Abstract
Soybean [Glycine max (L.) Merr.] is a widely cultivated crop, whose growth and development are usually influenced by fluctuating light environment in fields. In the present study, two soybean cultivars (Nandou12 and Nan 032-4) were selected to study the regulatory mechanisms of capability to do photosynthetic work under different light intensities. Results showed that the net photosynthetic rate (P n ) of Nandou 12, which has a higher yield in field condition, was significantly higher than that of Nan 032-4 under all the light intensities studied. Measurements on stomatal conductance (G s) and intercellular CO2 concentration (C i) suggested that the difference of P n between these two cultivars was mainly caused by non-stomatal factors. Transcript detection found that the expression of genes encoding plastid terminal oxidase (PTOX) and alternative oxidase (AOX), which represent the terminal oxidases of chlororespiration in chloroplasts and alternative respiration in mitochondria, respectively, was up-regulated in both cultivars when light intensity increased, implying potential roles of these two terminal oxidases in photosynthetic regulation. Further analysis showed that the expression level of PTOX increased more obviously in Nandou 12, together with higher non-photochemical quenching (NPQ) and higher activities of superoxide dismutase (SOD) and ascorbate peroxidase (APX) than that in Nan 032-4, when light intensity increased. However, Nan 032-4 performed a more obvious up-regulation of AOX genes, as well as higher activities of NAD-malate dehydrogenase (MDH) and NADP-MDH than Nandou 12, when light intensity increased. These distinctions were consequently suggested to be potential reasons for the difference of photosynthetic performance between two soybean cultivars.
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References
Baker NR, Oxborough K (2004) Chlorophyll fluorescence as a probe of photosynthetic productivity. In: Papageorgiou GC, Govindjee (ed) Chlorophyll a fluorescence: a signature of photosynthesis. Kluwer academic, London, pp 65–82
Chmeliov J, Trinkunas G, van Amerongen H, Valkunas L (2014) Light harvesting in a fluctuating antenna. J Am Chem Soc 136:8963–8972
Feng H, Guan D, Sun K, Wang Y, Zhang T, Wang R (2013) Expression and signal regulation of the alternative oxidase genes under abiotic stresses. Acta Biochim Biophys Sin 45:985–994
Gamboa J, Muñoz R, Quiles MJ (2009) Effects of antimycin A and n-propyl gallate on photosynthesis in sun and shade plants. Plant Sci 177:643–647
Giannopolitis CN, Ries SK (1977) Superoxide dismutase: I. Occurrence in higher plants. Plant Physiol 59:309–314
Gong W, Qi P, Du J, Sun X, Wu X, Song C, Liu W, Wu Y, Yu X, Yong T, Wang X, Yang F, Yan Y, Yang W (2014) Transcriptome analysis of shade-induced inhibition on leaf size in relay intercropped soybean. PLoS ONE 9:e98465
Heyno E, Gross CM, Laureau C, Culcasi M, Pietri S, Krieger-Liszkay A (2009) Plastid alternative oxidase (PTOX) promotes oxidative stress when overexpressed in tobacco. J Biol Chem 284:31174–31180
Ibáñnez H, Ballester A, Muñoz R, Quiles MJ (2010) Chlororespiration and tolerance to drought, heat and high illumination. J Plant Physiol 167:732–738
Ivanov AG, Rosso D, Savitch LV, Stachula P, Rosembert M, Oquist G, Hurry V, Hüner NP (2012) Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana. Photosynth Res 113:191–206
Johnson GN, Stepien P (2016) Plastid terminal oxidase as a route to improving plant stress tolerance: known knowns and known unknowns. Plant Cell Physiol 57:1387–1396
Kono M, Terashima I (2014) Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. J Photoch Photobio B 137:89–99
Krieger-Liszkay A, Feilke K (2016) The dual role of the plastid terminal oxidase PTOX: between a protective and a pro-oxidant function. Front Plant Sci 6:1147
Kuntz M (2004) Plastid terminal oxidase and its biological significance. Planta 218:896–899
Laureau C, Paepe RD, Latouche G, Moreno-Chacón M, Finazzi G, Kuntz M, Cornic G, Streb P (2013) Plastid terminal oxidase (PTOX) has the potential to act as a safety valve for excess excitation energy in the alpine plant species Ranunculus glacialis L. Plant, Cell Environ 36:1296–1310
Lei T, Feng H, Sun X, Dai QL, Zhang F, Liang HG, Lin HH (2010) The alternative pathway in cucumber seedlings under low temperature stress was enhanced by salicylic acid. Plant Growth Regul 60:35–42
Lennon AM, Prommeenate P, Nixon PJ (2003) Location, expression and orientation of the putative chlororespiratory enzymes, Ndh and IMMUTANS, in higher-plant plastids. Planta 218:254–260
Li Q, Yao Z, Mi H (2016) Alleviation of photoinhibition by co-ordination of chlororespiration and cyclic electron flow mediated by NDH under heat stressed condition in tobacco. Front Plant Sci. 7:285
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV–VIS spectroscopy. In: Wrolstad RE (ed) Current protocols in food analytical chemistry. Wiley, Corvallis, pp F4.3.1–F4.3.8
