Abstract
The effects of the exogenous application of nitric oxide (NO, in the form of sodium nitroprusside, SNP) on the diurnal variation in photosynthesis, chlorophyll content, chlorophyll fluorescence, light response curve and the net assimilation of CO2 against intercellular CO2 concentration (A-Ci) curve parameters were investigated in the leaves of bamboo (Indocalamus barbatus McClure) exposed to simulated acid rain (SAR, pH 3.0) stress. According to the results of the diurnal variation in photosynthesis, foliar applications of 100–400 mg/L SNP effectively inhibited the decrease in net photosynthetic rate (Pn) as a result of non-stomatal factors, and mitigated midday depression under acid rain stress. The mitigating effect was most pronounced at 400 mg/L SNP. However, at higher concentrations of SNP (700 and 1000 mg/L), the mitigating effect became weak and even counterproductive. The results of the chlorophyll content, light response and A-Ci curve parameters suggested that the regulating role of NO against acid rain in the photosynthetic processes occurs through improving not only the efficiency of the light-harvesting and the activity of photosynthetic apparatus, but also the absorption of CO2 and the availability of CO2 for photosynthesis. The results of the chlorophyll fluorescence investigation further indicated that NO protected PSII activity from the damage of acid rain toxicity by enhancing the electron transport activity and photochemical efficiency, especially concerning the increase in the proportion of PSII open reaction centers. Furthermore, NO induced an increase in photorespiration (Rp), rather than an increase in non-photochemical quenching (NPQ), to dissipate the excessive excitation energy, which provided some protection to the photosynthetic apparatus under acid rain stress.
Similar content being viewed by others
References
Asgher M, Per TS, Masood A, Fatma M, Freschi L, Corpas FJ, Khan NA (2016) Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress. Environ Sci Pollut Res. doi:10.1007/s11356-016-7947-8
Athanassios M, Dominique J, Vasileios Z, Georgia T (2016) Citrus plants: a model system for unlocking the secrets of NO and ROS-inspired priming against salinity and drought. Front Plant Sci 7:553
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
Chen J, Wang WH, Liu TW, Wu FH, Zheng HL (2013) Photosynthetic and antioxidant responses of Liquidambar formosana and Schima superba seedlings to sulfuric-rich and nitric-rich simulated acid rain. Plant Physiol Biochem 64:41–51
Coilatz GD (1997) Influence of certain environment factors on photorespiration in Simmondsia chinesis. Planta 134(2):127–132
Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604–611
Cui J, Yue YD, Tang F, Wang J (2011) HPTLC analysis of the flavonoids in eight species of Indocalamus leaves. JPC-J Planar Chromatogr 24(5):394–399
Dolatabadian A, Sanavy SAMM, Gholamhoseini M, Joghan AK, Majdi M, Kashkooli AB (2013) The role of calcium in improving photosynthesis and related physiological and biochemical attributes of spring wheat subjected to simulated acid rain. Physiol Mol Biol Plants 19(2):189–198
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Ann Rev Plant Physiol 33:317–345
Fatma M, Khan NA (2014) Nitric oxide protects photosynthetic capacity inhibition by salinity in Indian mustard. J Funct Environ Bot 4:106–116
Fatma M, Masood A, Per TS, Khan NA (2016a) Nitric oxide alleviates salt stress inhibited photosynthetic performance by interacting with sulfur assimilation in mustard. Front Plant Sci 7:521
Fatma M, Masood A, Per TS, Rasheed F, Khan NA (2016b) Interplay between nitric oxide and sulfur assimilation in salt tolerance in plants. Crop J 4:153–161
Gill SS, Tajrishi M, Madan M, Tuteja N (2013) A DESD-box helicase functions in salinity stress tolerance by improving photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. PB1). Plant Mol Biol 82:1–22
Gong B, Miao L, Kong WJ, Bai JG, Wang XF, Wei M, Shi QH (2014) Nitric oxide, as a downstream signal, plays vital role in auxin induced cucumber tolerance to sodic alkaline stress. Plant Physiol Biochem 83:258–266
Guo ZW, Zhuang MH, Li YC, Chen SL, Yang QP (2015) Adaptability of Indocalamus decorus to climate change based on physiological and biochemical responses to elevated carbon dioxide and ozone. iForest 9:311–317
He XY, Fu SL, Chen W, Zhao TH, Xu S, Tuba Z (2007) Changes in effects of ozone exposure on growth, photosynthesis, and respiration of Ginkgo biloba in Shenyang urban area. Photosynthetica 45(4):555–561
Hu HQ, Wang LH, Liao CY, Fan CX, Zhou Q, Huang XH (2014) Combined effects of lead and acid rain on photosynthesis in soybean seedlings. Biol Trace Elem Res 161:136–142
Jin SL, Yin YG (2012) In vivo antioxidant activity of total flavonoids from Indocalamus leaves in aging mice caused by d-galactose. Food Chem Toxicol 50:3814–3818
Liang CJ, Wang WM (2013) Antioxidant response of soybean seedlings to joint stress of lanthanum and acid rain. Environ Sci Pollut Res 20:8182–8191
Ling DJ, Huang QC, Ouyang Y (2010) Impacts of simulated acid rain on soil enzyme activities in a latosol. Ecotox Environ Safe 73:1914–1918
