Nitrogen-fixing bacteria alleviates competition between arbuscular mycorrhizal fungi and Solidago canadensis for nutrients under nitrogen limitation

doi:10.17521/cjpe.2020.0114

Abstract

Abstract:

Aims Arbuscular mycorrhizal fungi (AMF) form symbiotic relationships with most terrestrial plants, contributing to the nutrient uptake of host plants. While little is known on how rhizospheric microorganisms affect the relationships between AMF and host plants under nutritional stress. We hypothesize that AMF may compete for nutrients with host plants in extremely nutrient-limited environments, such as nitrogen deficient habitats, and nitrogen-fixing bacteria will alleviate the competition.
Methods In order to test our hypotheses, we grew Solidago canadensis plants under nitrogen deficient treatments. We inoculated plants with AMF and a nitrogen-fixing bacterium to test the relationships among the host plant and microorganisms.
Important findings Under the lowest nitrogen level (0.025 mmol·L^-1 N of ammonium nitrogen), the growth of S. canadensis was more restricted with AMF colonization, suggesting competition between AMF and the host. However, with the inoculation of nitrogen-fixing bacterium, AMF colonization was promoted and plant growth was increased. These results indicate that nitrogen-fixing bacteria could moderate the competition for nutrients between AMF and their host under nitrogen deficiency. This study improves our understanding of the invasion mechanisms of alien plants, where they interact with different microorganisms under extreme nutrient stress.

Key words: arbuscular mycorrhizal fungi, nitrogen limitation, nutrients competition, nitrogen-fixing bacteria, invasive plant

PANG Fang, XIA Wei-Kang, HE Min, QI Shan-Shan, DAI Zhi-Cong, DU Dao-Lin. Nitrogen-fixing bacteria alleviates competition between arbuscular mycorrhizal fungi and Solidago canadensis for nutrients under nitrogen limitation[J]. Chin J Plant Ecol, 2020, 44(7): 782-790.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2020.0114

https://www.plant-ecology.com/EN/Y2020/V44/I7/782

Figures/Tables 8

Fig. 1 Electrophoretogram of the isolated nitrogen-fixing bacterium. A, 16S rDNA. B, Nitrogen-fixing gene nifH. DL, DNA marker; NC, negative control; JS106, Paenibacillus stellifer ScRB-JS106.

Fig. 2 Neighbour-joining tree of the isolated nitrogen-fixing bacterium, ScRB-JS106, based on 16S rDNA. Sequences for the other isolates were downloaded from GenBank.

Fig. 3 Growth of Solidago canadensis under different concentrations of ammonium chloride (mean ± SE, n = 4). CK, negative control (10 mmol·L-1 N). Different lowercase letters indicate significant differences (Duncan’s test, p < 0.05).

Fig. 4 Growth of Solidago canadensis under different concentrations of potassium nitrate (mean ± SE, n = 4). CK, negative control (10 mmol·L-1 N). Different lowercase letters indicate significant differences (Duncan’s test, p < 0.05).

Fig. 5 Root colonization rate of Solidago canadensis inoculated with various arbuscular mycorrhizal fungi and nitrogen-fixing bacteria (mean ± SE, n = 6). A, Glomus etunicatum (GE). B, Glomus intraradices (GI). C, Glomus mosseae (GM). JS106, Paenibacillus stellifer ScRB-JS106. ns, no significant difference (p > 0.05).

Fig. 6 Growth of Solidago canadensis inoculated with Glomus etunicatum and nitrogen-fixing bacteria under nitrogen limitation (mean ± SE, n = 6). GE, G. etunicatum. JS106, Paenibacillus stellifer ScRB-JS106. CK, un-inoculated control. ns, no significant difference (p > 0.05).

Fig. 7 Growth of Solidago canadensis inoculated with Glomus intraradices and nitrogen-fixing bacteria (mean ± SE, n = 6). GI, Glomus intraradices. JS106, Paenibacillus stellifer ScRB-JS106. CK, un-inoculated control. ns, no significant difference (p > 0.05).

