Beneficial rhizobacterium provides positive plant–soil feedback effects to Ageratina adenophora
SUN Yuan-yuan1, ZHANG Qiu-xin1, ZHAO Yun-peng1, DIAO Yue-hui1, GUI Fu-rong2, YANG Guo-qing1
1 College of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, P.R.China 2 College of Plant Protection, Yunnan Agricultural University, Kunming 650201, P.R.China
Rhizosphere microbial communities play important roles in facilitating or inhibiting the establishment of exotic species. Since some invasive plants interact with soil microbial communities such as rhizosphere bacteria, changes triggered by rhizosphere bacteria may alter competitive interactions between exotic and native plants. This study compared the Bacillus cereus content in soils with different degrees of Ageratina adenophora invasion, and investigated the effects of A. adenophora allelochemicals on B. cereus growth and soil characteristics and the feedback effects of B. cereus on A. adenophora growth. Bacillus cereus content in the rhizosphere of A. adenophora increased with intensification of the invasion process, and newly invaded soil contained almost twice as much bacteria as noninvaded soil. When rhizosphere soil was added to the root exudates of A. adenophora, the contents of B. cereus were twice as much as the control, except on the first day. Certain soil parameters increased significantly, such as ammonium nitrogen (NH4+-N) and available phosphorus (AP), which were increased by 41 and 27%, respectively. Soil treatment with B. cereus promoted the degradation of two allelochemicals from the rhizosphere of A. adenophora, amorpha-4,7(11)-dien-8-one and 6-hydroxy-5-isopropy1-3,8-dimethyl-4a,5,6,7,8,8a-hexahydraphthalen-2(1H)-one, to varying degrees; and increased the germination rate by 50%, root length by 117%, shoot length by 48% and fresh weight by 81% for A. adenophora compared to those of untreated soil. Our results confirmed that the invasion of A. adenophora will promote an increase of B. cereus, a beneficial rhizosphere bacterium, which in turn induces a positive feedback effect on A. adenophora.
SUN Yuan-yuan, ZHANG Qiu-xin, ZHAO Yun-peng, DIAO Yue-hui, GUI Fu-rong, YANG Guo-qing.
2021.
Beneficial rhizobacterium provides positive plant–soil feedback effects to Ageratina adenophora. Journal of Integrative Agriculture, 20(5): 1327-1335.
Artursson V, Jansson J K. 2003. Use of bromodeoxyuridine immunocapture to identify active bacteria associated with arbuscular mycorrhizal hyphae. Applied and Environmental Microbiology, 69, 6208–6215.
Bao S D. 2000. Soil and Agricultural Chemistry Analysis. Chinese Agriculture Press, Beijing. pp. 106–108. (in Chinese)
Beckstead J, Meyer S E, Connolly B M, Huck M B, Street L E. 2010. Cheatgrass facilitates spillover of a seed bank pathogen onto native grass species. Journal of Ecology, 98, 168–177.
Bertin C, Yang X H, Weston L A. 2003. The role of root exudates and allelochemicals in the rhizosphere. Plant and Soil, 256, 67–83.
Bever J D. 2002. Negative feedback within a mutualism: Host-specific growth of mycorrhizal fungi reduces plant benefit. Philosophical Transactions of the Royal Society (B: Biological Sciences), 269, 2595–2601.
Boudiaf I, Baudoin E, Sanguin H, Beddiar A, Thioulouse J, Galiana A, Prin Y, Roux C L, Lebrun M, Duponnois R. 2013. The exotic legume tree species, Acacia mearnsii, alters microbial soil; functionalities and the early development of a native tree species; Quercus suber, in North Africa. Soil Biology and Biochemistry, 65, 172–179.
Callaway R M, Ridenour W M. 2004. Novel weapons: Invasive success and the evolution of increased competitive ability. Frontiers in Ecology and the Environment, 8, 436–443.
Callaway R M, Thelen G C, Barth S, Ramsey P W, Gannon J E. 2004. Soil fungi alter interactions between the invader Centaurea maculosa and north American natives. Ecology, 85, 1062–1071.
Chen S Y, Zhang Y X, Cai X Q. 2003. Antagonistic mechanism of three antagonistic bacteria against great brown spot disease of narcissus leaf. Chinese Journal of Biological Control, 19, 11–15. (in Chinese)
Elgersma K J, Ehrenfeld J G. 2011. Linear and non-linear impacts of a non-native plant invasion on soil microbial community structure and function. Biological Invasions, 13, 757–768.
Fitter A H. 2003. Making allelopathy respectable. Science, 301, 1337–1338.
Flory S L, Clay K, Thrall P. 2013. Pathogen accumulation and long-term dynamics of plant invasions. Journal of Ecology, 101, 607–613.
Hawkes C V, Wren I, Herman D J, Firestone M K. 2005. Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecology Letters, 8, 976–985.
