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Life has always found a way to preserve itself. One strategy that has been developed for this purpose is sexual reproduction. In land plants, the gynoecium is considered to be at the top of evolutionary innovation, since it has been a key factor in the success of the angiosperms. The gynoecium is composed of carpels with different tissues that need to develop and differentiate in the correct way. In order to control and guide gynoecium development, plants have adapted elements of pre-existing gene regulatory networks (GRNs) but new ones have also evolved. The GRNs can interact with internal factors (e.g. hormones and other metabolites) and external factors (e.g. mechanical signals and temperature) at different levels, giving robustness and flexibility to gynoecium development. Here, we review recent findings regarding the role of cytokinin–auxin crosstalk and the genes that connect these hormonal pathways during early gynoecium development. We also discuss some examples of internal and external factors that can modify GRNs. Finally, we make a journey through the flowering plant lineage to determine how conserved are these GRNs that regulate gynoecium and fruit development.

Recent advances in molecular phylogenetics and a series of important palaeobotanical discoveries have revolutionized our understanding of angiosperm diversification. Yet, the origin and early evolution of their most characteristic feature, the flower, remains poorly understood. In particular, the structure of the ancestral flower of all living angiosperms is still uncertain. Here we report model-based reconstructions for ancestral flowers at the deepest nodes in the phylogeny of angiosperms, using the largest data set of floral traits ever assembled. We reconstruct the ancestral angiosperm flower as bisexual and radially symmetric, with more than two whorls of three separate perianth organs each (undifferentiated tepals), more than two whorls of three separate stamens each, and more than five spirally arranged separate carpels. Although uncertainty remains for some of the characters, our reconstruction allows us to propose a new plausible scenario for the early diversification of flowers, leading to new testable hypotheses for future research on angiosperms. The fossil record of flowers is limited, necessitating other approaches to understanding floral evolution. Here, Sauquet and colleagues reconstruct the characteristics and diversification of ancient angiosperm flowers by combining models of flower evolution with an extensive database of extant floral traits.

One of the crucial steps in the life cycle of angiosperms is the development of carpels. They are the most complex plant organs, harbor the seeds, and, after fertilization, develop into fruits and are thus an important ecological and economic trait. CRABS CLAW (CRC), a YABBY protein and putative transcription factor, is one of the major carpel developmental regulators in that includes a C2C2 zinc finger and a domain with similarities to an HMG box. CRC is involved in the regulation of processes such as carpel fusion and growth, floral meristem termination, and nectary formation. While its genetic interactions with other carpel development regulators are well described, its biochemical properties and molecular way of action remain unclear. We combined Bimolecular Fluorescence Complementation, Yeast Two-Hybrid, and Yeast One-Hybrid analyzes to shed light on the molecular biology of CRC. Our results showed that CRC dimerizes, also with other YABBY proteins, via the YABBY domain, and that its DNA binding is mainly cooperative and is mediated by the YABBY domain. Further, we identified that CRC is involved in floral meristem termination via transcriptional repression while it acts as a transcriptional activator in nectary development and carpel fusion and growth control. This work increases our understanding on how YABBY transcription factors interact with other proteins and how they regulate their targets.

Flowers are reproductive organs and precursors to fruits and seeds. While the basic tenets of the ABCE model of flower development are conserved in angiosperms, different flowering plants exhibit different and sometimes unique characteristics. A distinct feature of strawberry (Fragaria spp.) flowers is the development of several hundreds of individual apocarpous (unfused) carpels. These individual carpels are arranged in a spiral pattern on the subtending stem tip, the receptacle. Therefore, the receptacle is an integral part of the strawberry flower and is of significant agronomic importance, being the precursor to strawberry fruit. Taking advantage of next-generation sequencing and laser capture microdissection, we generated different tissue-and stage-transcriptomic profiling of woodland strawberry (Fragaria vesca) flower development. Using pairwise comparisons and weighted gene coexpression network analysis, we identified modules of coexpressed genes and hub genes of tissue-specific networks. Of particular importance is the discovery of a developing receptacle-specific module exhibiting similar molecular features to those of young floral meristems. The strawberry homologs of a number of meristem regulators, including LOST MERISTEM and WUSCHEL, are identified as hub genes operating in the developing receptacle network. Furthermore, almost 25% of the F-box genes in the genome are transiently induced in developing anthers at the meiosis stage, indicating active protein degradation. Together, this work provides important insights into the molecular networks underlying strawberry's unique reproductive developmental processes. This extensive floral transcriptome data set is publicly available and can be readily queried at the project Web site, serving as an important genomic resource for the plant biology research community.

The molecular and genetic networks underlying the determination of floral organ identity are well studied, but much less is known about how the flower is partitioned into four developmentally distinct whorls. The SUPERMAN gene is required for proper specification of the boundary between stamens in whorl 3 and carpels in whorl 4, as superman mutants exhibit supernumerary stamens but usually lack carpels. However, it has remained unclear whether extra stamens in superman mutants originate from an organ identity change in whorl 4 or the overproliferation of whorl 3. Using live confocal imaging, we show that the extra stamens in superman mutants arise from cells in whorl 4, which change their fate from female to male, while floral stem cells proliferate longer, allowing for the production of additional stamens.

