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Developmental Genetics of the Perianthless Flowers and Bracts of a Paleoherb Species, Saururus Chinensis

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Developmental Genetics of the Perianthless Flowers and Bracts of a Paleoherb Species, Saururus Chinensis Developmental Genetics of the Perianthless Flowers and Bracts of a Paleoherb Species, Saururus chinensis Yin-He Zhao1,2, Zachary Larson-Rabin1, Guo-Ying Wang3, Michael Mo¨ ller4, Cheng-Yun Li2, Jin- Peng Zhang3, Hong-Tao Li1, De-Zhu Li1* 1 Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China, 2 College of Agronomy, and Key Laboratory for Plant Pathology of Yunnan Province, Yunnan Agricultural University, Kunming, China, 3 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China, 4 Royal Botanic Garden Edinburgh, Edinburgh, Scotland, United Kingdom Abstract Saururus chinensis is a core member of Saururaceae, a perianthless (lacking petals or sepals) family. Due to its basal phylogenetic position and unusual floral composition, study of this plant family is important for understanding the origin and evolution of perianthless flowers and petaloid bracts among angiosperm species. To isolate genes involved in S. chinensis flower development, subtracted floral cDNA libraries were constructed by using suppression subtractive hybridization (SSH) on transcripts isolated from developing inflorescences and seedling leaves. The subtracted cDNA libraries contained a total of 1,141 ESTs and were used to create cDNA microarrays to analyze transcript profiles of developing inflorescence tissues. Subsequently, qRT-PCR analyses of eight MADS-box transcription factors and in situ hybridizations of two B-class MADS-box transcription factors were performed to verify and extend the cDNA microarray results. Finally, putative phylogenetic relationships within the B-class MADS-box gene family were determined using the discovered S. chinensis B-class genes to compare K-domain sequences with B genes from other basal angiosperms. Two hundred seventy-seven of the 1,141 genes were found to be expressed differentially between S. chinensis inflorescence tissues and seedling leaves, 176 of which were grouped into at least one functional category, including transcription (14.75%), energy (12.59%), metabolism (9.12%), protein-related function (8.99%), and cellular transport (5.76%). qRT-PCR and in situ hybridization of selected MADS-box genes supported our microarray data. Phylogenetic analysis indicated that a total of six B-class MADS-box genes were isolated from S. chinensis. The differential regulation of S. chinensis B-class MADS- box transcription factors likely plays a role during the development of subtending bracts and perianthless flowers. This study contributes to our understanding of inflorescence development in Saururus, and represents an initial step toward understanding the formation of petaloid bracts in this species. Citation: Zhao Y-H, Larson-Rabin Z, Wang G-Y, Mo¨ller M, Li C-Y, et al. (2013) Developmental Genetics of the Perianthless Flowers and Bracts of a Paleoherb Species, Saururus chinensis. PLoS ONE 8(1): e53019. doi:10.1371/journal.pone.0053019 Editor: Ive De Smet, University of Nottingham, United Kingdom Received July 4, 2012; Accepted November 22, 2012; Published January 30, 2013 Copyright: ß 2013 Zhao et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the Ministry of Science and Technology of China [2004DKA30430]; the National Natural Science Foundation of China [NSFC30860130 and NSFC31060166]; the Yunnan Natural Science Foundation [2007C209M]; and the Large-scale Scientific Facilities of the Chinese Academy of Sciences program [2009-LSFGBOWS-01]. Z.L.R. was supported by a Chinese Academy of Sciences Young International Scientist Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction LATA (PI), one C gene, AGAMOUS (AG), and four E genes SEPALLATA1 (SEP1), SEPALLATA2 (SEP2), SEPALLATA3 The morphological diversity of angiosperm flowers represents a (SEP3), and SEPALLATA4 (SEP4). With the exception of AP2, breathtaking exposition of the power of evolution. Through a these floral homeotic genes belong to MADS-box gene family, process known as the ABCE model of floral morphogenesis, named for the MADS sequence motif that encodes a domain combinations of transcription factor proteins specify organ controlling both DNA binding and homo-dimerization or hetero- identities in developing flowers, typically leading to the outgrowth dimerization with other transcription factors [4,10,11,12]. The of sepals, petals, stamens and pistils [1–3]. In the ABCE model, A- subset of plant MADS-box genes that control floral organ type transcription