三种盐胁迫对互花米草和芦苇光合作用的影响

doi:10.17521/cjpe.2015.0010

摘要/Abstract

摘要：

互花米草(Spartina alterniflora)的入侵给海岸带盐沼生态系统的结构和功能带来了显著影响。互花米草盐沼中的硫含量高于附近的土著芦苇(Phragmites australis)盐沼。为探讨硫元素对互花米草和芦苇竞争过程的可能影响及其作用机制, 以50 mmol·L^-1的Na₂SO₄和Na₂S对互花米草和芦苇进行处理, 分析处理前后5天内两种植物光合气体交换和叶绿素荧光指标变化的差异, 实验另设等Na⁺浓度的NaCl处理作为比较。研究发现: Na₂S对互花米草和芦苇光合作用影响的差异最大, NaCl次之, Na₂SO₄最小。Na₂S处理后, 互花米草净光合速率(P_n)出现显著上升, 芦苇P_n值大幅度下降。互花米草的光饱和点(I_sat)上升而芦苇的I_sat值无变化。表明Na₂S处理对互花米草的光合能力有促进作用, 但对芦苇的光合能力有抑制作用。NaCl处理后互花米草P_n值也出现小幅上升, 而芦苇P_n值略有下降。Na₂SO₄处理对互花米草和芦苇的P_n值均无显著影响。除Na₂SO₄处理的互花米草外, 不同盐处理后的互花米草和芦苇非光化学淬灭(NPQ)均出现上升趋势。研究结果表明互花米草对环境硫胁迫的适应能力显著高于芦苇, 暗示盐沼高硫环境尤其是硫化物有助于互花米草相对于芦苇的竞争, 也很可能是其形成单一植被的重要原因之一。

关键词: 生物入侵, 盐沼生态系统, 互花米草, 芦苇, 硫环境, 盐胁迫, 光合作用

Abstract: Aims

The invasion of Spartina alterniflora has imposed significant influences on structure and functioning of coastal saltmarshes. The Spartina marsh has been found to contain relatively higher sulfur content than the adjacent native Phragmites marsh. This research is aimed to investigate if sulfur helps with S. alterniflora in competition over Phragmites australis.

<i>Methods</i>

Seedlings of S. alterniflora and P. australis were grown in an imitated mesocosm on the campus of Nanjing University. Three common salts of the sea water, Na₂SO₄, Na₂S and NaCl were respectively added to the cultural medium. Light response curves of the plants before and during the four days of treatments were obtained by measuring gas exchange with varying light levels. Maximum quantum yield of photosynthesis II (PSII) and light induction curves were also measured by chlorophyll fluorescence analysis.

<i>Important findings</i>

Among the three salts, Na₂S caused the greatest difference in the response of photosynthesis between S. alterniflora and P. australis, and Na₂SO₄ had the least effect. The Na₂S treatment significantly increased net photosynthetic rate (P_n) and light saturation point (I_sat) in S. alterniflora, but decreased P_n in P. australis. The NaCl treatment also increased P_n in S. alterniflora to a less degree and decreased P_n in P. australis. The Na₂SO₄ treatment had little effect on P_n in both S. alterniflora and P. australis. The non-photochemical quenching (NPQ) in P. australis were promoted by all three salts, whereas it was only affected by Na₂S and NaCl in S. alterniflora. Our results suggest that S. alterniflora has significantly greater tolerance to sulfate and sulfide than P. australis. Therefore, sulfuric compounds and especially sulfide in saltmarsh environments might benefit the competition of S. alterniflora over P. australis, which could contribute to the formation of the mono-specific vegetation of the invasive S. alterniflora.

