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Orchids are some of the most popular ornamental plants worldwide. Orchid floral morphology has increasingly attracted horticultural and commercial attention. Although multiple genes have been shown to be involved in the formation of the orchid flower, the underlying multi-level regulatory networks are largely unknown. In this study, we analyzed the ontogeny of flower development in  Cymbidium ensifolium , a traditional orchid in the tropical and subtropical regions of Asia, by performing deep sequencing of the transcriptome of individual flower organs to discover organ-specific genes potentially involved in their growth. We identified 3,017 differentially-expressed genes (DEGs) during the development of various flower organs, and observed over-representation of  GROWTH-REGULATING FACTORS  ( GRFs ) specific to flower column (gynostemium). Eleven  C. ensifolium GRFs  ( CeGRFs ) from our transcriptome data clustered into five phylogenetic subgroups. Ten of these  GRFs  shared a region complementary to  C. ensifolium  microRNA396 ( Ce -miR396), and degradome sequencing confirmed the cleavage of transcripts derived from seven  CeGRFs . We cloned  Ce- miR396 and used a protoplast-based transient expression system to overexpress it in  Cymbidium  protoplasts. We observed a significant decrease in the transcripts of several  CeGRFs  in flowers and leaves, indicating a potential role for miR396–GRF module in organ development through the cleavage of distinct  CeGRFs . Temporal and spatial expression analysis indicated that most  CeGRF  transcripts accumulated in flower buds and column tissues, where  Ce -miR396 expression was the lowest. Expression dynamics in wild type and floral-defective mutants further confirmed a strong correlation between  Ce -miR396,  CeGRFs , and flower organ development and column specification. Moreover, overexpression of  Ce -miR396 in  Nicotiana tabacum  resulted in curved pistils and reduced fertility, implying that the conserved role of  Ce -miR396 in floral development. These results provide tools to better understand the biological roles of  GRFs  in orchid development, and open new avenues for the diversification of orchid floral patterns.

frontiers in plant science

Organ-Specific Gene Expression Reveals the Role of the Cymbidium ensifolium-miR396/Growth-Regulating Factors Module in Flower Development of the Orchid Plant Cymbidium ensifolium