NODULE CHARACTERISTICS OF THREE-YEAR-OLD CARAGANA MICROPHYLLA AND THEIR RESPONSES TO ENVIRONMENTAL CHANGES IN AN INNER MONGOLIA GRASSLAND

doi:10.3773/j.issn.1005-264x.2009.06.017

Abstract

Abstract:

Aims Caragana microphylla widely spreads in Inner Mongolia grasslands as a dominant shrubby legume. Its nodule growth has been poorly addressed. Our objective is to examine nodule characteristics and their responses to different environmental factors to provide insights into their nitrogen fixing and nitrogen cycling processes under future changing environments.

Methods We conducted a field experiment in 2008 using open-top chambers at the Inner Mongolia Grassland Ecosystem Research Station of Chinese Academy of Sciences. We examined the number, weight and length of nodules of three-year-old C. microphylla individuals and their responses to nitrogen addition, drought, water addition and elevated atmospheric CO₂ concentration.

Important findings Nodules were mainly distributed in lateral roots, and most had buff or brown color. Nodule shapes were diverse, being pyriform, globular, claviform, fusiform, and Y shaped. Root growth and nodule growth were significantly inhibited under the nitrogen addition treatment, resulting in roots being whitened and most nodules dead and black-brown. Drought depressed root nodulation, with mean length of nodules decreased significantly by 50.4% compared with that under normal water supply. Water addition stimulated root growth and nodule growth. Roots nodulated best under the combined treatment of water addition, elevated CO₂ and non-nitrogen addition, with maximum mean length and weight of individual nodules and the maximum nodule weight per plant. Nodules in fibers relatively increased with increasing water supply. Nodule growth did not significantly respond to elevated CO₂. Nodule number is more sensitive to environmental changes than nodule size, there are significant nitrogen × water interactions on nodule number and weight per plant and the effects of three environmental factors on nodule growth are different. The negative effect of nitrogen is larger than the positive effects of water and elevated CO ₂. It is inferred that water is the major factor affecting the infection of rhizobia and the generation of nodules in this semiarid grassland ecosystem.

Key words: grassland ecosystem, Caragana microphylla, nodule, nitrogen addition, soil water levels, elevated atmospheric CO₂ concentration

ZHANG Can-Juan, WU Dong-Xiu, ZHANG Lin, ZHAN Xiao-Yun, ZHOU Shuang-Xi, YANG Yun-Xia. NODULE CHARACTERISTICS OF THREE-YEAR-OLD CARAGANA MICROPHYLLA AND THEIR RESPONSES TO ENVIRONMENTAL CHANGES IN AN INNER MONGOLIA GRASSLAND[J]. Chin J Plant Ecol, 2009, 33(6): 1165-1176.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.3773/j.issn.1005-264x.2009.06.017

