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Conservation and transmission of seed bacterial endophytes across generations following crossbreeding and repeated inbreeding of rice at different geographic locations.

ABSTRACT: There are comparatively diverse bacterial communities inside seeds, which are vertically transmitted and conserved, becoming sources of endophytes in the next generation of host plants. We studied how rice seed endophyte composition changed over time following crossbreeding, repeated inbreeding, subsequent human selection and planting of different rice seeds in different ecogeographical locations. Using terminal-restriction fragment length polymorphism analysis to study bacterial communities, we observed that diversity between the original parents and their offspring may show significant differences in richness, evenness and diversity indices. Heat maps reveal substantial contributions of both or either parent in the shaping of the bacterial seed endophytes of the offspring. Most of the terminal restriction fragments (T-RFs) of the subsequent progeny could be traced to any or both of its parents while unique T-RFs of the offspring suggest external sources of colonization particularly when the seeds were cultivated in different locations. Many similar groups of endophytic bacteria persist in the seeds even after recultivation in different locations, indicating resilience to environmental changes and conservation of bacteria across generations. This study suggests that parent plants contributed to the shaping of seed bacterial endophytes of their offspring, although it is also possible that these soil grown rice plants recruit similar populations of endophytes from the soil generation after generation. This study also highlights some bacterial groups belonging to Herbaspirillum, Microbacterium, Curtobacterium, Stenotrophomonas, Xanthomonas and Enterobacter that may be part of a transmitted and conserved "core microbiota" that are ubiquitous and dominant members of the endophytic communities of the rice seeds.

SUBMITTER: Walitang DI

PROVIDER: S-EPMC6436425 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Conservation and transmission of seed bacterial endophytes across generations following crossbreeding and repeated inbreeding of rice at different geographic locations.

Walitang Denver I DI Kim Chan-Gi CG Jeon Sunyoung S Kang Yeongyeong Y Sa Tongmin T

MicrobiologyOpen 20180610 3

There are comparatively diverse bacterial communities inside seeds, which are vertically transmitted and conserved, becoming sources of endophytes in the next generation of host plants. We studied how rice seed endophyte composition changed over time following crossbreeding, repeated inbreeding, subsequent human selection and planting of different rice seeds in different ecogeographical locations. Using terminal-restriction fragment length polymorphism analysis to study bacterial communities, we ...[more]

PMID: 29888428

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Project description:Endophytes are non-pathogenic microbes living inside plants. We asked whether endophytic species were conserved in the agriculturally important plant genus Zea as it became domesticated from its wild ancestors (teosinte) to modern maize (corn) and moved from Mexico to Canada. Kernels from populations of four different teosintes and 10 different maize varieties were screened for endophytic bacteria by culturing, cloning and DNA fingerprinting using terminal restriction fragment length polymorphism (TRFLP) of 16S rDNA. Principle component analysis of TRFLP data showed that seed endophyte community composition varied in relation to plant host phylogeny. However, there was a core microbiota of endophytes that was conserved in Zea seeds across boundaries of evolution, ethnography and ecology. The majority of seed endophytes in the wild ancestor persist today in domesticated maize, though ancient selection against the hard fruitcase surrounding seeds may have altered the abundance of endophytes. Four TRFLP signals including two predicted to represent Clostridium and Paenibacillus species were conserved across all Zea genotypes, while culturing showed that Enterobacter, Methylobacteria, Pantoea and Pseudomonas species were widespread, with γ-proteobacteria being the prevalent class. Twenty-six different genera were cultured, and these were evaluated for their ability to stimulate plant growth, grow on nitrogen-free media, solubilize phosphate, sequester iron, secrete RNAse, antagonize pathogens, catabolize the precursor of ethylene, produce auxin and acetoin/butanediol. Of these traits, phosphate solubilization and production of acetoin/butanediol were the most commonly observed. An isolate from the giant Mexican landrace Mixteco, with 100% identity to Burkholderia phytofirmans, significantly promoted shoot potato biomass. GFP tagging and maize stem injection confirmed that several seed endophytes could spread systemically through the plant. One seed isolate, Enterobacter asburiae, was able to exit the root and colonize the rhizosphere. Conservation and diversity in Zea-microbe relationships are discussed in the context of ecology, crop domestication, selection and migration.

