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Summary Arbuscular mycorrhizal fungi (AMF) form beneficial associations with plants, and are thought to have been critical to the adaptation of the ancestor of terrestrial plants during the transition onto land. However, the ability of AMF to associate with aquatic plants is unclear. To address this, we used 65 publicly available genomes and transcriptomes (25 freshwater, 23 terrestrial and 17 marine plants) to interrogate the genomic potential to form AMF associations in aquatic plant lineages in the order Alismatales. We explored the presence or absence of homologs of 45 genes, with a a special focus on six critical genes including three that co-evolved with AMF associations (RAD1, STR1, STR2) and three necessary for intracellular symbiosis (SymRK, CCaMK/DMI3, CYCLOPS/IDP3). Our results indicate a pattern likely consistent with independent gene losses (or extreme divergence) of symbiosis genes across aquatic lineages suggesting a possible inability to form AMF associations. However, some of these conserved genes (i.e.,CCaMK/DMI3) are purported to function in other types of fungal symbioses, such as ectomycorrhizal symbiosis, and were observed here in a subset of aquatic lineages, including seagrasses. Overall, our findings highlight the complex evolutionary trajectories of symbiosis-related genes in aquatic plants, suggesting that while AMF associations may have been lost in certain lineages, others have genes that may allow them to form alternative fungal symbioses which may still play an underappreciated role in their ecology.
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IPD3, a master regulator of arbuscular mycorrhizal symbiosis, affects genes for immunity and metabolism of non-host Arabidopsis when restored long after its evolutionary loss
Abstract Arbuscular mycorrhizal symbiosis (AM) is a beneficial trait originating with the first land plants, which has subsequently been lost by species scattered throughout the radiation of plant diversity to the present day, including the modelArabidopsis thaliana. To explore if elements of this apparently beneficial trait are still present and could be reactivated we generatedArabidopsisplants expressing a constitutively active form ofInteracting Protein of DMI3, a key transcription factor that enables AM within the Common Symbiosis Pathway, which was lost fromArabidopsisalong with the AM host trait. We characterize the transcriptomic effect of expressingIPD3inArabidopsiswith and without exposure to the AM fungus (AMF)Rhizophagus irregularis, and compare these results to the AM modelLotus japonicusand itsipd3knockout mutantcyclops-4. Despite its long history as a non-AM species, restoringIPD3in the form of its constitutively active DNA-binding domain toArabidopsisaltered expression of specific gene networks. Surprisingly, the effect of expressingIPD3inArabidopsisand knocking it out inLotuswas strongest in plants not exposed to AMF, which is revealed to be due to changes inIPD3genotype causing a transcriptional state, which partially mimics AMF exposure in non-inoculated plants. Our results indicate that molecular connections to symbiosis machinery remain in place in this nonAM species, with implications for both basic science and the prospect of engineering this trait for agriculture.
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- Award ID(s):
- 1828820
- PAR ID:
- 10491265
- Publisher / Repository:
- Springer Science + Business Media
- Date Published:
- Journal Name:
- Plant Molecular Biology
- Volume:
- 114
- Issue:
- 2
- ISSN:
- 0167-4412
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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