Transcriptome profiling of Desmos chinensis: revealing the molecular basis of dipartite perianth evolution in the early-divergent angiosperm family Annonaceae

Abstract

During the past 200 million years of speciation and hybridization, angiosperm genome structure has evolved and diversified in size and composition. While many angiosperm taxa experienced genome duplication and different degrees of transposable element proliferation, the homeotic control of floral development has remained conservative. The MIKC-type MADS-domain proteins are transcription factors that dictate organ identity during floral organogenesis. The classic “ABCDE” MADS-box gene expression model proposed for the core eudicots is not fully applicable to early-divergent angiosperms, in which a gradual transition is apparent between sepal-like outer tepals and petal-like inner tepals, leading to the proposed “fading-borders” expression model. Flowers in the Annonaceae deviate from other early-divergent angiosperms in possessing a distinctive dipartite perianth. Petals in the Annonaceae (‘bracteopetals’) have furthermore presumably evolved independently from andropetals in core eudicots. The degree of differentiation of petals from sepals in Annonaceae flowers is generally of functional significance (e.g., enabling the evolution of largely or fully enclosed pollination chambers during anthesis). Little is known of the genome and genetic control of floral development in the Annonaceae. The application of massive parallel sequencing techniques such as RNAseq provides opportunities to profile the transcriptomes of non-model organisms. In addition to a developmental study, we characterized the floral and leaf transcriptome of Desmos chinensis, a representative of the Annonaceae that possesses a dipartite perianth and which shares the basic floral Bauplan of the family, in order to understand the genetics of its floral development. Transcriptomes of developing and mature Desmos chinensis floral organs and leaves were sequenced using the high-throughput Illumina sequencing platform. After filtering, 16,098 genes and 22,112 transcripts were recovered from de novo assembly. We identified possible coding regions and compared them against five public databases. Based on sequence homology against the NCBI non-redundant protein database, transcripts were annotated with 3,991 unique gene ontology (GO) terms and categorized into functional groups. Functional group enrichment analysis was used to identify groups with significant expression level changes during organ development. Transcripts that are commonly differentially expressed among developing and mature floral organs and leaves were identified using the digital gene expression data. We identified 41 putative homeotic MADS-box gene homologs and their respective expression levels in order to determine whether Annonaceae flowers are consistent with the MADS-box gene “fading borders” expression model. Other floral developmental regulators of Desmos chinensis were also discovered. While many questions remain unresolved at the transcription level, our data emphasises the importance and potential of extending further studies into systems biology, and help understand floral developmental biology as biological networks.