Domestication affects the composition, diversity, and co-occurrence of the cereal seed microbiota

Abdullaeva, Yulduzkhon; Manirajan, Binoy Ambika; Honermeier, Bernd; Schnell, Sylvia; Cardinale, Massimiliano

doi:10.1016/j.jare.2020.12.008

Cited by 80 publications

(74 citation statements)

References 84 publications

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“…Notably, many crop, plant, and vegetable seeds were also reported to be inhabited by some of these bacterial genera (Johnston-Monje et al, 2016;Liu et al, 2017;Adam et al, 2018;Berg and Raaijmakers, 2018;Khalaf and Raizada, 2018;López et al, 2018;Wassermann et al, 2019a;Abdullaeva et al, 2021;Hone et al, 2021). However, despite the enormous potential of seed microbiomes to promote plant growth and sustainable agricultural practices, the impact of current international seed storage strategies on the seed microbial diversity and composition has not yet been evaluated (Berg and Raaijmakers, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…Some bacterial genera including Pseudomonas , Bacillus , Bradyrhizobium , Streptomyces , Rahnella , and Azospirillum and fungi, e.g., Piriformospora and Trichoderma , have proven to be promising in plant growth promotion in soybean production ( Tsavkelova et al, 2006 ; Ramírez and Kloepper, 2010 ; Schmidt et al, 2015 ; Bakhshandeh et al, 2020 ). Notably, many crop, plant, and vegetable seeds were also reported to be inhabited by some of these bacterial genera ( Johnston-Monje et al, 2016 ; Liu et al, 2017 ; Adam et al, 2018 ; Berg and Raaijmakers, 2018 ; Khalaf and Raizada, 2018 ; López et al, 2018 ; Wassermann et al, 2019a ; Abdullaeva et al, 2021 ; Hone et al, 2021 ). However, despite the enormous potential of seed microbiomes to promote plant growth and sustainable agricultural practices, the impact of current international seed storage strategies on the seed microbial diversity and composition has not yet been evaluated ( Berg and Raaijmakers, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

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Implications of Seed Vault Storage Strategies for Conservation of Seed Bacterial Microbiomes

et al. 2021

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Global seed vaults are important, as they conserve plant genetic resources for future breeding to improve crop yield and quality and to overcome biotic and abiotic stresses. However, little is known about the impact of standard storage procedures, such as seed drying and cold storage on the seed bacterial community, and the ability to recover seed-associated bacteria after storage. In this study, soybean [Glycine max (L.) Merr.] seeds were analyzed to characterize changes in the bacterial community composition and culturability under varying storage conditions. The G. max bacterial microbiome was analyzed from undried seed, dried seed, and seed stored for 0, 3, 6, and 14months. Storage temperatures consisted of −20°C, 4°C, and room temperature (RT), with −20°C being commonly used in seed storage vaults globally. The seed microbiome of G. max was dominated by Gammaproteobacteria under all conditions. Undried seed was dominated by Pantoea (33.9%) and Pseudomonas (51.1%); however, following drying, the abundance of Pseudomonas declined significantly (0.9%), Pantoea increased significantly (73.6%), and four genera previously identified including Pajaroellobacter, Nesterenkonia, env.OPS_17, and Acidibacter were undetectable. Subsequent storage at RT, 4, or −20°C maintained high-abundance Genera at the majority of time points, although RT caused greater fluctuations in abundances. For many of the low-abundance Genera, storage at −20°C resulted in their gradual disappearance, whereas storage at 4°C or RT resulted in their more rapid disappearance. The changes in seed bacterial composition were reflected by cultured bacterial taxa obtained from the stored G. max seed. The main taxa were largely culturable and had similar relative abundance, while many, but not all, of the low-abundance taxa were also culturable. Overall, these results indicate that the initial seed drying affects the seed bacterial composition, suggesting that microbial isolation prior to seed drying is recommended to conserve these microbes. The standard seed storage condition of −20°C is most suitable for conservation of the bacterial seed microbiome, as this storage temperature slows down the loss of seed bacterial diversity over longer time periods, particularly low-abundance taxa.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Implications of Seed Vault Storage Strategies for Conservation of Seed Bacterial Microbiomes

et al. 2021

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“…Seed-associated endophytes have been described as capable of performing different functions essential for the plant, such as phytohormone production (Shahzad et al 2017;Alibrandi et al 2018), seedling and plant growth promotion (Rahman et al 2018;White et al 2017;Hardoim et al 2012), siderophore production (Díaz Herrera et al 2016;Alibrandi et al 2018), as well as antifungal property and antibiotic production (Verma et al 2017;Fürnkranz et al 2012;Donnarumma et al 2011). Moreover, it has been recently shown in cereals that seed-associated bacteria have coevolved with the plant hosts during domestication, likely as a result of mutualistic reciprocal advantage (Abdullaeva et al 2021).…”

