Responses of biomass allocation patterns to nitrogen addition of Cunninghamia lanceolata seedlings

doi:10.17521/cjpe.2021.0135

Abstract

Abstract:

Aims Sharply increasing atmospheric nitrogen (N) deposition may have profound effects on carbon (C) fixation and allocation of plants. However, a comprehensive understanding of how nitrogen addition influences allocation dynamics of carbohydrates among different organs in plants is still lacking.
Methods In this study, a pot experiment of seedlings of Cunninghamia lanceolate was established to investigate the allocation pattern and regulation mechanism of non-structural carbohydrates (NSC) and structural carbohydrates (SC) in different organs of C. lanceolate seedlings after N addition. The concentrations and pool sizes of NSC and SC were measured.
Important findings The results showed that: (1) N addition significantly increased the net photosynthetic rate by 143.96%, but decreased the concentration and pool size of NSC in needles. There was no significant change in the components of NSC concentration and pool in current-year stems. Furthermore, N addition resulted in a significant decrease in the starch concentration of one-year-old stems, but a non-significant change in soluble sugar concentration. In addition, the components of NSC concentration and pool in seedlings roots also tended to decrease. (2) After N addition, the ratio of below- to above-ground biomass decreased by 22.09%, and the ratio of below- to above-ground SC pool also decreased by 31.07%, and the ratio of below- to above-ground NSC pool showed no significant difference between control and N addition treatment. (3) N addition significantly increased the phosphorus (P) pool size in the above-ground part and decreased the ratio of below- to above-ground P pool, while the ratio of below- to above-ground N pool showed no obvious difference between control and N addition treatment. (4) Under N addition, soil pH decreased significantly from 4.94 to 4.02, ammonium and nitrate nitrogen concentration increased by 7.17 times and 11.55 times, respectively, and soil available P concentration increased by 42.86%, while the activities of urease (62.75%) and acid phosphatase (56.52%) in the soil decreased significantly compared to control. Our results indicates that C. lanceolate seedlings increased nutrient uptake amount mainly by the construction of root structure, but not by the allocation of more NSC to the root under low nutrient conditions, while nutrient alleviation driven by nitrogen addition resulted in more carbohydrates allocation to above-ground organs, resulting in the accumulation of SC in above-ground parts.

Key words: nitrogen addition, biomass allocation, carbohydrates, non-structural carbohydrates, phosphorus, optimal partitioning theory

WANG Jiao, GUAN Xin, ZHANG Wei-Dong, HUANG Ke, ZHU Mu-Nan, YANG Qing-Peng. Responses of biomass allocation patterns to nitrogen addition of Cunninghamia lanceolata seedlings[J]. Chin J Plant Ecol, 2021, 45(11): 1231-1240.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2021.0135

https://www.plant-ecology.com/EN/Y2021/V45/I11/1231

Figures/Tables 9

Fig. 1 Effect of nitrogen addition on net photosynthetic rate (A), total plant biomass (B) and biomass of different organs (O) (C) of Cunninghamia lanceolate seedlings (mean ± SE, n = 5). CK, control, no nitrogen fertilizer addition; N, nitrogen addition. CN, current-year needles; CR, coarse roots; CS, current-year stems; FR, fine roots; ON, one-year-old needles; OS, one-year- old stems. Different lowercase letters indicate significant difference between treatments (p < 0.05).

Fig. 2 Effect of nitrogen addition on the concentration of non-structural carbohydrates (NSC)(A), soluble sugar (B) starch (C), and the pool sizes of non-structural carbohydrates (NSC)(D), soluble sugar (E) and starch (F) in different organs (O) of Cunninghamia lanceolate seedlings (mean ± SE, n = 5). CN, current-year needles; CR, coarse roots; CS, current-year stems; FR, fine roots; ON, one-year-old needles; OS, one-year-old stems. CK, control, no nitrogen fertilizer addition; N, nitrogen addition. The different lowercase letters of the same organs indicate significant difference between treatments (p < 0.05).

Table 1 Effect of nitrogen (N) addition on the concentrations of non-structural carbohydrates (NSC), soluble sugar, starch, N and phosphorus (P) in different organs of Cunninghamia lanceolate seedlings

器官 Organ	NSC (mg·g^-1)	可溶性糖 Soluble sugar (mg·g^-1)	淀粉 Starch (mg·g^-1)	N (mg·g^-1)	P (mg·g^-1)
CN	↓	↓	↓	↑	↑
ON	↓	↓	↓	↑	↑
CS	0	0	0	↑	0
OS	0	0	↓	↑	↑
CR	0	0	0	↑	0
FR	0	0	0	↑	0

Fig. 3 Effect of nitrogen addition on nitrogen (N) concentration (A), phosphorus (P) concentration (B), the pool sizes of N (C) and the pool sizes of P (D) in different organs (O) of Cunninghamia lanceolate seedlings (mean ± SE, n = 5). CN, current-year needles; CR, coarse roots; CS, current-year stems; FR, fine roots; ON, one-year-old needles; OS, one-year-old stems. CK, control, no nitrogen fertilizer addition; N, nitrogen addition. The different lowercase letters of the same organs indicate significant difference between treatments (p < 0.05).

