Plant neighbor detection and allelochemical response are driven by root-secreted signaling chemicals

Kong, Chui‐Hua; Zhang, Songzhu; Li, Yonghua; Xia, Zhichao; Yang, Xiao‐Sheng; Meiners, Scott J.; Wang, Peng

doi:10.1038/s41467-018-06429-1

Cited by 209 publications

(220 citation statements)

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“…In addition to regulating plant physiological and morphological responses [12,13], a growing number of studies have demonstrated that these phytohormones also sculpt the root microbiome [14,15]. For instance, the secretion of root salicylic acid (SA) is involved in plant neighbour detection and shapes the root microbiome by modulating taxonomic groups of bacteria [9,10]. Similar functions have been reported for jasmonic acid (JA) and its derivatives [16].…”

Section: Introductionmentioning

confidence: 81%

“…In natural environments, plants constantly adjust the composition and concentration of root metabolites in response to various kinds of biotic stressors, such as neighbour competition, pathogen infection and herbivore attack [5][6][7]. This may result in allelochemical responses to neighbouring plants, reduced plant susceptibility to pathogen attack or the prevention of grazing by herbivores [8,9]. However, relatively few studies have sought to understand the mechanisms and effects of stress-induced root-secreted metabolites on rhizosphere microbiota [10,11].…”

Section: Introductionmentioning

confidence: 99%

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Root ethylene mediates rhizosphere microbial community reconstruction when chemically detecting cyanide produced by neighbouring plants

et al. 2020

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Background: Stress-induced hormones are essential for plants to modulate their microbiota and dynamically adjust to the environment. Despite the emphasis of the role of the phytohormone ethylene in the plant physiological response to heterospecific neighbour detection, less is known about how this activated signal mediates focal plant rhizosphere microbiota to enhance plant fitness. Here, using 3 years of peanut (Arachis hypogaea L.), a legume, and cyanide-containing cassava (Manihot esculenta Crantz) intercropping and peanut monocropping field, pot and hydroponic experiments in addition to exogenous ethylene application and soil incubation experiments, we found that ethylene, a cyanide-derived signal, is associated with the chemical identification of neighbouring cassava and the microbial re-assemblage in the peanut rhizosphere. Results: Ethylene production in peanut roots can be triggered by cyanide production of neighbouring cassava plants. This gaseous signal alters the microbial composition and re-assembles the microbial co-occurrence network of peanut by shifting the abundance of an actinobacterial species, Catenulispora sp., which becomes a keystone in the intercropped peanut rhizosphere. The re-assembled rhizosphere microbiota provide more available nutrients to peanut roots and support seed production. Conclusions: Our findings suggest that root ethylene acts as a signal with a dual role. It plays a role in perceiving biochemical cues from interspecific neighbours, and also has a regulatory function in mediating the rhizosphere microbial assembly, thereby enhancing focal plant fitness by improving seed production. This discovery provides a promising direction to develop novel intercropping strategies for targeted manipulations of the rhizosphere microbiome through phytohormone signals.

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Section: Introductionmentioning

confidence: 81%

Section: Introductionmentioning

confidence: 99%

Root ethylene mediates rhizosphere microbial community reconstruction when chemically detecting cyanide produced by neighbouring plants

et al. 2020

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“…officinale roots (Huang et al, ). In general, physical (e.g., light and contact), chemical (e.g., volatile and exudates), and biological (e.g., arbuscular mycorrhizal fungi) factors may trigger neighbourhood effects and affect plant growth and defence (Babikova et al, ; Crepy & Casal, ; Erb et al, ; Hu, Robert, et al, ; Kong et al, ; Semchenko, Saar, & Lepik, ; Yang, Callaway, & Atwater, ). As C .…”