Fig. 8 Growth of Solidago canadensis inoculated with Glomus mosseae and nitrogen-fixing bacteria (mean ± SE, n = 6). GM, G. mosseae. JS106, Paenibacillus stellifer ScRB-JS106. CK, un-inoculated control. ns, no significant difference (p > 0.05).

References 49

[1]	Battini F, Grønlund M, Agnolucci M, Giovannetti M, Jakobsen I (2017). Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria. Scientific Reports, 7, 4686. DOI: 10.1038/s41598-017-04959-0. DOI URL PMID
[2]	Bloom AJ, Chapin III FS, Mooney HA (1985). Resource limitation in plants—An economic analogy. Annual Review of Ecology, Evolution, and Systematics, 16, 363-392.
[3]	Bonfante P, Genre A (2010). Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Communications, 1, 48. DOI: 10.1038/ncomms1046. DOI URL PMID
[4]	Bunn RA, Lekberg Y, Gallagher C, Rosendahl S, Ramsey PW (2014). Grassland invaders and their mycorrhizal symbionts: a study across climate and invasion gradients. Ecology and Evolution, 4, 794-805. URL PMID
[5]	Cambui CA, Svennerstam H, Gruffman L, Nordin A, Ganeteg U, Näsholm T (2011). Patterns of plant biomass partitioning depend on nitrogen source. PLOS ONE, 6, e19211. DOI: 10.1371/journal.pone.0019211. URL PMID
[6]	Chandrasekaran M, Boughattas S, Hu SJ, Oh SH, Sa TM (2014). A meta-analysis of arbuscular mycorrhizal effects on plants grown under salt stress. Mycorrhiza, 24, 611-625. URL PMID
[7]	Chen Q, Wu WW, Qi SS, Cheng H, Li Q, Ran Q, Dai ZC, Du DL, Egan S, Thomas T (2020). Arbuscular mycorrhizal fungi improve the growth and disease resistance of the invasive plantWedelia trilobata. Journal of Applied Microbiology, 2019,0665. DOI: 10.1111/jam.14415.
[8]	Chen YL, Chen BD, Liu L, Hu YJ, Xu TL, Zhang X (2014). The role of arbuscular mycorrhizal fungi in soil nitrogen cycling. Acta Ecologica Sinica, 34, 4807-4815.
	[ 陈永亮, 陈保冬, 刘蕾, 胡亚军, 徐天乐, 张莘 (2014). 丛枝菌根真菌在土壤氮素循环中的作用. 生态学报, 34, 4807-4815.]
[9]	Cheng JK, Yue MF, Yang HR, Chen BM, Xin GR (2019). Do arbuscular mycorrhizal fungi help the native speciesBidens biternata resist the invasion of Bidens alba? Plant and Soil, 444, 443-455.
[10]	Ci E, Gao M (2004). Research progress on biological nitrogen fixation. Chinese Agricultural Science Bulletin, 20(1), 25-28.
	[ 慈恩, 高明 (2004). 生物固氮的研究进展. 中国农学通报, 20(1), 25-28.]
[11]	Cocking EC (2003). Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant and Soil, 252, 169-175.
[12]	Dai ZC, Fu W, Qi SS, Zhai DL, Chen SC, Wan LY, Huang P, Du DL (2016a). Different responses of an invasive clonal plant Wedelia trilobata and its native congener to gibberellin: implications for biological invasion. Journal of Chemical Ecology, 42, 85-94. URL PMID
[13]	Dai ZC, Fu W, Wan LY, Cai HH, Wang N, Qi SS, Du DL (2016b). 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 URL PMID
[14]	Ding Y, Wang J, Liu Y, Chen S (2005). Isolation and identification of nitrogen-fixing bacilli from plant rhizospheres in Beijing region. Journal of Applied Microbiology, 99, 1271-1281. DOI URL PMID
[15]	Franche C, Lindström K, Elmerich C (2009). Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant and Soil, 321, 35-59.
