Abstract
Photosynthesis is the most important source of dry matter production directly influencing grain filling in wheat. Croatian winter wheat varieties, ‘Vulkan’ and ‘Golubica’ have similar genetic yield potential but in previous years ‘Golubica’ failed to achieve it. In order to find reasons of that, we evaluated photosynthetic (JIP test) and oxidative pathways (antioxidative enzymes and non-enzymatic components) in flag leaves of both wheat varieties from flowering till late milk development stage. The maximum quantum yield of PSII (TR0/ABS) and performance index on absorption basis (PIABS) during experimental period indicated functional photosynthetic process, but according to other JIP test parameters down-regulation of PSII occurred in flag leaves of both varieties. In leaves of variety ‘Golubica’, significant inactivation of active reaction centers altogether with enlargement of carotenoids content imply on induction of photoinhibition. Also, at oxidative metabolism level, increase of catalase activity, hydrogen peroxide and malondialdehyde content in flag leaves of variety ‘Golubica’ imply on structural and functional changes and oxidative stress state in cell. Changes of photosynthetic and oxidative metabolism level in flag leaves of variety ‘Golubica’ imply on earlier onset of senescence than in ‘Vulkan’. Reduced time of photosynthetic product accumulation and its translocation into grain could be the reasons for ‘Golubica’ immanent underproduction.
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References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
Bolhár-Nordenkampf HR, Long SP, Baker NR, Öquist G, Schreiber U, Lechner EG (1989) Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current instrumentation. Funct Ecol 3:497–514. https://doi.org/10.2307/2389624
Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Caverzan A, Casassola A, Patussi Brammer S (2016) Antioxydant responses of wheat plants under stress. Genet Mol Biol 39(1):1–6. https://doi.org/10.1590/1678-4685-GMB-2015-0109
Christen D, Schönmann S, Jermini M, Strasser RJ, Defago G (2007) Characterisation and early detection of grapevine (Vitis vinifera) stress responses to esca disease by in situ chlorophyll fluorescence and comparison with drought stress. Environ Exp Bot 60:504–514. https://doi.org/10.1016/j.envexpbot.2007.02.003
De Simone V, Soccio M, Borelli GM, Pastore D, Trono D (2014) Stay-green trait-antioxidant status interrelationship in durum wheat (Triticum durum) flag leaf during post-flowering. J Plant Res 127:159–171. https://doi.org/10.1007/s10265-013-0584-0
Dey SK, Dey J, Patra S, Pothal D (2007) Changes in the antioxidative enzyme activities and lipid peroxidation in wheat seedlings exposed to cadmium and lead stress. Braz J Plant Physiol 19(1):53–60. https://doi.org/10.1590/S1677-04202007000100006
Eckhardt U, Grimm B, Hortensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plant. Plant Mol Biol 56:1–14. https://doi.org/10.1007/s11103-004-2331-3
Falqueto AR, dos Santos PN, Fontes RV, Silva DM (2013) Analysis of chlorophyll a fluorescence of two mangrove species of Vitoria Bay (ES, Brazil) to natural variation of tide. Revista Biociências 18(2):14–23
Force L, Critchley C, van Rensen JJS (2003) New fluorescence parameters for monitoring photosynthesis in plants. Photosynth Res 78:17–23. https://doi.org/10.1023/A:1026012116709
Ge P, Hao P, Cao M, Guo G, Lv D, Subburaj S, Li X, Yan X, Xiao J, Ma W, Yan Y (2013) iTRAQ-based quantitative proteomic analysis reveals new metabolic pathways of wheat seedling growth under hydrogen peroxide stress. Proteomics 13:3046–3058. https://doi.org/10.1002/pmic.201300042
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Gregersen PL, Holm PB, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biol 10(1):37–49. https://doi.org/10.1111/j.1438-8677.2008.00114.x
