Nuclear phylotranscriptomics and phylogenomics support numerous polyploidization events and hypotheses for the evolution of rhizobial nitrogen-fixing symbiosis in Fabaceae

Zhao, Yiyong; Zhang, Rong; Jiang, Kai; Qi, Ji; Hu, Yi; Guo, Jing; Zhu, Renbin; Zhang, Taikui; Egan, Ashley N.; Yi, Ting Shuang; Huang, Chien-Hua; Mā, Hong

doi:10.1016/j.molp.2021.02.006

Cited by 96 publications

(95 citation statements)

References 134 publications

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“…This is consistent with other studies based on nuclear genes from transcriptomes and/or genomes of 333 genera of Fabaceae, in which F. macrophylla was also suggested to be closely related to a clade consisting of Dolichos , Dunbaria , Cajanus and Rhynchosia (Zhao et al. 2021 ).…”

supporting

confidence: 92%

The complete chloroplast genome of Flemingia macrophylla (Willd.) Prain (Fabaceae) from Guangxi, China

Qin

Cui

et al. 2021

Mitochondrial DNA Part B

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supporting

confidence: 92%

The complete chloroplast genome of Flemingia macrophylla (Willd.) Prain (Fabaceae) from Guangxi, China

Qin

Cui

et al. 2021

Mitochondrial DNA Part B

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“…Recent advances in deep- and genus-level legume phylogenomics using both plastid and nuclear genes ( Cannon et al, 2015 ; LPWG et al, 2017 ; Vatanparast et al, 2018 ; Ojeda et al, 2019 ; Koenen et al, 2020a , b , 2021 ; Oyebanji et al, 2020 ; Zhang et al, 2020 ; Zhao et al, 2021 ) have contributed to the resolution of some of the obscure deep relationships in the Papilionoideae. Still, many morphological key genera in the early-diverging lineages outside the agriculturally important NPAAA clade ( Cardoso et al, 2012a , 2013a ) have not been evaluated in any phylogenomic study.…”

Section: Introductionmentioning

confidence: 99%

Highly Resolved Papilionoid Legume Phylogeny Based on Plastid Phylogenomics

et al. 2022

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Comprising 501 genera and around 14,000 species, Papilionoideae is not only the largest subfamily of Fabaceae (Leguminosae; legumes), but also one of the most extraordinarily diverse clades among angiosperms. Papilionoids are a major source of food and forage, are ecologically successful in all major biomes, and display dramatic variation in both floral architecture and plastid genome (plastome) structure. Plastid DNA-based phylogenetic analyses have greatly improved our understanding of relationships among the major groups of Papilionoideae, yet the backbone of the subfamily phylogeny remains unresolved. In this study, we sequenced and assembled 39 new plastomes that are covering key genera representing the morphological diversity in the subfamily. From 244 total taxa, we produced eight datasets for maximum likelihood (ML) analyses based on entire plastomes and/or concatenated sequences of 77 protein-coding sequences (CDS) and two datasets for multispecies coalescent (MSC) analyses based on individual gene trees. We additionally produced a combined nucleotide dataset comprising CDS plus matK gene sequences only, in which most papilionoid genera were sampled. A ML tree based on the entire plastome maximally supported all of the deep and most recent divergences of papilionoids (223 out of 236 nodes). The Swartzieae, ADA (Angylocalyceae, Dipterygeae, and Amburaneae), Cladrastis, Andira, and Exostyleae clades formed a grade to the remainder of the Papilionoideae, concordant with nine ML and two MSC trees. Phylogenetic relationships among the remaining five papilionoid lineages (Vataireoid, Dermatophyllum, Genistoid s.l., Dalbergioid s.l., and Baphieae + Non-Protein Amino Acid Accumulating or NPAAA clade) remained uncertain, because of insufficient support and/or conflicting relationships among trees. Our study fully resolved most of the deep nodes of Papilionoideae, however, some relationships require further exploration. More genome-scale data and rigorous analyses are needed to disentangle phylogenetic relationships among the five remaining lineages.

