Persistence of plant-mediated microbial soil legacy effects in soil and inside roots

Hannula, S. Emilia; Heinen, Robin; Huberty, Martine; Steinauer, Katja; Long, Jonathan R. De; Jongen, Renske; Bezemer, T. Martijn

doi:10.1038/s41467-021-25971-z

Cited by 109 publications

(118 citation statements)

References 72 publications

(117 reference statements)

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“…Consistent with this and our results, Crème et al (2018) [ 75 ] observed that despite the insertion of three years of temporary grasslands within the crop rotation, the biogeochemical signature of the soil organic matter was more similar to the continuous cropping system than to the permanent grassland. Moreover, plant species can also affect differently soil microbial communities through a myriad of processes [ 8 , 80 ] and create legacies that are detectable under subsequent plant communities [ 81 ], therefore also explaining the similarities between temporary grassland and continuous cropping [ 82 ]. Overall, we found that prior cropping systems that were at least three-year-old continued to play a role in shaping microbial community composition across groups, which highlight the importance to consider legacies of past land-use when assessing the impact of management practices.…”

Section: Discussionmentioning

confidence: 99%

Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity

Romdhane

Spor

Banerjee

et al. 2022

Environmental Microbiome

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Background Soil microbial communities are major drivers of cycling of soil nutrients that sustain plant growth and productivity. Yet, a holistic understanding of the impact of land-use intensification on the soil microbiome is still poorly understood. Here, we used a field experiment to investigate the long-term consequences of changes in land-use intensity based on cropping frequency (continuous cropping, alternating cropping with a temporary grassland, perennial grassland) on bacterial, protist and fungal communities as well as on their co-occurrence networks. Results We showed that land use has a major impact on the structure and composition of bacterial, protist and fungal communities. Grassland and arable cropping differed markedly with many taxa differentiating between both land use types. The smallest differences in the microbiome were observed between temporary grassland and continuous cropping, which suggests lasting effects of the cropping system preceding the temporary grasslands. Land-use intensity also affected the bacterial co-occurrence networks with increased complexity in the perennial grassland comparing to the other land-use systems. Similarly, co-occurrence networks within microbial groups showed a higher connectivity in the perennial grasslands. Protists, particularly Rhizaria, dominated in soil microbial associations, as they showed a higher number of connections than bacteria and fungi in all land uses. Conclusions Our findings provide evidence of legacy effects of prior land use on the composition of the soil microbiome. Whatever the land use, network analyses highlighted the importance of protists as a key element of the soil microbiome that should be considered in future work. Altogether, this work provides a holistic perspective of the differential responses of various microbial groups and of their associations to agricultural intensification.

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Section: Discussionmentioning

confidence: 99%

Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity

Romdhane

Spor

Banerjee

et al. 2022

Environmental Microbiome

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“…Also from a microbial perspective such longer term soil legacy effects are becoming increasingly probable. For example, Wippel et al (2021) indicate that early‐arriving microbial root endophytes are resilient to invasion by later‐arriving microbiota and Hannula et al (2021) show that microbial soil legacies acquired by plant species seedlings persist inside plant roots over at least 5‐month time. Soil legacy effects may thus especially play an important role on the longer term growth and competition of plants.…”

Section: Discussionmentioning

confidence: 99%

Plant life‐history traits rather than soil legacies determine colonisation of soil patches in a multi‐species grassland

et al. 2022

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Interactions between plants and soil biota are increasingly shown to play critical roles in plant species coexistence processes. Plant species coexistence is thought to be promoted via biotic legacies that plant species leave behind in the soil after a plant disappears. These soil legacies are hypothesised to supress colonisation success when the preceding plant is of the same species, that is, when a plant species encounters its own, species‐specific soil antagonists. However, colonisation of vacant spots in plant communities is in the first place determined by the ability of plants to reach such vacant locations. We currently lack an understanding of the explicit role of soil legacy effects and their relative contribution to colonisation processes in plant communities consisting of plant species inherently differing in colonisation ability. In experimental, outdoor plant communities consisting of eight grassland species, we tested the effect of five differently conditioned soil patches on plant species colonisation success over three consecutive growing seasons. We found that colonisation success was largely determined by the species' reproductive strategy, lateral spread and growth rate, and not by the plant species that conditioned the soil patch. Fast spreading, clonal plant species reached the soil patches first and initially attained the highest biomass inside the patch. One year later, slower spreading plant species colonised the patch via seedlings. Species with intrinsically high growth rates attained the highest biomass, decreasing biomass of the initial colonisers. While subtle differences between conditioned soil patches did occur, these were not strong enough to overcome the inherent differences in colonisation ability between the various plant species. Synthesis. Our results reject the hypothesis that colonisation of vacant soil patches in plant communities is strongly affected by the legacy that is left behind by the preceding plant species. Instead, plant species life‐history strategy plays a prominent role, driving sequential plant species replacements. Based on our results and recent accounts in literature we present a conceptual model for local cyclic dynamics in grassland communities, where soil legacy plays a role in affecting the performance of established plant species rather than colonisation of vacant patches.

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“…Defensive secondary metabolites of the benzoxazinoids that are released by cereal roots increase jasmonate signaling for plant defense, however, plant growth can be decreased and the rhizosphere microbial composition is modified to improve insect herbivore resistance, even in the next plant generation [79] . The concept of a “soil-borne legacy” suggests a suppressive memory to benefit future plant generations growing in the same soil [80] , [81] , [82] . This suppressive memory to boost plant health is thought to be an beneficial microbial attractive result by the modification plant root exudates [83] .…”

Section: Plant-beneficial Functions Of the Rhizosphere Microbiomementioning

confidence: 99%

Rhizosphere microbiome: Functional compensatory assembly for plant fitness

Xun

Shao

Shen

et al. 2021

Computational and Structural Biotechnology Journal

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Environmental pressure to reduce our reliance on agrochemicals and the necessity to increase crop production in a sustainable way have made the rhizosphere microbiome an untapped resource for combating challenges to agricultural sustainability. In recent years, substantial efforts to characterize the structural and functional diversity of rhizosphere microbiomes of the model plant Arabidopsis thaliana and various crops have demonstrated their importance for plant fitness. However, the plant benefiting mechanisms of the rhizosphere microbiome as a whole community rather than as an individual rhizobacterium have only been revealed in recent years. The underlying principle dominating the assembly of the rhizosphere microbiome remains to be elucidated, and we are still struggling to harness the rhizosphere microbiome for agricultural sustainability. In this review, we summarize the recent progress of the driving factors shaping the rhizosphere microbiome and provide community-level mechanistic insights into the benefits that the rhizosphere microbiome has for plant fitness. We then propose the functional compensatory principle underlying rhizosphere microbiome assembly. Finally, we suggest future research efforts to explore the rhizosphere microbiome for agricultural sustainability.

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Persistence of plant-mediated microbial soil legacy effects in soil and inside roots

Cited by 109 publications

References 72 publications

Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity

Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity

Plant life‐history traits rather than soil legacies determine colonisation of soil patches in a multi‐species grassland

Rhizosphere microbiome: Functional compensatory assembly for plant fitness

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