Key words: biological invasion, saltmarsh ecosystem, Spartina alterniflora, Phragmites australis, sulfur enviroment, salt stress, photosynthesis

胡楚琦, 刘金珂, 王天弘, 王文琳, 卢山, 周长芳. 三种盐胁迫对互花米草和芦苇光合作用的影响. 植物生态学报, 2015, 39(1): 92-103. DOI: 10.17521/cjpe.2015.0010

HU Chu-Qi,LIU Jin-Ke,WANG Tian-Hong,WANG Wen-Lin,LU Shan,ZHOU Chang-Fang. Influence of three types of salt stress on photosynthesis in Spartina alterniflora and Phragmites australis. Chinese Journal of Plant Ecology, 2015, 39(1): 92-103. DOI: 10.17521/cjpe.2015.0010

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2015.0010

https://www.plant-ecology.com/CN/Y2015/V39/I1/92

图/表 8

参考文献 40

35	(in Chinese with English abstract) [袁琳, 张利权, 古志钦 (2010). 入侵植物互花米草(Spartina alterniflora)叶绿素荧光对淹水胁迫的响应. 环境科学学报, 30, 882-889.]
36	Zhou CF, An SQ, Deng ZF, Yin DQ, Zhi YB, Sun ZY, Zhao H, Zhou LX, Fang C, Qian C (2009). Sulfur storage changed by exotic Spartina alterniflora in coastal saltmarshes of China. Ecological Engineering, 35, 536-543.
37	Zhou CF, An SQ, Zhao CJ, Fang C, Lu XM, Zhao H, Liu JN (2009). Th`e influence of Spartina alterniflora invasion on emission of DMS and N2O in coastal salt marsh. Marine Sciences, 33(2), 17-21.
	(in Chinese with English abstract) [周长芳, 安树青, 赵聪蛟, 方超, 陆霞梅, 赵晖, 刘静娜 (2009). 互花米草入侵对海岸盐沼二甲基硫及氧化亚氮气体释放的影响. 海洋科学, 33(2), 17-21.]
38	Zhou CF, Shen WY, Lu CM, Wang HX, Xiao Y, Zhao YQ, An SQ (2014). Effects of salinity on the photosynthesis of two Poaceous Halophytes. Clean-Soil, Air, Water, doi: 10.1002/clen.201300840.
39	Zhu XG, Zhang QD (1999). Advances in the research on the effects of NaCl on photosynthesis. Chinese Bulletin of Botany, 16, 332-338.
	(in Chinese with English abstract) [朱新广, 张其德 (1999). NaCl对光合作用影响的研究进展. 植物学通报, 16, 332-338.]
40	Zhu YH, Tu NM, Xiao HQ, Guan GS, Wang H, Cai Q, Deng LC, Wei Y, Yi D, Huang ZC, Li HL (2008). Effects of sulfur nutrition on photosynthesis and chlorophyll fluorescence of tobacco leaves. Acta Ecologica Sinica, 28, 1000-1005.
1	An SQ, Gu BH, Zhou CF, Wang ZS, Deng ZF, Zhi YB, Li HL, Chen L, Yu DH, Liu YH (2007).Spartina invasion in China: Implications for invasive species management and future research. Weed Research, 47, 183-191.
2	Anttila CK, Daehler CC, Rank NE, Strong DR (1998). Greater male fitness of a rare invader (Spartina alterniflora, Poaceae) threatens a common native (Spartina foliosa) with hybridization. American Journal of Botany, 85, 1597-1601.
3	Arim M, Abades SR, Neill PE, Lima M, Marquet PA (2006). Spread dynamics of invasive species. Proceedings of the National Academy of Sciences of the United States of America, 103, 374-378.
4	Armstrong J, Armstrong W (2005). Rice: sulfide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Annals of Botany, 96, 625-638.
5	Belnap J, Phillips SL, Sherrod SK, Moldenke A (2005). Soil biota can change after exotic plant invasion: Does this affect ecosystem processes?Ecology, 86, 3007-3017.
6	Carlson PR, Forrest J (1982). Uptake of dissolved sulfide by Spartina alterniflora: Evidence from natural sulfur isotope abundance ratios. Science, 216, 633-635.
7	Chen ZY, Li B, Chen JK (2004). Ecological consequences and management of Spartina spp. invasions in coastal ecosystems. Biodiversity Science, 12, 280-289.
	(in Chinese with English abstract) [陈中义, 李博, 陈家宽 (2004). 米草属植物入侵的生态后果及管理对策. 生物多样性, 12, 280-289.]
