New insights into the phylogeny of the TMBIM superfamily across the tree of life: Comparative genomics and synteny networks reveal independent evolution of the BI and LFG families in plants

Gamboa-Tuz, Samuel David; Pereira-Santana, Alejandro; Zhao, Tao; Schranz, M. Eric; Castaño, Enrique; Rodríguez-Zapata, Luis Carlos

doi:10.1016/j.ympev.2018.04.032

Cited by 21 publications

(23 citation statements)

References 78 publications

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“…We found that progeny derived from a single asexually-reproducing M. persicae clone O female stably colonizes nine divergent plant species of five families that span the Angiosperm phylogeny (27), demonstrating that M. persicae is truly polyphagous. Because genome annotation pipelines are generally focused on protein-coding genes, the majority Ya family members were not annotated in the first version of the M. persicae genome annotation (22).…”

Section: Discussionmentioning

confidence: 93%

An aphid host-responsive RNA transcript that migrates systemically in plants promotes aphid reproduction

Chen

Singh

et al. 2019

Preprint

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Aphids are sap-feeding insects that colonize a broad range of plant species and often cause feeding damage and transmit plant pathogens, including bacteria, viruses and viroids. These insects feed from the plant vascular tissue, predominantly the phloem. However, it remains largely unknown how aphids, and other sap-feeding insects, establish intimate long-term interactions with plants. To identify aphid virulence factors, we took advantage of the ability of the green peach aphid Myzus persicae to colonize divergent plant species. We found that a M. persicae clone of near-identical females establishes stable colonies on nine plant species of five representative plant eudicot and monocot families that span the angiosperm phylogeny. Members of the novel aphid Ya family are differentially expressed in aphids on the nine plant species, are co-regulated and organized as tandem repeats in aphid genomes. Interestingly, aphids translocate Ya transcripts into plants and some transcripts migrate systemically within several plant species. RNAi-mediated knock down of Ya genes reduces M. persicae fecundity and M. persicae produces more progeny on transgenic plants that heterologously produce one of the systemically migrating Ya transcripts as a long non-coding (lnc)RNA. Taken together, our work led to the discovery of a new host-responsive aphid gene family that operate as virulence factors. Transcripts of this family translocate into plants, including a lncRNA that migrates systemically and promotes aphid reproduction.Significance StatementThe green peach aphid Myzus persicae causes yield losses of a diverse range of economically important crops primarily as a vector of more than 100 different plant pathogens. We found that a single genotype of M. persicae is able to colonize nine plant species, including diverse dicots and maize, indicating that this aphid is truly polyphagous. Members of a new aphid Ya family undergoes coordinated expression changes in M. persicae depending on the plant species. The aphids translocate Ya transcripts into plants during feeding and these RNAs migrate to systemic leaves. Moreover, heterologous in planta expression of M. persicae Ya1 as a long non-coding RNA promotes aphid reproduction. Our findings indicate that cross kingdom deployment of RNA is more common than thought.

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Section: Discussionmentioning

confidence: 93%

An aphid host-responsive RNA transcript that migrates systemically in plants promotes aphid reproduction

Chen

Singh

et al. 2019

Preprint

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“…The global phylogenetic and synteny network analyses generated a robust six-group classification system for ARF genes and indicated pervasive intra-group syntenic phylogenetic relationships. To elaborate the evolutionary processes within each of the six groups, individual phylogenetic trees for angiosperm genes in each of the six groups were estimated separately and syntenic connections within each network community were mapped onto the six gene trees (Gamboa-Tuz et al , 2018). Along with the ARF geness identified from Phytozome plant genomes, the ARF genes from basal angiosperms (also ANA grade) and magnoliids were incorporated in the phylogenetic analyses, however these ARF gene sequences were derived from transcriptomes and thus did not provide syntenic information.…”

Section: Resultsmentioning

confidence: 99%

Evolution of Auxin Response Factors in plants characterized by phylogenomic synteny network analyses