factors specify the respective identities of the first identities and development, the MIKC or Type II genes, also and second whorl organs, i.e., the sepals and petals. The B-class encode three other domains that are conserved to varying degrees: genes are also involved in petal identity specification in combina- an Intervening domain and a Keratin-like domain that facilitate tion with A-class genes, but they combine with C-class genes in the dimerization, and a C-terminal domain that is involved both in third whorl to specify androecium development, while the transcriptional activation and in connecting the protein to larger gynoecium in the fourth whorl is specified by C genes, but not protein complexes [5,13]. The 80-amino acid K domain features by A or B genes [1–7]. In all four whorls, E-class genes combine several (abcdefg)n heptad repeats, in which a and d residues are with A, B or C genes to specify organ identities [3,8,9]. In hydrophobic, forming three amphipathic a-helices (K1, K2 and Arabidopsis thaliana, there are two A genes, APETALA1 (AP1) and K3). These a-helices form a structure that is essential for APETALA2 (AP2), two B genes, APETALA3 (AP3) and PISTIL- dimerization, such as in the AP3/PI heterodimer required for PLOS ONE | www.plosone.org 1 January 2013 | Volume 8 | Issue 1 | e53019 Flora Developmental Genetics of a Paleoherb The origin of petals has been a popular topic of research and theory, and the function and evolution of the B-class genes have been central to such research because of their roles in petal development [22,24]. The history of B gene functional evolution is complex, however, since B gene expression has also been found in gymnosperm androecia and in other non-petal angiosperm organs, such as the staminodes of Aquilegia sp. [25–28]. The perianthless paleoherb S. chinensis provides a unique opportunity to study the genetics of floral development in a basal angiosperm, whose bracts are at least analogs of petals and perhaps the petaloidy of the bracts that subtend the flowers could share functional homology with second whorl petals of other taxa. In this work, we constructed tissue-specific cDNA libraries using suppression subtracted hybridization (SSH), and assigned the S. chinensis genes to functional categories. We then compared expression profiles of bracts subtending flowers, stamens and carpels using cDNA microarrays, and validated the results for key genes by qRT-PCR. We also performed phylogenetic analysis to compare S. chinensis B-class genes with their homologues in other plant species. Finally, we investigated B-class gene expression and transcript localization within subtending bracts and floral organs by in situ hybridization. Figure 1. Functional classification of unique S. chinensis ESTs Results according to the MIPS Functional Catalogue scheme. doi:10.1371/journal.pone.0053019.g001 Construction of forward and reverse subtracted cDNA libraries specification of petal and stamen identity in developing Arabidopsis To isolate transcripts with differential abundance between S. flowers [13–15]. chinensis leaves, subtending bracts, and floral organs, an inflores- Although most floral developmental genetics research initially cence-enriched cDNA library was constructed using suppression focused on the model eudicots Arabidopsis thaliana and Antirrhinum subtractive hybridization (SSH). Following two rounds of hybrid- majus, understanding the evolution of angiosperms will require ization and amplification, a set of forward and reverse subtracted research into the developmental genetics of flowers from diverse cDNAs of high quality were cloned to construct the forward and species across the phylogenetic tree of the angiosperm clade, with reverse SSH libraries. The positive control template in the special attention given to species of the basal lineages [16]. The Advantage cDNA PCR Kit was used to ensure the efficiency of phylogenetic position and unusual flower composition of the basal the PCR system. In addition, subtraction efficiency was verified by species Saururus chinensis render it attractive for the study of flower analysis of levels of the conserved a–tubulin control. The a- developmental genetics in general and MADS-box genes in TUBULIN (JK704891) band could be observed after 18 cycles of particular. This species is a member of Saururaceae, a family amplification from the unsubtracted cDNA population, while 28 which is a member of an early divergent angiosperm lineage cycles were necessary to amplify an observable a-TUBULIN (magnoliids) [16–18]. Inflorescences emerge sequentially, each product from the subtracted cDNA population. comprising a single
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