MawuAP1 promotes flowering and fruit development in the basal angiosperm Magnolia wufengensis (Magnoliaceae)

The APETALA1/SQUAMOSA (AP1/SQUA)-like genes of flowering plants play crucial roles in the development processes of floral meristems, sepals, petals and fruits. Although many of the AP1/SQUA-like genes have been characterized in angiosperms, few have been identified in basal angiosperm taxa. Therefore, the functional evolution of the AP1/SQUA subfamily is still unclear. We characterized an AP1 homolog, MawuAP1, from Magnolia wufengensis that is an ornamental woody plant belonging to the basal angiosperms. Gene sequence and phylogenetic analyses suggested that MawuAP1 was clustered with the FUL-like homologous genes of basal angiosperms and had FUL motif and paleoAP1 motif domain, but it did not have the euAP1 motif domain of core eudicots. Expression pattern analysis showed that MawuAP1 was highly expressed in vegetative and floral organs, particularly in the early stage of flower bud development and pre-anthesis. Protein–protein interaction pattern analysis revealed that MawuAP1 has interaction with an A-class gene (MawuAP1), C-class gene (MawuAG-1) and E-class gene (MawuAGL9) of the MADS-box family genes. Ectopic expression in Arabidopsis thaliana indicated that MawuAP1 could significantly promote flowering and fruit development, but it could not restore the sepal and petal formation of ap1 mutants. These results demonstrated that there are functional differences in the specification of sepal and petal floral organs and development of fruits among the AP1/SQUA-like genes, and functional conservation in the regulation of floral meristem. These findings provide strong evidence for the important functions of MawuAP1 in floral meristem determination, promoting flowering and fruit development, and further highlight the importance of AP1/SQUA subfamily in biological evolution and diversity.

Retracing the contours of the early angiosperm environmental niche

Background and Aims Our aim was to understand the environmental conditions of the emergence and radiation of early angiosperms. Such a question has long remained controversial because various approaches applied in the past have drawn conflicting images of early angiosperm ecology. Methods We provided a new perspective on the question by using support vector machines to model the environmental niche of 51 species belonging to ten genera of extant lineages that diverged early during angiosperm evolution (basal angiosperms). Then, we analysed the resulting pattern of niche overlap and determined whether this pattern deviates from what would be expected on the basis of a null model or whether it might mirror a legacy of a common primitive niche based on a phylogenetic reconstruction. Key Results The niche of three-quarters of the species and all genera converged towards tropical montane cloud forests (TMCFs). The latitudinal pattern of basal angiosperm richness indeed culminated in the tropics, and the elevational pattern revealed a humpback curve peaking between 2000 m and 3500 m when accounting for the effect of area. At first glance, this diversity pattern does not significantly differ from null predictions. However, we revealed a tendency for the basal-most taxa to occur in TMCFs so that phylogenetic reconstructions indicated that the niche of the common ancestor of the sampled basal angiosperms had a probability of 0.85–0.93 to overlap with TMCFs. Conclusions Our new approach indicates that the environmental convergence of extant basal angiosperms towards TMCFs would reflect a legacy of an ancestral niche from which the least basal taxa would have diverged following a random pattern under geometric constraints.

Characterization of Two AGL6–Like Genes from a Chinese Endemic Woody Tree, Manglietia patungensis (Magnoliaceae) Provides Insight into Perianth Development and Evolution in Basal Angiosperms