Fig. 4 Effect of nitrogen addition on the ratio of below- to aboveground total biomass (A), non-structural carbohydrates (NSC) pool size (B) and structural carbohydrates (SC) pool size (C) of Cunninghamia lanceolate seedlings (mean ± SE, n = 5). CK, control, no nitrogen fertilizer addition; N, nitrogen addition. Different lowercase letters indicate significant difference between treatments (p < 0.05).

Table 2 Effect of nitrogen addition on the pool sizes of biomass, non-structural carbohydrates (NSC) and structural carbohydrates (SC)), nitrogen (N) and phosphorus (P) in the below- and aboveground of Cunninghamia lanceolate seedlings

器官 Organ	生物量 Biomass (g)	C (g)		N (g)	P (g)
器官 Organ	生物量 Biomass (g)	NSC	SC	N (g)	P (g)
CN	0	0	0	↑	↑
ON	0	0	0	0	0
CS	0	0	0	↑	0
OS	0	0	0	↑	↑
CR	0	0	0	0	0
FR	0	0	0	↑	0
地下总量(库) Belowground (pool)	0	0	0	↑	0
地上总量(库) Aboveground (pool)	0	0	0	↑	↑
地下/地上(库) Belowground/Aboveground (pool)	↓	0	↓	0	↓

Fig. 5 Effect of nitrogen addition on the ratio of below- to aboveground nitrogen (N) pool size (A) and phosphorus (P) pool size (B) of Cunninghamia lanceolate seedlings (mean ± SE, n = 5). CK, control, no nitrogen fertilizer addition; N, nitrogen addition. Different lowercase letters indicate significant difference between treatments (p < 0.05).

Table 3 Effect of nitrogen addition on soil pH, available phosphorus (AP), ammonium (NH4+-N) and nitrate nitrogen (NO3--N) concentrations of soil (mean ± SE, n = 5)

处理 Treatment	pH	有效磷 AP (mg·kg^-1)	铵态氮 NH₄⁺-N (mg·kg^-1)	硝态氮 NO₃^--N (mg·kg^-1)
CK	4.94 ± 0.09^a	0.28 ± 0.01^b	15.24 ± 0.49^b	4.92 ± 1.61^b
N	4.02 ± 0.04^b	0.40 ± 0.02^a	124.51 ± 7.42^a	61.75 ± 1.36^a

Fig. 6 Effect of nitrogen addition on urease (A), Leucine aminopeptidase (B), acid phosphatase (C) and N-acetyl-glucosidase (NAG)(D) activity of soil (mean ± SE, n = 5). CK, control, no nitrogen fertilizer addition; N, nitrogen addition. Different lowercase letters indicate significant difference between treatments (p < 0.05).

