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A comprehensive analysis of relative gene order, or microsynteny, can provide valuable information for understanding the evolutionary history of genes and genomes, and ultimately traits and species, across broad phylogenetic groups and divergence times. We have used our network-based phylogenomic synteny analysis pipeline to first analyze the overall patterns and major differences between 87 mammalian and 107 angiosperm genomes. These two important groups have both evolved and radiated over the last ∼170 MYR. Secondly, we identified the genomic outliers or “rebel genes” within each clade. We theorize that rebel genes potentially have influenced trait and lineage evolution. Microsynteny networks use genes as nodes and syntenic relationships between genes as edges. Networks were decomposed into clusters using the Infomap algorithm, followed by phylogenomic copy-number profiling of each cluster. The differences in syntenic properties of all annotated gene families, including BUSCO genes, between the two clades are striking: most genes are single copy and syntenic across mammalian genomes, whereas most genes are multicopy and/or have lineage-specific distributions for angiosperms. We propose microsynteny scores as an alternative and complementary metric to BUSCO for assessing genome assemblies. We further found that the rebel genes are different between the two groups: lineage-specific gene transpositions are unusual in mammals, whereas single-copy highly syntenic genes are rare for flowering plants. We illustrate several examples of mammalian transpositions, such as brain-development genes in primates, and syntenic conservation across angiosperms, such as single-copy genes related to photosynthesis. Future experimental work can test if these are indeed rebels with a cause.

Terpenes and terpenoids are key natural compounds for plant defense, development, and composition of plant oil. The synthesis and accumulation of a myriad of volatile terpenoid compounds in these plants may dramatically alter the quality and flavor of the oils, which provide great commercial utilization value for oil-producing plants. Terpene synthases ( TPSs ) are important enzymes responsible for terpenic diversity. Investigating the differentiation of the TPS gene family could provide valuable theoretical support for the genetic improvement of oil-producing plants. While the origin and function of TPS genes have been extensively studied, the exact origin of the initial gene fusion event - it occurred in plants or microbes - remains uncertain. Furthermore, a comprehensive exploration of the TPS gene differentiation is still pending. Here, phylogenetic analysis revealed that the fusion of the TPS gene likely occurred in the ancestor of land plants, following the acquisition of individual C- and N- terminal domains. Potential mutual transfer of TPS genes was observed among microbes and plants. Gene synteny analysis disclosed a differential divergence pattern between TPS-c and TPS-e/f subfamilies involved in primary metabolism and those (TPS-a/b/d/g/h subfamilies) crucial for secondary metabolites. Biosynthetic gene clusters (BGCs) analysis suggested a correlation between lineage divergence and potential natural selection in structuring terpene diversities. This study provides fresh perspectives on the origin and evolution of the TPS gene family.

Background In the evolutionary study of gene families, exploring the duplication mechanisms of gene families helps researchers understand their evolutionary history. The tubby-like protein (TLP) family is essential for growth and development in plants and animals. Much research has been done on its function; however, limited information is available with regard to the evolution of the TLP gene family. Herein, we systematically investigated the evolution of TLP genes in seven representative Poaceae lineages. Results Our research showed that the evolution of TLP genes was influenced not only by whole-genome duplication (WGD) and dispersed duplication (DSD) but also by transposed duplication (TRD), which has been neglected in previous research. For TLP family size, we found an evolutionary pattern of progressive shrinking in the grass family. Furthermore, the evolution of the TLP gene family was at least affected by evolutionary driving forces such as duplication, purifying selection, and base mutations. Conclusions This study presents the first comprehensive evolutionary analysis of the TLP gene family in grasses. We demonstrated that the TLP gene family is also influenced by a transposed duplication mechanism. Several new insights into the evolution of the TLP gene family are presented. This work provides a good reference for studying gene evolution and the origin of duplication.