The angiosperm order Malpighiales includes ∼16,000 species and constitutes up to 40% of the understory tree diversity in tropical rain forests. Despite remarkable progress in angiosperm systematics during the last 20 y, relationships within Malpighiales remain poorly resolved, possibly owing to its rapid rise during the mid-Cretaceous. Using phylogenomic approaches, including analyses of 82 plastid genes from 58 species, we identified 12 additional clades in Malpighiales and substantially increased resolution along the backbone. This greatly improved phylogeny revealed a dynamic history of shifts in net diversification rates across Malpighiales, with bursts of diversification noted in the Barbados cherries (Malpighiaceae), cocas (Erythroxylaceae), and passion flowers (Passifloraceae). We found that commonly used a priori approaches for partitioning concatenated data in maximum likelihood analyses, by gene or by codon position, performed poorly relative to the use of partitions identified a posteriori using a Bayesian mixture model. We also found better branch support in trees inferred from a taxon-rich, data-sparse matrix, which deeply sampled only the phylogenetically critical placeholders, than in trees inferred from a taxon-sparse matrix with little missing data. Although this matrix has more missing data, our a posteriori partitioning strategy reduced the possibility of producing multiple distinct but equally optimal topologies and increased phylogenetic decisiveness, compared with the strategy of partitioning by gene. These approaches are likely to help improve phylogenetic resolution in other poorly resolved major clades of angiosperms and to be more broadly useful in studies across the Tree of Life.

Key message The positive effect of VvWUS on carpel number variation in Vitis vinifera ‘Xiangfei’ is accomplished via forming the heterodimer with VvSTMa and VvSTMb proteins, which enhances the downstream VvAG2 gene expression during grapevine carpel formation. The WUSCHEL-CLAVATA3 signalling pathway plays an essential role in the shoot apical meristem (SAM) maintenance and floral organ development, influencing carpel number and fruit morphology in horticultural plants. This study investigates the role of VvWUS in regulating carpel number in the grapevine cultivar ‘Xiangfei’, which frequently produces flowers with multiple carpels. We found a positive correlation between VvWUS expression levels and carpel number variation among grapevine cultivars. Transgenic tomato plants overexpressing VvWUS exhibited an increased carpel number and a concomitant expression of SAM-related genes. Further experiments demonstrated that VvWUS interacts with VvSTMa and VvSTMb, forming heterodimers that are crucial for grapevine carpel development. VvWUS was also confirmed to activate VvAG2 expression. Our findings indicate that VvWUS positively regulates carpel number in grapevine by interacting with VvSTMa and VvSTMb and upregulating VvAG2 expression. These results provide a basis for molecular breeding aimed at increasing grape yield and fruit size.

Organ initiation from the shoot apical meristem first gives rise to leaves during vegetative development and then flowers during reproductive development. LEAFY (LFY) is activated after floral induction and together with other factors promotes the floral program. LFY functions redundantly with APETALA1 (AP1) to activate the class B genes APETALA3 (AP3) and PISTILLATA (PI), the class C gene AGAMOUS (AG), and the class E gene SEPALLATA3, which leads to the specification of stamens and carpels, the reproductive organs of flowers. Molecular and genetic networks that control the activation of AP3, PI, and AG in flowers have been well studied; however, much less is known about how these genes are repressed in leaves and how their repression is lifted in flowers. Here, we showed that two genes encoding Arabidopsis C2H2 ZINC FINGER PROTEIN (ZFP) transcription factors, ZP1 and ZFP8, act redundantly to directly repress AP3, PI, and AG in leaves. After LFY and AP1 are activated in floral meristems, they down-regulate ZP1 and ZFP8 directly to lift the repression on AP3, PI, and AG. Our results reveal a mechanism for how floral homeotic genes are repressed and derepressed before and after floral induction.

Key message We link key aspects of land plant reproductive evolution and detail how successive molecular changes leading to novel tissues and organs require co-evolution of communication systems between tissues. The transition of water-dependent reproduction of algae to mechanisms with very limited water dependence in many land plant lineages allowed plants to colonize diverse terrestrial environments, leading to the vast variety of extant plant species. The emergence of modified cell types, novel tissues, and organs enabled this transition; their origin is associated with the co-evolution of novel or adapted molecular communication systems and gene regulatory networks. In the light of an increasing number of genome sequences in combination with the establishment of novel genetic model organisms from diverse green plant lineages, our knowledge and understanding about the origin and evolution of individual traits that arose in a concerted way increases steadily. For example, novel members of gene families in signaling pathways emerged for communication between gametes and gametophytes with additional tissues surrounding the gametes. Here, we provide a comprehensive overview on the origin and evolution of reproductive novelties such as pollen grains, immobile sperms, ovules and seeds, carpels, gamete/gametophytic communication systems, double fertilization, and the molecular mechanisms that have arisen anew or have been co-opted during evolution, including but not limited to the incorporation of phytohormones, reactive oxygen species and redox signaling as well as small RNAs in regulatory modules that contributed to the evolution of land plant sexual reproduction.

Many insect species have acquired the ability to redirect plant development to form unique organs called galls, which provide these insects with unique, enhanced food and protection from enemies and the elements. Many galls resemble flowers or fruits, suggesting that elements of reproductive development may be involved. We tested this hypothesis using RNA sequencing to quantify the transcriptional responses of wild grapevine ( Vitis riparia ) leaves to a galling parasite, phylloxera ( Daktulosphaira vitifoliae ). If development of reproductive structures is part of gall formation, we expected to find significantly elevated expression of genes involved in flower and/or fruit development in developing galls as opposed to ungalled leaves. We found that reproductive gene ontology categories were significantly enriched in developing galls, and that expression of many candidate genes involved in floral development were significantly increased, particularly in later gall stages. The patterns of gene expression found in galls suggest that phylloxera exploits vascular cambium to provide meristematic tissue and redirects leaf development towards formation of carpels. The phylloxera leaf gall appears to be phenotypically and transcriptionally similar to the carpel, due to the parasite hijacking underlying genetic machinery in the host plant.