References 46

[1]	Ågren GI, Franklin O (2003). Root:shoot ratios, optimization and nitrogen productivity. Annals of Botany, 92, 795-800. DOI URL
[2]	Ågren GI, Wetterstedt JÅM, Billberger MFK (2012). Nutrient limitation on terrestrial plant growth—Modeling the interaction between nitrogen and phosphorus. New Phytologist, 194, 953-960. DOI URL
[3]	Ai ZM, Xue S, Wang GL, Liu GB (2017). Responses of non-structural carbohydrates and C:N:P stoichiometry of Bothriochloa ischaemum to nitrogen addition on the Loess Plateau, China. Journal of Plant Growth Regulation, 36, 714-722. DOI URL
[4]	Alderman PD, Boote KJ, Sollenberger LE, Coleman SW (2011). Carbohydrate and nitrogen reserves relative to regrowth dynamics of ‘Tifton 85’ bermudagrass as affected by nitrogen fertilization. Crop Science, 51, 1727-1738. DOI URL
[5]	Barrow NJ (2017). The effects of pH on phosphate uptake from the soil. Plant and Soil, 410, 401-410. DOI URL
[6]	Burton AJ, Pregitzer KS, Hendrick RL (2000). Relationships between fine root dynamics and nitrogen availability in Michigan northern hardwood forests. Oecologia, 125, 389-399. DOI PMID
[7]	Canham CD, Kobe RK, Latty EF, Chazdon RL (1999). Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia, 121, 1-11. DOI URL
[8]	Casson NJ, Eimers MC, Watmough SA (2012). An assessment of the nutrient status of sugar maple in Ontario: indications of phosphorus limitation. Environmental Monitoring and Assessment, 184, 5917-5927. DOI PMID
[9]	Chen J, van Groenigen KJ, Hungate BA, Terrer C, van Groenigen JW, Maestre FT, Ying SC, Luo Y, Jorgensen U, Sinsabaugh RL, Olesen JE, Elsgaard L (2020). Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems. Global Change Biology, 26, 5077-5086. DOI URL
[10]	Dakora FD, Phillips DA (2002). Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil, 245, 35-47. DOI URL
[11]	Davidson EA (2009). The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nature Geoscience, 2, 659-662. DOI URL
[12]	Deng Q, Hui DF, Dennis S, Reddy KC (2017). Responses of terrestrial ecosystem phosphorus cycling to nitrogen addition: a meta-analysis. Global Ecology and Biogeography, 26, 713-728. DOI URL
[13]	Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014). Nonstructural carbon in woody plants. Annual Review of Plant Biology, 65, 667-687. DOI URL
[14]	Dijkstra FA, Cheng WX (2007). Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecology Letters, 10, 1046-1053. PMID
[15]	Feng CY, Zheng CY, Tian D (2019). Impacts of nitrogen addition on plant phosphorus content in forest ecosystems and the underlying mechanisms. Chinese Journal of Plant Ecology, 43, 185-196. DOI URL
	[ 冯婵莹, 郑成洋, 田地 (2019). 氮添加对森林植物磷含量的影响及其机制. 植物生态学报, 43, 185-196.]
[16]	Fita A, Nuez F, Picó B (2011). Diversity in root architecture and response to P deficiency in seedlings of Cucumis melo L. Euphytica, 181, 323-339. DOI URL
[17]	Graham JH, Duncan LW, Eissenstat DM (1997). Carbohydrate allocation patterns in Citrus genotypes as affected by phosphorus nutrition, mycorrhizal colonization and mycorrhizal dependency. New Phytologist, 135, 335-343. DOI URL
[18]	Hartmann H, Adams HD, Hammond WM, Hoch G, Landhäusser SM, Wiley E, Zaehle S (2018). Identifying differences in carbohydrate dynamics of seedlings and mature trees to improve carbon allocation in models for trees and forests. Environmental and Experimental Botany, 152, 7-18. DOI URL
[19]	Knox KJE, Clarke PJ (2005). Nutrient availability induces contrasting allocation and starch formation in resprouting and obligate seeding shrubs. Functional Ecology, 19, 690-698. DOI URL
[20]	Kobe RK, Iyer M, Walters MB (2010). Optimal partitioning theory revisited: nonstructural carbohydrates dominate root mass responses to nitrogen. Ecology, 91, 166-179. DOI URL
[21]	Li RS, Yang QP, Zhang WD, Zheng WH, Chi YG, Xu M, Fang YT, Gessler A, Li MH, Wang SL (2017). Thinning effect on photosynthesis depends on needle ages in a Chinese fir ( Cunninghamia lanceolata) plantation. Science of the Total Environment, 580, 900-906. DOI URL
[22]	Li WB, Hartmann H, Adams HD, Zhang HX, Jin CJ, Zhao CY, Guan DX, Wang AZ, Yuan FH, Wu JB (2018). The sweet side of global change-dynamic responses of non-structural carbohydrates to drought, elevated CO₂ and nitrogen fertilization in tree species. Tree Physiology, 38, 1706-1723.
[23]	Li WB, Zhang HX, Huang GZ, Liu RX, Wu HJ, Zhao CY, McDowell NG (2020). Effects of nitrogen enrichment on tree carbon allocation: a global synthesis. Global Ecology and Biogeography, 29, 573-589. DOI URL
[24]	Li Y, Niu SL, Yu GR (2016). Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis. Global Change Biology, 22, 934-943. DOI URL
