Responses of photosynthetic pigments composition, nitrogen and phosphorus stoichiometric characteristics of Myriophyllum aquaticum to exogenous ammonium

doi:10.17521/cjpe.2021.0291

Abstract

Abstract:

Aims Myriophyllum aquaticum has high tolerance to high concentration of ammonium (NH₄⁺) and thus becomes the preferred species for swine wastewater treatment. It is of great significance to explore the effects of exogenous NH₄⁺ on the photosynthetic pigment composition and the stoichiometric characteristics of nitrogen (N) and phosphorus (P) of the M. aquaticum for improving the purifying efficiency of artificial wetlands system of M. aquaticum.

Methods Six NH₄⁺ concentration levels (0, 0.1, 1, 5, 15, 30 mmol·L^-1) were set up in this study. After 21 days of indoor cultivation, the contents of chlorophyll, N and P of M. aquaticum were measured to analyze their characteristics of changes.

Important findings The results showed that the relative stem height and biomass increased initially and then decreased, which were well fitted by a curve equation. Moreover, the peak of them appeared at 16.22 and 12.58 mmol·L^-1 exogenous NH₄⁺, respectively, via fitting non-linear Gaussian equation. With the increase of exogenous NH₄⁺ concentrations, the chlorophyll content in the leaves decreased significantly, but increased in the stems. In addition, there was a wide variation of chlorophyll a than chlorophyll b. The chlorophyll a/b did not change significantly among different NH₄⁺ treatments, except the value in the stems of 5 mmol·L^-1 NH₄⁺ treatment, which was significantly decreased. With the increase of exogenous NH₄⁺ concentrations, the N contents in the leaves and stems were significantly increased by 85%-235% and 127%-373%, respectively, and the P content in the leaves was increased by 49%-51% in comparison to the control (CK). When the concentrations of exogenous NH₄⁺ was no more than 15 mmol·L^-1, the N content and N:P ratio of the leaves and stems increased rapidly, so were relative stem height and relative biomass. Correlation analysis showed that the contents of N and P, and N:P ratio were negatively correlated with total chlorophyll content in the leaves, but positively correlated with total chlorophyll content in the stems. In conclusion, M. aquaticum grew well with larger biomass and higher absorption of N and P, when the concentrations of exogenous NH₄⁺ were in the range of 12-16 mmol·L^-1. Therefore, the constructed wetlands system planted with M. aquaticum can effectively remove N and P from polluted wastewater and achieve the purpose of efficient water purification.

Key words: Myriophyllum aquaticum, photosynthetic pigment, stoichiometry of nitrogen and phosphorus, ammonium

XIAN Ying-Nan, ZHANG Ying, LI Bao-Zhen, LUO Pei, XIAO Run-Lin, WU Jin-Shui. Responses of photosynthetic pigments composition, nitrogen and phosphorus stoichiometric characteristics of Myriophyllum aquaticum to exogenous ammonium[J]. Chin J Plant Ecol, 2022, 46(4): 451-460.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2021.0291

https://www.plant-ecology.com/EN/Y2022/V46/I4/451

Figures/Tables 7

Fig. 1 Effects of exogenous ammonium (NH4+) concentration on relative stem height and relative biomass of Myriophyllum aquaticum (mean ± SE, n = 24). Different lowercase letters indicate significant differences among different treatments (p < 0.05).

Fig. 2 Correlation between relative stem height (RSH) and relative biomass (RB) of Myriophyllum aquaticum and exogenous ammonium (NH4+) concentration (n = 24).

Fig. 3 Effects of exogenous ammonium (NH4+) concentration on chlorophyll (Chl) content and photosynthetic pigment component ratio of Myriophyllum aquaticum (mean ± SE, n = 24). Different lowercase letters indicate significant differences among different treatments (p < 0.05).

Fig. 4 Correlation between chlorophyll (Chl) content of Myriophyllum aquaticum and exogenous ammonium (NH4+) concentration (n = 24).

Fig. 5 Effects of exogenous ammonium (NH4+) concentration on nitrogen (N) and phosphorus (P) contents, and N:P ratio of Myriophyllum aquaticum (mean ± SE, n = 24).