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“…They were later observed in legumes, mostly in woody Caesalpinioideae (sensu LPWG (2017)) where they appeared to be relatively common ( de Faria et al, 1986de Faria et al, , 1987Fonseca et al, 2012). FT-type nodules have also been reported in a few legumes belonging to subfamily Papilionoideae, which is sister to Caesalpinioideae (Koenen et al, 2020b;Zhao et al, 2021), including tree genera such as Andira, Dahlstedtia and Hymenolobium, and members of tribe Brongniartieae (de Faria et al, 1986Faria et al, , 1987Sprent, , 2009Sprent et al, 2013Sprent et al, , 2017. Ultrastructural and histochemical analyses of FT-type nodules in Parasponia with rhizobia (Smith et al, 1986), actinorhizal nodules with Frankia (Pawlowski & Demchenko, 2012), and in some legumes (de Faria et al, 1986Faria et al, , 1987, revealed that FTs are superficially similar to the cell wall-bound "invasive" IT e.g.…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, nodulation involves structural and biochemical innovations underpinned by many genes, multiple developmental and signalling pathways, and coordination between the host and the microsymbiont (Brewin, 2004; Oldroyd & Downie, 2008; Oldroyd, 2013; Sprent et al , 2017; Ardley & Sprent, 2021; Ledermann et al , 2021), such that evolutionary gains of nodulation are likely to be more difficult than losses (van Velzen et al , 2018a; Edwards, 2019). Recently, the alternative hypothesis of a single evolutionary origin of nodulation followed by numerous parallel evolutionary losses has gained traction, notably from comparative genomic studies documenting pseudogenization or loss of key nodulation genes in non-nodulating species, indicative of secondary losses of nodulation (Griesmann et al , 2018; van Velzen et al , 2018a; Zhao et al , 2021). Re-examination of the structural and developmental homologies and commonalities in symbiotic gene function across nodulating lineages spanning the N 2 -fixing clade suggested that these also provide more compelling evidence for the single gain and multiple losses hypothesis (van Velzen et al , 2018a).…”

Section: Introductionmentioning

confidence: 99%

The innovation of the symbiosome has enhanced the evolutionary stability of nitrogen fixation in legumes

Faria

Ringelberg

Gross

et al. 2022

Preprint

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SummaryNitrogen-fixing symbiosis is globally important in ecosystem functioning and agriculture, yet the evolutionary history of nodulation remains the focus of considerable debate. Recent evidence suggesting a single origin of nodulation followed by massive parallel evolutionary losses raises questions about why a few lineages in the N2-fixing clade retained nodulation and diversified as stable nodulators while most did not. Within legumes, nodulation is restricted to the two most diverse subfamilies, Papilionoideae and Caesalpinioideae, which show stable retention of nodulation across their core clades.We characterize two nodule anatomy types across 128 species in 56 of the 150 genera of the legume subfamily Caesalpinioideae: 1) fixation thread nodules (FTs), where nitrogen-fixing bacteroids are retained within the apoplast in modified infection threads and 2) symbiosomes, where rhizobia are symplastically internalized in the host cell cytoplasm within membrane-bound symbiosomes.Using a robust phylogenomic tree based on 997 genes from 146 caesalpinioid genera, we show that losses of nodulation are more prevalent in lineages with FTs.We propose that evolution of the symbiosome allows for a more intimate and enduring symbiosis through greater compartmentalisation of their rhizobial microsymbionts, resulting in greater evolutionary stability of nodulation across this species-rich pantropical clade of legumes.

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Nuclear phylotranscriptomics and phylogenomics support numerous polyploidization events and hypotheses for the evolution of rhizobial nitrogen-fixing symbiosis in Fabaceae

Cited by 96 publications

References 134 publications

The complete chloroplast genome of Flemingia macrophylla (Willd.) Prain (Fabaceae) from Guangxi, China

The complete chloroplast genome of Flemingia macrophylla (Willd.) Prain (Fabaceae) from Guangxi, China

Highly Resolved Papilionoid Legume Phylogeny Based on Plastid Phylogenomics

The innovation of the symbiosome has enhanced the evolutionary stability of nitrogen fixation in legumes

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