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The Developmental and Genetic Bases of Apetaly in Bocconia Frutescens

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The Developmental and Genetic Bases of Apetaly in Bocconia Frutescens Arango‑Ocampo et al. EvoDevo (2016) 7:16 DOI 10.1186/s13227-016-0054-6 EvoDevo RESEARCH Open Access The developmental and genetic bases of apetaly in Bocconia frutescens (Chelidonieae: Papaveraceae) Cristina Arango‑Ocampo1, Favio González2, Juan Fernando Alzate3 and Natalia Pabón‑Mora1* Abstract Background: Bocconia and Macleaya are the only genera of the poppy family (Papaveraceae) lacking petals; how‑ ever, the developmental and genetic processes underlying such evolutionary shift have not yet been studied. Results: We studied floral development in two species of petal-less poppies Bocconia frutescens and Macleaya cordata as well as in the closely related petal-bearing Stylophorum diphyllum. We generated a floral transcriptome of B. frutescens to identify MADS-box ABCE floral organ identity genes expressed during early floral development. We performed phylogenetic analyses of these genes across Ranunculales as well as RT-PCR and qRT-PCR to assess loci- specific expression patterns. We found that petal-to-stamen homeosis in petal-less poppies occurs through distinct developmental pathways. Transcriptomic analyses of B. frutescens floral buds showed that homologs of all MADS-box genes are expressed except for the APETALA3-3 ortholog. Species-specific duplications of other ABCE genes inB. frute- scens have resulted in functional copies with expanded expression patterns than those predicted by the model. Conclusions: Petal loss in B. frutescens is likely associated with the lack of expression of AP3-3 and an expanded expression of AGAMOUS. The genetic basis of petal identity is conserved in Ranunculaceae and Papaveraceae although they have different number of AP3 paralogs and exhibit dissimilar floral groundplans. Keywords: ABCE model, AGAMOUS, APETALA3, Apetaly, Bocconia, Homeosis, Macleaya, Papaveraceae, Stylophorum Background often associated with changes in the mechanisms of pol- Flowers are evolutionary novelties of nearly 300,000 spe- lination [5]. cies. A typical flower has one or two whorls of sterile The Ranunculales, the largest order in basal eud- organs, collectively known as the perianth [1–3], which icots, exhibit an incredible array of floral forms which enclose the stamens and the carpels. Frequently, the range from perianth-less flowers (like in Eupteleaceae) perianth consists of an outer series of sepals (collectively to flowers with bipartite perianths (like in Papaveraceae termed calyx) and an inner series of petals (collectively and Ranunculaceae), sepaloid tepals (like in Menisper- termed corolla). Sepals often resemble leaves or bracts maceae) and petaloid tepals (like in Lardizabalaceae and in that they are persistent, protect the rest of the floral Berberidaceae) [6–8]. With 760 species in 41 genera, organs in the bud and often are photosynthetic, while the poppy family (Papaveraceae) is the second largest petals are colorful, attract pollinators, are rich in pig- of the order Ranunculales. As currently circumscribed ments, oils and waxes [3, 4]. The number and morphol- the Papaveraceae s. str. comprise the subfamilies Fuma- ogy of the perianth parts are extremely variable and are rioideae, with the tribes Fumarieae and Hypecoeae, and Papaveroideae, with the tribes Chelidonieae, Eschschol- zieae, Fumarioideae, Papavereae and Platystemoneae [9]. All Papaveraceae exhibit a dimerous floral plan with 2 *Correspondence: [email protected] deciduous sepals, 4 petals in two whorls, many stamens 1 Instituto de Biología, Universidad de Antioquia, Medellín, Colombia Full list of author information is available at the end of the article (up to 700) and 2(−8) fused carpels (Fig. 1a–d) [6]. The © 2016 The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Arango‑Ocampo et al. EvoDevo (2016) 7:16 Page 2 of 18 Fig. 1 Floral diversity in Papaveraceae. Petal‑bearing flowers in Papaver rhoeas (a), Eschscholzia californica (b) and Stylophorum diphyllum (c). d S. diphyllum floral diagram. e–m Petal‑less flowers. e–h Bocconia frutescens, preanthetic and anthetic flowers. i B. frutescens floral diagram. j–l Macleaya cordata, preanthetic and anthetic flowers. m M. cordata floral diagram. Arrow gynophore; c carpel, ip inner petal, op outer petal, s sepal, st stamen, * homeotic stamen; 1, first set of 4 true stamens on the first whorl in red indicate that these are the first stamens formed and that they occupy the same positions in both petalous and apetalous species serving as reference for the positioning of all other stamens; 2, second set of true stamens of the first whorl; 3, true stamens of the second whorl. 