Fig. 6 Correlation between nitrogen (N) and phosphorus (P) contents and N:P ratio and exogenous ammonium (NH4+) concentration in leaf (A) and stem (B) of Myriophyllum aquaticum (n = 24).

Table 1 Slopes of relationship between nitrogen (N) and phosphorus (P) contents and N:P ratio, and chlorophyll content of Myriophyllum aquaticum (n = 24)

叶绿素含量 Chlorophyll content	N	P	N:P
叶片 Leaf	-0.733 2^**	-0.584 6^**	-0.699 2^**
茎 Stem	0.724 0^**	0.485 4^*	0.664 5^**

References 50

[1]	Aerts R, Chapin III FS (1999). The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research, 30, 1-67.
[2]	Bieleski RL (1973). Phosphate pools, phosphate transport, and phosphate availability. Annual Review of Plant Physiology, 24, 225-252. DOI URL
[3]	Britto DT, Kronzucker HJ (2002). NH₄⁺toxicity in higher plants: a critical review. Journal of Plant Physiology, 159, 567-584. DOI URL
[4]	Cao T, Xie P, Ni LY, Wu AP, Zhang M, Wu SK, Smolders AJP (2007). The role of NH₄⁺ toxicity in the decline of the submersed macrophyte Vallisneria natans in lakes of the Yangtze River basin, China. Marine and Freshwater Research, 58, 581-587. DOI URL
[5]	Chao W, Song HZ, Pei FW, Hou J, Wei L, Wen JZ (2008). Metabolic adaptations to ammonia-induced oxidative stress in leaves of the submerged macrophyte Vallisneria natans (Lour.) Hara. Aquatic Toxicology, 87, 88-98. DOI PMID
[6]	Dhote S, Dixit S (2009). Water quality improvement through macrophytes—A review. Environmental Monitoring and Assessment, 152, 149-153. DOI URL
[7]	Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ (2010). Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytologist, 186, 593-608. DOI PMID
[8]	Fan HL, Xie LQ, Song XM, Xue QJ, Su XM, Cao Q, Zhao YY (2017). Responses and accumulation features of nitrogen and phosphorus of submerged vegetation under different nutrient levels. Environmental Science & Technology, 40(3), 42-48.
	[ 樊恒亮, 谢丽强, 宋晓梅, 薛庆举, 苏小妹, 操庆, 赵雁雁 (2017). 沉水植物对水体营养的响应及氮磷积累特征. 环境科学与技术, 40(3), 42-48.]
[9]	Fu MZ, Wang ZL, Pu XM, Xu ZJ, Zhu MY (2012). Changes of nutrient concentrations and N:P:Si ratios and their possible impacts on the Huanghai Sea ecosystem. Acta Oceanologica Sinica, 31, 101-112. DOI URL
[10]	Gao JQ, Liu LN, Ma N, Yang J, Dong ZK, Zhang JS, Zhang JL, Cai M (2020). Effect of ammonia stress on carbon metabolism in tolerant aquatic plant—Myriophyllum aquaticum. Environmental Pollution, 263, 114412. DOI URL
[11]	Gururani MA, Venkatesh J, Tran LSP (2015). Regulation of photosynthesis during abiotic stress-induced photoinhibition. Molecular Plant, 8, 1304-1320. DOI PMID
[12]	Güsewell S (2004). N:P ratios in terrestrial plants: variation and functional significance. New Phytologist, 164, 243- 266. DOI PMID
[13]	He L, Chen XX, Li W, Zhu TS, Wu Y, Zhang H, Zhang XL, Cao T, Ge G, Ni LY, Xie P (2018). Leaf carbon, nitrogen and phosphorus stoichiometric characteristics and photosynthetic pigments composition of four submerged macrophytes in response to various water depth in Lake Erhai, China. Journal of Lake Sciences, 30, 1413-1419. DOI URL
