío y anegamiento. Rev. Colomb. Cienc. Hortic. 10(1), 53-65. Doi: 10.17584/rcch.2016v10i1.5124

Casierra-Posada, C. and J. Cutler. 2017. Photosystem II fluorescence and growth in cabbage plants (Brassica oleracea var. capitata) grown under waterlogging stress. Rev. UDCA Act. Div. Cient. 20(2), 321-328. Doi: 10.31910/rudca.v20.n2.2017.390

Cruz, P., K. Acosta, J. Cure, and D. Rodríguez. 2007. Desarrollo y fenología del lulo Solanum quitoense var. septentrionale bajo polisombra desde siembra hasta primera fructificación. Agron. Colomb. 25(2), 288-298.

Do Nascimento, C.W.A. and M.C. Marques. 2018. Metabolic alterations and X-ray chlorophyll fluorescence for the early detection of lead stress in castor bean (Ricinus communis) plants. Acta Scient. Agron. 40, e30392-e39392. Doi: 10.4025/actasciagron.v40i1.39392

Else, M.A., F. Janowiak, C.J. Atkinson, and M.B. Jackson. 2009. Root signals and stomatal closure in relation to photosynthesis, chlorophyll a fluorescence and adventitious rooting of flooded tomato plants. Ann. Bot. 103(2), 313-323. Doi: 10.1093/aob/mcn208

Ezin, V., R. de la Pen, and A. Ahanchede. 2010. Flooding tolerance of tomato genotypes during vegetative and reproductive stages. Braz. J. Plant Physiol. 22(1), 131-142. Doi: 10.1590/S1677-04202010000200007

Fischer, G. and L.M. Melgarejo. 2020. The ecophysiology of cape gooseberry (Physalis peruviana L.) - an Andean fruit crop. A review. Rev. Colomb. Cienc. Hortic. 14(2). Doi: 10.17584/rcch.2020v14i2.10893
Fischer, G., L.M. Melgarejo, and J. Cutler. 2018. Pre-harvest factors that influence the quality of passion fruit: A review. Agron. Colomb. 36(3), 217-226. Doi: 10.15446/agron.colomb.v36n3.71751

Fischer, G., F. Ramírez, and F. Casierra-Posada. 2016. Ecophysiological aspects of fruit crops in the era of climate change. A review. Agron. Colomb. 34(2), 190-199. Doi: 10.15446/agron.colomb.v34n2.56799

Flórez-Velasco, N., H.E. Balaguera-López, and H. Restrepo-Díaz. 2015. Effects of foliar urea application on lulo (Solanum quitoense cv. septentrionale) plants grown under different waterlogging and nitrogen conditions. Sci. Hortic. 186, 154-162. Doi: 10.1016/j.scienta.2015.02.021

Gancel, A.L., P. Alter, C. Dhuique-Mayer, J. Ruales, and F. Vaillant. 2008. Identifying carotenoids and phenolic compounds in naranjilla (Solanum quitoense Lam.) var. Puyo hybrid, an andean fruit. J. Agr. Food Chem. 56(24), 11890-11899. Doi: 10.1021/jf801515p

Gómez, F., L. Rejo, J. García, and J. Cadeña. 2014. Lulo (Solanum quitoense [Lamarck.]) como cultivo novedoso en el paisaje agroecosistémico mexicano. Rev. Mex. Cienc. Agríc. 9(Spec. Numb.), 1741-1753. Doi: 10.29312/remexca.v0i9.1061

González, D., L. Ordóñez, P. Vanegas, and H. Vásquez. 2014. Cambios en las propiedades fisicoquímicas de frutos de lulo (Solanum quitoense Lam.) cosechados en tres grados de madurez. Acta Agron. 63(1), 11-17. Doi: 10.15446/acag.v63n1.31717

Huertas, I., R. Varástegui, L. Puentes, and L. Fernández. 2011. Modelo de dinámica de sistemas para las frutas orgánicas: lulo. Universidad Colegio Mayor de Nuestra Señora del Rosario, Bogota.

Hanelt, D. 2018. Photosynthesis assessed by chlorophyll fluorescence. pp. 169-198. In: Häder, D.-P. and G.S. Erzinger (eds.). Bioassays: advanced methods and applications. Elsevier, Amsterdam, The Netherlands. Doi: 10.1016/B978-0-12-811861-0.00009-7

Janowiak, F., M.A. Else, and M.B. Jackson. 2002. A loss of photosynthetic efficiency does not explain stomatal closure in flooded tomato plants. Adv. Agric. Sci. Probl. 481, 229-234.

Jiang, M. and J. Zhang. 2001. Effect of abscisic acid on active oxygen species, antioxidative defense system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol. 42, 1265-1273. Doi: 10.1093/pcp/pce162

Jiménez, J.d.l.C., J.A. Cardoso, D. Arango-Londoño, G. Fischer, and I. Rao. 2015. Influence of soil fertility on waterlogging tolerance of two Brachiaria grasses. Agron. Colomb. 33(1), 20-28. Doi:

Jiménez-Suancha, S.C., O.H. Alvarado, and H.E. Balaguera-López. 2015. Fluorescencia como indicador de estrés en Helianthus annuus L. Una revisión. Rev. Colomb. Cienc. Hortic. 9(1), 149-160. Doi: 10.17584/rcch.2015v9i1.3753