Manglietia patungensis (Magnoliaceae) exhibits radially symmetric flowers with perianth consisting of three separate sepaloid tepals in whorl 1 and six petaloid tepals in the inner two whorls, which shows an obvious difference from flowers of most Magnoliaceae species that contain three uniform petaloid tepals whorls, and make it an excellent model for understanding perianth morphology differentiation during early flower evolution. Here, two AGL6 orthologs, MapaAGL6-1 and MapaAGL6-2, were isolated from M. patungensis. Sequence alignment and phylogenetic analyses grouped both genes into the AGL6 lineage. MapaAGL6-1 is expressed only in the perianth whorls, while MapaAGL6-2 is strongly expressed in the perianth whorls but is lowly expressed in gynoecium. Furthermore, ectopic expression of MapaAGL6-1 results in strong complementation phenotypes in the Arabidopsis ap1-10 flower and production of normal floral organs in four floral whorls only with the petal number reduced in whorl 2, while ectopic expression of MapaAGL6-2 only results in petals partly rescued but failing to terminate carpelloid development in Arabidopsis ap1-10 mutant. In addition, the daughter lines generated from a cross between 35S::MapaAGL6-1 transgenic plants showing strong phenotypes and 35S::MapaAGL6-2 transgenic plants showing phenotypic changes produce normal flowers. Our results suggest that MapaAGL6-1 is a reasonable A-function gene controlling perianth identity in Magnoliaceae, which infers from its expression region and complementation phenotypes in Arabidopsis ap1 mutant, while MapaAGL6-2 is mainly involved in petaloid tepal development. Our data also provide a new clue to uncover the perianth development and early evolution in basal angiosperms.

The soursop genome and comparative genomics of basal angiosperms provide new insights on evolutionary incongruence

Deep relationships and the sequence of divergence among major lineages of angiosperms (magnoliids, monocots and eudicots) remain ambiguous and differ depending on analytical approaches and datasets used. Complete genomes potentially provide opportunities to resolve these uncertainties, but two recently published magnoliid genomes instead deliver further conflicting signals. To disentangle key angiosperm relationships, we report a high-quality draft genome for the soursop (Annona muricata, Annonaceae). We reconstructed phylogenomic trees and show that the soursop represents a genomic mosaic supporting different histories, with scaffolds almost exclusively supporting single topologies. However, coalescent methods and a majority of genes support magnoliids as sister to monocots and eudicots, where previous whole genome-based studies remained inconclusive. This result is clear and consistent with recent studies using plastomes. The soursop genome highlights the need for more early diverging angiosperm genomes and critical assessment of the suitability of such genomes for inferring evolutionary history.

The largest early-diverging angiosperm family is mostly pollinated by ovipositing insects and so are most surviving lineages of early angiosperms

Insect pollination in basal angiosperms is assumed to mostly involve ‘generalized' insects looking for food, but direct observations of ANITA grade (283 species) pollinators are sparse. We present new data for numerous Schisandraceae, the largest ANITA family, from fieldwork, nocturnal filming, electron microscopy, barcoding and molecular clocks to infer pollinator/plant interactions over multiple years at sites throughout China to test the extent of pollinator specificity. Schisandraceae are pollinated by nocturnal gall midges that lay eggs in the flowers and whose larvae then feed on floral exudates. At least three Schisandraceae have shifted to beetle pollination. Pollination by a single midge species predominates, but one species was pollinated by different species at three locations and one by two at the same location. Based on molecular clocks, gall midges and Schisandraceae may have interacted since at least the Early Miocene. Combining these findings with a review of all published ANITA pollination data shows that ovipositing flies are the most common pollinators of living representatives of the ANITA grade. Compared to food reward-based pollination, oviposition-based systems are less wasteful of plant gametes because (i) none are eaten and (ii) female insects with herbivorous larvae reliably visit conspecific flowers.

Leaf energy balance modelling as a tool to infer habitat preference in the early angiosperms

Despite more than a century of research, some key aspects of habitat preference and ecology of the earliest angiosperms remain poorly constrained. Proposed growth ecology has varied from opportunistic weedy species growing in full sun to slow-growing species limited to the shaded understorey of gymnosperm forests. Evidence suggests that the earliest angiosperms possessed low transpiration rates: gas exchange rates for extant basal angiosperms are low, as are the reconstructed gas exchange rates for the oldest known angiosperm leaf fossils. Leaves with low transpirational capacity are vulnerable to overheating in full sun, favouring the hypothesis that early angiosperms were limited to the shaded understorey. Here, modelled leaf temperatures are used to examine the thermal tolerance of some of the earliest angiosperms. Our results indicate that small leaf size could have mitigated the low transpirational cooling capacity of many early angiosperms, enabling many species to survive in full sun. We propose that during the earliest phases of the angiosperm leaf record, angiosperms may not have been limited to the understorey, and that some species were able to compete with ferns and gymnosperms in both shaded and sunny habitats, especially in the absence of competition from more rapidly growing and transpiring advanced lineages of angiosperms.