Chin J Plan Ecolo ›› 2016, Vol. 40 ›› Issue (6): 543-553.doi: 10.17521/cjpe.2015.0420

• Research Articles • Previous Articles     Next Articles

Effects of night warming on the uptake of inorganic nitrogen by two dominant species in subalpine coniferous forests

Bo TANG1,2, Huan YANG1,2, Chun-Ying YIN1,*(), Yu-Yu SUN1,2, Dong-Hui ZHENG1,2, Qing LIU1   

  1. 1Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China

    2University of Chinese Academy of Sciences, Beijing 100049, China
  • Received:2015-11-22 Accepted:2016-03-26 Online:2016-06-15 Published:2016-06-30
  • Contact: Chun-Ying YIN E-mail:yincy@cib.ac.cn

Abstract:

Aims Plant roots play a critical role in the uptake of nutrients, and nitrogen (N) absorption is considered as the first step and a pivotal process in N metabolism of plants. Our objective was to better understand the absorption of two major inorganic N forms (NH4+ and NO3-) in subalpine coniferous forests under global warming Methods Experimental warming using infrared heater was applied to two dominant species in subalpine coniferous forests of Sichuan, China, Picea asperata and Abies fargesiivar. faxoniana. The non-invasive micromeasurement technology was used to investigate the effects of warming on the uptake rates of NH4+ and NO3- and the potential interactions between these two ions.Important findings Results showed that the maximal net root uptake of NH4+ and NO3-occurred at a distance of 17-18 mm and 17 mm from root tips, respectively for P. asperata. and at a distance of 11 mm and 11.5 mm from root tips respectively for A. fargesiivar. faxoniana. Experimental warming elevated the uptake rates of NH4+ and NO3- in both species, but the interactions between NH4+ and NO3- differed between the two species. While NO3- uptake was inhibited in the presence of NH4+ for both P. asperataand A. fargesiivar. faxoniana, net NH4+ uptake was promoted by NO3- supply only in P. asperata roots under experimental warming.

Key words: night warming, N absorption, conifer tree, subalpine forest

Fig. 1

Effects of night warming on soil pH value (A), soil NO3--N (B) and NH4+-N concentration (C) (mean ± SE, n = 4). Different lowercase letters indicate significant differences between Picea asperata and Abies fargesii var. faxoniana under control (p < 0.05); Different capital letters indicate significant differences between P. asperata and A. fargesii var. faxoniana under night warming (p < 0.05); Asterisks indicate significant differences between night warming and control (*, p < 0.05; **, p < 0.01). PA, Picea asperata; AF, Abies fargesii var. faxoniana."

Fig. 2

Net NH4+ (A) and NO3- (B) fluxes along the root tip of Picea asperata (mean ± SE, n = 4). Positive and negative values indicate net influxes and effluxes, respectively. The measuring solution contained 1 mmol·L-1 KCl and 0.1 mmol·L-1 CaCl2 with pH equal to 5.5, and either 0.1 mmol·L-1 NH4Cl for NH4+ flux measurements or 0.1 mmol·L-1 KNO3 for NO3- flux measurements."

Fig. 3

Net NH4+ (A) and NO3- (B) fluxes along the root tip of Abies fargesii var. faxoniana (mean ± SE, n = 4). Positive and negative values indicate net influxes and effluxes, respectively. The measuring solution contained 1 mmol·L-1 KCl and 0.1 mmol·L-1 CaCl2 with pH equal to 5.5, and either 0.1 mmol·L-1 NH4Cl for NH4+ flux measurements or 0.1 mmol·L-1 KNO3 for NO3- flux measurements."

Fig. 4

Net root NH4+ influxes at the distance of 17-18 mm from the root tip of Picea asperata (A) and at the distance of 11 mm from the root tip of Abies fargesii var. faxoniana (B) in NH4NO3 measuring solution (0.1 mmol·L-1 NH4NO3, 1 mmol·L-1 KCl, 0.1 mmol·L-1 CaCl2, pH 5.5) and NH4Cl measuring solution (0.1 mmol·L-1 NH4Cl, 1 mmol·L-1 KCl, 0.1 mmol·L-1 CaCl2, pH 5.5) (mean ± SE, n = 4). Different lowercase and capital letters indicate significant effect (p < 0.05) of night warming on net NH4+ influxes measured in NH4NO3 and NH4Cl measuring solution, respectively. Asterisks indicate significant differences between the net NH4+ influxes measured in NH4NO3 and in NH4Cl solution (***, p < 0.005)."

