Conserved genomic context provides critical information for comparative evolutionary analysis. With the increase in numbers of sequenced plant genomes, synteny analysis can provide new insights into gene family evolution. Here, we exploit a network analysis approach to organize and interpret massive pairwise syntenic relationships. Specifically, we analyzed synteny networks of the MADS-box transcription factor gene family using 51 completed plant genomes. In combination with phylogenetic profiling, several novel evolutionary patterns were inferred and visualized from synteny network clusters. We found lineage-specific clusters that derive from transposition events for the regulators of floral development (APETALA3 and PI) and flowering time (FLC) in the Brassicales and for the regulators of root development (AGL17) in Poales. We also identified two large gene clusters that jointly encompass many key phenotypic regulatory Type II MADS-box gene clades (SEP1, SQUA, TM8, SEP3, FLC, AGL6, and TM3). Gene clustering and gene trees support the idea that these genes are derived from an ancient tandem gene duplication that likely predates the radiation of the seed plants and then expanded by subsequent polyploidy events. We also identified angiosperm-wide conservation of synteny of several other less studied clades. Combined, these findings provide new hypotheses for the genomic origins, biological conservation, and divergence of MADS-box gene family members.

/pdf/phylogenomic-synteny-network-analysis-of-mads-box-24flg4w8jy.pdf

Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation.

Classification and Phylogeny

The origin of flowers has puzzled plant biologists ever since Darwin referred to their sudden appearance in the fossil record as an abominable mystery. Flowers are considered to be an assembly of protective, attractive, and reproductive male and female leaf-like organs. Their origin cannot be understood by a morphological comparison to gymnosperms, their closest relatives, which develop separate male or female cones. Despite these morphological differences, gymnosperms and angiosperms possess a similar genetic toolbox consisting of phylogenetically related MADS domain proteins. Using ancestral MADS domain protein reconstruction, we trace the evolution of organ identity quartets along the stem lineage of crown angiosperms. We provide evidence that current floral quartets specifying male organ identity, which consist of four types of subunits, evolved from ancestral complexes of two types of subunits through gene duplication and integration of SEPALLATA proteins just before the origin of flowering plants. Our results suggest that protein interaction changes underlying this compositional shift were the result of a gradual and reversible evolutionary trajectory. Modeling shows that such compositional changes may have facilitated the evolution of the perfect, bisexual flower.

/pdf/the-origin-of-floral-organ-identity-quartets-1a70ec7fiv.pdf

The Origin of Floral Organ Identity Quartets

Members of SEPALLATA (SEP) and APETALA1 (AP1)/SQUAMOSA (SQUA) MADS-box transcription factor subfamilies play key roles in floral organ identity determination and floral meristem determinacy in the rosid species Arabidopsis (Arabidopsis thaliana). Here, we present a functional characterization of the seven SEP/AGL6 and four AP1/SQUA genes in the distant asterid species petunia (Petunia × hybrida). Based on the analysis of single and higher order mutants, we report that the petunia SEP1/SEP2/SEP3 orthologs together with AGL6 encode classical SEP floral organ identity and floral termination functions, with a master role for the petunia SEP3 ortholog FLORAL BINDING PROTEIN2 (FBP2). By contrast, the FBP9 subclade members FBP9 and FBP23, for which no clear ortholog is present in Arabidopsis, play a major role in determining floral meristem identity together with FBP4, while contributing only moderately to floral organ identity. In turn, the four members of the petunia AP1/SQUA subfamily redundantly are required for inflorescence meristem identity and act as B-function repressors in the first floral whorl, together with BEN/ROB genes. Overall, these data together with studies in other species suggest major differences in the functional diversification of the SEP/AGL6 and AP1/SQUA MADS-box subfamilies during angiosperm evolution.

https://hal.archives-ouvertes.fr/hal-02349131/document

Divergent Functional Diversification Patterns in the SEP/AGL6/AP1 MADS-Box Transcription Factor Superclade.