Liu F, Guo FQ (2013) Nitric oxide deficiency accelerates chlorophyll breakdown and stability loss of thylakoid membranes during dark-induced leaf senescence in Arabidopsis. Plos One 8:1–12
Liu J, Wang J, Wang X, Wang X, Wang R (2012) Regulation of exogenous nitric oxide on photosynthetic physiological response of Lolium perenne seedlings under NaHCO3 stress. Acta Ecol Sinica 32:3460–3466
Liu S, Dong YJ, Xu LL, Kong J (2014) Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings. Plant Growth Regul 73:67–78
Lüttge U, Kluge M, Bauer G (1996) Les cytosomes. In: Botanique: Traité fundamental. Lavoisier, Tec Doc, Paris, p 137–145
Mihailovic N, Drazic G (2011) Incomplete alleviation of nickel toxicity in bean by nitric oxide supplementation. Plant Soil Environ 57:396–401
Misra AN, Misra M, Singh R (2010) Nitric oxide biochemistry, mode of action and signaling in plants. J Med Plant Res 4:2729–2739
Misra AN, Vladkova R, Singh Misra M, Dobrikova AG, Apostolova EL (2014) Action and target sites of nitric oxide in chloroplasts. Nitric Oxide 39:35–45
Molassiotis A, Job D, Ziogas V, Tanou G (2016) Citrus plants: a model system for unlocking the secrets of NO and ROS-inspired priming against salinity and drought. Front Plant Sci 7:229
Procházková D, Haisel D, Wilhelmová N, Pavlíková D, Száková J (2013) Effects of exogenous nitric oxide on photosynthesis. Photosynthetica 51(4):483–489
Sanakis Y, Goussias C, Mason RP, Petrouleas V (1997) NO interacts with the tyrosine radical YD of photosystem II to form an iminoxyl radical. BioChemistry 36:1411–1417
Shi PJ, Xu Q, Sandhu HS, Gielis J, Ding YL, Li HR, Dong XB (2015) Comparison of dwarf bamboos (Indocalamus sp.) leaf parameters to determine relationship between spatial density of plants and total leaf area per plant. Ecol Evol 5(20):4578–4589
Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitricoxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455
Song LL, Ding W, Zhao MG, Sun BT, Zhang LX (2006) Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci 171(4):449–458
Song LL, Yue LL, Zhao HQ, Hou MF (2013) Protection effect of nitric oxide on photosynthesis in rice under heat stress. Acta Physiol Plant 35:3323–3333
State environmental protection administration of China (2005) The state of environment in China in 2004. Environ Prot 6:11–28
Sun ZG, Wang LH, Chen MM, Wang L, Liang CJ, Zhou Q, Huang XH (2012) Interactive effects of cadmium and acid rain on photosynthetic light reaction in soybean seedlings. Ecotox Environ Safe 79:62–68
Sun ZG, Wang LH, Zhou Q, Huang XH (2013) Effects and mechanisms of the combined pollution of lanthanum and acid rain on the root phenotype of soybean seedlings. Chemosphere 93:344–352
Tong GH, Liu TJ, Huang W (2005) Effect of simulated acid rain and its acidified soil on lipid peroxidation of wheat seedlings. Acta Ecol Sin 25:1510–1518 (Chinese)
Vladkova R, Dobrikova AG, Singh R, Misra AN, Apostolova E (2011) chloroplast thylakoid membranes treated with NO donor SNP: changes in flash oxygen evolution and chlorophyll fluorescence. Nitric Oxide 24:84–90
Wang M, Li QR, Fu SL, Dong BL (2005) Effects of exogenous nitric oxide on photosynthetic characteristics of poplar leaves under water stress. Chin J Appl. Eco 16:218–222 (Chinese)
Wang Q, Liang X, Dong Y, Xu L, Zhang X, Hou J, Fan ZY (2013) Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regul 69:11–20
Wang LH, Wang W, Zhou Q, Huang XH (2014) Combined effects of lanthanum(III) chloride and acid rain on photosynthetic parameters in rice. Chemosphere 112:355–361
Wang LN, Yang XY, Ren ZH, Hu XY, Wang XF (2015) Alleviation of photosynthetic inhibition in copper-stressed tomatoes through rebalance of ion content by exogenous nitric oxide. Turk J Bot 39:10–22
Wu XX, Ding HD, Chen JL, Zhang HJ, Zhu WM (2010) Attenuation of salt-induced changes in photosynthesis by exogenous nitric oxide in tomato (Lycopersicon esculentum Mill. L.) seedlings. Afr J Biotech 9:7837–7846
Yang W, Sun Y, Chen S, Jiang J, Chen F, Fang W, Liu Z (2011) The effect of exogenously applied nitric oxide on photosynthesis and antioxidant activity in heat stressed chrysanthemum. Biol Plant 55(4):737–740
Yang LT, Qi YP, Chen LS, Sang W, Lin XJ, Wu YL, Yang CJ (2012) Nitric oxide protects sour pummelo (Citrus grandis) seedlings against aluminum-induced inhibition of growth and photosynthesis. Environ Exp Bot 82:1–13
Zhang LX, Qiang H, Li SQ, Chen XL (2010) Effects of enhanced atmospheric ammonia on photosynthetic characteristics of two maize (Zea mays L.) cultivars with various nitrogen supply across long-term growth period and their diurnal change patterns. Photosynthetica 48(3):389–399
Acknowledgements
The present study was funded by National Science and Technology Ministry (2015BAD04B02) and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD). We thank LetPub (http://www.letpub.com) for their linguistic assistance during the preparation of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, T., Yang, W., Xie, Y. et al. Effects of exogenous nitric oxide on the photosynthetic characteristics of bamboo (Indocalamus barbatus McClure) seedlings under acid rain stress. Plant Growth Regul 82, 69–78 (2017). https://doi.org/10.1007/s10725-016-0239-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-016-0239-y