Abstract
Efficient seed dispersal in flowering plants is enabled by the development of fruits, which can be either dehiscent or indehiscent. Dehiscent fruits open at maturity to shatter the seeds, while indehiscent fruits do not open and the seeds are dispersed in various ways. The diversity in fruit morphology and seed shattering mechanisms is enormous within the flowering plants. How these different fruit types develop and which molecular networks are driving fruit diversification is still largely unknown, despite progress in eudicot model species. The orchid family, known for its astonishing floral diversity, displays a huge variation in fruit dehiscence types, which have been poorly investigated. We undertook a combined approach to understand fruit morphology and dehiscence in different orchid species to get more insight into the molecular network that underlies orchid fruit development. We describe fruit development in detail for the epiphytic orchid species Erycina pusilla and compare it to two terrestrial orchid species: Cynorkis fastigiata and Epipactis helleborine. Our anatomical analysis provides further evidence for the split carpel model, which explains the presence of three fertile and three sterile valves in most orchid species. Interesting differences were observed in the lignification patterns of the dehiscence zones. While C. fastigiata and E. helleborine develop a lignified layer at the valve boundaries, E. pusilla fruits did not lignify at these boundaries, but formed a cuticle-like layer instead. We characterized orthologs of fruit-associated MADS-domain transcription factors and of the Arabidopsis dehiscence-related genes INDEHISCENT (IND)/HECATE 3 (HEC3), REPLUMLESS (RPL) and SPATULA (SPT)/ALCATRAZ (ALC) in E. pusilla, and found that the key players of the eudicot fruit regulatory network appear well-conserved in monocots. Protein-protein interaction studies revealed that MADS-domain complexes comprised of FRUITFULL (FUL), SEPALLATA (SEP) and AGAMOUS (AG) /SHATTERPROOF (SHP) orthologs can also be formed in E. pusilla, and that the expression of HEC3, RPL, and SPT can be associated with dehiscence zone development similar to Arabidopsis. Our expression analysis also indicates differences, however, which may underlie fruit divergence.
Highlights
Developmental mechanisms driving fruit diversification are still poorly understood, despite progress in the study of fruit formation in model plant species such as Arabidopsis (Arabidopsis thaliana (L.) Heyhn) and tomato (Solanum lycopersicum L.) (Gu et al, 1998; Ferrandiz et al, 1999; Vrebalov et al, 2009; Pabon-Mora and Litt, 2011)
To investigate whether the regulatory network underlying fruit development in eudicots could to some extent be conserved in orchids, we investigated the fruit-expressed MADS-box genes in E. pusilla by performing detailed expression analysis and determining the protein-protein interactions of the proteins encoded by these genes
Fruit development starts around one day after pollination (1 days after pollination (DAP)) and the fruit reaches its final size at 16 weeks after pollination (16 WAP) (Figure S1)
Summary
Developmental mechanisms driving fruit diversification are still poorly understood, despite progress in the study of fruit formation in model plant species such as Arabidopsis (Arabidopsis thaliana (L.) Heyhn) and tomato (Solanum lycopersicum L.) (Gu et al, 1998; Ferrandiz et al, 1999; Vrebalov et al, 2009; Pabon-Mora and Litt, 2011). Research in monocots so far has focused mainly on cereal species such as rice, maize and wheat, all of which have relatively simple indehiscent fruits that consist of a one-layered pericarp. This leaves a big gap in the knowledge about evolution and development of fruits of other monocots, especially of the orchid family. Rasmussen and Johansen (2006) presented the “splitcarpel model” of the orchidaceous ovary, giving an explanation of the hexamerous pattern According to this model, a typical orchid ovary consists of three sterile valves (located at the sepal bases) and three fertile valves (located at the petal bases), each consisting of two carpel-halves (Figure 1). This would be in agreement with the split carpel model, where the fertile valves are the actual carpels, while the sterile valves are structures containing
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