Absence of petals, or being apetalous, is usually one of the most important features that characterizes a group of flowering plants at high taxonomic ranks (i.e., family and above). The apetalous condition, however, appears to be the result of parallel or convergent evolution with unknown genetic causes. Here we show that within the buttercup family (Ranunculaceae), apetalous genera in at least seven different lineages were all derived from petalous ancestors, indicative of parallel petal losses. We also show that independent petal losses within this family were strongly associated with decreased or eliminated expression of a single floral organ identity gene, APETALA3-3 ( AP3-3 ) , apparently owing to species-specific molecular lesions. In an apetalous mutant of Nigella , insertion of a transposable element into the second intron has led to silencing of the gene and transformation of petals into sepals. In several naturally occurring apetalous genera, such as Thalictrum , Beesia , and Enemion , the gene has either been lost altogether or disrupted by deletions in coding or regulatory regions. In Clematis , a large genus in which petalous species evolved secondarily from apetalous ones, the gene exhibits hallmarks of a pseudogene. These results suggest that, as a petal identity gene, AP3-3 has been silenced or down-regulated by different mechanisms in different evolutionary lineages. This also suggests that petal identity did not evolve many times independently across the Ranunculaceae but was lost in numerous instances. The genetic mechanisms underlying the independent petal losses, however, may be complex, with disruption of AP3-3 being either cause or effect.
Summary Elaborate petals are present in many flowering plants lineages and have greatly promoted the success and evolutionary radiation of these groups. How elaborate petals are made, however, remains largely unclear. Petals of Nigella (Ranunculaceae) have long been recognized as elaborate and can thus be an excellent model for the study of petal elaboration. Here, by conducting detailed morphological, micromorphological, anatomical, developmental and evolutionary studies on the petals of Nigella species, we explored the processes, general patterns and underlying mechanisms of petal elaboration. We found that petals of Nigella are highly complex, and the complexity can be reflected at various levels. We also found that evolutionary elaboration of the Nigella petals is a gradual process, involving not only modifications of pre‐existing structures but also de novo origination of new characters. Further investigations indicated that the elaboration and diversification of Nigella petals were accomplished by modifying the ancestral trajectory of petal development, a process known as developmental repatterning. Our results not only provide new insights into the development and evolution of elaborate petals, but also highlight the necessity of conducting multiple‐level investigations for understanding the processes, patterns and underlying mechanisms of plant evolution.
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.
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.
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In flowering plants, male gametophytes are generated in anthers from microsporocytes. However, more evidence is needed to reveal the genetic mechanisms which regulate the differentiation and interaction of these highly specialized cells in anthers. Here we report the characterization of a series of male-sterile cotton (Gossypium hirsutum) mutants, including mutants with normal fertility, semi-sterility and complete sterility. These mutants are forms of transgenic cotton containing RNAi vectors with partial cDNA fragments of GhSERK1. The GhSERK1 gene encodes a putative leucine-rich repeat receptor protein kinase (LRR-RLK), and generally has 11 domains. In previous research, we found plants containing GhSERK1 produce an abundance of male reproductive tissue. In this paper, three RNAi constructs were designed separately to analyze its function in anther. After the three RNAi vectors were transformed into the cotton, transgenic plants with the specialized fragment exhibited normal fertility or the pollen energy decreased slightly, as ones with the homologous fragments exhibited various degrees of male sterility with different expression levels of GhSERK1 mRNA. In conclusion, for the transgenic plants with conserved fragments, lower expression levels of GhSERK1 mRNA were in transgenic plants, and a higher degree of male sterility was observed. Taking together, these findings demonstrate the GhSERK1 gene has a role in the development of anthers, especially in the formation of pollen grains. Also, we infer there must be another homolog of GhSERK1 in cotton, and both of GhSERK1 and its homolog function redundantly as important control points in controlling anther pollen production.
Interactions among proteins of floral MADS-box genes in Nuphar pumila (Nymphaeaceae) and the most recent common ancestor of extant angiosperms help understand the underlying mechanisms of the origin of the flower Abstract Floral organ identity genes, most of which are MADS-box genes, play key roles in flower development and floral organ identity determination. To specify the identities of different floral organ types, proteins of the floral MADS-box genes need to form dimers and higher-level complexes before they bind to the control regions of downstream genes and regulate their expression. Previous studies have shown that understanding the evolution of the interactions among proteins of the floral MADS-box genes may be an excellent step towards uncovering the underlying mechanisms of the origin of the flower. Yet, due to the lack of such information in early-branching angiosperm lineages, it has been difficult to determine the evolutionary changes of the protein-protein interactions (PPIs) before and after the origin of the flower. In this study, we first isolated counterparts of the floral MADS-box genes from Nuphar pumila (Timm) D.C., a representative of the basalmost angiosperms Nymphaeales, and investigated the interactions among their proteins by carrying out yeast two-hybrid assays. We then estimated the PPIs in the most recent common ancestor of extant angiosperms by using two different methods: ancestral character state reconstruction and ancestral sequence reconstruction followed by yeast two-hybrid assay. Based on these results, we examined the evolutionary transitions of the PPIs before and after the occurrence of extant angiosperms, and discussed their contributions to the origin of the flower. We found that duplication and diversification of floral MADS-box genes, as well as non-random losses of some once-existed PPIs, have been the driving force of the origin of the flower.
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