Effects of native plant-soil microbe interaction on plant invasion

doi:10.17521/cjpe.2024.0017

Abstract

Abstract:

Alien plant invasions pose a significant threat to global ecological security. Various factors, including the ecological tolerance of alien plants and their interactions with biotic and abiotic elements such as rainfall, temperature, and soil nutrients, influence the dynamics of plant invasions. The interaction between plants and various micro-organisms plays an important role in regulating plant growth, development, and interspecific competition. Previous studies indicate that the interactions between native plants and different groups of soil microorganisms affect plant invasion through several pathways: 1) Pathogenic microorganisms may have more suppressive effects on native plants, facilitating the invasion of alien plants. 2) Symbiotic microorganisms can help native plants resist alien plant invasion, but disrupting these mutualistic associations may accelerate invasion. 3) Additionally, saprophytic microbiota may promote plant invasions by increasing the rate of nutrient cycling and facilitating these alien plants with high nutrient utilization efficiency. Compared to single-species invasions, multispecies invasions can increase invasive capacity through shared pathogen pressures, forming symbioses, and utilizing heterogeneous nutrients from saprophytic microorganisms. This interspecific synergistic effect can disrupt the balance between native plants and soil microbes. Furthermore, global changes may promote alien plant invasions through the detrimental effects of soil microbes on native plants. This review examines the impact of interactions between native plants and soil microbes on plant invasions and outlines directions for future research.

Key words: plant invasion, plant-soil microbe interactions, global change, single species invasion, multispecies invasion

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

https://www.plant-ecology.com/EN/Y2024/V48/I12/1547

Figures/Tables 5

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”)).

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^②Fusarium semitectum, Fusarium^①, 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^②Chromolaena odorata^①, 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^③Centaurea solstitialis^③
共生微生物 Symbiotic microorganism	菌根真菌 Mycorrhizal fungi	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^⑥Bidens pilosa^④, Xanthium strumarium^⑤, Vachellia farnesiana^⑥
腐生微生物 Saprophytic microorganism	革兰氏阴性菌、革兰氏阳性菌^⑦Gram-negative bacteria, Gram-positive bacteria^⑦	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^⑧⑨Microbes that accelerate the decomposition of plant litter can indirectly benefit alien plants that possess a superior ability to absorb the resulting nutrients^⑦⑧⑨	野黑樱桃、红槲栎^⑨Prunus serotina, Quercus rubra^⑨

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^②Fusarium semitectum, Fusarium^①, 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^②Chromolaena odorata^①, 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^③Centaurea solstitialis^③
共生微生物 Symbiotic microorganism	菌根真菌 Mycorrhizal fungi	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^⑥Bidens pilosa^④, Xanthium strumarium^⑤, Vachellia farnesiana^⑥
腐生微生物 Saprophytic microorganism	革兰氏阴性菌、革兰氏阳性菌^⑦Gram-negative bacteria, Gram-positive bacteria^⑦	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^⑧⑨Microbes that accelerate the decomposition of plant litter can indirectly benefit alien plants that possess a superior ability to absorb the resulting nutrients^⑦⑧⑨	野黑樱桃、红槲栎^⑨Prunus serotina, Quercus rubra^⑨

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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