Fig. 5

Net NO3- influxes at a distance of 17 mm from the root tip of Picea asperata (A) and at a distance of 11.5 mm from the root tip of Abies fargesii var. faxoniana (B) in NH4NO3 measuring solution (0.1 mmol·L-1 NH4NO3, 1 mmol·L-1 KCl, 0.1 mmol·L-1 CaCl2, pH 5.5) and KNO3 measuring solution (0.1 mmol·L-1 KNO3, 1 mmol·L-1 KCl, 0.1 mmol·L-1 CaCl2, pH 5.5) (mean ± SE, n = 4). Different lowercase and capital letters indicate significant effect (p < 0.05) of night warming on net NO3- influxes measured in NH4NO3 and KNO3 measuring solution, respectively. Asterisks indicate significant differences between the net NO3- influxes measured in NH4NO3 and in KNO3 solution (***, p < 0.005)."

[1] Alber A, Ehlting B, Ehlting J, Hawkins BJ, Rennenberg H (2012). Net NH4+ and NO3- flux, and expression of NH4+ and NO3- transporters in roots of Picea glauc.Trees, 26, 1403-1411.
[2] Babourina O, Voltchanskii K, Mcgann B, Newman I, Rengel Z (2007). Nitrate supply affects ammonium transport in canola roots.Journal of Experimental Botany, 58, 651-658.
[3] Bai WM, Wan SQ, Niu SL, Liu WX, Chen QS, Wang QB, Zhang WH, Han XG, Li LH (2010). Increased temperature and precipitation interact to affect root production, mortality, and turnover in a temperate steppe: Implications for ecosystem C cycling.Global Change Biology, 16, 1306-1316.
[4] Berges JA, Varela DE, Harrison PJ (2002). Effects of temper- ature on growth rate, cell composition and nitrogen metabolism in the marine diatom Thalassiosira pseudo- nana (Bacillariophyceae).Marine Ecology Progress Series, 225, 139-146.
[5] Bloom AJ, Meyerhoff PA, Taylor AR, Rost TL (2002). Root development and absorption of ammonium and nitrate from the rhizosphere.Journal of Plant Growth Regulation, 21, 416-431.
[6] Britto DT, Kronzucker HJ (2006). Futile cycling at the plasma membrane: A hallmark of low-affinity nutrient transport.Trends in Plant Science, 11, 529-534.
[7] Calatayud A, Gorbe E, Roca D, Martinez PF (2008). Effect of two nutrient solution temperatures on nitrate uptake, nitrate reductase activity, NH4+ concentration and chlorophyll a fluorescence in rose plants.Environmental and Experimental Botany, 64, 65-74.
[8] Colmer TD, Bloom AJ (1998). A comparison of NH4+ and NO3- net fluxes along roots of rice and maize.Plant, Cell & Environment, 21, 240-246.
[9] Cruz C, Lips SH, Martinsloucao MA (1995). Uptake regions of inorganic nitrogen in roots of carob seedlings.Physiologia Plantarum, 95, 167-175.
[10] Easterling DR, Horton B, Jones PD, Peterson TC, Karl TR, Parker DE, Salinger MJ, Razuvayev V, Plummer N, Jamason P, Folland CK (1997). Maximum and minimum temperature trends for the globe.Science, 277, 364-367.
[11] Elmendorf SC, Henry GHR, Hollister RD, Bjork RG, Bjorkman AD, Callaghan TV, Collier LS, Cooper EJ, Cornelissen JHC, Day TA, Fosaa AM, Gould WA, Gretarsdottir J, Harte J, Hermanutz L, Hik DS, Hofgaard A, Jarrad F, Jonsdottir IS, Keuper F, Klanderud K, Klein JA, Koh S, Kudo G, Lang SI, Loewen V, May JL, Mercado J, Michelsen A, Molau U, Myers-Smith IH, Oberbauer SF, Pieper S, Post E, Rixen C, Robinson CH, Schmidt NM, Shaver GR, Stenstrom A, Tolvanen A, Totland O, Troxler T, Wahren CH, Webber PJ, Welker JM, Wookey PA (2012). Global assessment of experimental climate warming on tundra vegetation: Heterogeneity over space and time.Ecology Letters, 15, 164-175.