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668
McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR, Hüner NPA (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim Biophys Acta 1807:954–967
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Nawrocki WJ, Tourasse NJ, Taly A, Rappaport F, Wollman FA (2015) The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Annu Rev Plant Biol 66:49–74
Noguchi K, Yoshida K (2008) Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8:87–99
Paredes M, Quiles MJ (2013) Stimulation of chlororespiration by drought under heat and high illumination in Rosa meillandina. J Plant Physiol 170:165–171
Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523–550
Quiles MJ (2006) Stimulation of chlororespiration by heat and high light intensity in oat plants. Plant, Cell Environ 29:1463–1470
Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant, Cell Environ 30:1041–1051
Sales CRG, Ribeiro RV, Silveira JAG, Machado EC, Martins MO, Lagôa AMMA (2013) Superoxide dismutase and ascorbate peroxidase improve the recovery of photosynthesis in sugarcane plants subjected to water deficit and low substrate temperature. Plant Physiol Biochem 73:326–336
Savitch LV, Ivanov AG, Krol M, Sprott DP, Öquist G, Huner NP (2010) Regulation of energy partitioning and alternative electron transport pathways during cold acclimation of lodgepole pine is oxygen dependent. Plant Cell Physiol 51:1555–1570
Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr Opin Biotechnol 26:25–30
Singh SK, Reddy VR (2015) Response of carbon assimilation and chlorophyll fluorescence to soybean leaf phosphorus across CO2: alternative electron sink, nutrient efficiency and critical concentration. J Photochem Photobiol, B 151:276–284
Su BY, Song YX, Song C, Cui L, Yong TW, Yang WY (2014) Growth and photosynthetic responses of soybean seedlings to maize shading in relay intercropping system in Southwest China. Photosynthetica 52:332–340
Sun X, Wen T (2011) Physiological roles of plastid terminal oxidase in plant stress responses. J Biosci 36:951–956
Sun Y, Liu X, Zhai H, Gao H, Yao Y, Du Y (2016) Responses of photosystem II photochemistry and the alternative oxidase pathway to heat stress in grape leaves. Acta Physiol Plant 38:232
Sun X, Chen XF, Du JB, Yang WY (2017) Expression of genes encoding key components of chlororespiration and cyclic electron transfer in soybean under different light qualities. Photosynthetica. 55:716–720
Suorsa M (2015) Cyclic electron flow provides acclimatory plasticity for the photosynthetic machinery under various environmental conditions and developmental stages. Front Plant Sci 6:800
Tallón C, Quiles MJ (2007) Acclimation to heat and high light intensity during the development of oat leaves increases the NADH DH complex and PTOX levels in chloroplasts. Plant Sci 173:438–445
Thirkettle-Watts D, McCabe TC, Clifton R, Moore C, Finnegan PM, Day DA, Whelan J (2003) Analysis of the alternative oxidase promoters from soybean. Plant Physiol 133:1158–1169
Tikkanen M, Grieco M, Nurmi M, Rantala M, Suorsa M, Aro EM (2012) Regulation of the photosynthetic apparatus under fluctuating growth light. Philos Trans R Soc Lond B Biol Sci 367:3486–3493
Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14:6805–6847
Wang D, Fu A (2016) The plastid terminal oxidase is a key factor balancing the redox state of thylakoid membrane. The Enzymes 40:143–171
Xu F, Yuan S, Lin HH (2011) Response of mitochondrial alternative oxidase (AOX) to light signals. Plant Signal Behav 6:55–58
Yu Q, Feilke K, Krieger-Liszkay A, Beyer P (2014) Functional and molecular characterization of plastid terminal oxidase from rice (Oryza sativa). Biochim Biophys Acta 1837:1284–1292
Zhang DW, Xu F, Zhang ZW, Chen YE, Du JB, Jia SD, Yuan S, Lin HH (2010) Effect of light on cyanide-resistant respiration and alternative oxidase function in Arabidopsis seedlings. Plant, Cell Environ 33:2121–2131
Zou JL, Liu WG, Yuan J, Luo L, Jiang T, Deng YC, Chen XF, Yang CY, Yang WY (2015) Marginal effect on phenotypic plasticity of strip cropping soybean. Chin J Oil Crop Sci 37:661–668
Acknowledgements
We are grateful to Prof. Hong-Hui Lin, Sichuan University, for helpful discussions. This study was funded by the National Key Research and Development Program of China (2016YFD0300209), the National Natural Science Foundation of China (31371555 and 31401308).
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Communicated by L. A. Kleczkowski.
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Sun, X., Liu, MJ., Yang, MY. et al. Implications of terminal oxidases in the regulation of soybean photosynthetic performance under different light intensities. Acta Physiol Plant 39, 266 (2017). https://doi.org/10.1007/s11738-017-2568-5
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DOI: https://doi.org/10.1007/s11738-017-2568-5