Gao

Rui

Oliver

et al. 2019

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16Auxin response factors (ARFs) have long been a research focus and represent a class of key regulators of plant growth 17 and development. Previous studies focusing genes from limited number of species were unable to uncover the 18 evolutionary trajectory of this family. Here, more than 3,500 ARFs collected from plant genomes and transcriptomes 19 covering major streptophyte lineages were used to reconstruct the broad-scale family phylogeny, where the early origin 20 and diversification of ARF in charophytes was delineated. Based on the family phylogeny, we proposed a unified six-21 group classification system for angiosperm ARFs. Phylogenomic synteny network analyses revealed the deeply 22 conserved genomic syntenies within each of the six ARF groups and the interlocking syntenic relationships connecting 23 distinct groups. Recurrent duplication events, such as those that occurred in seed plant, angiosperms, core eudicots and 24 grasses contributed the expansion of ARF genes which facilitated functional diversification. Ancestral transposition 25 activities in important plant families, including crucifers, legumes and grasses, were unveiled by synteny network 26 analyses. Ancestral gene duplications along with transpositions have profound evolutionary significance which may 27 have accelerated the functional diversification process of paralogues. Our study provides insights into the evolution of 28 ARFs which will enhance our current understandings for this important transcription factor family. 29 30

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“…Mammals possess six TMBIM subtypes (TMBIM1-6) (Hu et al ., 2009; Rojas-Rivera and Hetz, 2015). Only two subtypes, GAAP (LFG4/TMBIM4) and BI-1 (TMBIM6), are conserved in plants but several plant species show an intriguing expansion of the GAAP protein family (Gubser et al ., 2007; Gamboa-Tuz et al ., 2018). The Arabidopsis, rice ( Oryza sativa ) and the basal angiosperm Amborella trichopoda genomes contain five, seven and two putative GAAP s, respectively (Figure 1).…”

Section: Resultsmentioning

confidence: 99%

Golgi anti-apoptotic proteins are evolutionarily conserved ion channels that regulate cell death in plants

Sierla

Prole

Saraiva

et al. 2019

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Programmed cell death regulates developmental and stress responses in eukaryotes. Golgi anti-apoptotic proteins (GAAPs) are evolutionarily conserved cell death regulators. Human and viral GAAPs inhibit apoptosis and modulate intracellular Ca2+fluxes, and viral GAAPs form cation-selective channels. Although most mammalian cell death regulators are not conserved at the sequence level in plants, the GAAP gene family shows expansion, with five paralogues (AtGAAP1-5) in the Arabidopsis genome. We pursued molecular and physiological characterization of AtGAAPs making use of the advanced knowledge of their human and viral counterparts. Structural modeling of AtGAAPs predicted the presence of a channel-like pore, and electrophysiological recordings from purified AtGAAP3 reconstituted into lipid bilayers confirmed that plant GAAPs can function as ion channels. AtGAAP1 and AtGAAP4 localized exclusively to the Golgi within the plant cell, while AtGAAP2, AtGAAP3 and AtGAAP5 also showed tonoplastic localization. Gene expression analysis revealed differential spatial expression and abundance of transcript forAtGAAPparalogues in Arabidopsis tissues. We demonstrate that AtGAAP1-5 inhibit Bax-induced cell death in yeast. However, overexpression of AtGAAP1 induces cell death inNicotiana benthamianaleaves and lesion mimic phenotype in Arabidopsis. We propose that AtGAAPs function as Golgi-localized ion channels that regulate cell death by affecting ionic homeostasis within the cell.HighlightArabidopsis Golgi anti-apoptotic proteins (GAAPs) share functional conservation with their human and viral counterparts in cell death regulation and ion channel activityAbbreviationsAtGAAP,Arabidopsis thalianaGAAP; BI-1, Bax inhibitor-1; CFP, cyan fluorescent protein; CMLV, camelpox virus; ER, Endoplasmic reticulum; GAAP, Golgi anti-apoptotic protein; GFP, green fluorescent protein; hGAAP, human GAAP; LFG, Lifeguard; LMM, lesion mimic mutant; PCD, programmed cell death; TMBIM, transmembrane Bax inhibitor-1 motif-containing; TMDs, transmembrane domains; vGAAP, viral GAAP; YFP, yellow fluorescent protein

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New insights into the phylogeny of the TMBIM superfamily across the tree of life: Comparative genomics and synteny networks reveal independent evolution of the BI and LFG families in plants

Cited by 21 publications

References 78 publications

An aphid host-responsive RNA transcript that migrates systemically in plants promotes aphid reproduction

An aphid host-responsive RNA transcript that migrates systemically in plants promotes aphid reproduction

Evolution of Auxin Response Factors in plants characterized by phylogenomic synteny network analyses

Golgi anti-apoptotic proteins are evolutionarily conserved ion channels that regulate cell death in plants

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