Increase of nitrogen to promote growth of poplar seedlings and enhance photosynthesis under NaCl stress

Abstract

The solution culture method was used to study the effect of increasing nitrogen on the growth and photosynthesis of poplar seedlings under 100 mmol L⁻¹ NaCl stress. I Increase in nitrogen reduced stomatal limitation of leaves under NaCl stress, improved utilization of CO₂ by mesophyll cells, enhanced photosynthetic carbon assimilation capacity, significantly alleviated saline damage of NaCl, and promoted the accumulation of aboveground and root biomass. I Increased nitrogen enhanced photochemical efficiency (Ф _PSII) and electron transport rates, relieved the reduction of maximum photochemical efficiency (F _v/F _m) under NaCl, and reduced the degree of photoinhibition caused by NaCl stress. Increased nitrogen applications reduced the proportion of energy dissipating in the form of ineffective heat energy and hence a greater proportion of light energy absorbed by leaves was allocated to photochemical reactions. Under treatment with increased nitrogen, the synergistic effect of heat dissipation and the xanthophyll cycle in the leaves effectively protected photosynthetic PSII and enhanced light energy utilization of leaves under NaCl stress. The increased nitrogen promoted photosynthetic electron supply and transport ability under NaCl stress evident in enhanced functioning of the oxygen-evolving complex on the electron donor side of PS II. It increased the ability of the receptor pool to accept electrons on the PSII electron acceptor side and improved the stability of thylakoid membranes under NaCl stress. Therefore, increasing nitrogen applications under NaCl stress can promote poplar growth by improving the efficiency of light energy utilization.

Keywords

Poplar / Nitrogen / NaCl stress / Photosynthetic characteristics

References

[1] Ali A, Tucker TC, Thompson TL, Salim M. Effects of salinity and mixed ammonium and nitrate nutrition on the growth and nitrogen utilization of barley. J Agron Crop Sci, 2001, 186: 223-228.

[2] Ali S, Rizwan M, Qayyum MF, Ok YS, Ibrmahim M, Riaz M, Arif MS, Hafeez F, Al-webel MI, Shahzad AN. Biochar soil amendment on alleviation of drought and salt stress in plants: a critical review. Environ Sci Pollut Res Int, 2017, 24(14): 12700-12712.

[3] Apse MP, Blumwald E. Na⁺ transport in plants. FEBS Lett, 2007, 581(12): 2247-2254.

[4] Askari H, Edqvist J, Hajheidari M, Kafi M, Salekdeh GH. Effects of salinity levels on proteome of Suaeda aegyptiaca leaves. Proteomics, 2006, 6(8): 2542-2554.

[5] Bhatnagar MP, Vadez V, Sharma KK. Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep, 2008, 27: 411-424.

[6] Calderon JF, Louise EJ, Scow KM, Rolston DE. Microbial response to simulated tillage in cultivated and uncultivated soils. Soil Biol Biochem, 2000, 32(11): 1547-1559.

[7] Chen JQ, Li MQ. The relationship between nitrogen metabolism and photosynthesis in the leaves of higher plants. Plant Physiol Commun, 1984, 1: 1-8.

[8] Cheng YW, Qi YC, Zhu Q, Chen X, Wang N, Zhao X, Chen HY, Cui XJ, Xu LL, Zhang W. New changes in the plasma-membrane-associated proteome of rice roots under salt stress. Proteomics, 2009, 9(11): 3100-3114.

[9] Dąbrowski P, Baczewska AH, Pawluśkiewicz B, Paunov M, Aleksandrov V, Goltsev V, Kalaji MH. Prompt chlorophyll a, fluorescence as a rapid tool for diagnostic changes in PSII structure inhibited by salt stress in Perennial ryegrass. J Photochem Photobiol Biol, 2016, 157(7): 22-31.

[10] Foyer C, Ferrario-Mery S, Noctor G. Lea P, Morot-Gaudry JF. Interactions between carbon and nitrogen metabolism. Plant nitrogen, 2001, Berlin: Springer 237 254

[11] Gong B, Wen D, Vandenlangenberg K, Wei M, Wei M, Yang FJ, Shi QH, Wang XF. Comparative effects of NaCl and NaHCO₃, stress on photosynthetic parameters, nutrient metabolism, and the antioxidant system in tomato leaves. Sci Hortic, 2013, 157(3): 1-12.

