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Differential Co-Expression of DROOPING LEAF-Like and Class B MADS-Box Genes During Phalaenopsis Flower Development

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Differential Co-Expression of DROOPING LEAF-Like and Class B MADS-Box Genes During Phalaenopsis Flower Development International Journal of Molecular Sciences Article Extending the Toolkit for Beauty: Differential Co-Expression of DROOPING LEAF-like and Class B MADS-box Genes during Phalaenopsis Flower Development Francesca Lucibelli 1 , Maria Carmen Valoroso 1 , Günter Theißen 2, Susanne Nolden 2, Mariana Mondragon-Palomino 3,*,† and Serena Aceto 1,* 1 Department of Biology, University of Naples Federico II, 80126 Napoli, Italy; [email protected] (F.L.); [email protected] (M.C.V.) 2 Matthias Schleiden Institute of Genetics, Friedrich Schiller University Jena, 07743 Jena, Germany; [email protected] (G.T.); [email protected] (S.N.) 3 Department of Cell Biology and Plant Biochemistry, University of Regensburg, 93040 Regensburg, Germany * Correspondence: [email protected] (M.M.-P.); [email protected] (S.A.) † Current address: Biomax Informatics AG, 82152 Planegg, Germany. Abstract: The molecular basis of orchid flower development is accomplished through a specific regulatory program in which the class B MADS-box AP3/DEF genes play a central role. In particular, the differential expression of four class B AP3/DEF genes is responsible for specification of organ identities in the orchid perianth. Other MADS-box genes (AGL6 and SEP-like) enrich the molecular Citation: Lucibelli, F.; Valoroso, M.C.; program underpinning the orchid perianth development, resulting in the expansion of the original Theißen, G.; Nolden, S.; “orchid code” in an even more complex gene regulatory network. To identify candidates that could Mondragon-Palomino, M.; Aceto, S. interact with the AP3/DEF genes in orchids, we conducted an in silico differential expression analysis Extending the Toolkit for Beauty: in wild-type and peloric Phalaenopsis. The results suggest that a YABBY DL-like gene could be Differential Co-Expression of involved in the molecular program leading to the development of the orchid perianth, particularly DROOPING LEAF-like and Class B the labellum. Two YABBY DL/CRC homologs are present in the genome of Phalaenopsis equestris, MADS-box Genes during Phalaenopsis PeDL1 and PeDL2, and both express two alternative isoforms. Quantitative real-time PCR analyses Flower Development. Int. J. Mol. Sci. revealed that both genes are expressed in column and ovary. In addition, PeDL2 is more strongly 2021, 22, 7025. https://doi.org/ expressed the labellum than in the other tepals of wild-type flowers. This pattern is similar to that of 10.3390/ijms22137025 the AP3/DEF genes PeMADS3/4 and opposite to that of PeMADS2/5. In peloric mutant Phalaenopsis, where labellum-like structures substitute the lateral inner tepals, PeDL2 is expressed at similar levels Academic Editor: Pedro Martínez-Gómez of the PeMADS2-5 genes, suggesting the involvement of PeDL2 in the development of the labellum, together with the PeMADS2-PeMADS5 genes. Although the yeast two-hybrid analysis did not reveal Received: 3 June 2021 the ability of PeDL2 to bind the PeMADS2-PeMADS5 proteins directly, the existence of regulatory Accepted: 27 June 2021 interactions is suggested by the presence of CArG-boxes and other MADS-box transcription factor Published: 29 June 2021 binding sites within the putative promoter of the orchid DL2 gene. Publisher’s Note: MDPI stays neutral Keywords: DROOPING LEAF; flower development; gene expression; Orchidaceae; YABBY transcrip- with regard to jurisdictional claims in tion factors published maps and institutional affil- iations. 1. Introduction The Orchidaceae is one of the widely distributed and most diversified families of an- Copyright: © 2021 by the authors. giosperms. Their evolutionary success is possibly due to sundry causes such as epiphytism, Licensee MDPI, Basel, Switzerland. extraordinary adaptive capacities to different habitats, highly specialized pollination strate- This article is an open access article gies, and diversified flower morphology [1–3]. Despite the diversity of flower colors, distributed under the terms and sizes, shapes, and appendages, the floral organs of orchids share a common organiza- conditions of the Creative Commons tion (Figure1 ). There are three outer tepals in the first floral whorl; in the second whorl, Attribution (CC BY) license (https:// the three tepals are distinguished into two lateral inner tepals and a median inner tepal creativecommons.org/licenses/by/ called lip or labellum. This organ often has a peculiar morphology and bears distinct 4.0/). Int. J. Mol. Sci. 2021, 22, 7025. https://doi.org/10.3390/ijms22137025 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 19 called lip or labellum. This organ often has a peculiar morphology