[12] Enstone DE, Peterson CA, Hallgren SW (2001). Anatomy of seedling tap roots of loblolly pine (Pinus taeda L.).Trees, 15, 98-111.
[13] Fang YY, Babourina O, Rengel Z, Yang XE, Pu PM (2007). Spatial distribution of ammonium and nitrate fluxes along roots of wetland plants.Plant Science, 173, 240-246.
[14] Forde BG, Walch-Liu P (2009). Nitrate and glutamate as environmental cues for behavioural responses in plant roots.Plant, Cell & Environment, 32, 682-693.
[15] Gao Y, Smith GJ, Alberte RS (2000). Temperature dependence of nitrate reductase activity in marine phytoplankton: Biochemical analysis and ecological implications. Journal of Phycology, 36, 304-313.
[16] Garnett TP, Shabala SN, Smethurst PJ, Newman IA (2001). Simultaneous measurement of ammonium, nitrate and proton fluxes along the length of eucalypt roots.Plant and Soil, 236, 55-62.
[17] Garnett TP, Shabala SN, Smethurst PJ, Newman IA (2003). Kinetics of ammonium and nitrate uptake by eucalypt roots and associated proton fluxes measured using ion selective microelectrodes.Functional Plant Biology, 30, 1165-1176.
[18] Gobert A, Plassard C (2007). Kinetics of NO3- net fluxes in Pinus pinaster, Rhizopogon roseolus and their ectomy- corrhizal association, as affected by the presence of NH4+ and NO3-.Plant, Cell & Environment, 30, 1309-1319.
[19] Hawkins BJ, Boukcim H, Plassard C (2008). A comparison of ammonium, nitrate and proton net fluxes along seedling roots of Douglas-fir and lodgepole pine grown and measured with different inorganic nitrogen sources.Plant, Cell & Environment, 31, 278-287.
[20] Hawkins BJ, Robbins S (2010). pH affects ammonium, nitrate and proton fluxes in the apical region of conifer and soybean roots.Physiologia Plantarum, 138, 238-247.
[21] He JL, Qin JJ, Long LY, Ma YL, Li H, Li K, Jiang XN, Liu TX, Polle A, Liang ZS, Luo ZB (2011). Net cadmium flux and accumulation reveal tissue specific oxidative stress and detoxification in Populus ×canescens. Physiologia Plantarum, 143, 50-63.
[22] Henriksen GH, Raman DR, Walker LP, Spanswick RM (1992). Measurement of net fluxes of ammonium and nitrate at the surface of barley roots using ion-selective microelec- trodes. 2. Patterns of uptake along the root axis and evaluation of the microelectrode flux estimation technique.Plant Physiology, 99, 734-747.
[23] Ikeda M, Beitz E, Kozono D, Guggino WB, Agre P, Yasui M (2002). Characterization of aquaporin-6 as a nitrate channel in mammalian cells—Requirement of pore-lining residue threonine 63.Journal of Biological Chemistry, 277, 39873-39879.
[24] IPCC (2014). Climate change 2014: Synthesis report. In: Pachauri RK, Meyer LA eds. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland. 151.
[25] Jackson LE, Burger M, Cavagnaro TR (2008). Roots nitrogen transformations, and ecosystem services.Annual Review of Plant Biology, 59, 341-363.
[26] Johnson DW (2006). Progressive N limitation in forests: Review and implications for long-term responses to elevated CO2.Ecology, 87, 64-75.
[27] Kronzucker HJ, Siddiqi MY, Glass ADM, Kirk GJD (1999). Nitrate-ammonium synergism in rice. A subcellular flux analysis.Plant Physiology, 119, 1041-1045.
[28] Li Q, Li BH, Kronzucker HJ, Shi WM (2010). Root growth inhibition by NH4+ in Arabidopsis is mediated by the root tip and is linked to NH4+ efflux and GMPase activity.Plant, Cell & Environment, 33, 1529-1542.