	[ 何亮, 陈晓希, 李威, 朱天顺, 吴耀, 张欢, 张霄林, 曹特, 葛刚, 倪乐意, 谢平 (2018). 洱海4种沉水植物叶片的光合色素组成及C、N、P化学计量特征对水深的响应. 湖泊科学, 30, 1413-1419.]
[14]	Hu MH, Yuan JH, Xiang LC, Yang XE (2011). Influence of different nitrogen:phosphorus on growth characteristic of perennial aquatic plant. Chinese Journal of Environmental Engineering, 5, 2487-2493.
	[ 胡绵好, 袁菊红, 向律成, 杨肖娥 (2011). 不同氮磷比对多年生水生植物生长特性影响的研究. 环境工程学报, 5, 2487-2493.]
[15]	Jampeetong A, Brix H (2009a). Effects of NH₄⁺ concentration on growth, morphology and NH₄⁺ uptake kinetics of Salvinia natans. Ecological Engineering, 35, 695-702. DOI URL
[16]	Jampeetong A, Brix H (2009b). Nitrogen nutrition of Salvinia natans: effects of inorganic nitrogen form on growth, morphology, nitrate reductase activity and uptake kinetics of ammonium and nitrate. Aquatic Botany, 90, 67-73. DOI URL
[17]	Jampeetong A, Brix H, Kantawanichkul S (2012). Response of Salvinia cucullata to high NH₄⁺ concentrations at laboratory scales. Ecotoxicology and Environmental Safety, 79, 69-74. DOI PMID
[18]	Li X, Li YY, Li Y, Wu JS (2021). The phytoremediation of water with high concentrations of nitrogen and phosphorus contamination by three selected wetland plants. Journal of Water Process Engineering, 40, 101828. DOI: 10. 1016/j.jwpe.2020.101828. DOI URL
[19]	Liu F, Zhang SN, Wang Y, Li Y, Xiao RL, Li HF, He Y, Zhang MM, Wang D, Li X, Wu JS (2016). Nitrogen removal and mass balance in newly-formed Myriophyllum aquaticum mesocosm during a single 28-day incubation with swine wastewater treatment. Journal of Environment Management, 166, 596-604.
[20]	Liu MH, Xie TT, Yuan ZX, Li LJ, Li CX (2020). Carbon, nitrogen, and phosphorus ecological stoichiometric characteristics in leaves and fine roots of Taxodium distichum in the water-level fluctuation zone of the Three Gorges Reservoir region. Journal of Lake Sciences, 32, 1806-1816. DOI URL
	[ 刘明辉, 谢婷婷, 袁中勋, 李丽娟, 李昌晓 (2020). 三峡水库消落带适生树种落羽杉(Taxodium distichum)叶片-细根碳/氮/磷生态化学计量特征. 湖泊科学, 32, 1806-1816.]
[21]	Liu SB (2017). Effect of Different Ammonia Concentration on Physiological Characteristics, Nitrogen and Phosphorus Uptake of Myriophyllum aquaticum. Master degree dissertation, Hunan Agricultural University, Changsha. 20-67.
	[ 刘少博 (2017). 不同浓度铵态氮对绿狐尾藻的生理特征与氮磷吸收影响. 硕士学位论文, 湖南农业大学, 长沙. 20-67.]
[22]	Liu SB, Ran B, Zeng GJ, Li BZ, Zhu HM, Liu F, Xiao RL, Wu JS (2017). Physiological characteristics and nitrogen and phosphorus uptake of Myriophyllum aquaticum under high ammonium conditions. Environmental Science, 38, 3731- 3737. DOI URL
	[ 刘少博, 冉彬, 曾冠军, 李宝珍, 朱红梅, 刘锋, 肖润林, 吴金水 (2017). 高铵条件下绿狐尾藻的生理与氮磷吸收特征. 环境科学, 38, 3731-3737.]
[23]	Liu XH, Guo XC, Liu Y, Lu SY, Xi BD, Zhang J, Wang Z, Bi B (2019). A review on removing antibiotics and antibiotic resistance genes from wastewater by constructed wetlands: performance and microbial response. Environmental Pollution, 254, 112996. DOI: 10.1016/j.envpol.2019.112996. DOI URL
[24]	Loladze I, Elser JJ (2011). The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio. Ecology Letters, 14, 244-250. DOI PMID