[16]	Hodge A, Campbell CD, Fitter AH (2001). An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature, 413, 297-299. URL PMID
[17]	Jin L (2005). Ecology of Arbuscular Mycorrhizal Associations in Solidago canadensis, an Invasive Alien Plant. PhD dissertation, Fudan University, Shanghai.
	[ 金樑 (2005). 外来入侵种加拿大一枝黄花的菌根生态学研究. 博士学位论文, 复旦大学, 上海.]
[18]	Jin L, Gu YJ, Xiao M, Chen JK, Li B (2004). The history of Solidago canadensis invasion and the development of its mycorrhizal associations in newly-reclaimed land. Functional Plant Biology, 31, 979-986. URL PMID
[19]	Johnson N, Wilson G, Bowker M, Wilson J, Miller R (2010). Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proceedings of the National Academy of Sciences of the United States of America, 107, 2093-2098. URL PMID
[20]	Johnson NC (2010). Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist, 185, 631-647.
[21]	Khan AG (1974). The occurrence of mycorrhizas in halophytes, hydrophytes and xerophytes, and of Endogone spores in adjacent soils. Microbiology, 81, 7-14.
[22]	Lee MR, Tu C, Chen X, Hu SJ (2014). Arbuscular mycorrhizal fungi enhance P uptake and alter plant morphology in the invasive plant Microstegium vimineum. Biological Invasions, 16, 1083-1093.
[23]	Leigh J, Hodge A, Fitter AH (2009). Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. The New Phytologist, 181, 199-207.
[24]	Liu CL, Zuo WY, Zhao ZY, Qiu LH (2012). Bacterial diversity of different successional stage forest soils in Dinghushan. Acta Microbiologica Sinica, 52, 1489-1496. URL PMID
	[ 柳春林, 左伟英, 赵增阳, 邱礼鸿 (2012). 鼎湖山不同演替阶段森林土壤细菌多样性. 微生物学报, 52, 1489-1496.] PMID
[25]	Murugesan C, Boughattas S, Hu SJ, Oh SH, Sa T (2014). A meta-analysis of arbuscular mycorrhizal effects on plants grown under salt stress. Mycorrhiza, 24, 611-625. DOI URL PMID
[26]	Pepe A, Sbrana C, Ferrol N, Giovannetti M (2017). An in vivo whole-plant experimental system for the analysis of gene expression in extraradical mycorrhizal mycelium. Mycorrhiza, 27, 659-668. URL PMID
[27]	Phillips JM, Hayman DS (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55, 158-161.
[28]	Schmid B, Puttick GM, Burgess KH, Bazzaz FA (1988). Clonal integration and effects of simulated herbivory in old-field perennials. Oecologia, 75, 465-471. URL PMID
[29]	Shah M, Reshi Z, Rashid I (2008a). Mycorrhizal source and neighbour identity differently influence Anthemis cotula L. invasion in the Kashmir Himalaya, India. Applied Soil Ecology, 40, 330-337.
[30]	Shah MA, Reshi Z, Rashid I (2008b). Mycorrhizosphere mediated Mayweed chamomile invasion in the Kashmir himalaya, India. Plant and Soil, 312, 219-225.
[31]	Smith FA, Grace EJ, Smith SE (2009). More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytologist, 182, 347-358. DOI URL PMID
[32]	Smith SE, Read D (2008). Mycorrhizal Symbiosis. 3rd ed. Academic Press, Washington.
[33]	Smith SE, Smith FA (2011). Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology, 62, 227-250. URL PMID
[34]	Sun HW, Wang WL, Liu SJ, Hou MM, Xie TN, Liang ZH, Fan YN, Zhang YL (2014). Formation of rice root regulated by nitrogen deficiency. Acta Pedologica Sinica, 51, 1096-1102.