[29] Liu Q, Wu Y, He H (2001). Ecological problems of subalpine coniferous forest in the southwest of China.World Sci-Tech Research and Development, 23(2), 63-69. (in Chinese with English abstract)[刘庆, 吴彦, 何海 (2001). 中国西南亚高山针叶林的生态学问题. 世界科技研究与发展, 23(2), 63-69.]
[30] Luo Y, Wan S, Hui D, Wallace LL (2001). Acclimatization of soil respiration to warming in a tall grass prairie.Nature, 413, 622-625.
[31] Luo J, Qin J, He FF, Li H, Liu T, Polle A, Perg L, Luo ZB (2013). Net fluxes of ammonium and nitrate in association with H+ fluxes in fine roots of Populus popularis.Planta, 237, 919-931.
[32] Majdi H, Ohrvik J (2004). Interactive effects of soil warming and fertilization on root production, mortality, and longevity in a Norway spruce stand in Northern Sweden.Global Change Biology, 10, 182-188.
[33] Melillo JM, Butler S, Johnson J, Mohan J, Steudler P, Lux H, Tang J (2011). Soil warming, carbon-nitrogen interactions, and forest carbon budgets.Proceedings of the National Academy of Sciences of the United States of America, 108, 9508-9512.
[34] Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson AG, Escobar MA (2010). Distinct signalling pathways and tra- nscriptome response signatures differentiate ammonium- and nitrate-supplied plants.Plant, Cell & Environment, 33, 1486-1501.
[35] Peng SB, Huang JL, Sheehy JE, Laza RC, Visperas RM, Zhong XH, Centeno GS, Khush GS, Cassman KG (2004). Rice yields decline with higher night temperature from global warming.Proceedings of the National Academy of Sciences of the United States of America, 101, 9971-9975.
[36] Penuelas J, Sardans J, Estiarte M, Ogaya R, Carnicer J, Coll M, Barbeta A, Rivas-Ubach A, Llusia J, Garbulsky M, Filella I, Jump AS (2013). Evidence of current impact of climate change on life: A walk from genes to the biosphere.Global Change Biology, 19, 2303-2338.
[37] Plassard C, Guerin-Laguette A, Very AA, Casarin V, Thibaud JB (2002). Local measurements of nitrate and potassium fluxes along roots of maritime pine. Effects of ectomycorrhizal symbiosis.Plant, Cell & Environment, 25, 75-84.
[38] Pregitzer KS, Deforest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002). Fine root architecture of nine North American trees.Ecological Monographs, 72, 293-309.
[39] Sardans J, Peñuelas J, Prieto P, Estiarte M (2008). Drought and warming induced changes in P and K concentration and accumulation in plant biomass and soil in a Mediterranean shrubland.Plant and Soil, 306, 261-271.
[40] Sorgona A, Lupini A, Mercati F, Di Dio L, Sunseri F, Abenavoli MR (2011). Nitrate uptake along the maize primary root: An integrated physiological and molecular approach.Plant, Cell & Environment, 34, 1127-1140.
[41] Tang B, Yin CY, Wang YJ, Sun YY, Liu Q (2016). Positive effects of night warming on physiology of coniferous trees in late growing season: Leaf and root.Acta Oecologica, 73, 21-30.
[42] Taylor AR, Bloom AJ (1998). Ammonium, nitrate, and proton fluxes along the maize root.Plant, Cell & Environment, 21, 1255-1263.
[43] Vidmar JJ, Zhuo D, Siddiqi MY, Schjoerring JK, Touraine B, Glass ADM (2000). Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiology, 123, 307-318.