8	Chung C (2006). Forty years of ecological engineering with Spartina plantations in China. Ecological Engineering, 27, 49-57.
9	Daehler CC, Strong DR (1996). Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in pacific estuaries, USA. Biological Conservation, 78, 51-58.
10	Deng ZF, An SQ, Zhi YB, Zhou CF, Chen L, Zhao CJ, Fang SB, Li HL (2006). Preliminary studies on invasive model and outbreak mechanism of exotic species, Spartina alterniflora Loisel. Acta Ecologica Sinica, 26, 2678-2686.
	(in Chinese with English abstract) [邓自发, 安树青, 智颖飙, 周长芳, 陈琳, 赵聪蛟, 方淑波, 李红丽 (2006). 外来种互花米草入侵模式与爆发机制. 生态学报, 26, 2678-2686.]
11	Fang C, Zhao H, Zhou CF, Lu XM, Chen FF, Yang Q, An SQ (2007). The impact of Spartina alterniflora invasion on soil properties of coastal salt marsh in China. Journal of Nanjing University(Natural Scincnce), 43, 274-283.
	(in Chinese with English abstract) [方超, 赵晖, 周长芳, 陆霞梅, 陈奋飞, 杨茜, 安树青 (2007). 互花米草入侵对我国海岸盐沼土壤特性的影响. 南京大学学报(自然科学版), 43, 274-283.]
12	Gao S, Tanji KK, Scardaci SC (2004). Impact of rice straw incorporation on soil redox status and sulfide toxicity. Agronomy Journal, 96, 70-76.
13	Gu ZQ, Zhang LQ (2009). Physiological responses of Spartina alterniflora to long-term waterlogging stress. Acta Scientiae Circumstantiae, 29, 876-881.
	(in Chinese with English abstract) [古志钦, 张利权 (2009). 互花米草对持续淹水胁迫的生理响应. 环境科学学报, 29, 876-881.]
14	Hulme PE, Pysek P, Nentwig W, Vilà M (2009). Will threat of biological invasions unite the European Union?Science, 324, 40-41.
15	Jiang GM, Zhu GJ (2001). Effects of natural high temperature and irradiation on photosynthesis and related parameters in three arid sandy shrub species. Acta Phytoecologica Sinica, 25, 525-531.
	(in Chinese with English abstract) [蒋高明, 朱桂杰 (2001). 高温强光环境条件下3种沙地灌木的光合生理特点.植物生态学报, 25, 525-531.]
16	Kang H, Shi GY, Li JM (2009). Effects of NaCl stress on photosynthesis and parameters of Spartina alterniflora. Guangxi Sciences, 16, 451-454.
	(in Chinese with English abstract) [康浩, 石贵玉, 李佳枚 (2009). NaCl胁迫对互花米草光合作用及其参数的影响. 广西科学, 16, 451-454.]
17	Kathilankal JC, Mozdzer TJ, Fuentes JD, McGlathery KJ, D’Odorico P, Zieman JC (2011). Physiological responses of Spartina alterniflora to varying environmental conditions in Virginia marshes. Hydrobiologia, 669, 167-181.
18	Klepac-Ceraj V, Bahr M, Crump BC, Teske AP, Hobbie JE, Polz MF (2004). High overall diversity and dominance of microdiverse relationships in salt marsh sulphate-reducing bacteria. Environmental Microbiology, 6, 686-698.
19	Kocsis MG, Nolte KD, Rhodes D, Shen TL, Gage DA, Hanson AD (1998). Dimethylsulfoniopropionate biosynthesis in Spartina alterniflora. Plant Physiology, 117, 273-281.
20	Liang X, Zhang LQ, Zhao GQ (2006). A comparison of photosynthetic characteristics between Spartina alterniflora and Phragmites australis under different CO2 concentrations. Acta Ecologica Sinica, 26, 842-848.
	(in Chinese with English abstract) [梁霞, 张利权, 赵广琦 (2006). 芦苇与外来植物互花米草在不同CO2浓度下的光合特性比较. 生态学报, 26, 842-848.]
21	Maxwell K, Johnson GN (2000). Chlorophyll fluorescence—A practical guide. Journal of Experimental Botany, 51, 659-668.
22	Naidoo G, McKee KL, Mendelssohn IA (1992). Anatomical and metabolic responses to waterlogging and salinity in Spartina alterniflora and S. patens (Poaceae). American Journal of Botany, 79, 765-770.