Project description:BackgroundRice (Oryza sativa L. ssp. indica) seeds as plant microbiome present both an opportunity and a challenge to colonizing bacterial community living in close association with plants. Nevertheless, the roles and activities of bacterial endophytes remain largely unexplored and insights into plant-microbe interaction are compounded by its complexity. In this study, putative functions or physiological properties associated with bacterial endophytic nature were assessed. Also, endophytic roles in plant growth and germination that may allow them to be selectively chosen by plants were also studied.ResultsThe cultivable seed endophytes were dominated by Proteobacteria particularly class Gammaproteobacteria. Highly identical type strains were isolated from the seed endosphere regardless of the rice host's physiological tolerance to salinity. Among the type strains, Flavobacterium sp., Microbacterium sp. and Xanthomonas sp. were isolated from the salt-sensitive and salt-tolerant cultivars. PCA-Biplot ordination also showed that specific type strains isolated from different rice cultivars have distinguishing similar characteristics. Flavobacterium sp. strains are phosphate solubilizers and indole-3-acetic acid producers with high tolerance to salinity and osmotic stress. Pseudomonas strains are characterized as high siderophore producers while Microbacterium sp. and Xanthomonas sp. strains have very high pectinase and cellulase activity. Among the physiological traits of the seed endophytes, bacterial pectinase and cellulase activity are positively correlated as well as salt and osmotic tolerance. Overall characterization shows that majority of the isolates could survive in 4-8% salt concentration as well as in 0.6 M and 1.2 M sucrose solution. The activities of catalase, pectinase and cellulase were also observed in almost all of the isolates indicating the importance of these characteristics for survival and colonization into the seed endosphere. Seed bacterial endophytes also showed promising plant growth promoting activities including hormone modulation, nitrogen fixation, siderophore production and phosphate solubilization.ConclusionThough many of the isolates possess similar PGP and endophytic physiological traits, this study shows some prominent and distinguishing traits among bacterial groups indicating key determinants for their success as endophytes in the rice seed endosphere. Rice seeds are also inhabited by bacterial endophytes that promote growth during early seedling development.

Project description:BackgroundRice, which serves as a staple food for more than half of the world's population, is grown worldwide. The hybridization of wild and cultivated rice has enabled the incorporation of resistance to varying environmental conditions. Endophytic microbiota are known to be transferred with their host plants. Although some studies have reported on the endophytic microbiota of wild and cultivated rice, the inheritance from wild and cultivated rice accessions in next generations, in terms of endophytic microbiota, has not been examined.ResultsIn the present study, the endophytic microbial community structures of Asian and African wild and cultivated rice species were compared with those of their F1 offspring. High-throughput sequencing data of bacterial 16S rDNA and fungal internal transcribed spacer regions were used to classify the endophytic microbiota of collected samples of rice. Results indicated that when either African or Asian wild rice species were crossed with cultivated rice accessions, the first generation harbored a greater number of root endophytic fungi than the cultivated parent used to make the crosses. Network analysis of the bacterial and fungal operational taxonomic units revealed that Asian and African wild rice species clustered together and exhibited a greater number of significant correlations between fungal taxa than cultivated rice. The core bacterial genus Acidovorax and the core fungal order Pleosporales, and genera Myrothecium and Bullera connected African and Asian wild rice accessions together, and both the wild rice accessions with their F1 offspring. On the other hand, the core bacterial genus Bradyrhizobium and the core fungal genera Dendroclathra linked the African and Asian cultivated rice accessions together.ConclusionsThis study has theoretical significance for understanding the effect of breeding on the inheritance of endophytic microbiota of rice and identifying beneficial endophytic bacteria and fungi among wild and cultivated rice species, and their F1 offspring.

Dataset Information

Conservation and transmission of seed bacterial endophytes across generations following crossbreeding and repeated inbreeding of rice at different geographic locations.

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Conservation and transmission of seed bacterial endophytes across generations following crossbreeding and repeated inbreeding of rice at different geographic locations.

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