Analysis of the CYC/TB1 class of TCP transcription factors in basal angiosperms and magnoliids

Abstract

SUMMARYFlower monosymmetry contributes to specialized interactions between plants and their insect pollinators. In the magnoliids, flower monosymmetry is exhibited only in the Aristolochiaceae (Piperales). Aristolochia flowers develop a calyx-derived monosymmetric perianth that enhances pollination success by a flytrap mechanism. Aristolochia arborea forms additionally a special perianth outgrowth that mimics a mushroom to attract flies, the mushroom mimicry structure (MMS). In core eudicots, members of the CYC2 clade of TCP transcription factors are key regulators of corolla monosymmetry establishment. The CYC2 clade arose via core eudicot-specific duplications from ancestral CYC/TB1 genes. CYC/TB1 genes are also thought to affect monosymmetry formation in early diverging eudicot and monocot species. Here, we demonstrate that CYC/TB1 genes, named CYC-like genes (CYCL) are present in basal angiosperms and magnoliids. Expression analyses in A. arborea indicate that CYCL genes participate in perianth and MMS differentiation processes and do not support a CYCL gene function in initial flower monosymmetry formation. Heterologous CYCL and CYC2 gene overexpression studies in Arabidopsis show that Aristolochia CYCL proteins only perform a CYC2-like function when the CYCL TCP domain is replaced by a CYC2 domain. Comparative TCP domain analyses revealed that an LxxLL motif, known to mediate protein-protein interactions, evolved in the second helix of the TCP domain in the CYC2 lineage and contributes to CYC2-related functions. Our data imply that divergent evolution of the CYC/TB1 lineages caused significant changes in their coding regions, which together with cis-regulatory changes established the key CYC2 function in regulating eudicot flower monosymmetry.

TCP Transcription Factors at the Interface between Environmental Challenges and the Plant’s Growth Responses

“…TCP effect on floral development was shown in a wide range of plant species, including Arabidopsis , Antirrhinum, annual candytuft ( Iberis amara ) (Busch and Zachgo, 2007; Busch et al, 2012), angiosperms like Aristolochia arborea and Saruma henryi (Horn et al, 2015), Gerbera species (Broholm et al, 2008), rice (Yuan et al, 2009), sunflowers (Fambrini et al, 2012), peas (Wang et al, 2008), ragworts (Kim et al, 2008), Morrow’s honeysuckle ( Lonicera morrowii ) (Howarth and Donoghue, 2006), Knautia macedonica (Berger et al, 2016), and orchids (De Paolo et al, 2015). …”

“… Phylogenetic tree of plant species in which TCP transcription factors are involved in branching (Takeda et al, 2003; Aguilar-Martínez et al, 2007; Poza-Carrión et al, 2007; Bai et al, 2012; Braun et al, 2012; Drummond et al, 2015; Nicolas et al, 2015; Muhr et al, 2016) (blue dots), flower development (Linnaeus and Rudberg, 1744; Keeble et al, 1910; Corley et al, 2005; Costa et al, 2005; Busch and Zachgo, 2007; Broholm et al, 2008; Kim et al, 2008; Nag et al, 2009; Yuan et al, 2009; Howarth et al, 2011; Busch et al, 2012; Tähtiharju et al, 2012; Claßen-Bockhoff et al, 2013; Juntheikki-Palovaara et al, 2014; De Paolo et al, 2015; Horn et al, 2015; Lucero et al, 2015; Wang et al, 2008; Wang X.et al, 2015; Yang et al, 2015; Berger et al, 2016) (purple dots) or leaf development (Kosugi and Ohashi, 1997; Nath et al, 2003; Palatnik et al, 2003; Koyama et al, 2007, 2010a,b; Ori et al, 2007; Efroni et al, 2008; Kieffer et al, 2011; Mimida et al, 2011; Sarvepalli and Nath, 2011; Danisman et al, 2012, 2013; Aguilar-Martínez and Sinha, 2013; Burko et al, 2013; Tao et al, 2013; Zhou et al, 2013; Ballester et al, 2015; