Effects of endophytic nitrogen-fixing bacteria on the growth strategy of an invasive plant Sphagneticola trilobata under different nitrogen levels

doi:10.17521/cjpe.2022.0004

Abstract

Abstract:

Aims Many factors can influence the invasiveness of alien plants, and among them endophytes may play a key role. Thus, the aim of this study is to investigate the effects of endophytic nitrogen-fixing bacteria on the growth strategy of invasive plants.

Methods We grew the invasive plant Sphagneticola trilobata and its native congener S. calendulacea infected by endophytic nitrogen-fixing bacteria or not under two nitrogen levels (low and high) and compared their growth and total nitrogen content.

Important findings The endophytic bacteria Kosakonia sp. WTB-JS007, isolated from S. trilobata, had different effects on the growth strategy of the two species (S. trilobata and S. calendulacea) and such an effect did not depend on the nitrogen levels. Under the low nitrogen level, inoculation with WTB-JS007 showed no significant effect on the growth or total nitrogen content of S. calendulacea, but significantly increased aboveground biomass (by 30.48%), promoted stolon length, decreased belowground biomass (by 56.58%), and enhanced total nitrogen content (by 47.51%) of S. trilobata. Similarly, under the high nitrogen level, endophytic bacteria stimulated the aboveground growth of S. trilobata, but had no effect on that of S. calendulacea. These results suggest that endophytic nitrogen-fixing bacteria can differently affect the growth, biomass allocation and nitrogen uptake of invasive and its co-occurring native plant species. Such a difference in the growth strategy can facilitate the rapid growth and expansion of the aboveground part of invasive plants and thus promote their invasiveness.

Key words: invasive plant, aseptic culture system, nitrogen, growth strategy, new habitat expansion

WANG Jing-Jing, WANG Jia-Hao, HUANG Zhi-Yun, Vanessa Chiamaka OKECHUKW, HU Die, QI Shan-Shan, DAI Zhi-Cong, DU Dao-Lin. Effects of endophytic nitrogen-fixing bacteria on the growth strategy of an invasive plant Sphagneticola trilobata under different nitrogen levels[J]. Chin J Plant Ecol, 2023, 47(2): 195-205.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2022.0004

https://www.plant-ecology.com/EN/Y2023/V47/I2/195

Figures/Tables 5

Fig. 1 Identification of nitrogen-fixing bacteria strain WTB-JS007. A, Colony morphology of WTB-JS007 on LB plate. B, Scanning electronic microscopy (SEM) of WTB-JS007. C, Phylogenetic tree of WTB-JS007 based on 16S rRNA gene sequence. D, Nitrogen fixation primer (F1-nifH-3r) PCR amplified gel electrophoresis. E, Phylogenetic tree of WTB-JS007 based on nitrogen fixation gene on the sequence amplified with nitrogen fixation primers. CK, control.

Fig. 2 Leaf area (A), stem length (B), number of roots (C) and root length (D) of Sphagneticola trilobata and S. calendulacea without (CK) or with nitrogen-fixing bacteria (WTB-JS007) under low (Low-N) and normal (Nor-N) nitrogen (mean ± SE, n = 4). Different lowercase letters indicate significant differences (p < 0.05) among different treatments of S. trilobata; different uppercase letters indicate significant differences (p < 0.05) among different treatments of S. calendulacea.

Fig. 3 Aboveground biomass (A), belowground biomass (B), specific leaf area (C) and root:shoot (D) of Sphagneticola trilobata and S. calendulacea without (CK) or with nitrogen-fixing bacteria (WTB-JS007) under low (Low-N) and normal (Nor-N) nitrogen (mean ± SE, n = 4). Different lowercase letters indicate significant differences (p < 0.05) among different treatments of S. trilobata; different uppercase letters indicate significant differences (p < 0.05) among different treatments of S. calendulacea.

Fig. 4 Nitrogen content of Sphagneticola trilobata and S. calendulacea without (CK) or with nitrogen-fixing bacteria (WTB-JS007) under low (Low-N) and normal (Nor-N) nitrogen (mean ± SE, n = 4). Different lowercase letters indicate significant differences (p < 0.05) among different treatments under the low-nitrogen level; different uppercase letters indicate significant differences (p < 0.05) among different treatments under the normal nitrogen level.

Fig. 5 Changes of the growth strategy of Sphagneticola trilobata under the colonization of endophytic nitrogen-fixing bacteria.

References 48

[1]	Adomako MO, Xue W, Du DL, Yu FH (2022). Soil microbe- mediated N:P stoichiometric effects on Solidago canadensis performance depend on nutrient levels. Microbial Ecology, 83, 960-970. DOI
[2]	Anas M, Liao F, Verma KK, Sarwar MA, Mahmood A, Chen ZL, Li Q, Zeng XP, Liu Y, Li YR (2020). Fate of nitrogen in agriculture and environment: agronomic, eco-physiological and molecular approaches to improve nitrogen use efficiency. Biological Research, 53, 47. DOI PMID
[3]	Balasundararajan V, Dananjeyan B (2019). Occurrence of diversified N-acyl homoserine lactone mediated biofilm- forming bacteria in rice rhizoplane. Journal of Basic Microbiology, 59, 1031-1039. DOI PMID
[4]	Bernacchi CJ, Coleman JS, Bazzaz FA, McConnaughay KDM (2000). Biomass allocation in old-field annual species grown in elevated CO₂ environments: no evidence for optimal partitioning. Global Change Biology, 6, 855-863. DOI URL
[5]	Chen L, Liang ZN, Zhu H (2015). Research advances in the studies of plant entophytic. Biotechnology Bulletin, 31, 30-34. DOI
	[陈龙, 梁子宁, 朱华 (2015). 植物内生菌研究进展. 生物技术通报, 31, 30-34.] DOI
[6]	Chen MY, Zhu B, Lin L, Yang LT, Li YR, An QL (2014). Complete genome sequence of Kosakonia sacchari type strain SP₁^T. Standards in Genomic Sciences, 9, 1311-1318. DOI URL
[7]	Cocking EC (2003). Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant and Soil, 252, 169-175. DOI URL
[8]	Dai ZC, Du DL, Si CC, Lin Y, Hao JL, Sun F (2009). A method to exactly measure the morphological quantity of leaf using Scanner and Image J Software. Guihaia, 29, 342-347.
	[戴志聪, 杜道林, 司春灿, 林英, 郝建良, 孙凤 (2009). 用扫描仪及Image J软件精确测量叶片形态数量特征的方法. 广西植物, 29, 342-347.]
[9]	Dai ZC, Fu W, Wan LY, Cai HH, Wang N, Qi SS, Du DL (2016). Different growth promoting effects of endophytic bacteria on invasive and native clonal plants. Frontiers in Plant Science, 7, 706. DOI: 10.3389/fpls.2016.00706. DOI
[10]	Dai ZC, Wan LY, Qi SS, Rutherford S, Ren GQ, Wan JSH, Du DL (2020). Synergy among hypotheses in the invasion process of alien plants: a road map within a timeline. Perspectives in Plant Ecology, Evolution and Systematics, 47, 125575. DOI: 10.1016/j.ppees.2020.125575. DOI
[11]	Dipta B, Bhardwaj S, Kaushal M, Kirti S, Sharma R (2019). Obliteration of phosphorus deficiency in plants by microbial interceded approach. Symbiosis, 78, 163-176. DOI
[12]	Fedorov DN, Ivanova EG, Doronina NV, Trotsenko IA (2008). A new system of degenerate oligonucleotide primers for detection and amplification of nifHD genes. Mikrobiologiia, 77, 286-288. PMID
[13]	Franche C, Lindström K, Elmerich C (2009). Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant and Soil, 321, 35-59. DOI URL
[14]	Funk JL (2008). Differences in plasticity between invasive and native plants from a low resource environment. Journal of Ecology, 96, 1162-1173. DOI URL
[15]	Funk JL (2013). The physiology of invasive plants in low-resource environments. Conservation Physiology, 1, cot026. DOI: 10.1093/conphys/cot026. DOI
[16]	Hardoim PR, van Overbeek LS, van Elsas JD (2008). Properties of bacterial endophytes and their proposed role in plant growth. Trends in Microbiology, 16, 463-471. DOI PMID
[17]	Hoagland DR, Arnon DI (1950). The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular, 347, 23-32.
[18]	Javed Q, Sun JF, Azeem A, Jabran K, Du DL (2020). Competitive ability and plasticity of Wedelia trilobata (L.) under wetland hydrological variations. Scientific Reports, 10, 9431. DOI: 10.1038/s41598-020-66385-z. DOI
