Chin J Plant Ecol ›› 2024, Vol. 48 ›› Issue (12): 1547-1560.DOI: 10.17521/cjpe.2024.0017 cstr: 32100.14.cjpe.2024.0017
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YANG Jia-Ting1,2, PAN Ying-Ji1,*()(
), CHANG Chun-Ling1, LIU Yan-Jie1
Received:
2024-01-19
Accepted:
2024-06-14
Online:
2024-12-20
Published:
2024-12-20
Contact:
PAN Ying-Ji
Supported by:
YANG Jia-Ting, PAN Ying-Ji, CHANG Chun-Ling, LIU Yan-Jie. Effects of native plant-soil microbe interaction on plant invasion[J]. Chin J Plant Ecol, 2024, 48(12): 1547-1560.
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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2024.0017
Fig. 1 Hypotheses on plant invasion and plant-soil microbe interactions. Blue arrows indicate negative effect, while red arrows indicate positive effects.
Fig. 2 A literature search on the effects of native plant-soil microbe interactions (pathogenic, symbiotic and saprophytic microorganisms) on alien plant invasion. The data sources used were the China National Knowledge Infrastructure (CNKI) and Web of Science. The search focused on publications from January 1, 2000, to December 31, 2022, covering a wide range of microbial interactions. The search terms included: TS = ((“pathogenic microorganism” OR “soil microbe” OR “plant-microbe interactions”) AND (“plant invasion”)); TS = ((“symbiotic microorganism” OR “soil microbe” OR “plant-microbe interactions”) AND (“plant invasion”)); TS = ((“saprophytic microorganism” OR “soil microbe” OR “plant-microbe interactions”) AND (“plant invasion”)).
微生物主要类群 Most dominant microbe | 菌群 Flora | 菌群与植物互作 Plant-microbe interactions | 外来植物 Alien plant species |
---|---|---|---|
病原微生物 Pathogenic microorganism | 半裸镰孢菌、镰刀菌①、油壶菌、格孢腔菌、白粉菌等② Fusarium semitectum, Fusarium①, Olpidium, Pleosporales, Erysiphales, etc.② | 病原微生物可能导致本地植物枯死; 而本地植物相比外来植物需要消耗更多的防御成本以抵御病原菌, 外来植物由此获得入侵优势; 此情况在环境高养分供应下养分波动时加剧 Pathogenic microorganisms may cause the death of native plants that otherwise incur higher metabolic costs to defend against pathogenic attacks. Increased nutrient availability can exacerbate the negative effects of pathogens on native plants | 飞机草①、互花米草、大狼耙草、鬼针草、一年蓬等② Chromolaena odorata①, Spartina alterniflora, Bidens frondose, Bidens pilosa, Erigeron annuus, etc.② |
共生微生物 Symbiotic microorganism | 菌根真菌 Mycorrhizal fungi | 本地植物与共生微生物的共生关系会抑制外来植物生长 The symbiotic relationship between native plants and symbiotic microorganism suppresses alien plants growth | 长刺矢车菊③ Centaurea solstitialis③ |
微生物解除与本地植物的共生关系转向与外来植物共生, 可能降低干旱胁迫对外来植物的伤害 When microbes disrupt mutualistic associations between native plants and their symbiotic microorganisms and then establish symbiotic relationships with alien plants, the alien plants may become more resilient to drought stress | 鬼针草④、瘤突苍耳⑤、金合欢⑥ Bidens pilosa④, Xanthium strumarium⑤, Vachellia farnesiana⑥ | ||
腐生微生物 Saprophytic microorganism | 革兰氏阴性菌、革兰氏阳性菌⑦ Gram-negative bacteria, Gram-positive bacteria⑦ | 微生物分解凋落物为植物提供营养⑦; 外来植物依靠自身养分利用优势获得比本地植物更多的营养⑧⑨ Microbes that accelerate the decomposition of plant litter can indirectly benefit alien plants that possess a superior ability to absorb the resulting nutrients⑦⑧⑨ | 野黑樱桃、红槲栎⑨ Prunus serotina, Quercus rubra⑨ |
Table 1 Impact of interactions among native plants and various microorganisms—pathogenic, symbiotic, and saprophytic—on the invasion of alien plants
微生物主要类群 Most dominant microbe | 菌群 Flora | 菌群与植物互作 Plant-microbe interactions | 外来植物 Alien plant species |
---|---|---|---|
病原微生物 Pathogenic microorganism | 半裸镰孢菌、镰刀菌①、油壶菌、格孢腔菌、白粉菌等② Fusarium semitectum, Fusarium①, Olpidium, Pleosporales, Erysiphales, etc.② | 病原微生物可能导致本地植物枯死; 而本地植物相比外来植物需要消耗更多的防御成本以抵御病原菌, 外来植物由此获得入侵优势; 此情况在环境高养分供应下养分波动时加剧 Pathogenic microorganisms may cause the death of native plants that otherwise incur higher metabolic costs to defend against pathogenic attacks. Increased nutrient availability can exacerbate the negative effects of pathogens on native plants | 飞机草①、互花米草、大狼耙草、鬼针草、一年蓬等② Chromolaena odorata①, Spartina alterniflora, Bidens frondose, Bidens pilosa, Erigeron annuus, etc.② |
共生微生物 Symbiotic microorganism | 菌根真菌 Mycorrhizal fungi | 本地植物与共生微生物的共生关系会抑制外来植物生长 The symbiotic relationship between native plants and symbiotic microorganism suppresses alien plants growth | 长刺矢车菊③ Centaurea solstitialis③ |