[12] Goss R, Bǒhme K, Wihelm C. The xanthophyll cycle of Mantoniella squamata converts violaxathin into antheraxanthin but not to zeaxanthin: consequences for the mechanism of enhanced non-photochemical energy dissipation. Planta, 1998, 205: 613-621.

[13] Govindjee. Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol, 1995, 22: 131-160.

[14] Hendrickson L, Furbank RT, Chow WS. A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res, 2004, 82: 73-81.

[15] Hu YB, Sun GY, Wang XC. Induction characteristics and response of photosynthetic quantum conversion to changes in irradiance in mulberry plants. J Plant Physiol, 2007, 164: 959-968.

[16] Huppe HC, Turpin DH. Intergration of carbon and nitrogen metabolism in plant and algal cells. Annu Rev Plant Physiol Plant Mol Biol, 1994, 45: 577-607.

[17] Klepper LA, Flesher D, Hageman RH. Generation of reduced nicotinamide adenine dinucleotide for nitrate reduction in green leaves. Plant Physiol, 1971, 48: 580-590.

[18] Li HD, Gao HY. Effects of different nitrogen application rate on allocation of photosynthetic electron flux in rumex K-1 leaves. J Plant Physiol Mol Biol, 2007, 33(5): 417-424.

[19] Li XP, Bjorkman O, Shi C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature, 2000, 403: 391-395.

[20] Maxwell K, Johnson GN. Chlorophyll fluorescence-A practical guide. J Exp Bot, 2000, 51(345): 659-668.

[21] Mi GH, Chen JF, Chun L, Guo YF, Tian QY, Zhang FS. Advances in study of factors affecting soil N mineralization in grassland ecosystems. Plant Nutr Fertil Sci, 2007, 13(1): 155-159.

[22] Mitsuya S, Takeoka Y, Miyake H. Effects of sodium chloride on foliar ultrastructure of sweet potato (Ipomoea batatas Lam.) plantlets grown under light and dark conditions in vitro. J Plant Physiol, 2000, 157(6): 661-667.

[23] Munns R, James RA, Läuchli A. Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot, 2006, 57(5): 1025-1043.

[24] Nathawat NS, Kuhad MS, Goswami CL, Patel AL, Kumar R. Interactive effect of N source on salinity on growth indices and ion content of Indian mustard. J Plant Nutr, 2007, 30: 569-598.

[25] Pompeiano A, Giannini V, Gaetani M, Vita F, Guglielminetti L, Bonari E, Volterrani M. Response of warm-season grasses to N fertilization and salinity. Sci Hortic, 2014, 177: 92-98.

[26] Reddy AR, Chaitanya KV, Vivekanandan M. Drought induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol, 2004, 161(11): 1189-1202.

[27] Robinson JM. Carbon dioxide and nitrite photoassimilatory processes do not intercompete for reducing equivalents in spinach and soybean leaf chloroplasts. Plant Physiol, 1986, 80: 676-684.

[28] Shangguan ZP, Shao MA, Dyckmans J. Effect of nitrogen nutrition and water deficit on net photosynthetic rate and chlorophyll fluorescence in winter wheat. J Plant Physiol, 2000, 156(1): 46-51.

[29] Skeffington MJS, Jeffrey DW. Response of America maritime (Mill.)Willd and Plantago martima L. from an Irish salt marsh to nitrogen and salinity. New Phytol, 1988, 110(3): 399-408.

[30] Song J, Feng G, Tian CY, Zhang FS. Osmotic adjustment traits of Suaeda physophora, Haloxylon ammodendron, and Haloxylon persicum, in field or controlled conditions. Plant Sci, 2006, 170(1): 113-119.

[31] Song Y, Zhang YX, Guo N, Sun GY. Effects of lights intensity on chlorophyll fluorescence characteristics and energy allocation pathways in leaves of Populus simonii ×  P. nigra seedlings after chilling stress. J Anhui Agric Sci, 2013, 41(10): 4421-4423.