Kadereit, J.W., C. Körner, B. Kost, and U. Sonnewald. 2014. Lehrbuch der Pflanzenwissenschaften. Begründet von Eduard Strasburger. 37. Auflage. Springer Spektrum, Berlin/Heidelberg, Germany. Doi: 10.1007/978-3-642-54435-4

Laan, P., M. Tosserams, C.W.P.M. Blom, and B.W. Veen. 1990. Internal oxygen transport in Rumex species and its significance for respiration under hypoxic conditions. Plant Soil 122, 39-46. Doi: 10.1007/BF02851908

Lichtenthaler, H.K., C. Buschmann, and M. Knapp. 2005. How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43(3), 379-393. Doi: 10.1007/s11099-005-0062-6

Marques, M.C., C.W.A. Nascimento, A.J. da Silva, and A. da Silva Gouveia-Neto. 2017. Tolerance of an energy crop (Jatropha curcas L.) to zinc and lead assessed by chlorophyll fluorescence and enzyme activity. S. Afr. J. Bot. 112, 275-282. Doi: 10.1016/j.sajb.2017.06.009

Melgarejo, L.M. (ed.). 2010. Experimentos en fisiología vegetal. Universidad Nacional de Colombia, Bogota.

Mielke, M.S. and B. Schaffer. 2010. Leaf gas exchange, chlorophyll fluorescence and pigment indexes of Eugenia uniflora L. in response to changes in light intensity and soil flooding. Tree Physiol. 30(1), 45-55. Doi: 10.1093/treephys/tpp095

Mittler, R. 2006. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11(1), 15-19. Doi: 10.1016/j.tplants.2005.11.002

Moreno, A. and G. Fischer. 2014. Efectos del anegamiento en los frutales. Una revisión. Temas Agrarios 19(1), 108-125. Doi: 10.21897/rta.v19i1.729

Moreno, D., D.C. Rodríguez, and H.E. Balaguera. 2019. Physiological responses of tree species to waterlogging condition. Colomb. For. 22(1), 51-67. Doi: 10.14483/2256201X.13453

Orjuela-Castro, J., F. Morales-Aguilar, and L. Mejía-Flórez. 2017. ¿Cuál es la mejor cadena de suministro para frutas perecederas, lean o ágil?. Rev. Colomb. Cienc. Hortíc. 11(2), 294-305. Doi: 10.17584/rcch.2017v11i2.5950

Oh, M. and S. Komatsu. 2015. Characterization of proteins in soybean roots under flooding and drought stresses. J. Proteomics 114, 161-181. Doi: 10.1016/j.jprot.2014.11.008

Rohaček, K. 2002. Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40(1), 13-29. Doi: 10.1023/A:1020125719386

Sánchez-Reinoso, A.D., G.A. Ligarreto-Moreno, and H. Restrepo-Díaz. 2019. Chlorophyll fluorescence parameters as an indicator to identify drought susceptibility in common bush bean. Agronomy 9, 526. Doi: 10.3390/agronomy9090526

Schreiber, U., W. Bilger, and C. Neubauer. 1994. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. pp. 49-70. In: Schulze, E.D. and M.M. Caldwell (eds.). Ecophysiology of photosynthesis. Springer, Heidelberg, Germany. Doi: 10.1007/978-3-642-79354-7_3

Soleh, M.A., M. Ariyanti, I.R. Dewi, and M. Kadapi. 2018. Chlorophyll fluorescence and stomatal conductance of ten sugarcane varieties under waterlogging and fluctuation light intensity. Emir. J. Food Agric. 30(11), 935-940.

Taiz, L., E. Zeiger, I.A. Møller, and A. Murphy. 2018. Plant physiology and development. 6th ed. Oxford University Press, Oxford, UK.

Urbas, P. and K. Zobel. 2000. Adaptive and inevitable morphological plasticity of three herbaceous species in a multi-species community: field experiment with manipulated nutrients and light. Acta Oecol. 21, 139-147. Doi: 10.1016/S1146-609X(00)00115-6

Villarreal-Navarrete, A., G. Fischer, L.M. Melgarejo, G. Correa, and L. Hoyos-Carvajal. 2017. Growth response of the cape gooseberry (Physalis peruviana L.) to waterlogging stress and Fusarium oxysporum infection. Acta Hortic. 1178, 161-168. Doi: 10.17660/ActaHortic.2017.1178.28

Visser, E.J.W., Q. Zhang, F. De Gruyter, S. Martens, and H. Huber. 2015. Shade affects responses to drought and flooding – acclimation to multiple stresses in bittersweet (Solanum dulcamara L.). Plant Biol. 18, 112-119. Doi: 10.1111/plb.12304

Waldhoff, D., B. Furch, and W.J. Junk. 2002. Fluorescence parameters, chlorophyll concentration, and anatomical features as indicators for flood adaptation of an abundant tree species in Central Amazonia: Symmeria paniculata. Environ. Exp. Bot. 48(3), 225-235. Doi: 10.1016/S0098-8472(02)00037-0

Wu, X., Y. Tang, C. Li, C. Wu, and G. Huang. 2015. Chlorophyll fluorescence and yield responses of winter wheat to waterlogging at different growth stages. Plant Prod. Sci. 18(3), 284-294. Doi: 10.1626/pps.18.284

Yan, K., S. Zhao, M. Cui, G. Han, and P. Wen. 2018. Vulnerability of photosynthesis and photosystem I in Jerusalem artichoke (Helianthus tuberosus L.) exposed to waterlogging. Plant Physiol. Biochem. 125, 239-246. Doi: 10.1016/j.plaphy.2018.02.017


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