23	Otte ML, Wilson G, Morris JT, Moran BM (2004). Dimethylsulphoniopropionate (DMSP) and related compounds in higher plants. Journal of Experimental Botany, 55, 1919-1925.
24	Pagter M, Bragato C, Malagoli M, Brix H (2009). Osmotic and ionic effects of NaCl and Na2SO4 salinity on Phragmites australis. Aquatic Botany, 90, 43-51.
25	Renny-Byfield S, Ainouche M, Leitch IJ, Lim KY, Le Comber SC, Leitch AR (2010). Flow cytometry and GISH reveal mixed ploidy populations and Spartina nonaploids with genomes of S. alterniflora and S. maritime origin. Annals of Botany, 105, 527-533.
26	Seliskar DM, Smart KE, Higashikubo BT, Gallagher JL (2004). Seedling sulfide sensitivity among plant species colonizing Phragmites-infested wetlands. Wetlands, 24, 426-433.
27	Shen WY, Lu CM, Zhou CF (2011). Antioxidant systems of Spartina alterniflora and Phragmites australis responded differently to environmental sulfur stress. Journal of Fudan University(Natural Scincnce), 50, 653-661.
	(in Chinese with English abstract ) [沈文燕, 陆长梅, 周长芳 (2011). 互花米草和芦苇抗氧化系统在抵御硫胁迫过程中的响应差异. 复旦学报(自然科学版), 50, 653-661.]
28	Stribling JM (1997). The relative importance of sulfate availability in the growth of Spartina alterniflora and Spartina cynosuroides. Aquatic Botany, 56, 131-143.
29	Wang Q, An SQ, Ma ZJ, Zhao B, Chen JK, Li B (2006). Invasive Spartina alterniflora: Biology, ecology and management. Acta Phytotaxonomica Sinica, 44, 559-588.
	(in Chinese with English abstract) [王卿, 安树青, 马志军, 赵斌, 陈家宽, 李博 (2006). 入侵植物互花米草——生物学、生态学及管理. 植物分类学报, 44, 559-588.]
30	Wu Y, Gao L, Cao MJ, Xiang CB (2007). Plant sulfur metabolism, regulation, and biological functions. Chinese Bulletin of Botany, 24, 735-761.
	(in Chinese with English abstract) [吴宇, 高蕾, 曹民杰, 向成斌 (2007). 植物硫营养代谢、调控与生物学功能. 植物学通报, 24, 735-761.]
31	Xiao Y, Tang JB, An SQ (2011). Responses of growth and sexual reproduction of Phragmites australis and Spartina alterniflora to salinity stress. Chinese Journal of Ecology, 30, 267-272.
	(in Chinese with English abstract) [肖燕, 汤俊兵, 安树青 (2011). 芦苇、互花米草的生长和繁殖对盐分胁迫的响应. 生态学杂志, 30, 267-272.]
32	Ye Q, Hou ZH, Liu J, Liu RQ, Liu X (2011). H2O2 involvement in H2S-induced stomatal closure of Arabidopsis thaliana L. Plant Physiology Journal, 47, 1195-1200.
	(in Chinese with English abstract) [叶青, 侯智慧, 刘菁, 刘瑞清, 刘新 (2011). H2O2介导H2S诱导的拟南芥气孔关闭. 植物生理学报, 47, 1195-1200.]
33	Ye ZP, Yu Q (2007). Comparison of a new model of light response of photosynthesis with traditional models. Journal of Shenyang Agriculture University, 38, 771-775.
	(in Chinese with English abstract) [叶子飘, 于强 (2007). 一个光合作用光响应新模型与传统模型的比较. 沈阳农业大学学报, 38, 771-775.]
34	Ye ZP, Yu Q (2008). Comparison of new and several classical models of photosynthesis in response to irradiance. Journal of Plant Ecology (Chinese Version), 32, 1356-1361.
	(in Chinese with English abstract) [叶子飘, 于强 (2008). 光合作用光响应模型的比较. 植物生态学报, 32, 1356-1361.]
35	Yuan L, Zhang LQ, Gu ZQ (2010). Responses of chlorophyll fluorescence of an invasive plant Spartina alterniflora to continuous waterlogging. Acta Scientiae Circumstantiae, 30, 882-889.
40	(in Chinese with English abstract) [朱英华, 屠乃美, 肖汉乾, 关广晟, 王辉, 蔡奇, 邓力超, 危跃, 易迪, 黄泽春, 李海林 (2008). 硫对烟草叶片光合特性和叶绿素荧光参数的影响. 生态学报, 28, 1000-1005.]

