Exploring the evolutionary origin of floral organs of Erycina pusilla, an emerging orchid model system

Abstract

BackgroundThousands of flowering plant species attract pollinators without offering rewards, but the evolution of this deceit is poorly understood. Rewardless flowers of the orchid Erycina pusilla have an enlarged median sepal and incised median petal (‘lip’) to attract oil-collecting bees. These bees also forage on similar looking but rewarding Malpighiaceae flowers that have five unequally sized petals and gland-carrying sepals. The lip of E. pusilla has a ‘callus’ that, together with winged ‘stelidia’, mimics these glands. Different hypotheses exist about the evolutionary origin of the median sepal, callus and stelidia of orchid flowers.ResultsThe evolutionary origin of these organs was investigated using a combination of morphological, molecular and phylogenetic techniques to a developmental series of floral buds of E. pusilla. The vascular bundle of the median sepal indicates it is a first whorl organ but its convex epidermal cells reflect convergence of petaloid features. Expression of AGL6 EpMADS4 and APETALA3 EpMADS14 is low in the median sepal, possibly correlating with its petaloid appearance. A vascular bundle indicating second whorl derivation leads to the lip. AGL6 EpMADS5 and APETALA3 EpMADS13 are most highly expressed in lip and callus, consistent with current models for lip identity. Six vascular bundles, indicating a stamen-derived origin, lead to the callus, stelidia and stamen. AGAMOUS is not expressed in the callus, consistent with its sterilization. Out of three copies of AGAMOUS and four copies of SEPALLATA, EpMADS22 and EpMADS6 are most highly expressed in the stamen. Another copy of AGAMOUS, EpMADS20, and the single copy of SEEDSTICK, EpMADS23, are most highly expressed in the stelidia, suggesting EpMADS22 may be required for fertile stamens.ConclusionsThe median sepal, callus and stelidia of E. pusilla appear to be derived from a sepal, a stamen that gained petal identity, and stamens, respectively. Duplications, diversifying selection and changes in spatial expression of different MADS-box genes shaped these organs, enabling the rewardless flowers of E. pusilla to mimic an unrelated rewarding flower for pollinator attraction. These genetic changes are not incorporated in current models and urge for a rethinking of the evolution of deceptive flowers.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0938-7) contains supplementary material, which is available to authorized users.

B and E MADS‐box genes determine the perianth formation in Cymbidium goeringii Rchb.f

“…Our results agree with previous work reporting SEP ‐like genes from orchids are expressed in all flower organs during development (Xu et al , Chang et al , Acri‐Nunes‐Miranda and Mondragon‐Palomino , Pan et al , Lin et al , Dirks‐Mulder et al ). These suggest SEP ‐like genes in orchids are involved in identifying properties of all four floral organ whorls.…”

How different is similar – exploring development of Ceropegia sandersonii pitfall flowers to elucidate convergent evolution of floral synorganization

“…Interestingly, no AGL6 expression was detected in the early oral buds or any of the mature organs of C. sandersonii owers that are all radially symmetric. This nding is in contrast with previous ndings of Pabón-Mora et al (26), who detected AGL6 expression in the bilaterally symmetric sepals and ovules of the pipevine Aristolochia mbriata and Dirks-Mulder et al (33) and Pramanik et al (34), who detected AGL6 expression in the bilaterally symmetric sepals, petals, stelidia and gynostemium in the rst, second, third and fourth whorl of the owers of the orchid species Erycina pusilla, Phaelonopsis equestris and P. pulcherrima.…”

“…No E-class gene expression was found in the mature corona of Ceropegia sandersonii. In the callus on the orchid labellum, also an organ of staminal identity (33,34), E-class gene expression was found. Expression was more pronounced in early than late developmental stages of the callus and thus, E-class gene expression may take place in the early stage Ceropegia corona as well.…”

“…In Aristolochia, genes involved in oral development and organ identity are continuously better understood (25)(26)(27), and in orchids, deceptive species such as Phalaenopsis equestris and Erycina pusilla are well studied with regard to the genetic background of oral development (28)(29)(30)(31)(32)(33)(34). Here we present the rst data on MADS-box gene expression during development of radially symmetric pitfall owers of Ceropegia sandersonii, the parachute plant; it is the rst oral transcriptome analyses for Ceropegia in general.…”

Phylogenetics of Dendrochilum (Orchidaceae): Evidence of pronounced morphological homoplasy and predominantly centric endemism

“…Spurred sepals and petals often contain nectar or other rewards for relatively long-tongued pollinators. The function of stelidia is increasingly uncovered as positioning short-tonged pollinators in an orchid flower so that specific body parts are exposed to the rostellum and/or stigma to promote removal or deposition of pollinia (Dirks-Mulder & al., 2017). It might be that the species previously recognized as genus Bracisepalum are pollinated by relatively long-tongued Lepidoptera that hover in front of the flowers rather than landing on them so that the need for stelidia disappeared; further pollination studies are needed to support or reject this hypothesis.…”