https://www.plant-ecology.com/EN/Y2009/V33/I6/1165

Figures/Tables 4

References 49

[1]	Almeida JPF, Hartwig UA, Frehner M, Nosberger J, Luscher A (2000). Evidence that P deficiency induces N feedback regulation of symbiotic N ₂ fixation in white clover ( Trifolium repens L.). Journal of Experimental Botany, 51,1289-1297. URL PMID
[2]	Aranjuelo I, Irigoyen JJ, Nogues S, Sanchez-Diaz M (2009). Elevated CO ₂ and water-availability effect on gas exchange and nodule development in N ₂-fixing alfalfa plants. Environmental and Experimental Botany, 65,18-26. DOI URL
[3]	Armstrong RD, Kuskopf BJ, Millar G, Whitbread AM, Standley J (1999). Changes in soil chemical and physical properties following legumes and opportunity cropping on a cracking clay soil. Australian Journal of Experimental Agriculture, 39,445-456. DOI URL
[4]	Arnone JA, Gordon JC (1990). Effect of nodulation, nitrogen fixation and CO ₂ enrichment on the physiology, growth and dry mass allocation of seedlings of Alnus rubra Bong. New Phytologist, 116,55-66. DOI URL
[5]	Bai YF, Han XG, Wu JG, Chen ZG, Li LH (2004). Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature, 431,181-184. URL PMID
[6]	Becker M, Diekmann KH, Ladha JK, Dedatta SK, Ottow JCG (1991). Effect of NPK on growth and nitrogen fixation of Sesbania rostrata as a green manure for lowland rice ( Oryza sativa L.). Plant and Soil, 132,149-158. DOI URL
[7]	Bordeleau LM, Prévost D (1994). Nodulation and nitrogen fixation in extreme environments. Plant and Soil, 161,115-125.
[8]	Chen SP (陈世苹), Bai YF (白永飞), Han XG (韩兴国), An JL (安吉林), Guo FC (郭富存) (2004). Variations in foliar carbon isotope composition and adaptive strategies of Carex korshinskyi along a soil moisture gradient. Acta Phytoecologica Sinica(植物生态学报), 28,515-522. (in Chinese with English abstract)
[9]	Djekoun A, Planchon C (1991). Water status effect on dinitrogen fixation and photosynthesis in soybean. Agronomy Journal, 83,316-322.
[10]	Ebersberger D, Niklaus PA, Kandeler E (2003). Long term CO ₂ enrichment stimulates N-mineralisation and enzyme activities in calcareous grassland. Soil Biology & Biochemistry, 35,965-972.
[11]	Editorial Group of Inner Mongolia Flora (内蒙古植物志编写组) (1977). Flora China Intramongolicae (内蒙古植物志). Vol.3. Inner Mongolia People’s Press, Huhhot, 29, 175. (in Chinese)
[12]	Glasener KM, Wagger MG, Mackown CT, Volk RJ (2002). Contributions of shoot and root nitrogen-15 labeled legume nitrogen sources to a sequence of three cereal crops. Soil Science Society of America Journal, 66,523-530.
[13]	Goi SR, Sprent JI, JacobNeto J (1997). Effect of different sources of N ₂ on the structure of Mimosa caesalpiniaefolia root nodules. Soil Biology & Biochemistry, 29,983-987.
[14]	Graham PH (1992). Stress tolerance in rhizobium and bradyrhizobium, and nodulation under adverse soil- conditions. Canadian Journal of Microbiology, 38,475-484.
[15]	Haase S, Neumann G, Kania A, Kuzyakov Y, Romheld V, Kandeler E (2007). Elevation of atmospheric CO ₂ and N-nutritional status modify nodulation, nodule-carbon supply, and root exudation of Phaseolus vulgaris L. Soil Biology & Biochemistry, 39,2208-2221.
[16]	Hafner H, Ndunguru BJ, Bationo A, Marschner H (1992). Effect of nitrogen, phosphorus and molybdenum application on growth and symbiotic N ₂-fixation of groundnut in an acid sandy soil in Niger. Fertilizer Research, 31,69-77.
[17]	Hartwig UA, Sadowsky MJ (2006). Biological nitrogen fixation:a key process for the response of grassland ecosystems to elevated atmospheric [CO ₂]. In:Nösberger J, Long SP, Norby RJ, Stitt M, Hendrey GR, Blum H eds. Ecological Studies. Heidelberg, Springer, Berlin, 325-336.
[18]	He HB (何恒斌), Hao YG (郝玉光), Ding Q (丁琼), Jia GX (贾桂霞) (2006). Characteristics of plant community of Ammopiptanthus mongolicus and the diversity of its nodules. Journal of Beijing Forestry University (北京林业大学学报), 28,123-128. (in Chinese with English abstract)
[19]	Hu SJ, Tu C, Chen X, Gruver JB (2006). Progressive N limitation of plant response to elevated CO ₂: a microbiological perspective. Plant and Soil, 289,47-58.
[20]	Hua L (华珞), He ZJ (何忠俊), Wei DP (韦东普), Chen SB (陈世宝), Bai LY (白玲玉) (2003). Influences of the compound effects between nitrogen and zinc on growth, N-fixation and transfer of fixed nitrogen of white clover in mixed culture. Acta Ecologica Sinica(生态学报), 23,264-270. (in Chinese with English abstract)
[21]	Huang CY, Boyer JS, Vanderhoef LN (1975). Limitation of acetylene reduction (nitrogen-fixation) by photosynthesis in soybean having low water potentials. Plant Physiology, 56,228-232. DOI URL PMID
[22]	Hungate BA, Dijkstra P, Johnson DW, Hinkle CR, Drake BG (1999). Elevated CO ₂ increases nitrogen fixation and decreases soil nitrogen mineralization in Florida scrub oak. Global Change Biology, 5,781-789.
[23]	Hungate BA, Stiling PD, Dijkstra P, Johnson DW, Ketterer ME, Hymus GJ, Hinkle CR, Drake BG (2004). CO ₂ elicits long-term decline in nitrogen fixation. Science, 304,1291-1291. URL PMID