Multidrug and toxic compound extrusion (MATE) transporters comprise a multigene family that mediates multiple functions in plants through the efflux of diverse substrates including organic molecules, specialized metabolites, hormones, and xenobiotics. MATE classification based on genome-wide studies remains ambiguous, likely due to a lack of large-scale phylogenomic studies and/or reference sequence datasets. To resolve this, we established a phylogeny of the plant MATE gene family using a comprehensive kingdom-wide phylogenomic analysis of 74 diverse plant species. We identified more than 4,000 MATEs, which were classified into 14 subgroups based on a systematic bioinformatics pipeline using USEARCH, blast+ and synteny network tools. Our classification was performed using a four-step process, whereby MATEs sharing ≥ 60% protein sequence identity with a ≤ 1E-05 threshold at different sequence lengths (either full-length, ≥ 60% length, or ≥ 150 amino acids) or retaining in the similar synteny blocks were assigned to the same subgroup. In this way, we assigned subgroups to 95.8% of the identified MATEs, which we substantiated using synteny network clustering analysis. The subgroups were clustered under four major phylogenetic groups and named according to their clockwise appearance within each group. We then generated a reference sequence dataset, the usefulness of which was demonstrated in the classification of MATEs in additional species not included in the original analysis. Approximately 74% of the plant MATEs exhibited synteny relationships with angiosperm-wide or lineage-, order/family-, and species-specific conservation. Most subgroups evolved independently, and their distinct evolutionary trends were likely associated with the development of functional novelties or the maintenance of conserved functions. Together with the systematic classification and synteny network profiling analyses, we identified all the major evolutionary events experienced by the MATE gene family in plants. We believe that our findings and the reference dataset provide a valuable resource to guide future functional studies aiming to explore the key roles of MATEs in different aspects of plant physiology. Our classification framework can also be readily extendable to other (super) families.

AP2/ERF transcription factor family plays an important role in plant development and stress responses. Previous studies have shed light on the evolutionary trajectory of the AP2 and DREB subfamilies. However, knowledge about the evolutionary history of the ERF subfamily in angiosperms still remains limited. In this study, we performed a comprehensive analysis of the ERF subfamily from 107 representative angiosperm species by combining phylogenomic and synteny network approaches. We observed that the expansion of the ERF subfamily was driven not only by whole-genome duplication (WGD) but also by tandem duplication (TD) and transposition duplication events. We also found multiple transposition events in Poaceae, Brassicaceae, Poales, Brassicales, and Commelinids. These events may have had notable impacts on copy number variation and subsequent functional divergence of the ERF subfamily. Moreover, we observed a number of ancient tandem duplications occurred in the ERF subfamily across angiosperms, e.g., in Subgroup IX, IXb originated from ancient tandem duplication events within IXa. These findings together provide novel insights into the evolution of this important transcription factor family.

Rosa chinensis, an important ancestor species of Rosa hybrida, the most popular ornamental plant species worldwide, produces flowers with diverse colors and fragrances. The R2R3-MYB transcription factor family controls a wide variety of plant-specific metabolic processes, especially phenylpropanoid metabolism. Despite their importance for the ornamental value of flowers, the evolution of R2R3-MYB genes in plants has not been comprehensively characterized. In this study, 121 predicted R2R3-MYB gene sequences were identified in the rose genome. Additionally, a phylogenomic synteny network (synnet) was applied for the R2R3-MYB gene families in 35 complete plant genomes. We also analyzed the R2R3-MYB genes regarding their genomic locations, Ka/Ks ratio, encoded conserved motifs, and spatiotemporal expression. Our results indicated that R2R3-MYBs have multiple synteny clusters. The RcMYB114a gene was included in the Rosaceae-specific Cluster 54, with independent evolutionary patterns. On the basis of these results and an analysis of RcMYB114a-overexpressing tobacco leaf samples, we predicted that RcMYB114a functions in the phenylpropanoid pathway. We clarified the relationship between R2R3-MYB gene evolution and function from a new perspective. Our study data may be relevant for elucidating the regulation of floral metabolism in roses at the transcript level.

This study performed a phylogenomic analysis of the C2H2 gene family across 30 Basidiomycota species, identifying 1032 genes distributed across six evolutionary clades (Groups I–VI). Functional diversification and lineage-specific expansions were observed: Group II (37.1%) formed a conserved core, while wood decayers (e.g., Schizophyllum commune) and edible fungi (e.g., Pleurotus ostreatus) exhibited clade-specific expansions in Groups III and V, respectively. Physicochemical profiling revealed an acidic bias in Agaricomycotina proteins (pI 4.3–5.8) compared to alkaline trends in pathogens (Ustilaginomycotina/Pucciniomycotina; pI 8.3–8.6). Comparative genomics indicated that saprotrophs retained long genes (12.4 kb) with abundant introns (mean = 6.2/gene), whereas pathogens exhibited genomic streamlining (introns ≤ 2). Synteny network analysis revealed high ancestral conservation in core clusters (Cluster_1–2: 58% homologs) under strong purifying selection (Ka/Ks = 0.18–0.22), while peripheral clusters (Cluster_Mini) approached neutral evolution (Ka/Ks = 0.73). This study reveals stage-specific expression dynamics of 17 C2H2 zinc finger genes in Sarcomyxa edulis, highlighting their roles in coordinating developmental transitions (e.g., SeC2H2_1 in low-temperature adaptation, SeC2H2_7/12 in primordia initiation, and SeC2H2_8/9/13 in fruiting body maturation) through temporally partitioned regulatory programs, providing insights into fungal morphogenesis and stress-responsive adaptation. These findings underscore the dual role of C2H2 genes in sustaining conserved regulatory networks and facilitating ecological adaptation, providing new insights into fungal genome evolution.

