Transmission of synthetic seed bacterial communities to radish seedlings: impact on microbiota assembly and plant phenotype

Abstract

Seed-borne microorganisms can be pioneer taxa during germination and seedling emergence. Still, the identity and phenotypic effects of these taxa that constitute a primary inoculum of plant microbiota is mostly unknown. Here, we studied the transmission of bacteria from radish seeds to seedlings using the inoculation of individual seed-borne strains and synthetic communities (SynComs) under in vitro conditions. The SynComs were composed of highly abundant and prevalent, sub-dominant or rare bacterial seed taxa. We monitored the transmission of each strain alone or in communities using gyrB gene amplicon sequencing and assessed their impacts on germination and seedling phenotype. All strains and SynComs successfully colonized seedlings and we were able to reconstruct a richness gradient (6, 8 and 12 strains) on both seeds and seedlings. Stenotrophomonas rhizophila became dominant on seedlings of the three SynComs but most strains had variable transmission success (i.e increasing, stable or decreasing during seed to seedling transition) that also depended on the SynCom richness. Some seed-borne strains (Pseudomonas viridiflava, Paenibacillus sp) had detrimental effects on germination and seedling development. Abnormal seedling morphologies were also observed with SynComs but their proportions decreased at the highest richness level. Interestingly, the three bacterial strains identified as core taxa of radish seeds (Pseudomonas viridiflava, Pantoea agglomerans, Erwinia persicina) were associated with detrimental effects on seedling phenotypes either in isolation or in SynComs. These results confirm that the plant core microbiome includes pathogenic and not only commensal or mutualistic taxa. Altogether, these results show that SynCom inoculation can effectively manipulate seed and seedling microbiota diversity and highlight strong fitness differences between native seed-borne taxa in the colonization of these habitats.

The type VI secretion system of Stenotrophomonas rhizophilaCFBP13503 limits the transmission of Xanthomonas campestris pv. campestris 8004 from radish seeds to seedlings

“…This is the case for the T6SS of S. rhizophila CFBP13503 and more generally for strains affiliated with the S. rhizophila complex, including the type strain DSM14405 T (Wolf et al., 2002 ). S. rhizophila strains are not only known for their ability to colonize a wide range of plant species following seed inoculation (Schmidt et al., 2012 ; Simonin et al., 2023 ) but also to exhibit antifungal (Berg & Ballin, 1994 ) and antibacterial activities (Lottmann et al., 1999 ). For instance, the strain S. rhizophila DSM14405 T protects plants against Fusarium solani and displays antagonistic activity against various phytopathogenic fungi under high salt conditions (Egamberdieva et al., 2011 ).…”

“…Three subsamples of 300 radish seeds ( Raphanus sativus ‘Flamboyant 5’) were surface sterilized using the protocol described in Simonin et al. ( 2023 ). Sterilized seeds were dried 30 min before inoculation in a laminar flow cabinet.…”

“…This is the case for the T6SS of S. rhizophila CFBP13503 and more generally for strains affiliated with the S. rhizophila complex, including the type strain DSM14405 T (Wolf et al, 2002). S. rhizophila strains are not only known for their ability to colonize a wide range of plant species following seed inoculation (Schmidt et al, 2012;Simonin et al, 2023) but also to exhibit antifungal (Berg & Ballin, 1994) and antibacterial…”

“…Diversity surveys of the radish seed microbiota have highlighted that Xcc shares the same habitat as numerous bacterial strains related to the S. rhizophila species (Rezki et al., 2016 , 2018 ). Strains of S. rhizophila are efficient seedling colonizers of cotton, tomato, sweet pepper (Schmidt et al., 2012 ) and radish (Simonin et al., 2023 ) as well as commonly isolated in the rhizosphere of different plant species including rapeseed (Berg et al., 1996 ) and potato (Lottmann et al., 1999 ). The type strain of S. rhizophila , DSM14405 T , can protect plants against osmotic stress (Alavi et al., 2013 ; Egamberdieva et al., 2011 ) and limits the growth of fungal pathogens (Minkwitz & Berg, 2001 ).…”

The Type VI secretion systemof Stenotrophomonas rhizophilaCFBP13503 limits the transmission ofXanthomonas campestrispv. campestris8004 from radish seeds to seedlings

“…Diversity surveys of the radish seed microbiota have highlighted that Xcc shares the same habitat as numerous bacterial strains related to the S. rhizophila species (Rezki et al, 2016(Rezki et al, , 2018. Strains of S. rhizophila are efficient seedling colonizers of cotton, tomato, sweet pepper (Schmidt et al, 2012) and radish (Simonin et al, 2023) as well as commonly isolated in the rhizosphere of different plant species including rapeseed (Berg et al, 1996) and potato (Lottmann et al, 1999). The type strain of S. rhizophila, DSM14405 T , can protect plants against osmotic stress (Alavi et al, 2013;Egamberdieva et al, 2011) and limits the growth of fungal pathogens (Minkwitz and Berg, 2001).…”