[24]	IPCC (2007). Climate Chang 2007: the Physical Science Basis. Contribution of Working GroupⅠ to the Fourth Assessment Report of the IPCC. Cambridge University Press,Cambridge,UK.
[25]	Kirda C, Danso SKA, Zapata F (1989). Temporal water-stress effects on nodulation, nitrogen accumulation and growth of soybean. Plant and Soil, 120,49-55.
[26]	Ledgard SF, Sprosen MS, Steele KW (1996). Nitrogen fixation by nine white clover cultivars in grazed pasture, as affected by nitrogen fertilization. Plant and Soil, 178,193-203.
[27]	Ladrera R, Marino D, Larrainzar E, Gonzalez EM, Arrese-Igor C (2007). Reduced carbon availability to bacteroids and elevated ureides in nodules, but not in shoots, are involved in the nitrogen fixation response to early drought in soybean. Plant Physiology, 145,539-546. DOI URL PMID
[28]	Li XZ (李香真), Chen ZZ (陈佐忠) (1998). Influences of stocking rates on C, N, P contents in plant-soil system. Acta Agrestia Sinica(草地学报), 6,90-98. (in Chinese with English abstract)
[29]	Mytton LR, Cresswell A, Colbourn P (1993). Improvement in soil structure associated with white clover. Grass and Forage Science, 48,84-90.
[30]	Niu SL (牛书丽), Jiang GM (蒋高明) (2004). The importance of legume in China grassland ecosystem and the advances in physiology and ecology studies. Chinese Bulletin of Botany(植物学通报), 21,9-18. (in Chinese with English abstract)
[31]	Pan QM (潘庆民), Bai YF (白永飞), Han XG (韩兴国), Yang JC (杨景成) (2005). Effects of nitrogen addition on a Leymus chinensis population in typical steppe of Inner Mongolia. Acta Phytoecologica Sinica(植物生态学报), 29,311-317. (in Chinese with English abstract)
[32]	Peoples MB, Herridge DF, Ladha JK (1995). Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production. Plant and Soil, 174,3-28.
[33]	Rainbird RM, Thorne JH, Hardy RWF (1984). Role of amides, amino acids, and ureides in the nutrition of developing soybean seeds. Plant Physiology, 74,329-334. DOI URL PMID
[34]	Rigaud J (1981). Comparison of the efficiency of nitrate and nitrogen fixation in crop yield. In: Bewley JD ed. Nitrogen and Carbon Metabolism. Martinus Nijhoff, the Hague Press, Netherlands, 18-46.
[35]	Serraj R (2003). Effects of drought stress on legume symbiotic nitrogen fixation: physiological mechanisms. Indian Journal of Experimental Biology, 41,1136-1141. URL PMID
[36]	Serraj R, Sinclair TR, Purcell LC (1999). Symbiotic N ₂ fixation response to drought. Journal of Experimental Botany, 50,143-155.
[37]	Streeter J, Wong PP (1988). Inhibition of legume nodule formation and N ₂ fixation by nitrate. Critical Reviews in Plant Sciences, 7,1-23.
[38]	Sun ZR (孙志蓉), Zhai MP (翟明普), Wang WQ (王文全) (2006). Study on seedling nodule characteristics of Caragana microphylla. Forestry Science & Technology(林业科技), 31,6-9. (in Chinese with English abstract)
[39]	Tao L (陶林), Gao HW (高洪文), Fan FC (樊奋成) (2005). The dynamics of nitrogen fixation ability to root nodule of Caragana microphylla Lam. Grassland of China(中国草地), 27,53-56. (in Chinese with English abstract)
[40]	Thomas RB, Bashkin MA, Richter DD (2000). Nitrogen inhibition of nodulation and N ₂ fixation of a tropical N ₂-fixing tree ( Gliricidia sepium) grown in elevated atmospheric CO ₂. New Phytologist, 145,233-243.
[41]	Thomas RJ (1992). The role of the legume in the nitrogen cycle of productive and sustainable pastures. Grass and Forage Science, 47,133-142.
[42]	Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002). Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry, 57,1-45.
[43]	Volk M, Niklaus PA, Korner C (2000). Soil moisture effects determine CO ₂ responses of grassland species. Oecologia, 125,380-388. DOI URL PMID
[44]	Wang FJ (王芳玖) (1985). Primary investigation on the root nodulation of wild legume plants. In: Inner Mongolia Grassland Ecosystem Research Station, the Chinese Academy of Sciences ed.Research on Grassland Ecosystem No.5 (草原生态系统研究第五集). Science Press, Beijing, 124-134. (in Chinese)
[45]	Wang WW (王卫卫), Hu ZH (胡正海) (2003). Characteristics related to symbiotic nitrogen fixation of legumes in northwest arid zone of China. Acta Botanica Boreali-occidentalia Sinica(西北植物学报), 23,1163-1168. (in Chinese with English abstract)
[46]	Xiong XG (熊小刚), Han XG (韩兴国), Bai YF (白永飞), Pan QM (潘庆民) (2003). Increased distribution of Caragana microphylla in rangelands and its causes and consequences in Xilin River Basin. Acta Pratacultural Science(草业学报), 12,57-62. (in Chinese with English abstract)
[47]	Yao XC (姚新春), Shi SL (师尚礼), Wang YL (王亚玲) (2007). Effect of intermittent drought on nodule formation of alfalfa. Acta Agrestia Sinica (草地学报), 15,216-220. (in Chinese with English abstract)
[48]	Zhao XY (赵献英), Yao YC (姚彦臣), Yang RR (杨汝荣) (1988). Eco-geographical characteristics and its prospect of natural rangelands in Xilin River Basin. In: Inner Mongolia Grassland Ecosystem Research Station, The Chinese Academy of Sciences ed. Research on Grassland Ecosystem No.3 (草原生态系统研究第三册). Science Press, Beijing, 227-268.
[49]	Zuo YM (左元梅), Liu YX (刘永秀), Zhang FS (张福锁) (2003). Effects of the NO ₃ ^--N on nodule formation and nitrogen fixing of peanut. Acta Ecologica Sinica(生态学报), 23,758-764. (in Chinese with English abstract)