微生物解除与本地植物的共生关系转向与外来植物共生, 可能降低干旱胁迫对外来植物的伤害 When microbes disrupt mutualistic associations between native plants and their symbiotic microorganisms and then establish symbiotic relationships with alien plants, the alien plants may become more resilient to drought stress | 鬼针草④、瘤突苍耳⑤、金合欢⑥ Bidens pilosa④, Xanthium strumarium⑤, Vachellia farnesiana⑥ | ||
腐生微生物 Saprophytic microorganism | 革兰氏阴性菌、革兰氏阳性菌⑦ Gram-negative bacteria, Gram-positive bacteria⑦ | 微生物分解凋落物为植物提供营养⑦; 外来植物依靠自身养分利用优势获得比本地植物更多的营养⑧⑨ Microbes that accelerate the decomposition of plant litter can indirectly benefit alien plants that possess a superior ability to absorb the resulting nutrients⑦⑧⑨ | 野黑樱桃、红槲栎⑨ Prunus serotina, Quercus rubra⑨ |
Fig. 3 Conceptual framework illustrating the effects of soil microbe-native plant interactions on alien plant invasions. Blue arrows indicate negative effect, red arrows indicate positive effects, while dashed arrows represent hypothesized interactions between plants and soil microbes based on existing research. The impact of three main groups of soil microbes—pathogenic, symbiotic, and saprophytic—on native and alien plants can be summarized as follows. (1) Pathogenic microorganisms: native plants can be inhibited by local pathogenic microorganisms (the accumulation of local pathogens hypothesis), while alien plants gain competitive advantages over native plants through the enemy release hypothesis (① Eppinga et al., 2006; ② Nijjer et al., 2007; ③ Keane & Crawley, 2002; ④ Blumenthal, 2006; ⑤ Dewalt et al., 2004; ⑥ Zhang et al., 2023). (2) Symbiotic microorganisms: native plants provide habitat and carbon to symbiotic microorganisms, which in turn enhance nutrient uptake and growth of native plants. The mutualisms between the microbes and native plants can suppress alien plant growth (⑦ Fu et al., 2017; ⑧ Zheng et al., 2023). In plant invasions, these microbes can alter nutrient cycling, either by disrupting existing mutualisms with native plants or forming new ones with alien plants, thereby promoting alien plant growth (⑨ Callaway et al., 2008; ⑩ Waller et al., 2016; ⑪ Fumanal et al., 2006). (3) Saprophytic microorganisms: native plants provide carbon to saprophytic microorganisms, which decompose plant litter. This decomposition can benefit alien plants with higher nutrient absorption capacity (⑦ Fu et al., 2017; ⑫ Dyderski & Jagodziński, 2019; ⑬ Heckman et al., 2019). In multi-species invasions, symbiotic microorganisms and saprophytic microorganisms beneficial to native plants may be suppressed (⑭ Kourtev et al., 2002). We propose the following hypotheses: (1) Alien plants may share pathogen pressure and gain competitive advantages (⑮ Zhang, 2021). (2) Disruption of native plant-symbiotic mutualisms may occur, and increased diversity of symbiotic microorganisms could favor multi-species invasions (⑩ Waller et al., 2016; ⑪ Fumanal et al., 2006). (3) Saprophytic microorganisms may enhance nutrient cycling, and interactions among multiple invasive species could further accelerate decomposition and nutrient uptake, potentially giving alien plants an advantage in multi-species invasions (⑫ Dyderski & Jagodziński, 2019; ⑬ Heckman et al., 2019).
Fig. 4 Case studies examining the effects of interactions between soil microbes and native plants on alien plant invasions under conditions of global change. Blue arrows indicate negative effects, while red arrows indicate positive effects on the interactions between plants and soil microbes. Global change could influence alien plant invasions through several mechanisms: nitrogen deposition (① Fang et al., 2021; ② Wang, 2019; ③ Song et al., 2011), elevated CO2 concentrations, and drought stress, which may decrease the abundance of symbiotic microbes which form mutualisms with native plants (④ Callaway et al., 2004; ⑤ Laungani & Knops, 2009). Additionally, drought stress and nutrient fluctuations might increase the abundance of native pathogenic microorganisms (⑥ Fahey et al., 2020; ⑦ Zhang et al., 2023b; ⑧ Nijjer et al., 2007; ⑨ Zhang et al., 2023). Alien plants could be less affected compared to native plants due to enemy release (⑩ Keane & Crawley, 2002).
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