He W, Guo L W, Fan P H, Guo B, Fu Y P, Wei Y H. 2015. Allelopathy and the rhizospere bacterial community structure of Oxytropis ochrocephala. Acta Prataculturae Sinica, 24, 21–29. (in Chinese)
He W M, Feng Y L, Ridenour W M, Thelen G C, Pollock J L, Diaconu A, Callaway R M. 2009. Novel weapons and invasion: Biogeographic differences in the competitive effects of Centaurea maculosa and its root exudate (+/–)-catechin. Oecologia, 159, 803–815.
Inderjit S. 2005. Soil microorganisms: An important determinant of allelopathic activity. Plant and Soil, 274, 227–236.
Inderjit S, Wardle D A, Karban R, Callaway R M. 2011. The ecosystem and evolutionary contexts of allelopathy. Trends in Ecology and Evolution, 26, 655–662.
Keane R M, Crawley M J. 2002. Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution, 17, 164–170.
Klironomos J N. 2003. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology, 84, 2292–2301.
Li X R, Li L. 2013. Research progress of plant allelopathic substances and soil microorganisms. Guangdong Agricultural Sciences, 40, 178–181. (in Chinese)
Li Y P, F Y L, Chen Y J, Tian Y H. 2015. Soil microbes alleviate allelopathy of invasive plants. Science Bulletin, 60, 1083–1091.
Mangla S, Inderjit S, Callaway R M. 2008. Exotic invasive plant accumulates native soil pathogens which inhibit native plants. Journal of Ecology, 96, 58–67.
Mitchell C E, Power A G. 2003. Release of invasive plants from fungal and viral pathogens. Nature, 421, 625–627.
Niu H B, Liu W X, Wan F H, Liu B. 2007. An invasive aster (Ageratina adenophora) invades and dominates forest understories in China: Altered soil microbial communities facilitate the invader and inhibit natives. Plant and Soil, 294, 73–85. (in Chinese)
Pu P, Zhang M, Zhang L N. 2013. A study on temperature and time conditions of colorimetric method in measuring soil available phosphorus. Advanced Materials Research, 838, 2047–2051.
Rekha K, Baskar B, Santhanam S, Usha B. 2017. Plant growth promoting rhizobacteria Bacillus subtilis RR4 isolated from rice rhizosphere induces malic acid biosynthesis in rice roots. Canadian Journal of Microbiology, 64, 20–27.
Sripontan Y, Tan C W, Hung M H, Young C C. 2014. Effects of plant-growth-promoting microorganisms and fertilizers on growth of cabbage and tomato and Spodoptera litura performance. Journal of Asia-Pacific Entomology, 17, 587–593.
Tian Y H, Feng Y L, Liu C. 2007. Addition of activated charcoal to soil after clearing Ageratina adenophora stimulates growth of forbs and grasses in China. Tropical Grasslands. 41, 285–291.
Vanwallendael A, Hamann E, Franks S J. 2018. Evidence for plasticity, but not local adaptation, in invasive Japanese knotweed (Reynoutria japonica) in North America. Evolution and Ecology, 32, 395–410.
Vivanco J M, Bais H P, Stermitz F R, Callaway R M. 2004. Biogeographical variation in community response to root allelochemistry: Novel weapons and exotic invasion. Ecology Letters, 7, 285–292.
Wan F H, Liu W X, Guo J Y, Qiang S, Li B P, Wang J J, Yang Q G, Niu H B, Gui F R, Huang W K, Jiang Z L, Wang W Q. 2010. Invasive mechanism and control strategy of Ageratina adenophora (Sprengel). Science China (Life Sciences), 53, 1291–1298.
Weidenhamer J D, Callaway R M. 2010. Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. Journal of Chemical Ecology, 36, 59–69.
Yang G Q, Guo J, Song S J, Gui F R. 2014. Effects of leaf punch and plant removal on contents of three allelochemicals in roots of Ageratina adenophora. Guangdong Agricultural Sciences, 41, 79–82. (in Chinese)
Yang G Q, Guo J, Zhu X Z, Shao H, Gao T. 2016. Soil chemicals from sticky snakeroot (Ageratina adenophora, Compositae) are phytotoxic. Weed Science, 64, 223–230.
Yang G Q, Qiu W R, Jin Y N, Wan F H. 2013. Potential allelochemicals from root exudates of invasive Ageratina adenophora. Allelopathy Journal, 32, 233–242.
Yang G Q, Wan F H, Liu W X. 2008. Allelopathy research progress on an invasive weed, Ageratina adenophora Sprengel. Acta Phytotaxonomica Sinica, 35, 463–468. (in Chinese)
Yang G Q, Wan F H, Liu W X, Zhang X W. 2006. Physiological effects of allelochemicals from leachates of Ageratina adenophora (Spreng.) on rice seedlings. Allelopathy Journal, 18, 237–245.
Yu X J, Yu D, Lu J, Keping M. 2005. A new mechanism of invader success: Exotic plant inhibits natural vegetation restoration by changing soil microbe community. Chinese Science Bulletin, 50, 1105–1112.