处理 Treatment	根瘤特征 Nodule characteristics
处理 Treatment	大小及多少 Size and quantity	颜色及形态 Color and form	着生部位 Position
N⁰H^-C	很小很少 Few; small	小球状; 褐色 Small globular; Brown	着生于主根上部 Nodules on the upper part of taproot
N⁰H^-E	较小较少 Less and smaller than CK	小球状、梨状; 褐色 Small globular or small pyriform; Brown	主要着生于主根 Nodules on taproot mainly
N⁰H⁰C (CK)	中等大小, 相对较少 Medium quantity; medium size	小型(68%): 梨状、球状, 棕黄色或浅黄色; 中型(30%): 棒状、纺锤状, 棕褐色; 大型(2%): Y状, 棕褐色 Miniature (68%): pyriform or globular, tan or buff; Medium (30%): claviform or fusiform, pitchy; Large (2%): Y, pitchy	多生于侧根 Nodules on lateral roots mainly
N⁰H⁰E	较大较多 Larger quantity than CK; Larger size than CK	小型(56%): 球状; 中型(40%): 纺锤状、梨状; 大型(4%): Y状; 均为棕褐色 Miniature (56%): globular, pitchy; Medium (40%): fusiform or pyriform, pitchy; Large (4%): Y, pitchy	多生于侧根 Nodules on lateral roots mainly
N⁰H⁺C	大、多且饱满 Many; large and plump, more and larger than N⁰H⁰E	小型(55%): 梨状、球状, 棕黄色或浅黄色; 中型(40%): 棒状、梨状, 褐色; 大型(5%): 掌状、珊瑚状, 深褐色 Miniature (55%): pyriform or globular, tan or buff; Medium (40%): claviform or pyriform, brown; Large (5%): palmated or coralliform, dark brown	主要着生于侧根和须根 Nodules on lateral roots or fibres mainly
N⁰H⁺E	很大很多且饱满 Maximum in quantity and size, plump	小型(50%): 球状, 棕黄色; 中型(40%): 梨形, 褐色; 大型(10%): 棒状、掌状、珊瑚状和纺锤状, 深褐色 Miniature (50%): globular, tan; Medium (40%): pyriform, brown; Large (10%): claviform, palmated, coralliform or fusiform, dark brown	主要着生于侧根和须根 Nodules oin lateral roots or fibres mainly
N⁺H^-C	仅有几个干瘪根瘤 No live nodules, only a couple of wizened nodules	–	–
N⁺H^-E	几乎没有活根瘤, 有少量干瘪根瘤 Almost no live nodules, a few wizened nodules	–	–
N⁺H⁰C	几乎没有活根瘤, 有少量干瘪根瘤 Almost no live nodules, a few wizened nodules	–	–
N⁺H⁰E	活根瘤极小极少, 有少量干瘪根瘤 Very few and very small live nodules; a few wizened nodules	小球形, 黑褐色 Small globular; Black brown	着生于主根 Nodules on taproot
N⁺H⁺C	活根瘤极小极少, 比N⁺H⁰E稍多; 干瘪根瘤较多 Very few and very small live nodules, slightly more than N⁺H⁰E; more wizened nodules than N⁺H⁰E	小球状、粒状, 黑褐色 Small globular or granular; Black brown	簇生于主根 Nodules fascinated on taproot
N⁺H⁺E	活根瘤极小极少, 比N⁺H⁺C稍多; 干瘪根瘤较多 Very few and very small live nodules, slightly more than N⁺H⁺C; more wizened nodules than N⁺H⁰E	椭圆状、小球状, 黑褐色 Ellipsoid or small globular; Black brown	簇生于主根 Nodules fascinated on taproot