[25]	Liu X, Zhao WR, Meng MJ, Fu ZY, Xu LH, Zha Y, Yue JM, Zhang SF, Zhang JC (2018). Comparative effects of simulated acid rain of different ratios of SO₄^2- to NO₃^- on fine root in subtropical plantation of China. Science of the Total Environment, 618, 336-346. DOI URL
[26]	Lu XK, Mo JM, Gilliam FS, Zhou GY, Fang YT (2010). Effects of experimental nitrogen additions on plant diversity in an old-growth tropical forest. Global Change Biology, 16, 2688-2700. DOI URL
[27]	Mäkelä A, Valentine HT, Helmisaari HS (2008). Optimal co-allocation of carbon and nitrogen in a forest stand at steady state. New Phytologist, 180, 114-123. DOI URL
[28]	Martínez-Vilalta J, Sala A, Asensio D, Galiano L, Hoch G, Palacio S, Piper FI, Lloret F (2016). Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis. Ecological Monographs, 86, 495-516. DOI URL
[29]	Mo QF, Chen YQ, Yu SQ, Fan YX, Peng ZT, Wang WJ, Li ZA, Wang FM (2020). Leaf nonstructural carbohydrate concentrations of understory woody species regulated by soil phosphorus availability in a tropical forest. Ecology and Evolution, 10, 8429-8438. DOI URL
[30]	Palacio S, Hoch G, Sala A, Körner C, Millard P (2014). Does carbon storage limit tree growth? New Phytologist, 201, 1096-1100. DOI PMID
[31]	Portsmuth A, Niinemets Ü (2007). Structural and physiological plasticity in response to light and nutrients in five temperate deciduous woody species of contrasting shade tolerance. Functional Ecology, 21, 61-77.
[32]	Pregitzer KS, Burton AJ, Zak DR, Talhelm AF (2008). Simulated chronic nitrogen deposition increases carbon storage in Northern Temperate forests. Global Change Biology, 14, 142-153. DOI URL
[33]	Qi Y, Huang YM, Wang Y, Zhao J, Zhang JH (2011). Biomass and its allocation of four grassland species under different nitrogen levels. Acta Ecologica Sinica, 31, 5121-5129.
	[ 祁瑜, 黄永梅, 王艳, 赵杰, 张景慧 (2011). 施氮对几种草地植物生物量及其分配的影响. 生态学报, 31, 5121-5129.]
[34]	Reay DS, Dentener F, Smith P, Grace J, Feely RA (2008). Global nitrogen deposition and carbon sinks. Nature Geoscience, 1, 430-437. DOI URL
[35]	Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, et al. (2008). Stoichiometry of soil enzyme activity at global scale. Ecology Letters, 11, 1252-1264. DOI PMID
[36]	Sinsabaugh RL, Reynolds H, Long TM (2000). Rapid assay for amidohydrolase (urease) activity in environmental samples. Soil Biology & Biochemistry, 32, 2095-2097. DOI URL
[37]	Wang B, Gong JR, Zhang ZH, Yang B, Liu M, Zhu CC, Shi JY, Zhang WY, Yue KX (2019). Nitrogen addition alters photosynthetic carbon fixation, allocation of photoassimilates, and carbon partitioning of Leymus chinensis in a temperate grassland of Inner Mongolia. Agricultural and Forest Meteorology, 279, 107743. DOI: 10.1016/j.agrformet.2019.107743. DOI URL
[38]	Wiley E, Helliker B (2012). A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytologist, 195, 285-289. DOI PMID
[39]	Würth MKR, Peláez-Riedl S, Wright SJ, Körner C (2005). Non-structural carbohydrate pools in a tropical forest. Oecologia, 143, 11-24. DOI URL
[40]	Yan LF, Yang QP, Zheng WH, Huang K, Zhao FX (2020). Responses of non-structural carbohydrates in above-ground tissues/organs and root to shading and light restoration in Cunninghamia lanceolata saplings. Acta Botanica Boreali- Occidentalia Sinica, 40, 311-318.
	[ 闫丽飞, 杨庆朋, 郑文辉, 黄苛, 赵峰侠 (2020). 杉木幼苗非结构性碳水化合物对遮阴及恢复光照的响应. 西北植物学报, 40, 311-318.]
[41]	Yan ZB, Guan HY, Han WX, Han TS, Guo YL, Fang JY (2016). Reproductive organ and young tissues show constrained elemental composition in Arabidopsis thaliana. Annals of Botany, 117, 431-439. DOI URL
[42]	Yang QP, Liu LL, Zhang WD, Xu M, Wang SL (2015). Different responses of stem and soil CO₂ efflux to pruning in a Chinese fir (Cunninghamia lanceolata) plantation. Trees, 29, 1207-1218. DOI URL
[43]	Yang QP, Zhang WD, Li RS, Xu M, Wang SL (2016). Different responses of non-structural carbohydrates in above- ground tissues/organs and root to extreme drought and re-watering in Chinese fir ( Cunninghamia lanceolata) saplings. Trees, 30, 1863-1871. DOI URL
[44]	Zhang Y, Zhou ZC, Yang Q (2013a). Genetic variations in root morphology and phosphorus efficiency of Pinus massoniana under heterogeneous and homogeneous low phosphorus conditions. Plant and Soil, 364, 93-104. DOI URL
[45]	Zhang Y, Zhou ZC, Yang Q (2013b). Nitrogen (N) deposition impacts seedling growth of Pinus massoniana via N:P ratio effects and the modulation of adaptive responses to low P (phosphorus). PLOS ONE, 8, e79229. DOI: 10.1371/journal.pone.0079229. DOI URL
[46]	Zhang YH, Loreau M, Lü XT, He NP, Zhang GM, Han XG (2016). Nitrogen enrichment weakens ecosystem stability through decreased species asynchrony and population stability in a temperate grassland. Global Change Biology, 22, 1445-1455. DOI URL