[25]	Luo P, Liu F, Liu XL, Wu X, Yao R, Chen L, Li X, Xiao RL, Wu JS (2017). Phosphorus removal from lagoon-pretreated swine wastewater by pilot-scale surface flow constructed wetlands planted with Myriophyllum aquaticum. Science of the Total Environment, 576, 490-497. DOI URL
[26]	Ma XX, Hong JT, Wang XD (2019). C:N:P stoichiometry of perennial herbs’ organs in the alpine steppe of the northern Tibetan Plateau. Journal of Mountain Science, 16, 2039- 2047. DOI URL
[27]	Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK (2006). Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere, 65, 1027-1039. PMID
[28]	Nakaji T, Fukami M, Dokiya Y, Izuta T (2001). Effects of high nitrogen load on growth, photosynthesis and nutrient status of Cryptomeria japonica and Pinus densiflora seedlings. Trees, 15, 453-461. DOI URL
[29]	Nielsen SL, Sand-Jensen K (1989). Regulation of photosynthetic rates of submerged rooted macrophytes. Oecologia, 81, 364-368. DOI URL
[30]	Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA (2013). Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications, 4, 2934. DOI: 10.1038/ncomms3934. DOI PMID
[31]	Reich PB, Oleksyn J, Wright IJ (2009). Leaf phosphorus influences the photosynthesis-nitrogen relation: a cross-biome analysis of 314 species. Oecologia, 160, 207-212. DOI URL
[32]	Smith FW, Jackson WA (1987). Nitrogen enhancement of phosphate transport in roots of Zea mays L. Plant Physiology, 84, 1319-1324. DOI PMID
[33]	Sterner RW, Elser JJ (2003). Ecological Stoichiometry. Princeton University Press, Princeton, USA.
[34]	Su SQ, Zhou YM, Qin J, Wang W, Yao WZ, Song L (2012). Physiological responses of Egeria densa to high ammonium concentration and nitrogen deficiency. Chemosphere, 86, 538-545. DOI URL
[35]	Wang CX, He GX, Song ZB, Fan B, Zhang MY, Fang HD, Wang YD, Shi LT (2019). Effects of soil nitrogen and phosphorus levels on leaf nitrogen and phosphorus contents and photosynthesis of Tamarindus indica L. in Yuanjiang and Yuanmou dry-hot valley. Chinese Journal of Ecology, 38, 710-718.
	[ 王春雪, 何光熊, 宋子波, 樊博, 张梦寅, 方海东, 王艳丹, 史亮涛 (2019). 元江元谋干热河谷土壤氮磷水平对酸角叶片氮磷含量及光合的影响. 生态学杂志, 38, 710-718.]
[36]	Wang D, Li HF, Liu F, Wang Y, Zhong YC, He Y, Xiao RL, Wu JS (2016). Interception effect of ecological ditch on nitrogen transport in agricultural runoff in subtropical China. Environmental Science, 37, 1717-1723.
	[ 王迪, 李红芳, 刘锋, 王毅, 钟元春, 何洋, 肖润林, 吴金水 (2016). 亚热带农区生态沟渠对农业径流中氮素迁移拦截效应研究. 环境科学, 37, 1717-1723.]
[37]	Wang LS, Li X, Li YY, Zhang MY, Wu JS (2021). Nitrogen and phosphorus removal in surface flow constructed wetland planted with Myriophyllum elatinoides treating swine wastewater in subtropical central China. Environmental Science, 42, 1433-1442.
	[ 王丽莎, 李希, 李裕元, 张满意, 吴金水 (2021). 亚热带丘陵区绿狐尾藻人工湿地处理养猪废水氮磷去向. 环境科学, 42, 1433-1442.]
[38]	Wang Z (2019). Study on the Response of Ammonium Nitrogen Stress in Water by the Myriophyllum verticillatum L. of Submerged Plant. Master degree dissertation, Shanghai Normal University, Shanghai. 45-46.
	[ 王哲 (2019). 沉水植物狐尾藻(Myriophyllum verticillatum L.)对水体铵态氮胁迫响应的研究. 硕士学位论文, 上海师范大学, 上海. 45-46.]