Jahns P, Holzwarth AR (2012) The role of xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193. https://doi.org/10.1016/j.bbabio.2011.04.012
Jiang GM, Sun JZ, Liu HQ, Qu CM, Wang KJ, Guo RJ, Bai KZ, Gao LM, Kuang TY (2003) Changes in the rate of photosynthesis accompanying the yield increase in wheat cultivars released in the past 50 years. J Plant Res 116:347–354. https://doi.org/10.1007/s10265-003-0115-5
Kalaji HM, Oukarroum A, Alexandrov V, Kouzmanova M, Brestic M, Zivcak M, Samborska IA, Cetner MD, Allekhverdiev SI, Goltsev V (2014) Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurement. Plant Physiol Biochem 81:16–25. https://doi.org/10.1016/j.plaphy.2014.03.029
Kovačević J, Kovačević M, Cesar V, Drezner G, Lalić A, Lepeduš H, Zdunić Z, Jurković Z, Dvojković K, Katanić Z, Kovačević V (2013) Photosynthetic efficiency and quantitative reaction of bread winter wheat to mild short-term drought conditions. Turk J Agric For 37:385–393. https://doi.org/10.3906/tar-1202-27
Lepeduš H, Gaća V, Viljevac M, Kovač S, Fulgosi H, Šimić D, Jurković V, Cesar V (2011) Changes in photosynthetic performance and antioxidative strategies during maturation of Norway maple (Acer platanoides L.) leaves. Plant Physiol Biochem 49:368–376. https://doi.org/10.1016/j.plaphy.2010.12.011
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Lidon FC, Loureiro AS, Vieira DE, Bilho EA, Nobre P, Costa R (2001) Photoinhibition in chilling stressed wheat and maize. Photosynthetica 39(2):161–166. https://doi.org/10.1023/A:1013726303948
Lu C, Lu Q, Zhang J, Kuang T (2001) Characterization of photosynthetic pigment composition, photosystem II photochemistry and thermal energy dissipation during leaf senescence of wheat plants grown in the field. J Exp Bot 52(362):1805–1810. https://doi.org/10.1093/jexbot/52.362.1805
Lu Q, Lu C, Zhang J, Kuang T (2002) Photosynthesis and chlorophyll a fluorescence during flag leaf senescence of field-grown wheat plants. J Plant Physiol 159:1173–1178. https://doi.org/10.1078/0176-1617-00727
Lu Q, Wen X, Lu C, Zhang Q, Kuang T (2003) Photoinhibition and photoprotection in senescent leaves of field-grown wheat plants. Plant Physiol Biochem 41:749–754. https://doi.org/10.1016/S0981-9428(03)00098-6
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–662. https://doi.org/10.1093/jexbot/51.345.659
Mittler R, Vanderauwera S, Gollera M, van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 10(9):490–498. https://doi.org/10.1016/j.tplants.2004.08.009
Monneveux P, Pastenes C, Reynolds MP (2003) Limitations to photosynthesis under light and heat stress in three high-yielding wheat genotypes. J Plant Physiol 160:657–666. https://doi.org/10.1078/0176-1617-00772
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Panda D, Sarkar RK (2013) Natural leaf senescence: probed by chlorophyll fluorescence, CO2 photosynthetic rate and antioxidant enzyme activities during grain filling in different rice cultivars. Physiol Mol Biol Plants 19(1):43–51. https://doi.org/10.1007/s12298-012-0142-6
Siegel BZ, Galston W (1967) The isoperoxidases of Pisum sativum. Plant Physiol 42:221–226
Španić V, Horvat D, Dvojković K (2008) Comparison of quantitative traits in old and modern wheat varieties. Cereal Res Commun 36:1283–1286
Španić V, Viljevac Vuletić M, Abičić I, Marček T (2017) Early response of wheat antioxidant system with special reference to Fusarium head blight stress. Plant Physiol Biochem 115:34–43. https://doi.org/10.1016/j.plaphy.2017.03.010
Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescent transient as a tool to characterise and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. CRC Press, New York, pp 445–483