无性器官的亚科的基因被显示了在繁殖机关身份决心，水果，和种子开发起关键作用。他们深深地在 eudicot 种类并且特别在 Arabidopsis 被学习了。最近，米饭的无性器官的亚科在花开发为他们的角色被学习了，庞大的数据被产生了。在这评论，我们提供这些数据的概述并且讨论在米饭和 Arabidopsis 之间的基因函数的保存。

The Ins and Outs of the Rice AGAMOUS Subfamily

Petals can be simple or elaborate, depending on whether they have lobes, teeth, fringes, or appendages along their margins, or possess spurs, scales, or other types of modifications on their adaxial/abaxial side, or both. Elaborate petals have been recorded in 23 orders of angiosperms and are generally believed to have played key roles in the adaptive evolution of corresponding lineages. The mechanisms underlying the formation of elaborate petals, however, are largely unclear. Here, by performing extensive transcriptomic and functional studies on Nigella damascena (Ranunculaceae), we explore the mechanisms underlying elaborate petal development and specialized character formation. In addition to the identification of genes and programs that are specifically/preferentially expressed in petals, we found genes and programs that are required for elaborate rather than simple petal development. By correlating the changes in gene expression with those in petal development, we identified 30 genes that are responsible for the marginal/ventral elaboration of petals and the initiation of several highly specialized morphological characters (e.g., pseudonectaries, long hairs, and short trichomes). Expression and functional analyses further confirmed that a class I homeodomain-leucine zipper family transcription factor gene, Nigella damascena LATE MERISTEM IDENTITY1 (NidaLMI1), plays important roles in the development of short trichomes and bifurcation of the lower lip. Our results not only provide the first portrait of elaborate petal development but also pave the way to understanding the mechanisms underlying lateral organ diversification in plants.

Identification of the Key Regulatory Genes Involved in Elaborate Petal Development and Specialized Character Formation in Nigella damascena (Ranunculaceae)

AP1/FUL, SEP, AGL6, and FLC subfamily genes play important roles in flower development. The phylogenetic relationships among them, however, have been controversial, which impedes our understanding of the origin and functional divergence of these genes. One possible reason for the controversy may be the problems caused by changes in the exon-intron structure of genes, which, according to recent studies, may generate non-homologous sites and hamper the homology-based sequence alignment. In this study, we first performed exon-by-exon alignments of these and three outgroup subfamilies (SOC1, AG, and STK). Phylogenetic trees reconstructed based on these matrices show improved resolution and better congruence with species phylogeny. In the context of these phylogenies, we traced evolutionary changes of exon-intron structures in each subfamily. We found that structural changes have occurred frequently following gene duplication and speciation events. Notably, exons 7 and 8 (if present) suffered more structural changes than others. With the knowledge of exon-intron structural changes, we generated more reasonable alignments containing all the focal subfamilies. The resulting trees showed that the SEP subfamily is sister to the monophyletic group formed by AP1/FUL and FLC subfamily genes and that the AGL6 subfamily forms a sister group to the three abovementioned subfamilies. Based on this topology, we inferred the evolutionary history of exon-intron structural changes among different subfamilies. Particularly, we found that the eighth exon originated before the divergence of AP1/FUL, FLC, SEP, and AGL6 subfamilies and degenerated in the ancestral FLC-like gene. These results provide new insights into the origin and evolution of the AP1/FUL, FLC, SEP, and AGL6 subfamilies.

/pdf/prevalent-exon-intron-structural-changes-in-the-apetala1-1pl31dqy8i.pdf

Prevalent Exon-Intron Structural Changes in the APETALA1/FRUITFULL, SEPALLATA, AGAMOUS-LIKE6, and FLOWERING LOCUS C MADS-Box Gene Subfamilies Provide New Insights into Their Evolution.