[39]	Wei XY (2019). Ecological Response of Seed Germination and Seedling Growth of Scirpus mariqueter to Salinity and N/P Ratio Gradients. Master degree dissertation, East China Normal University, Shanghai.
	[ 魏晓宇 (2019). 海三棱藨草种子萌发及幼苗生长对盐度和氮磷比梯度的生态响应. 硕士学位论文, 华东师范大学, 上海.]
[40]	Xiao SM (2019). Effects of Different N Concentrations on Growth and N and P Absorption of Myriophyllume latinoides Gaudich. Master degree dissertation, Hunan Agricultural University, Changsha. 14-44.
	[ 肖顺明 (2019). 不同氮、磷浓度对绿狐尾藻生长及氮、磷吸收的影响研究. 硕士学位论文, 湖南农业大学, 长沙. 14-44.]
[41]	Xu XP, Fu XD, Liao H (2016). Advances in study of ammonium assimilation and its regulatory mechanism in plants. Chinese Bulletin of Botany, 51, 152-166.
	[ 徐晓鹏, 傅向东, 廖红 (2016). 植物铵态氮同化及其调控机制的研究进展. 植物学报, 51, 152-166.] DOI
[42]	Yang HM, Wang DM (2011). Advances in the study on ecological stoichiometry in grass-environment system and its response to environmental factors. Acta Prataculturae Sinica, 20, 244-252.
	[ 杨惠敏, 王冬梅 (2011). 草-环境系统植物碳氮磷生态化学计量学及其对环境因子的响应研究进展. 草业学报, 20, 244-252.]
[43]	Zhan JC, Wang LJ, Huang WD (2002). Effects of low light environment on the growth and photosynthetic characteristics of grape leaves. Journal of China Agricultural University, (3), 75-78.
	[ 战吉成, 王利军, 黄卫东 (2002). 弱光环境下葡萄叶片的生长及其在强光下的光合特性. 中国农业大学学报, (3), 75-78.]
[44]	Zhang SN, Liu F, Xiao RL, He Y, Wu JS (2017). Nitrogen removal in Myriophyllum aquaticum wetland microcosms for swine wastewater treatment: ¹⁵N-labelled nitrogen mass balance analysis. Journal of the Science of Food and Agriculture, 97, 505-511. DOI URL
[45]	Zhang Y, Li BZ, Liu F, Luo P, Wang Y, Liu D, Wu XW, Zhang ZH, Wu JS (2021). Transcriptomic and physiological analysis revealed the ammonium tolerance mechanisms of Myriophyllum aquaticum. Environmental and Experimental Botany, 187, 104462. DOI: 10.1016/j.envexpbot.2021.104462. DOI URL
[46]	Zhang Y, Li BZ, Liu F, Luo P, Xiao RL, Wu JS (2021). Physiological response of Myriophyllum aquaticum exposed to different NH₄⁺/NO₃^- ratios. Journal of Hydroecology, 42(1), 84-90.
	[ 张瑛, 李宝珍, 刘锋, 罗沛, 肖润林, 吴金水 (2021). 绿狐尾藻对不同铵硝配比的生理响应. 水生态学杂志, 42(1), 84-90.]
[47]	Zhao W (2013). Responses of Vallisneria spiralis and Elodea nuttalli to Ammonium Nitrogen and Phosphorus Concentrations in Water Environment. Master degree dissertation, Huazhong Agricultural University, Wuhan. 19-31.
	[ 赵温 (2013). 苦草和伊乐藻对水体铵态氮、磷浓度的响应. 硕士毕业论文, 华中农业大学, 武汉. 19-31.]
[48]	Zhou QY (2017). Ammonium Nitrogen Tolerance Research on Submerged Plant—Myriophlyllum aquaticum. Master degree dissertation, Zhengzhou University, Zhengzhou. 30-61.
	[ 周清扬 (2017). 绿狐尾藻耐铵态氮性能的研究. 硕士学位论文, 郑州大学, 郑州. 30-61.]
[49]	Zhou QY, Gao JQ, Zhang RM, Zhang RQ (2017). Ammonia stress on nitrogen metabolism in tolerant aquatic plant—Myriophyllum aquaticum. Ecotoxicology and Environmental Safety, 143, 102-110. DOI URL
[50]	Zhu HX, Zhang SN, Peng YX, Liu F, Xiao RL (2020). Effect of Myriophyllum elatinoides wetland on nitrogen removal from swine wastewater under different pollution loads. Trans- actions of the Chinese Society of Agricultural Engineering, 36, 217-224.
	[ 朱辉翔, 张树楠, 彭英湘, 刘锋, 肖润林 (2020). 绿狐尾藻湿地对养殖废水中不同污染负荷氮去除效应. 农业工程学报, 36, 217-224.]