4. True stamens of the third whorl. Bars a–c 7 mm; e, g, h 10 mm; f 2 mm, j, l 8 mm; = = = = k 4 mm = only exceptions to this floral groundplan are the natu- and E determine the identity of all floral organs [12–14]. rally occurring mutants in Sanguinaria canadensis L., However, all the MADS-box gene lineages have suffered which possess eight petals in four whorls as a result of duplications during the course of angiosperm evolution, a stamen-to-petal homeosis, and all species in the sister making the model difficult to extrapolate to non-model genera Bocconia Plum. ex L., and Macleaya R. Br., which flowering plants [15–20]. According to the model, petal lack petals likely as a result of a petal-to-stamen homeo- identity depends on the combination of A and B and E sis (Fig. 1e–m) [10, 11]. This variation provides an excel- class genes and the repression of C class genes [12, 14, lent comparative morphological platform for studying 21]. Both A and B gene lineages have undergone duplica- the genetic basis of petal identity in non-model organ- tions in the core eudicots, basal eudicots and monocots isms. The framework for comparison is the ABCE genetic [16, 22, 23]. In basal eudicots, local duplications in both model of flower development established in Arabidop- gene lineages have also been detected [23–25]. A class sis thaliana that describes how specific combinations of genes duplicated once, before the diversification of the four classes of MADS-box transcription factors A, B, C Ranunculales, resulting in two FUL-like clades named Arango‑Ocampo et al. EvoDevo (2016) 7:16 Page 3 of 18 RanFL1 and RanFL2 [24]. Gene copies have been func- Pabón-Mora 250, NY); and Stylophorum diphyllum tionally characterized in Eschscholzia californica Cham. (voucher: USA, New York, Bronx, Living collections, and Papaver somniferum L. (Papaveraceae) and in Aqui- New York Botanical Garden, April 16, 2011, N. Pabón- legia coerulea E. James. (Ranunculaceae). FUL-like genes Mora 254, NY). in Papaveraceae control flowering time, inflorescence Material for gene expression studies was collected in architecture, floral meristem, sepal identity and fruit liquid nitrogen directly from field collections fromBocco - development. Only papsfl1-/fl2-downregulated individu- nia frutescens (voucher: Colombia, Antioquia, Rionegro, als show atypical green areas in the outer petals, but have August 1, 2014, N. Pabón-Mora and C. Arango-Ocampo normal inner petals [26]. In Ranunculaceae, AqcFL1A 337, HUA). Material was collected separately from floral and AqcFL1B (RanFL1 clade) play roles in inflorescence buds, anthetic flowers, fruits and leaves. Floral buds were architecture and leaf morphogenesis, but their role in collected in four different developmental stages: The first sepal and petal development is unclear [27]. On the other (S0) is characterized by having stigmas inserted into the hand, AP2-like genes are expressed during carpel, fruit green sepals, the second (S1) is characterized by having and leaf development and possibly do not control peri- slightly exerted stigmas through the green sepals, the anth development [23]. third (S2) is characterized by having fully exerted, non- B class genes duplicated two times consecutively in the rotated stigmas over the green sepals, and the fourth Ranunculales resulting in the APETALA3I (AP3I), AP3II (S3) is characterized by having fully exerted rotated (90°) and AP3III clades [7, 21, 25]. However, the Papaver- stigmas over the pink sepals. For stages S1, S2, S3 floral aceae only have members of the AP3I and AP3III clades, organs were also dissected into sepals, stamens and car- whereas the Ranunculaceae have gene representatives in pels. Fruits were separated into young green fruits (Fr1) all clades [25]. Gene copies have been functionally char- and mature yellow fruits (Fr2) (Figs. 1e–h, 8a–i). Biologi- acterized in Papaver somniferum, Nigella damascena and cal replicates of these collections were made to corrobo- Aquilegia coerulea and in general have shown subfunc- rate gene expression via qRT-PCR. tionalization [25, 28–30]. In P. somniferum PapsAP3-1 is responsible for the identity of petals, whereas PapsAP3-2 Morphological studies controls the identity of stamens. In A. coerulea, AqAP3- Vegetative and flowering shoots of B. frutescens, M. cor- 1 specifies the identity of staminodia, whereas AqAP3-2 data and S. diphyllum (Figs. 1, 2, 3) were fixed for 48 h is responsible for identity of stamens and AqAP3-3 spe- in formalin–acetic acid–ethanol (3.7 % formaldehyde, cifically controls petal identity [25, 29, 31]. Finally, in N. 5 % glacial acetic acid, 50 % ethanol) and then trans- damascena NdAP3-3 is responsible for petal and outer ferred and stored in 70 % ethanol. For SEM, buds were stamen identity, while NdAP3-1 and NdAP3-2 control dissected in 90 % ethanol under a Zeiss Stemi DV4 ste- stamen identity [30, 32]. reoscope and then dehydrated in an absolute ethanol/ This work aims to identify the developmental and acetone series.
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