and bears distinct color patterns (Figure 1a,b). Female and male reproductive organs are fused to form the gyno- stemium or column, at whose apex are located the pollinia. The ovary is placed at the base of the gynostemium, and its development is activated by pollination [4]. Int. J. Mol. Sci. 2021, 22, 7025 The labellum is a central organ in orchid pollination because of its2 ofstrikingly 18 distinct morphology and its direct opposition to the gynostemium. Therefore, its showy color pat- terns and structures are visual attractants and it act as a landing platform that guides pol- linators towards the gynostemium. Because the labellum is the uppermost perianth organ, color patterns (Figure1a,b). Female and male reproductive organs are fused to form the its role in pollination depends on becoming the lowermost through resupination, a 180° gynostemium or column, at whose apex are located the pollinia. The ovary is placed at the developmental rotation of the flower pedicel or ovary (Figure 1a) [5]. base of the gynostemium, and its development is activated by pollination [4]. Figure 1. Wild-type and peloric mutants of Phalaenopsis.(a) Wild-type P. aphrodite;(b) floral buds at Figure 1. Wild-type and peloric mutants of Phalaenopsis. (a) Wild-type P. aphrodite; (b) floral buds at stages B1–B5 and floral organsstages at the B1–B5 OF stage and floralof the organs wild-type at the P. OFaphrodite stage; of(c) the flower wild-type of the P.wild-type aphrodite Phalaenopsis;(c) flower of hyb. the “Athens”; wild-type (d) flower of the peloricPhalaenopsis mutant Phalaenopsishyb. “Athens”; hyb. ( d“Athens”;) flower of (e the) flower peloric of mutantthe peloricPhalaenopsis mutant Phalaenopsishyb. “Athens”; hyb. ( e“Joy) flower Fairy of Tale”. The arrow in (a)the indicates peloric mutantthe pointPhalaenopsis of rotationhyb. of the “Joy pedicel Fairy duri Tale”.ng Theresupination. arrow in (a)Size indicates of the de thevelopmental point of rotation stages: B1 (0.5–1 cm), B2 (1–1.5of the cm), pedicel B3 (1.5–2 during cm), resupination. B4 (2–2.5 cm), Size B5 of (2.5–3 the developmental cm), OF (open stages: flower). B1 1, (0.5–1 outercm), tepals; B2 (1–1.52, lateral cm), inner B3 tepals; 3, labellum; 4,(1.5–2 column; cm), 5, B4 ovary; (2–2.5 2/3, cm), labellum-like B5 (2.5–3 cm), organs. OF (open flower). 1, outer tepals; 2, lateral inner tepals; 3, labellum; 4, column; 5, ovary; 2/3, labellum-like organs. Bilateral symmetry or zygomorphy in orchids is a syndrome defined by the associa- The labellumtion is of a centralseveral organcharacters in orchid (e.g., pollinationlabellum and because the developmental of its strikingly suppression distinct of adaxial morphology andstamens). its direct This opposition association to took the place gynostemium. early in Orchidaceae Therefore, evolution its showy and color became the basis patterns and structuresfor the progressive are visual addition attractants of andfurther it act innovations as a landing like platform pollinaria, that a spur, guides or showy mark- pollinators towardsings on the the gynostemium. labellum [4]. The Because concurrence the labellum of these is floral the uppermost features is perianthconsidered a key mor- organ, its role inphological pollination innovation depends onin becomingthe two most the lowermostderived and through diverse resupination, orchid subfamilies a Epiden- 180◦ developmentaldroideae rotation and Orchidoideae of the flower pedicel[4]. Together or ovary they (Figure mediate1a) the [5 ].specialized relationships of this Bilateral symmetryfamily with or zygomorphy pollinators, infacilitating orchids is the a syndrome processes defined of prezygotic by the association reproductive isolation of several characters[6,7]. (e.g., labellum and the developmental suppression of adaxial stamens). This association tookBecause place earlyof the in central Orchidaceae role of the evolution labellum and in orchid became reproduction, the basis for its the developmental progressive additionorigin ofis furthera subject innovations of intense likestudy pollinaria, [4,8–10]. aIn spur, the orlast showy decade, markings several ongene regulatory the labellum [4].models The concurrence inspired by of the these more floral general features angiospe is consideredrm ABC a keymodel morphological [11,12] helped to explain innovation in the two most derived and diverse orchid subfamilies Epidendroideae and Orchidoideae [4]. Together they mediate the specialized relationships of this family with pollinators, facilitating the processes of prezygotic reproductive isolation [6,7]. Because of the central role of the labellum in orchid reproduction, its developmental origin is a subject of intense study [4,8–10]. In the last decade, several gene regulatory models inspired by the more general angiosperm ABC model [11,12] helped to explain the developmental specification of the distinct
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