[19]	Leishman MR, Haslehurst T, Ares A, Baruch Z (2007). Leaf trait relationships of native and invasive plants: community- and global-scale comparisons. New Phytologist, 176, 635-643. DOI PMID
[20]	Li H, Liao D, Su JQ, Huang FY, Hong YW (2014). Diversity and function of endophytic bacteria in roots of exotic plant Spartina alterniflora. Chinese Journal of Applied and Environmental Biology, 20, 856-862.
	[李虎, 廖丹, 苏建强, 黄福义, 洪有为 (2014). 外来种互花米草根内细菌多样性及功能. 应用与环境生物学报, 20, 856-862.]
[21]	Li Q, Chen Q, He FR, Bharani M, Dai ZC, Qi SS, Du DL (2020). Arbuscular mycorrhizal fungi promote the growth of Wedelia trilobata and the absorption of insoluble phosphorus. Journal of Tropical and Subtropical Botany, 28, 339-346.
	[李琴, 陈琪, 贺芙蓉, Bharani M, 戴志聪, 祁珊珊, 杜道林 (2020). 丛枝菌根真菌促进南美蟛蜞菊生长及对难溶磷的吸收. 热带亚热带植物学报, 28, 339-346.]
[22]	Littschwager J, Lauerer M, Blagodatskaya E, Kuzyakov Y (2010). Nitrogen uptake and utilisation as a competition factor between invasive Duchesnea indica and native Fragaria vesca. Plant and Soil, 331, 105-114. DOI URL
[23]	Liu YT, Dai ZC, Xue YL, Sun JF, Zhu F, Du DL (2013). Prediction of suitable area of an alien invasive species (Wedelia trilobata) in China. Guangdong Agricultural Sciences, 40(14), 174-178.
	[刘勇涛, 戴志聪, 薛永来, 孙见凡, 朱方, 杜道林 (2013). 外来入侵植物南美蟛蜞菊在中国的适生区预测. 广东农业科学, 40(14), 174-178.]
[24]	Matzek V (2011). Superior performance and nutrient-use efficiency of invasive plants over non-invasive congeners in a resource-limited environment. Biological Invasions, 13, 3005-3014. DOI URL
[25]	Mei C, Flinn BS (2010). The use of beneficial microbial endophytes for plant biomass and stress tolerance improvement. Recent Patents on Biotechnology, 4, 81-95. PMID
[26]	Murashige T, Skoog F (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum, 15, 473-497. DOI URL
[27]	Noori F, Etesami H, Najafi Zarini H, Khoshkholgh-Sima NA, Hosseini Salekdeh G, Alishahi F (2018). Mining alfalfa (Medicago sativa L.) nodules for salinity tolerant non- rhizobial bacteria to improve growth of alfalfa under salinity stress. Ecotoxicology and Environmental Safety, 162, 129-138. DOI URL
[28]	Oldroyd GED, Leyser O (2020). A plantʼs diet, surviving in a variable nutrient environment. Science, 368, eaba0196. DOI: 10.1126/science.aba0196. DOI
[29]	Paini DR, Sheppard AW, Cook DC, de Barro PJ, Worner SP, Thomas MB. (2016). Global threat to agriculture from invasive species. Proceedings of the National Academy of Sciences of the United States of America, 113, 7575-7579. DOI PMID
[30]	Pang F, Xia WK, He M, Qi SS, Dai ZC, Du DL (2020). Nitrogen-fixing bacteria alleviates competition between arbuscular mycorrhizal fungi and Solidago canadensis for nutrients under nitrogen limitation. Chinese Journal of Plant Ecology, 44, 782-790. DOI URL
	[庞芳, 夏维康, 何敏, 祁珊珊, 戴志聪, 杜道林 (2020). 固氮菌缓解氮限制环境中丛枝菌根真菌对加拿大一枝黄花的营养竞争. 植物生态学报, 44, 782-790.]
[31]	Pyšek P, Hulme PE, Simberloff D, Bacher S, Blackburn TM, Carlton JT, Dawson W, Essl F, Foxcroft LC, Genovesi P, Jeschke JM, Kühn I, Liebhold AM, Mandrak NE, Meyerson LA, et al. (2020). Scientists’ warning on invasive alien species. Biological Reviews of the Cambridge Philosophical Society, 95, 1511-1534. DOI URL
[32]	Qi SS, Dai ZC, Miao SL, Zhai DL, Si CC, Huang P, Wang RP, Du DL (2014). Light limitation and litter of an invasive clonal plant, Wedelia trilobata, inhibit its seedling recruitment. Annals of Botany, 114, 425-433. DOI URL