[44] Walch-Liu P, Forde BG (2008). Nitrate signalling mediated by the NRT1.1 nitrate transporter antagonises L-glutamate- induced changes in root architecture.Plant Journal, 54, 820-828.
[45] Walker MD, Wahren CH, Hollister RD, Henry GHR, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB, Epstein HE, Jonsdottir IS, Klein JA, Mag- nusson B, Molau U, Oberbauer SF, Rewa SP, Robinson CH, Shaver GR, Suding KN, Thompson CC, Tolvanen A, Totland O, Turner PL, Tweedie CE, Webber PJ, Wookey PA (2006). Plant community responses to experimental warming across the tundra biome.Proceedings of the National Academy of Sciences of the United States of America, 103, 1342-1346.
[46] Wall GW, Kimball BA, White JW, Ottman MJ (2011). Gas exchange and water relations of spring wheat under full-season infrared warming.Global Change Biology, 17, 2113-2133.
[47] Wan S, Luo Y, Wallace L (2002). Changes in microclimate induced by experimental warming and clipping in tallgrass prairie.Global Change Biology, 8, 754-768.
[48] Wang AF, Roitto M, Lehto T, Zwiazek JJ, Calvo-Polanco M, Repo T (2013). Waterlogging under simulated late-winter conditions had little impact on the physiology and growth of Norway spruce seedlings.Annals of Forest Science, 70, 781-790.
[49] Wang KY (2004). Processes of Subalpine Forest Ecosystem in Western Sichuan. Sichuan Science and Technology Press, Chengdu. (in Chinese)[王开运 (2004). 川西亚高山森林群落生态系统过程. 四川科学技术出版社, 成都.]
[50] Xia J, Han Y, Zhang Z, Zhang Z, Wan S (2009). Effects of diurnal warming on soil respiration are not equal to the summed effects of day and night warming in a temperate steppe.Biogeosciences, 6, 1361-1370.
[51] Xu Y, Sun T, Yin LP (2006). Application of non-invasive microsensing system to simultaneously measure both H+ and O2 fluxes around the pollen tube.Journal of Integrative Plant Biology, 48, 823-831.
[52] Xu GH, Fan XR, Miller AJ (2012). Plant nitrogen assimilation and use efficiency.Annual Review of Plant Biology, 63, 153-182.
[53] Yin CY, Pu XZ, Xiao QY, Zhao CZ, Liu Q (2014). Effects of night warming on spruce root around non-growing season vary with branch order and month.Plant and Soil, 380, 249-263.
[54] Young EB, Dring MJ, Savidge G, Birkett DA, Berges JA (2007). Seasonal variations in nitrate reductase activity and internal N pools in intertidal brown algae are correlated with ambient nitrate concentrations. Plant, Cell & Environment, 30, 764-774.
[55] Yu XZ, Zhang FZ (2012). Activities of nitrate reductase and glutamine synthetase in rice seedlings during cyanide metabolism.Journal of Hazardous Materials, 225, 190-194.
[56] Zhao CZ, Liang J, He J, Liu Q (2012). Effects of elevated temperature and nitrogen fertilization on nitrogen metabolism and nutrient status of two coniferous species.Soil Science and Plant Nutrition, 58, 772-782.
[57] Zhuo DG, Okamoto M, Vidmar JJ, Glass ADM (1999). Regulation of a putative high-affinity nitrate transporter (Nrt2;1At) in roots of Arabidopsis thaliana.Plant Journal, 17, 563-568.
[1] GUO Cai-Hong, YANG Wan-Qin, WU Fu-Zhong, XU Zhen-Feng, YUE Kai, NI Xiang-Yin, YUAN Ji, YANG Fan, TAN Bo. Effects of forest gap size on initial decomposition of twig litter in the subalpine forest of western Sichuan, China [J]. Chin J Plan Ecolo, 2018, 42(1): 28-37.
