Lu Xinmin's research group proposed a new hypothesis that phytophagous insects and soil organisms synergistically promote plant invasion

Nanhu News Network News (correspondent Gao Lunlun) Recently, the Lu Xinmin research group of PI of the College of Plant Science and Technology, the State Key Laboratory of Agricultural Microbiology, and Hubei Hongshan Laboratory of our university integrated years of field investigation and soil feedback experiments to put forward for the first time a new hypothesis of enhanced soil-mediated invasion self-reinforcement upon herbivory hypothesis）
。 The results were published online in the journal
New Phytologist under the title "Aboveground herbivory can promote exotic plant invasion through intra- and inter specific aboveground-belowground interactions.
"

The invasion of alien species seriously threatens agricultural security, ecological security and national security, and effectively curbing the invasion of alien species is an important part of the rural revitalization strategy, and clarifying the invasion mechanism of alien species is the basis for
achieving this goal.
Academics generally believe that escaping the regulation of natural enemies of origin specificity is an important reason for
the successful invasion of exotic plants.
Accordingly, invasive plants are controlled (i.
e.
biological control)
through the introduction and release of specific natural enemies.
However, in practice, although some natural enemies seriously harm the target plant, they do not effectively inhibit the invasion
of the target plant.
In addition, despite serious native predators, some alien species can still successfully invade.

This suggests that some other mechanisms may facilitate plant invasion in the case of natural predators, but this is currently not explored
.

Alternanthera philoxeroides is one of the first invasive species announced in China and an important malignant weed
in agriculture 。 In the early stage, the research group discussed the regulatory effects of plant-eating insects and soil organisms on the invasion of Lotus l.
chinena (ISME Journal 2018; Annals of Botany 2021) and its biocontrol response to climate change (Global Change Biology 2013; Ecology Letters 2015）
。 On this basis, the research group carried out a large-scale survey from 2017 to 2019, and compared with the previous results, it was found that from 2014 to 2019, the population of Agasicles hygrophila was introduced to spread significantly to high latitudes.
The damage to A.
sessilis and the native plant A.
sessilis intensified, while the competitive advantage of A.
sessilis in invasive communities remained unchanged, and the risk of introduction of lotus seeds into insects was high
.

Fig.
1 Effects of soil organisms on invasive and native plants and insect larvae when feeding on insects without (a) and (b
).
The solid blue line represents the promoting effect, the solid red line represents the inhibitory effect, and the thickness of the line indicates the relative intensity
of the action.

In order to explore the causes of the above phenomena, the research group used the new framework of soil bio-plant-insect interaction cycle to carry out experimental research
.
It was found that insect feeding changed the structure of the plant rhizosphere microbiome, prolonged the asymmetric inhibitory effect of rhizosphere organisms on lotus seeds, and at the same time, the rhizosphere soil of the syrhizophren was fed to improve the insect resistance level
of the same planting plants in the later stage.
Based on this, the research group proposed Enhanced soil-mediated invasion self-reinforcement upon herbivory hypothesis (Figure 1), which enriched the existing theory of
species invasion.
This study also reveals a new non-target risk of biological control, which provides a basis for improving existing biological control practices (i.
e.
, the impact on aboveground and subsurface ecosystems needs to be comprehensively investigated before releasing biocontrol natural enemies).

Doctoral students Gao Lunlun, Wei Chunqiang and He Yifan are the co-first authors of the paper, Professor Lu Xinmin is the corresponding author of the paper, researcher Wu Yuqing of the Henan Academy of Agricultural Sciences participated in the project research, and Dr.
Rutger A.
Wilschut of the University of Konstanz and the University of Wagellingen in the Netherlands participated in the writing of the
article.
The research was supported
by the "14th Five-Year Plan" major project of the Ministry of Science and Technology, the National Natural Science Foundation of China, and the basic scientific research fund of the central universities.

Reviewed by: Lu Xinmin

【English Summary】

•Aboveground herbivores and soil biota profoundly affect plant invasions.
However, how they interactively affect plant invasions through plant-soil feedbacks (PSF), remains unclear.

•To explore how herbivory by the introduced beetle Agasicles hygrophila affects Alternanthera philoxeroides invasions in China, we integrated multi-year field surveys and a two-year PSF-experiment, in which we examined how herbivory affects PSFs on the performance of native and invasive plants and the introduced beetles.

•Despite increased herbivory from A.
hygrophila, A.
philoxeroides dominance over co-occurring congeneric native A.
sessilis remained constant from 2014 to 2019.
While occurring at lower abundances, A.
sessilis experienced similar herbivore damage, suggesting apparent competitive effects.
Our experiments revealed that herbivory on A.
philoxeroides altered soil microbial communities, prolonged its negative PSF on A.
sessilis and decreased A.
hygrophila larvae performance on the next-generation invasive plants.
Consequently, A.
hygrophila larvae performed better on leaves of natives than of invasives when grown in soils conditioned by invasive plants defoliated by the introduced beetles.

•Our findings suggest that aboveground herbivory might promote rather than suppress A.
philoxeroides invasion by enhancing its soil-mediated self-reinforcement, providing a novel mechanistic understanding of plant invasions.
These findings highlight the need to incorporate an aboveground-belowground perspective during the assessment of potential biocontrol agents.

【Paper Link】

https://doi.
org/10.
1111/nph.
18520