Section: Introductionmentioning

confidence: 99%

The cypsela (achene) of Echinacea purpurea as a diffusion unit of a community of microorganisms

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Viola

Miceli

et al. 2021

Appl Microbiol Biotechnol

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Echinacea purpurea is a plant cultivated worldwide for its pharmaceutical properties, mainly related to the stimulation of the immune system in the treatment of respiratory infections. The cypselas (fruits) of E. purpurea were examined in order to investigate the presence, localization and potential function(s) of endophytic microorganisms. Electron and confocal microscopy observations showed that three different components of microorganisms were associated to cypselas of E. purpurea: (i) one endocellular bacterial component in the cotyledons, enclosed within the host membrane; (ii) another more generic bacterial component adhering to the external side of the perianth; and (iii) a fungal component inside the porous layer of the perianth, the woody and porous modified residual of the flower, in the form of numerous hyphae able to cross the wall between adjacent cells. Isolated bacteria were affiliated to the genera Paenibacillus, Pantoea, and Sanguibacter. Plate tests showed a general resistance to six different antibiotics and also to an antimicrobial-producing Rheinheimera sp. test strain. Finally, microbiome-deprived E. purpurea seeds showed a reduced ability to germinate, suggesting an active role of the microbiome in the plant vitality. Our results suggest that the endophytic bacterial community of E. purpurea, previously found in roots and stem/leaves, might be already carried at the seed stage, hosted by the cotyledons. A further microbial fungal component is transported together with the seed in the perianth of the cypsela, whose remarkable structure may be considered as an adaptation for fungal transportation, and could influence the capability of the seed to germinate in the soil.Key Points• The fruit of Echinacea purpurea contains fungi not causing any damage to the plant.• The seed cotyledons contain endocellular bacteria.• Seed/fruit deprived of the microbiome showed a reduced ability to germinate.

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“…ParaFit compares two distance matrices constructed from host and microbial phylogenetic distances and tests for random associations between the groups [52]. Positive correlations can indicate host-microbe coevolution [32, 53]. Tests for cophylogeny conducted on all samples collected on day 38 regardless of treatment using ParaFit (ParaFitGlobal=1.6024, p=0.001, permutations=999), and PACo (PACo=0.999, p=0.003) revealed significant global-fit cophylogenetic relationships.…”

Section: Resultsmentioning

confidence: 99%

Evolutionary History Impacts Phyllosphere Community Assembly on Forage Grasses

Nüsslein

2021

Preprint

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Benefits leaf bacterial communities provide to plant hosts are reduced by external stress. Understanding how plant hosts impact phyllosphere community assembly, how microbes influence plant traits, and how this interaction changes under stress will advance our insight into the evolutionary relationship between plants and their microbial communities. We investigated phyllosphere community assembly change over time, between host species, and under drought stress on three native temperate grasses and three non-native tropical grasses. By growing them together, effects of host geography and differences in environmental variables were eliminated allowing us to test evolutionary history on community assembly. We found evidence of phylosymbiosis which increased significantly under drought stress, indicating phyllosphere communities and their response to stress relate to grass species phylogeny. We also show native temperate grasses displayed stronger cophylogenetic relationships between grass hosts and their microbial communities and had increased selection by host species over time compared to non-native tropical hosts. Interestingly, the functional marker gene nifH, though differentially present on all host species was not susceptible to drought. The evidence of shared evolutionary history, presence of functionally important bacteria, and responses to drought suggest that microbial communities are important plant traits that coevolve alongside their plant hosts.

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Domestication affects the composition, diversity, and co-occurrence of the cereal seed microbiota

Abstract: Graphical abstract

Cited by 80 publications

References 84 publications

Implications of Seed Vault Storage Strategies for Conservation of Seed Bacterial Microbiomes

Implications of Seed Vault Storage Strategies for Conservation of Seed Bacterial Microbiomes

The cypsela (achene) of Echinacea purpurea as a diffusion unit of a community of microorganisms

Evolutionary History Impacts Phyllosphere Community Assembly on Forage Grasses

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