[2] Kai-Jun YANG, Wan-Qin YANG, Yu TAN, Ruo-Yang HE, Li-Yan ZHUANG, Zhi-Jie LI, Bo TAN, Zhen-Feng XU. Short-term responses of winter soil respiration to snow removal in a Picea asperata forest of western Sichuan [J]. Chin J Plan Ecolo, 2017, 41(9): 964-971.
[3] Jinhong Yuan, Jingrui Li, Haiyan Zhang. Structure and Function of Copper Transporters in Plants [J]. Chin Bull Bot, 2016, 51(6): 849-858.
[4] LI Han,WU Fu-Zhong,YANG Wan-Qin,XU Li-Ya,NI Xiang-Yin,HE Jie,HU Yi. Effects of forest gap on hemicellulose dynamics during foliar litter decomposition in an subalpine forest [J]. Chin J Plan Ecolo, 2015, 39(3): 229-238.
[5] HE Jie, YANG Wan-Qin, NI Xiang-Yin, LI Han, XU Li-Ya, and WU Fu-Zhong. Effects of snow patch on the dynamics of potassium and sodium during litter decomposition in winter in a subalpine forest of western Sichuan [J]. Chin J Plan Ecolo, 2014, 38(6): 550-561.
[6] Xiaoli Yan, Weikai Bao. Ground bryophyte diversity in secondary birch forests in western Sichuan, China [J]. Biodiv Sci, 2011, 19(3): 327-334.
[7] LIU En-Ke, MEI Xu-Rong, GONG Dao-Zhi, YAN Chang-Rong, ZHUANG Yan. Effects of drought on N absorption and utilization in winter wheat at different developmental stages [J]. Chin J Plan Ecolo, 2010, 34(5): 555-562.
[8] CHEN Zhi, YIN Hua-Jun, WEI Yun-Yan, LIU Qing. Short-term effects of night warming and nitrogen addition on soil available nitrogen and microbial properties in subalpine coniferous forest, Western Sichuan, China [J]. Chin J Plan Ecolo, 2010, 34(11): 1254-1264.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] . [J]. Chin Bull Bot, 2002, 19(01): 121 -124 .
[2] ZHANG Shi-Gong;GAO Ji-Yin and SONG Jing-Zhi. Effects of Betaine on Activities of Membrane Protective Enzymes in Wheat (Triticum aestivum L.) Seedlings Under NaCl Stress[J]. Chin Bull Bot, 1999, 16(04): 429 -432 .
[3] SHE Chao-WenSONG Yun-Chun LIU Li-Hua. Analysis on the G_banded Karyotypes and Its Fluctuation at Different Mitotic Phases and Stages in Triticum tauschii (Aegilops squarrosa)[J]. Chin Bull Bot, 2001, 18(06): 727 -734 .
[4] Guijun Yang, Wenjiang Huang, Jihua Wang, Zhurong Xing. Inversion of Forest Leaf Area Index Calculated from Multi-source and Multi-angle Remote Sensing Data[J]. Chin Bull Bot, 2010, 45(05): 566 -578 .
[5] Man Chen, YishengTu, Linan Ye, Biyun Yang. Effect of Amino Acids on Thallus Growth and Huperzine-A Accumulation in Huperzia serrata[J]. Chin Bull Bot, 2017, 52(2): 218 -224 .
[6] Yefei Shang, Ming Li, Bo Ding, Hao Niu, Zhenning Yang, Xiaoqiang Chen, Gaoyi Cao, Xiaodong Xie. Advances in Auxin Regulation of Plant Stomatal Development[J]. Chin Bull Bot, 2017, 52(2): 235 -240 .
[7] CUI Xiao-Yong, Du Zhan-Chi, Wang Yan-Fen. Photosynthetic Characteristics of a Semi-arid Sandy Grassland Community in Inner Mongolia[J]. Chin J Plan Ecolo, 2000, 24(5): 541 -546 .
[8] LI Wei, ZHANG Ya-Li, HU Yuan-Yuan, YANG Mei-Sen, WU Jie, and ZHANG Wang-Feng. Research on the photoprotection and photosynthesis characteristics of young cotton leaves under field conditions[J]. Chin J Plan Ecolo, 2012, 36(7): 662 -670 .
[9] WEI Jie, YU Hui, KUANG Ting-Yun, BEN Gui-Ying. Ultrastructure of Polygonum viviparum L. Grown at Different Elevations on Qinghai Plateau[J]. Chin J Plan Ecolo, 2000, 24(3): 304 -307 .
[10] CHEN Jin, LI Yang, HUANG Jian-Hui. Decomposition of mixed litter of four dominant species in an Inner Mongolia steppe[J]. Chin J Plan Ecolo, 2011, 35(1): 9 -16 .