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Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts.

ABSTRACT: The life cycles of many organisms are constrained by the seasonality of resources. This is particularly true for leaf-mining herbivorous insects that use deciduous leaves to fuel growth and reproduction even beyond leaf fall. Our results suggest that an intimate association with bacterial endosymbionts might be their way of coping with nutritional constraints to ensure successful development in an otherwise senescent environment. We show that the phytophagous leaf-mining moth Phyllonorycter blancardella (Lepidoptera) relies on bacterial endosymbionts, most likely Wolbachia, to manipulate the physiology of its host plant resulting in the 'green-island' phenotype--photosynthetically active green patches in otherwise senescent leaves--and to increase its fitness. Curing leaf-miners of their symbiotic partner resulted in the absence of green-island formation on leaves, increased compensatory larval feeding and higher insect mortality. Our results suggest that bacteria impact green-island induction through manipulation of cytokinin levels. This is the first time, to our knowledge, that insect bacterial endosymbionts have been associated with plant physiology.

SUBMITTER: Kaiser W

PROVIDER: S-EPMC2894905 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts.

Kaiser Wilfried W Huguet Elisabeth E Casas Jérôme J Commin Céline C Giron David D

Proceedings. Biological sciences 20100331 1692

The life cycles of many organisms are constrained by the seasonality of resources. This is particularly true for leaf-mining herbivorous insects that use deciduous leaves to fuel growth and reproduction even beyond leaf fall. Our results suggest that an intimate association with bacterial endosymbionts might be their way of coping with nutritional constraints to ensure successful development in an otherwise senescent environment. We show that the phytophagous leaf-mining moth Phyllonorycter blan ...[more]

PMID: 20356892

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Project description:The microbiota of invasive animal species may be pivotal to their adaptation and spread, yet the processes driving the assembly and potential sources of host-microbiota remain poorly understood. Here, we characterized microbiota of four Liriomyza leaf miner fly species totaling 310 individuals across 43 geographical populations in China and assessed whether the microbiota of the wild leaf miner was acquired from the soil microbiota or the host plant microbiota, using high-throughput 16S rRNA sequencing. Bacterial communities differed significantly among four leaf miner species but did not mirror host phylogeny. Microbiota diversity in the native L. chinensis was significantly higher than in three invasive leaf miners (i.e., L. trifolii, L. huidobrensis, and L. sativae), yet the microbial community of the invasive species exhibited a more connected and complex network structure. Structural equation models revealed that host species identity was more important than environmental factors (e.g., geography, climate, or plants) in shaping microbiota composition. Using neutral and null model analyses, we found that deterministic processes like variable selection played a primary role in driving microbial community assembly, with some influence by stochastic processes like drift. The relative degree of these processes governing microbiota was likely correlated with host species but independent of either geographical or climatic factors. Finally, source tracking analysis showed that leaf miners might acquire microbes from their host plant rather than the soil. Our results provide a robust assessment of the ecological processes governing bacterial community assembly and potential sources of microbes in invasive leaf miners. IMPORTANCE The invasion of foreign species, including leaf miners, is a major threat to world biota. Host-associated microbiota may facilitate host adaption and expansion in a variety of ways. Thus, understanding the processes that drive leaf miner microbiota assembly is imperative for better management of invasive species. However, how microbial communities assemble during the leaf miner invasions and how predictable the processes remain unexplored. This work quantitatively deciphers the relative importance of deterministic process and stochastic process in governing the assembly of four leaf miner microbiotas and identifies potential sources of leaf miner-colonizing microbes from the soil-plant-leaf miner continuum. Our study provides new insights into the mechanisms underlying the drive of leaf miner microbiota assembly.

Project description:Identification of mechanisms that allow some species to outcompete others is a fundamental goal in ecology and invasive species management. One useful approach is to examine congeners varying in invasiveness in a comparative framework across native and invaded ranges. Acacia species have been widely introduced outside their native range of Australia, and a subset of these species have become invasive in multiple parts of the world. Within specific regions, the invasive status of these species varies. Our study examined whether a key mechanism in the life history of Acacia species, the legume-rhizobia symbiosis, influences acacia invasiveness on a regional scale. To assess the extent to which species varying in invasiveness correspondingly differ with regard to the diversity of rhizobia they associate with, we grew seven Acacia species ranging in invasiveness in California in multiple soils from both their native (Australia) and introduced (California) ranges. In particular, the aim was to determine whether more invasive species formed symbioses with a wider diversity of rhizobial strains (i.e. are more promiscuous hosts). We measured and compared plant performance, including aboveground biomass, survival, and nodulation response, as well as rhizobial community composition and richness. Host promiscuity did not differ among invasiveness categories. Acacia species that varied in invasiveness differed in aboveground biomass for only one soil and did not differ in survival or nodulation within individual soils. In addition, acacias did not differ in rhizobial richness among invasiveness categories. However, nodulation differed between regions and was generally higher in the native than introduced range. Our results suggest that all Acacia species introduced to California are promiscuous hosts and that host promiscuity per se does not explain the observed differences in invasiveness within this region. Our study also highlights the utility of assessing potential mechanisms of invasion in species' native and introduced ranges.

Dataset Information

Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts.

Publications

Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts.

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