处理后天数 Day after treatment	互花米草 S. alterniflora			芦苇 P. australis
处理后天数 Day after treatment	Na₂SO₄	Na₂S	NaCl	Na₂SO₄	Na₂S	NaCl
0	19.92 ± 1.44^a	21.25 ± 0.58^a	16.53 ± 1.33^a	17.89 ± 1.90^a	17.98 ± 2.50^a	15.65 ± 0.24^a
1	18.43 ± 1.30^a	23.61 ± 1.67^ab	16.16 ± 0.91^a	16.36 ± 2.75^a	14.03 ± 3.19^a	15.76 ± 2.20^a
2	18.67 ± 1.80^a	25.39 ± 1.16^b	18.11 ± 1.48^a	16.81 ± 2.21^a	15.08 ± 2.52^a	14.54 ± 0.12^a
3	20.36 ± 1.12^a	24.41 ± 0.58^ab	19.33 ± 1.42^a	17.47 ± 2.27^a	13.54 ± 2.43^a	13.07 ± 1.44^a
4	22.07 ± 2.05^a	26.11 ± 0.43^b	17.60 ± 1.31^a	16.93 ± 2.42^a	11.64 ± 3.81^a	12.42 ± 1.07^a

处理后天数 Day after treatment	互花米草 S. alterniflora			芦苇 P. australis
处理后天数 Day after treatment	Na₂SO₄	Na₂S	NaCl	Na₂SO₄	Na₂S	NaCl
0	19.92 ± 1.44^a	21.25 ± 0.58^a	16.53 ± 1.33^a	17.89 ± 1.90^a	17.98 ± 2.50^a	15.65 ± 0.24^a
1	18.43 ± 1.30^a	23.61 ± 1.67^ab	16.16 ± 0.91^a	16.36 ± 2.75^a	14.03 ± 3.19^a	15.76 ± 2.20^a
2	18.67 ± 1.80^a	25.39 ± 1.16^b	18.11 ± 1.48^a	16.81 ± 2.21^a	15.08 ± 2.52^a	14.54 ± 0.12^a
3	20.36 ± 1.12^a	24.41 ± 0.58^ab	19.33 ± 1.42^a	17.47 ± 2.27^a	13.54 ± 2.43^a	13.07 ± 1.44^a
4	22.07 ± 2.05^a	26.11 ± 0.43^b	17.60 ± 1.31^a	16.93 ± 2.42^a	11.64 ± 3.81^a	12.42 ± 1.07^a