Strasser RJ, Srivastava A, Tsimilli-Michael M (2004) Analysis of chlorophyll a fluorescence transient. In: Govindjee GC (ed) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 321–362
Sylvester-Bradley R, Scott RK, Wright CE (1990) Physiology in the production and improvement of cereals. Home-grown cereals authority research review, vol 18. HGCA, London
Szabó I, Bergantino E, Giacometti GM (2005) Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation. EMBO Rep 6(7):629–634. https://doi.org/10.1038/sj.embor.7400460
Tanaka R, Tanaka A (2011) Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. Biochim Biophys Acta 1807:968–976. https://doi.org/10.1016/j.bbabio.2011.01.002
Tanaka A, Ito H, Tanaka R, Tanaka NK, Yoshida K, Okada K (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci USA 95:12719–12723. https://doi.org/10.1073/pnas.95.21.12719
Triantaphylides C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219–228. https://doi.org/10.1016/j.tplants.2009.01.008
Tsimilli-Michael M, Eggenberg P, Biro B, Köves-Pechy K, Vörös I, Strasser RJ (2000) Synergistic and antagonistic effects of arbuscular mycorrhizal fungi and Azospirillum and Rhizobium nitrogen-fixers on the photosynthetic activity of alfalfa, probed by the polyphasic chlorophyll a fluorescence transient O-J-I-P. Appl Soil Ecol 15:169–182. https://doi.org/10.1016/S0929-1393(00)00093-7
van Heerden PDR, Swanepoel JW, Krüger GHJ (2007) Modulation of photosynthesis by drought in two desert scrub species exhibiting C3-mode CO2 assimilation. Environ Exp Bot 61:124–136. https://doi.org/10.1016/j.envexpbot.2007.05.005
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Verma S, Dubey RS (2003) Leads toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655. https://doi.org/10.1016/S0168-9452(03)00022-0
Yang X, Chen X, Ge Q, Li B, Tong Y, Li Z, Kuang T, Lu C (2007) Characterization of photosynthesis of flag leaves in a wheat hybrid and its parents grown under field conditions. J Plant Physiol 164:318–326. https://doi.org/10.1016/j.jplph.2006.01.007
Yang DQ, Luo YL, Dong WH, Yin YP, Li Y, Wang ZL (2018) Response of photosystem II performance and antioxidant enzyme activities in stay-green wheat to cytokinin. Photosynthetica 56(2):567–577. https://doi.org/10.1007/s11099-017-0708-1
Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee Sarin NB (2010) Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress. Biochim Biophys Acta 1797(8):1428–1438. https://doi.org/10.1016/j.bbabio.2010.02.002
Zadoks JC, Chang TT, Konzac FC (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421. https://doi.org/10.1111/j.1365-3180.1974.tb01084.x
Zhang CJ, Chen GX, Gao XX, Chu CJ (2006) Photosynthetic decline in flag leaves of two field-grown spring wheat cultivars with different senescence properties. S Afr J Bot 72:15–23. https://doi.org/10.1016/j.sajb.2005.03.002
Zhao H, Dai T, Jing Q, Jiang D, Cao W (2007) Leaf senescence and grain filling affected by post-anthesis high temperatures in two different wheat cultivars. Plant Growth Regul 51:149–158. https://doi.org/10.1007/s10725-006-9157-8
Živčák M, Brestič M, Olšovská K, Slamka P (2008) Performance index as a sensitive indicator of water stressin Triticum aestivum L. Plant Soil Environ 54:133–139
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This work has been supported in part by Croatian Science Foundation (HRZZ-UIP-2014-9188) and Agricultural Institute Osijek.
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Viljevac Vuletić, M., Marček, T. & Španić, V. Photosynthetic and antioxidative strategies of flag leaf maturation and its impact to grain yield of two field-grown wheat varieties. Theor. Exp. Plant Physiol. 31, 387–399 (2019). https://doi.org/10.1007/s40626-019-00153-x
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DOI: https://doi.org/10.1007/s40626-019-00153-x