[32] Strasser BJ. Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res, 1997, 52(2): 147-155.

[33] Strasser RJ, Srivastava A, Govindjee. Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol, 1995, 61(1): 32-42.

[34] Takahashi M, Shigeto J, Sakamoto A, Morikawa H. Selective nitration of PsbO1, PsbO2, and PsbP1 decreases PSII oxygen evolution and photochemical efficiency in intact leaves of Arabidopsis. Plant Signal Behav, 2017 12 10 e1376157

[35] Tian JC, Wang XC, Liu GT. The coupling and regulation between photosynthesis and nitrogen, carbon metablolism in plant. Chin Bull Life Sci, 2010, 13(4): 145-147.

[36] Wang LY, Zhao KF. Effect of NaCl stress on ion compartmentation, photosynthesis and growth of Salicornia bigelovii Torr. J Plant Physiol Mol Biol, 2004, 30(1): 94-98.

[37] Wang BS, Luttg U, Ratajczak R. Effects of salt treatment and osmotic stress on V-ATPase and V-Pase in leaves of the halophyte Suaedasalsa. J Exp Bot, 2001, 52(365): 2355-2365.

[38] Wang CH, Xing XR, Han XG. Advances in study of factors af fecting soil N mineralization in grassland ecosystems. Chin J Appl Ecol, 2004, 15(11): 2184-2188.

[39] Wang XY, Wei SS, Dong ST, Liu P, Zhang JW, Zhao B. Regulation of nitrogen on protein expression of summer maize (Zea mays L.) leaves at filling stage. Sci Agric Sin, 2015, 48(9): 1727-1736.

[40] Wu H, Liu X, You L, Zhang LB, Zhou D, Feng JH, Zhao JM, Yu JB. Effects of salinity on metabolic profiles, gene expressions, and antioxidant enzymes in Halophyte Suaeda salsa. J Plant Growth Regul, 2012, 31(3): 332-341.

[41] Xu N, Zhang HH, Gu SY, Li X, Zhu YW, Yang Y, Liu L, Zhang XL. Effects of increased NO₃ ⁻–N application on PSII functionin leaves of Morus alba seedlings under Na₂CO₃ stress. Prata Cultural Sci, 2017, 34(1): 67-74.

[42] Yamori W, Noguchi KO, Hikosaka K, Terashima I. Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiol, 2010, 152: 388-399.

[43] Yan SH, Ji J, Wang G. Effects of salt stress on plants and the mechanism of salt tolerance. World Sci Technol Res Dev, 2006, 28(4): 70-76.

[44] Yang Y, Ma M, Zheng QS, Liu ZJ, Guo SW. Response of canola seedlings to salt stress under different nitrogen forms. Plant Nutr Fertil Sci, 2012, 18(5): 1220-1227.

[45] Yuan JF, Tian CY, Feng G, Ma HY. Effects of nitrate on the root growth and salt tolerance of Suaeda physophora seedlings under NaCl stress. Plant Nutr Fertil Sci, 2009, 15(4): 953-959.

[46] Zhang HH, Zhong HX, Wang JF, Sui X, Xu N, Gu SY. Adaptive changes in chlorophyll content and photosynthetic features to low light in Physocarpus amurensis Maxim and Physocarpus opulifolius “Diabolo”. Peer J, 2016 4 3 e2125

[47] Zhang HH, Xu N, Li X, GU SY. Overexpression of 2-Cys Prx increased salt tolerance of photosystem II (PSII) in tobacco. Int J Agric Biol, 2017, 19(4): 735-745.

[48] Zhao N, Wang SJ, Ma XJ, Zhu HP, Sa G, Sun J, Li NF, Zhao CJ, Zhao R, Chen SL. Extracellular ATP mediates cellular K⁺/Na⁺, homeostasis in two contrasting poplar species under NaCl stress. Trees, 2016, 30(3): 825-837.

[49] Zhou YH, Lam HM, Zhang JH. Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J Exp Bot, 2007, 5(58): 1207-1217.

[50] Zhu JK. Plant salt tolerance. Trends Plant Sci, 2001, 6(2): 66-71.