处理 Treatment	根瘤特征 Nodule characteristics
处理 Treatment	大小及多少 Size and quantity	颜色及形态 Color and form	着生部位 Position
N⁰H^-C	很小很少 Few; small	小球状; 褐色 Small globular; Brown	着生于主根上部 Nodules on the upper part of taproot
N⁰H^-E	较小较少 Less and smaller than CK	小球状、梨状; 褐色 Small globular or small pyriform; Brown	主要着生于主根 Nodules on taproot mainly
N⁰H⁰C (CK)	中等大小, 相对较少 Medium quantity; medium size	小型(68%): 梨状、球状, 棕黄色或浅黄色; 中型(30%): 棒状、纺锤状, 棕褐色; 大型(2%): Y状, 棕褐色 Miniature (68%): pyriform or globular, tan or buff; Medium (30%): claviform or fusiform, pitchy; Large (2%): Y, pitchy	多生于侧根 Nodules on lateral roots mainly
N⁰H⁰E	较大较多 Larger quantity than CK; Larger size than CK	小型(56%): 球状; 中型(40%): 纺锤状、梨状; 大型(4%): Y状; 均为棕褐色 Miniature (56%): globular, pitchy; Medium (40%): fusiform or pyriform, pitchy; Large (4%): Y, pitchy	多生于侧根 Nodules on lateral roots mainly
N⁰H⁺C	大、多且饱满 Many; large and plump, more and larger than N⁰H⁰E	小型(55%): 梨状、球状, 棕黄色或浅黄色; 中型(40%): 棒状、梨状, 褐色; 大型(5%): 掌状、珊瑚状, 深褐色 Miniature (55%): pyriform or globular, tan or buff; Medium (40%): claviform or pyriform, brown; Large (5%): palmated or coralliform, dark brown	主要着生于侧根和须根 Nodules on lateral roots or fibres mainly
N⁰H⁺E	很大很多且饱满 Maximum in quantity and size, plump	小型(50%): 球状, 棕黄色; 中型(40%): 梨形, 褐色; 大型(10%): 棒状、掌状、珊瑚状和纺锤状, 深褐色 Miniature (50%): globular, tan; Medium (40%): pyriform, brown; Large (10%): claviform, palmated, coralliform or fusiform, dark brown	主要着生于侧根和须根 Nodules oin lateral roots or fibres mainly
N⁺H^-C	仅有几个干瘪根瘤 No live nodules, only a couple of wizened nodules	–	–
N⁺H^-E	几乎没有活根瘤, 有少量干瘪根瘤 Almost no live nodules, a few wizened nodules	–	–
N⁺H⁰C	几乎没有活根瘤, 有少量干瘪根瘤 Almost no live nodules, a few wizened nodules	–	–
N⁺H⁰E	活根瘤极小极少, 有少量干瘪根瘤 Very few and very small live nodules; a few wizened nodules	小球形, 黑褐色 Small globular; Black brown	着生于主根 Nodules on taproot
N⁺H⁺C	活根瘤极小极少, 比N⁺H⁰E稍多; 干瘪根瘤较多 Very few and very small live nodules, slightly more than N⁺H⁰E; more wizened nodules than N⁺H⁰E	小球状、粒状, 黑褐色 Small globular or granular; Black brown	簇生于主根 Nodules fascinated on taproot
N⁺H⁺E	活根瘤极小极少, 比N⁺H⁺C稍多; 干瘪根瘤较多 Very few and very small live nodules, slightly more than N⁺H⁺C; more wizened nodules than N⁺H⁰E	椭圆状、小球状, 黑褐色 Ellipsoid or small globular; Black brown	簇生于主根 Nodules fascinated on taproot