[35]	Tanaka Y, Yano K (2005). Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell and Environment, 28, 1247-1254.
[36]	Tang JJ, Zhang Q, Yang RY, Chen X (2009). Effects of exotic plant Solidago canadensis L. on local arbuscular mycorrhizal fungi. Bulletin of Science and Technology, 25, 233-237.
	[ 唐建军, 张倩, 杨如意, 陈欣 (2009). 外来植物加拿大一枝黄花对入侵地丛枝菌根真菌(AMF)的影响. 科技通报, 25, 233-237.]
[37]	Thornley JHM (1972). A balanced quantitative model for root:shoot ratios in vegetative plants. Annals of Botany, 36, 431-441.
[38]	Tilman D, Wedin DA (1991). Plant traits and resource reduction for five grasses growing on a nitrogen gradient. Ecology, 72, 685-700.
[39]	Wang B (2013). Effects of Allelopathy and Arbuscular Mycorrhizae in the Invasion of Solidago canadensis L. Master degree dissertation, Zhejiang University, Hangzhou.
	[ 王兵 (2013). 化感作用与丛枝菌根在加拿大一枝黄花入侵过程中的作用研究. 硕士学位论文, 浙江大学, 杭州.]
[40]	Wang CQ, Liu S, Wang XL, Chen HW, Wu YJ, Wang ZG (2015). Isolation, identification and characteristics of authigenic azotobacters from the rhizosphere of soybean. Soybean Science, 34, 850-854.
	[ 王超群, 刘帅, 王晓璐, 陈慧文, 吴勇军, 王志刚 (2015). 大豆根际高效自生固氮菌分离鉴定与特性研究. 大豆科学, 34, 850-854.]
[41]	Wang YH, Wang MQ, Li Y, Wu AP, Huang JY (2018). Effects of arbuscular mycorrhizal fungi on growth and nitrogen uptake of Chrysanthemum morifolium under salt stress. PLOS ONE, 13, e0196408. DOI: 10.1371/journal.pone. 0196408. URL PMID
[42]	Werner PA, Gross RS, Bradbury IK (1980). The biology of Canadian.: 45.Solidago canadensis L. Canadian Journal of Plant Science, 60, 1393-1409.
[43]	Wilson GWT, Hickman KR, Williamson MM (2012). Invasive warm-season grasses reduce mycorrhizal root colonization and biomass production of native prairie grasses. Mycorrhiza, 22, 327-336. URL PMID
[44]	Yang JY, Wang YH, Wen GS, Yi LT (2013). Effects of AM fungi and simulated nitrogen deposition on the growth and biomass accumulation of Solidago canadensis seedings. Chinese Journal of Ecology, 32, 2953-2958.
	[ 杨剑宇, 王艳红, 温国胜, 伊力塔 (2013). AMF和模拟氮沉降对加拿大一枝黄花(Solidago canadensis)幼苗生长和生物量积累的影响. 生态学杂志, 32, 2953-2958.]
[45]	Yang RY, Zhou G, Zan ST, Guo FY, Su NN, Li J (2014). Arbuscular mycorrhizal fungi facilitate the invasion of Solidago canadensis L. in southeastern China. Acta Oecologica, 61, 71-77.
[46]	Yang XY (2007). Allelopathic Effects of Invasive Weeds on Arbuscular Mycorrhizae of Native Plants. Master degree dissertation, Zhejiang University, Hangzhou.
	[ 杨贤燕 (2007). 外来杂草对本地植物丛枝菌根的化感作用.硕士学位论文, 浙江大学, 杭州.]
[47]	Zhang FJ, Li Q, Chen FX, Xu HY, Inderjit , Wan FH (2017). Arbuscular mycorrhizal fungi facilitate growth and competitive ability of an exotic species Flaveria bidentis. Soil Biology & Biochemistry, 115, 275-284.
[48]	Zhou G, Zan S, Guo FY, Su NN, Li J (2014). Arbuscular mycorrhizal fungi facilitate the invasion of Solidago canadensis L. in southeastern China. Acta Oecologica, 61, 71-77.
[49]	Zhu C, Tian GL, Luo GW, Kong YL, Guo JJ, Wang M, Guo SW, Ling N, Shen QR (2018). N-fertilizer-driven association between the arbuscular mycorrhizal fungal community and diazotrophic community impacts wheat yield. Agriculture Ecosystems & Environment, 254, 191-201.