[33]	Qi SS, He FR, Wang JJ, Li Q, Dai ZC, Du DL (2020). Effects of arbuscular mycorrhizal fungi on the growth and the competition of an invasive plant Wedelia trilobata. Microbiology China, 47, 3801-3810.
	[祁珊珊, 贺芙蓉, 汪晶晶, 李琴, 戴志聪, 杜道林 (2020). 丛枝菌根真菌对入侵植物南美蟛蜞菊生长及竞争力的影响. 微生物学通报, 47, 3801-3810.]
[34]	Ren GQ, He FR, Sun JF, Hu WJ, Azeem A, Qi SS, Yang B, Cui MM, Jiang K, Du DL (2021). Resource conservation strategy helps explain patterns of biological invasion in a low-N environment. Biochemical Systematics and Ecology, 94, 104295. DOI: 10.1016/j.bse.2020.104205. DOI
[35]	Ren GQ, Li Q, Li Y, Li J, Adomako MO, Dai ZC, Li GL, Wan LY, Zhang B, Zou CB, Ran Q, Du DL (2019). The enhancement of root biomass increases the competitiveness of an invasive plant against a co-occurring native plant under elevated nitrogen deposition. Flora, 261, 151486. DOI: 10.1016/j.flora.2019.151486. DOI
[36]	Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006). Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters, 9, 981-993. PMID
[37]	Rosenblueth M, Martínez-Romero E (2006). Bacterial endophytes and their interactions with hosts. Molecular Plant-Microbe Interactions, 19, 827-837. DOI PMID
[38]	Rout ME, Chrzanowski TH, Westlie TK, DeLuca TH, Callaway RM, Holben WE (2013). Bacterial endophytes enhance competition by invasive plants. American Journal of Botany, 100, 1726-1737. DOI PMID
[39]	Sambrook HC (1989). Molecular cloning : a laboratory manual. Cold Spring Harbor Perspectives in Biology, 10, 5-10.
[40]	Saravanan VS, Madhaiyan M, Osborne J, Thangaraju M, Sa TM (2008). Ecological occurrence of Gluconacetobacter diazotrophicus and nitrogen-fixing Acetobacteraceae members: their possible role in plant growth promotion. Microbial Ecology, 55, 130-140. PMID
[41]	Sardans J, Peñuelas J (2012). The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiology, 160, 1741-1761. DOI PMID
[42]	Wan FH, Guo JY, Wang DH (2002). Alien invasive species in China: their damages and management strategies. Biodiversity Science, 10, 119-125. DOI URL
	[万方浩, 郭建英, 王德辉 (2002). 中国外来入侵生物的危害与管理对策. 生物多样性, 10, 119-125.] DOI
[43]	Wang MN, Dai ZC, Qi SS, Wang XY, Du DL (2014). Main hypotheses and research progress of alien plant invasion mechanism. Jiangsu Agricultural Sciences, 42, 378-382.
	[王明娜, 戴志聪, 祁珊珊, 王晓莹, 杜道林 (2014). 外来植物入侵机制主要假说及其研究进展. 江苏农业科学, 42, 378-382.]
[44]	Wang YJ, Chen D, Yan R, Yu FH, van Kleunen M (2019). Invasive alien clonal plants are competitively superior over co-occurring native clonal plants. Perspectives in Plant Ecology, Evolution and Systematics, 40, 125484. DOI: 10.1016/j.ppees.2019.125484. DOI
[45]	Wang YJ, Müller-Schärer H, van Kleunen M, Cai AM, Zhang P, Yan R, Dong BC, Yu FH (2017). Invasive alien plants benefit more from clonal integration in heterogeneous environments than natives. New Phytologist, 216, 1072-1078. DOI URL
[46]	Wu YM, Leng ZR, Li J, Jia H, Yan CL, Hong HL, Wang Q, Lu YY, Du DL (2022). Increased fluctuation of sulfur alleviates cadmium toxicity and exacerbates the expansion of Spartina alterniflora in coastal wetlands. Environmental Pollution, 292, 118399. DOI: 10.1016/j.envpol.2021.118399. DOI
[47]	Wu YQ, Hu YJ, Liao FL (2005). Wedelia trilobata—A species from introduced to potential invasive. Guihaia, 25, 413-418.
	[吴彦琼, 胡玉佳, 廖富林 (2005). 从引进到潜在入侵的植物——南美蟛蜞菊. 广西植物, 25, 413-418.]
[48]	Yu WB, Li SP (2020). Modern coexistence theory as a framework for invasion ecology. Biodiversity Science, 28, 1362-1375. DOI URL