PipX is a unique cyanobacterial protein identified by its ability to bind to PII and NtcA, two key regulators involved in the integration of signals of the nitrogen/carbon and energy status, with a tremendous impact on nitrogen assimilation and gene expression in cyanobacteria. PipX provides a mechanistic link between PII, the most widely distributed signaling protein, and NtcA, a global transcriptional regulator of cyanobacteria. PII, required for cell survival unless PipX is inactivated or down-regulated, functions by protein–protein interactions with transcriptional regulators, transporters, and enzymes. In addition, PipX appears to be involved in a wider signaling network, supported by the following observations: (i) PII–PipX complexes interact with PlmA, an as yet poorly characterized transcriptional regulator also restricted to cyanobacteria; (ii) the pipX gene is functionally connected with pipY, a gene encoding a universally conserved pyridoxal phosphate binding protein (PLPBP) involved in vitamin B6 and amino acid homeostasis, whose loss-of-function mutations cause B6-dependent epilepsy in humans, and (iii) pipX is part of a relatively robust, six-node synteny network that includes pipY and four additional genes that might also be functionally connected with pipX. In this overview, we propose that the study of the protein–protein interaction and synteny networks involving PipX would contribute to understanding the peculiarities and idiosyncrasy of signaling pathways that are conserved in cyanobacteria.

Terpenes are pivotal for plant growth, development, and adaptation to environmental stresses. With the advent of extensive genomic data and sophisticated bioinformatics tools, new insights into the evolutionary dynamics and functional diversification of terpene synthases (TPSs) have emerged. Despite genome-wide identifications of the TPS family in certain species, comprehensive cross-species analyses remain scarce. In this study, we conducted a genome-wide identification and subgroup classification of TPS families across 115 angiosperms with available genomic sequences. Our phylogenomic synteny network analysis elucidated the complex evolutionary history of TPS genes, revealing notable expansions and contractions among subgroups. Specifically, TPS-a showed significant expansion, while TPS-b was variably lost in some Poaceae, indicating adaptive responses. TPS-c maintained considerable conservation across species, whereas TPS-e/f diverged into distinct evolutionary trajectories despite functional overlap, with TPS-e further splitting into two angiosperm-specific clades. The TPS-g subgroup displayed lineage-restricted distribution, primarily in super-rosids and monocots. Notably, TPS-d and TPS-h subgroups were absent in angiosperms. Employing Rosa chinensis as a case study, we identified RcTPS23, a conserved bifunctional terpene synthase, highlighting the utility of cross-species synteny data in functional prediction. This comprehensive analysis elucidates the phylogenetic and functional landscape of TPS subgroups in angiosperms, providing a robust framework for predicting TPS function and guiding further functional investigations.

Gene tree discordance in large genomic data sets can be caused by evolutionary processes such as incomplete lineage sorting and hybridization, as well as model violation, and errors in data processing, orthology inference, and gene tree estimation. Species tree methods that identify and accommodate all sources of conflict are not available, but a combination of multiple approaches can help tease apart alternative sources of conflict. Here, using a phylotranscriptomic analysis in combination with reference genomes, we test a hypothesis of ancient hybridization events within the plant family Amaranthaceae s.l. thatwas previously supported bymorphological, ecological, and Sanger-based molecular data. The data set included seven genomes and 88 transcriptomes, 17 generated for this study. We examined gene-tree discordance using coalescent-based species trees and network inference, gene tree discordance analyses, site pattern tests of introgression, topology tests, synteny analyses, and simulations. We found that a combination of processes might have generated the high levels of gene tree discordance in the backbone of Amaranthaceae s.l. Furthermore, we found evidence that three consecutive short internal branches produce anomalous trees contributing to the discordance. Overall, our results suggest that Amaranthaceae s.l. might be a product of an ancient and rapid lineage diversification, and remains, and probably will remain, unresolved. This work highlights the potential problems of identifiability associated with the sources of gene tree discordance including, in particular, phylogenetic network methods. Our results also demonstrate the importance of thoroughly testing for multiple sources of conflict in phylogenomic analyses, especially in the context of ancient, rapid radiations. We provide several recommendations for exploring conflicting signals in such situations.