Section: Discussionmentioning

confidence: 99%

“…In an earlier study, we found that the presence of C. stoebe enhanced the performance of M. melolontha larvae feeding on T. officinale roots . In general, physical (e.g., light and contact), chemical (e.g., volatile and exudates), and biological (e.g., arbuscular mycorrhizal fungi) factors may trigger neighbourhood effects and affect plant growth and defence (Babikova et al, 2013;Crepy & Casal, 2015;Erb et al, 2015;Hu, Robert, et al, 2018;Kong et al, 2018;Semchenko, Saar, & Lepik, 2014;Yang, Callaway, & Atwater, 2015). As C. stoebe constitutively releases large amounts of sesquiterpenes into the rhizosphere , we hypothesized that root VOCs may be responsible for the plant- Plant VOCs can influence herbivore performance directly or indirectly by changing the chemistry of receiver plants (Engelberth et al, 2004;Erb et al, 2015;Huang et al, 2018;Sugimoto et al, 2014;Veyrat, Robert, Turlings, & Erb, 2016;Ye et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants

Huang

Gfeller

Erb

2019

Plant Cell & Environment

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Volatile organic compounds (VOCs) emitted by plant roots can influence the germination and growth of neighbouring plants. However, little is known about the effects of root VOCs on plant–herbivore interactions of neighbouring plants. The spotted knapweed (Centaurea stoebe) constitutively releases high amounts of sesquiterpenes into the rhizosphere. Here, we examine the impact of C. stoebe root VOCs on the primary and secondary metabolites of sympatric Taraxacum officinale plants and the resulting plant‐mediated effects on a generalist root herbivore, the white grub Melolontha melolontha. We show that exposure of T. officinale to C.stoebe root VOCs does not affect the accumulation of defensive secondary metabolites but modulates carbohydrate and total protein levels in T. officinale roots. Furthermore, VOC exposure increases M. melolontha growth on T. officinale plants. Exposure of T. officinale to a major C. stoebe root VOC, the sesquiterpene (E)‐β‐caryophyllene, partially mimics the effect of the full root VOC blend on M. melolontha growth. Thus, releasing root VOCs can modify plant–herbivore interactions of neighbouring plants. The release of VOCs to increase the susceptibility of other plants may be a form of plant offense.

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“…We recently demonstrated that loliolide induced resistance to multiple herbivore pests, such as the two-spotted spider mite (Tetranychus urticae), western flower thrips (Frankliniella occidentalis), and common cutworm (Spodoptera litura), through the activation of JA-independent defense responses [5]. Loliolide has also been shown to function as an allelochemical in plant-plant communications [6,7]. Loliolide is produced via the chemical or enzymatic degradation process of α-carotene and β-carotene [5,[8][9][10].…”

Section: Introductionmentioning

confidence: 99%

α-Ionone, an Apocarotenoid, Induces Plant Resistance to Western Flower Thrips, Frankliniella occidentalis, Independently of Jasmonic Acid

2019

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Apocarotenoids, such as β-cyclocitral, α-ionone, β-ionone, and loliolide, are derived from carotenes via chemical or enzymatic processes. Recent studies revealed that β-cyclocitral and loliolide play an important role in various aspects of plant physiology, such as stress responses, plant growth, and herbivore resistance. However, information on the physiological role of α-ionone is limited. We herein investigated the effects of α-ionone on plant protection against herbivore attacks. The pretreatment of whole tomato (Solanum lycopersicum) plants with α-ionone vapor decreased the survival rate of western flower thrips (Frankliniella occidentalis) without exhibiting insecticidal activity. Exogenous α-ionone enhanced the expression of defense-related genes, such as basic β-1,3-glucanase and basic chitinase genes, in tomato leaves, but not that of jasmonic acid (JA)-or loliolide-responsive genes. The pretreatment with α-ionone markedly decreased egg deposition by western flower thrips in the JA-insensitive Arabidopsis (Arabidopsis thaliana) mutant coi1-1. We also found that common cutworm (Spodoptera litura) larvae fed on α-ionone-treated tomato plants exhibited a reduction in weight. These results suggest that α-ionone induces plant resistance to western flower thrips through a different mode of action from that of JA and loliolide.

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Plant neighbor detection and allelochemical response are driven by root-secreted signaling chemicals

Cited by 209 publications

References 60 publications

Root ethylene mediates rhizosphere microbial community reconstruction when chemically detecting cyanide produced by neighbouring plants

Root ethylene mediates rhizosphere microbial community reconstruction when chemically detecting cyanide produced by neighbouring plants

Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants

α-Ionone, an Apocarotenoid, Induces Plant Resistance to Western Flower Thrips, Frankliniella occidentalis, Independently of Jasmonic Acid

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