Pseudonectaries, or false nectaries, the glistening structures that resemble nectaries or nectar droplets but do not secrete nectar, show considerable diversity and play important roles in plant-animal interactions. The morphological nature, optical features, molecular underpinnings and ecological functions of pseudonectaries, however, remain largely unclear. Here, we show that pseudonectaries of Nigella damascena (Ranunculaceae) are tiny, regional protrusions covered by tightly arranged, non-secretory polygonal epidermal cells with flat, smooth and reflective surface, and are clearly visible even under ultraviolet light and bee vision. We also show that genes associated with cell division, chloroplast development and wax formation are preferably expressed in pseudonectaries. Specifically, NidaYABBY5, an abaxial gene with ectopic expression in pseudonectaries, is indispensable for pseudonectary development: knockdown of it led to complete losses of pseudonectaries. Notably, when flowers without pseudonectaries were arrayed beside those with pseudonectaries, clear differences were observed in the visiting frequency, probing time and visiting behavior of pollinators (i.e., honey bees), suggesting that pseudonectaries serve as both visual attractants and nectar guides.

/pdf/the-morphology-molecular-development-and-ecological-function-2h4cqh9s66.pdf

The morphology, molecular development and ecological function of pseudonectaries on Nigella damascena (Ranunculaceae) petals

Petals can be simple or elaborate, depending on whether they have complex basic structures and/or highly specialized epidermal modifications. It has been proposed that the independent origin and diversification of elaborate petals have promoted plant-animal interactions and, therefore, the evolutionary radiation of corresponding plant groups. Recent advances in floral development and evolution have greatly improved our understanding of the processes, patterns and mechanisms underlying petal elaboration. In this review, we compare the developmental processes of simple and elaborate petals, concluding that elaborate petals can be achieved through four main ways of modifications (i.e., marginal elaboration, ventral elaboration, dorsal elaboration and surface elaboration). Meanwhile, although different types of elaborate petals were made through different ways of modifications, they are all results of changes in the expression patterns of genes involved in organ polarity establishment and/or the proliferation, expansion and differentiation of cells. Deployment of existing genetic materials to a new function was also shown to be a key to the making of elaborate petals during evolution.

Petal development and elaboration.

Complex color patterns on petals are widespread in flowering plants, yet the mechanisms underlying their formation remain largely unclear. Here, by conducting detailed morphological, anatomical, biochemical, optical, transcriptomic, and functional studies, we investigated the cellular bases, chromogenic substances, reflectance spectra, developmental processes, and underlying mechanisms of complex color pattern formation on Nigella orientalis petals. We found that the complexity of the N. orientalis petals in color pattern is reflected at multiple levels, with the amount and arrangement of different pigmented cells being the key. We also found that biosynthesis of the chromogenic substances of different colors is sequential, so that one color/pattern is superimposed on another. Expression and functional studies further revealed that a pair of R2R3-MYB genes function cooperatively to specify the formation of the eyebrow-like horizontal stripe and the Mohawk haircut-like splatters. Specifically, while NiorMYB113-1 functions to draw a large splatter region, NiorMYB113-2 functions to suppress the production of anthocyanins from the region where a gap will form, thereby forming the highly specialized pattern. Our results provide a detailed portrait for the spatiotemporal dynamics of the coloration of N. orientalis petals and help better understand the mechanisms underlying complex color pattern formation in plants.

Xuehao Fu

Papers

Identification of the Key Regulatory Genes Involved in Elaborate Petal Development and Specialized Character Formation in Nigella damascena (Ranunculaceae)

Prevalent Exon-Intron Structural Changes in the APETALA1/FRUITFULL, SEPALLATA, AGAMOUS-LIKE6, and FLOWERING LOCUS C MADS-Box Gene Subfamilies Provide New Insights into Their Evolution.

The morphology, molecular development and ecological function of pseudonectaries on Nigella damascena (Ranunculaceae) petals

Petal development and elaboration.

Mechanisms underlying the formation of complex color patterns on Nigella orientalis (Ranunculaceae) petals.