Dataset Information

Root volatiles in plant-plant interactions I: High root sesquiterpene release is associated with increased germination and growth of plant neighbours.

ABSTRACT: Volatile organic compounds (VOCs) emitted by plant leaves can influence the physiology of neighbouring plants. In contrast to leaf VOCs, little is known about the role of root VOCs in plant-plant interactions. Here, we characterize constitutive root VOC emissions of the spotted knapweed (Centaurea stoebe) and explore the impact of these VOCs on the germination and growth of different sympatric plant species. We show that C. stoebe roots emit high amounts of sesquiterpenes, with estimated release rates of (E)-?-caryophyllene above 3 ?g g-1 dw hr-1 . Sesquiterpene emissions show little variation between different C. stoebe populations but vary substantially between different Centaurea species. Through root transcriptome sequencing, we identify six root-expressed sesquiterpene synthases (TPSs). Two root-specific TPSs, CsTPS4 and CsTPS5, are sufficient to produce the full blend of emitted root sesquiterpenes. VOC-exposure experiments demonstrate that C. stoebe root VOCs have neutral to positive effects on the germination and growth of different sympatric neighbours. Thus, constitutive root sesquiterpenes produced by two C. stoebe TPSs are associated with facilitation of sympatric neighbouring plants. The release of root VOCs may thus influence plant community structure in nature.

SUBMITTER: Gfeller V

PROVIDER: S-EPMC6850102 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Root volatiles in plant-plant interactions I: High root sesquiterpene release is associated with increased germination and growth of plant neighbours.

Gfeller Valentin V Huber Meret M Förster Christiane C Huang Wei W Köllner Tobias G TG Erb Matthias M

Plant, cell & environment 20190328 6

Volatile organic compounds (VOCs) emitted by plant leaves can influence the physiology of neighbouring plants. In contrast to leaf VOCs, little is known about the role of root VOCs in plant-plant interactions. Here, we characterize constitutive root VOC emissions of the spotted knapweed (Centaurea stoebe) and explore the impact of these VOCs on the germination and growth of different sympatric plant species. We show that C. stoebe roots emit high amounts of sesquiterpenes, with estimated release ...[more]

PMID: 30737807

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Project description:Volatile compounds produced by plant-associated microorganisms represent a diverse resource to promote plant growth and health. Here, we investigated the effect of volatiles from root-associated Microbacterium species on plant growth and development. Volatiles of eight strains induced significant increases in shoot and root biomass of Arabidopsis but differed in their effects on root architecture. Microbacterium strain EC8 also enhanced root and shoot biomass of lettuce and tomato. Biomass increases were also observed for plants exposed only briefly to volatiles from EC8 prior to transplantation of the seedlings to soil. These results indicate that volatiles from EC8 can prime plants for growth promotion without direct and prolonged contact. We further showed that the induction of plant growth promotion is tissue specific; that is, exposure of roots to volatiles from EC8 led to an increase in plant biomass, whereas shoot exposure resulted in no or less growth promotion. Gas chromatography-quadrupole time of flight mass spectometry (GC-QTOF-MS) analysis revealed that EC8 produces a wide array of sulfur-containing compounds, as well as ketones. Bioassays with synthetic sulfur volatile compounds revealed that the plant growth response to dimethyl trisulfide was concentration-dependent, with a significant increase in shoot weight at 1 ?M and negative effects on plant biomass at concentrations higher than 1 mM. Genome-wide transcriptome analysis of volatile-exposed Arabidopsis seedlings showed upregulation of genes involved in assimilation and transport of sulfate and nitrate. Collectively, these results show that root-associated Microbacterium primes plants, via the roots, for growth promotion, most likely via modulation of sulfur and nitrogen metabolism.IMPORTANCE In the past decade, various studies have described the effects of microbial volatiles on other (micro)organisms in vitro, but their broad-spectrum activity in vivo and the mechanisms underlying volatile-mediated plant growth promotion have not been addressed in detail. Here, we revealed that volatiles from root-associated bacteria of the genus Microbacterium can enhance the growth of different plant species and can prime plants for growth promotion without direct and prolonged contact between the bacterium and the plant. Collectively, these results provide new opportunities for sustainable agriculture and horticulture by exposing roots of plants only briefly to a specific blend of microbial volatile compounds prior to transplantation of the seedlings to the greenhouse or field. This strategy has no need for large-scale introduction or root colonization and survival of the microbial inoculant.

Project description:Plants live in a social environment, with interactions among neighbours a ubiquitous aspect of life. Though many of these interactions occur in the soil, our understanding of how plants alter root growth and the patterns of soil occupancy in response to neighbours is limited. This is in contrast to a rich literature on the animal behavioural responses to changes in the social environment. For plants, root behavioural changes that alter soil occupancy patterns can influence neighbourhood size and the frequency or intensity of competition for soil resources; issues of fundamental importance to understanding coexistence and community assembly. Here we report a large comparative study in which individuals of 20 species were grown with and without each of two neighbour species. Through repeated root visualization and analyses, we quantified many putative root behaviours, including the extent to which each species altered aspects of root system growth (e.g. rooting breadth, root length, etc.) in response to neighbours. Across all species, there was no consistent behavioural response to neighbours (i.e. no general tendencies towards root over-proliferation nor avoidance). However, there was a substantial interspecific variation showing a continuum of behavioural variation among the 20 species. Multivariate analyses revealed two novel and predominant root behavioural strategies: (i) size-sensitivity, in which focal plants reduced their overall root system size in response to the presence of neighbours, and (ii) location-sensitivity, where focal plants adjusted the horizontal and vertical placement of their roots in response to neighbours. Of these, size-sensitivity represents the commonly assumed response to competitive encounters-reduced growth. However, location sensitivity is not accounted for in classic models and concepts of plant competition, though it is supported from recent work in plant behavioural ecology. We suggest that these different strategies could have important implications for the ability of a plant to persist in the face of strong competitors, and that location sensitivity may be a critical behavioural strategy promoting competitive tolerance and coexistence.

Dataset Information

Root volatiles in plant-plant interactions I: High root sesquiterpene release is associated with increased germination and growth of plant neighbours.

Publications

Root volatiles in plant-plant interactions I: High root sesquiterpene release is associated with increased germination and growth of plant neighbours.

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