处理后天数 Day after treatment	互花米草 S. alterniflora			芦苇 P. australis
处理后天数 Day after treatment	Na₂SO₄	Na₂S	NaCl	Na₂SO₄	Na₂S	NaCl
0	0.048 ± 0.004^a	0.050 ± 0.001^a	0.041 ± 0.000^a	0.038 ± 0.003^a	0.037 ± 0.001^a	0.036 ± 0.002^ab
1	0.047 ± 0.002^a	0.045 ± 0.002^ab	0.045 ± 0.000^ab	0.039 ± 0.001^a	0.026 ± 0.005^a	0.038 ± 0.002^ab
2	0.048 ± 0.004^a	0.040 ± 0.002^b	0.043 ± 0.003^ab	0.039 ± 0.004^a	0.028 ± 0.005^a	0.034 ± 0.003^a
3	0.054 ± 0.002^a	0.042 ± 0.003^ab	0.045 ± 0.003^ab	0.038 ± 0.003^a	0.030 ± 0.006^a	0.041 ± 0.001^b
4	0.050 ± 0.001^a	0.046 ± 0.003^ab	0.050 ± 0.003^b	0.037 ± 0.001^a	0.027 ± 0.006^a	0.038 ± 0.001^ab

处理后天数 Day after treatment	互花米草 S. alterniflora			芦苇 P. australis
处理后天数 Day after treatment	Na₂SO₄	Na₂S	NaCl	Na₂SO₄	Na₂S	NaCl
0	0.048 ± 0.004^a	0.050 ± 0.001^a	0.041 ± 0.000^a	0.038 ± 0.003^a	0.037 ± 0.001^a	0.036 ± 0.002^ab
1	0.047 ± 0.002^a	0.045 ± 0.002^ab	0.045 ± 0.000^ab	0.039 ± 0.001^a	0.026 ± 0.005^a	0.038 ± 0.002^ab
2	0.048 ± 0.004^a	0.040 ± 0.002^b	0.043 ± 0.003^ab	0.039 ± 0.004^a	0.028 ± 0.005^a	0.034 ± 0.003^a
3	0.054 ± 0.002^a	0.042 ± 0.003^ab	0.045 ± 0.003^ab	0.038 ± 0.003^a	0.030 ± 0.006^a	0.041 ± 0.001^b
4	0.050 ± 0.001^a	0.046 ± 0.003^ab	0.050 ± 0.003^b	0.037 ± 0.001^a	0.027 ± 0.006^a	0.038 ± 0.001^ab

处理后天数 Day after treatment	互花米草 S. alterniflora			芦苇 P. australis
处理后天数 Day after treatment	NaCl	Na₂SO₄	Na₂S	NaCl	Na₂SO₄	Na₂S
0	2 440.0 ± 136.2^a	2 067.1 ± 75.6^a	2 258.1 ± 198.7^a	1 815.1 ± 166.1^a	2 081.2 ± 169.7^a	1 911.2 ± 77.0^a
1	2 517.8 ± 180.3^a	2 366.9 ± 413.6^a	2 246.4 ± 124.7^a	1 958.9 ± 66.4^a	1 943.5 ± 239.8^a	2 141.6 ± 113.0^a
2	2 520.5 ± 0.8^a	2 221.7 ± 315.2^a	2 313.3 ± 182.0^a	1 973.9 ± 132.6^a	1 970.5 ± 130.5^a	1 924.3 ± 124.7^a
3	2 475.9 ± 149.5^a	1 951.2 ± 224.0^a	2 438.8 ± 170.1^a	1 747.9 ± 161.2^a	1 942.0 ± 98.4^a	2 054.1 ± 98.6^a
4	2 371.4 ± 191.0^a	2 230.3 ± 114.1^a	2 613.2 ± 191.2^a	1 905.5 ± 118.9^a	1 917.9 ± 177.4^a	1 788.5 ± 114.7^a