变量 Source of variation	df	单株根瘤数量 Number of root nodules per plant	单株根瘤重量 Weight of root nodules per plant	根瘤平均长度 Mean length of root nodules	根瘤平均重量 Mean weight of root nodules
N	1	44.12^**	19.64^**	64.21^**	53.45^**
H₂O	2	17.01^**	9.37^**	17.89^**	21.60^**
CO₂	1	1.72 ^NS	1.12 ^NS	2.77 ^NS	2.60 ^NS
N×H₂O	2	13.41^**	8.13^**	0.84 ^NS	1.47 ^NS
N×CO₂	1	0.46 ^NS	0.72 ^NS	1.25 ^NS	0.13 ^NS
H₂O×CO₂	2	0.45 ^NS	0.30 ^NS	0.35 ^NS	1.16 ^NS
N×H₂O×CO₂	2	0.76 ^NS	0.33 ^NS	0.08 ^NS	1.28 ^NS

变量 Source of variation	df	单株根瘤数量 Number of root nodules per plant	单株根瘤重量 Weight of root nodules per plant	根瘤平均长度 Mean length of root nodules	根瘤平均重量 Mean weight of root nodules
N	1	44.12^**	19.64^**	64.21^**	53.45^**
H₂O	2	17.01^**	9.37^**	17.89^**	21.60^**
CO₂	1	1.72 ^NS	1.12 ^NS	2.77 ^NS	2.60 ^NS
N×H₂O	2	13.41^**	8.13^**	0.84 ^NS	1.47 ^NS
N×CO₂	1	0.46 ^NS	0.72 ^NS	1.25 ^NS	0.13 ^NS
H₂O×CO₂	2	0.45 ^NS	0.30 ^NS	0.35 ^NS	1.16 ^NS
N×H₂O×CO₂	2	0.76 ^NS	0.33 ^NS	0.08 ^NS	1.28 ^NS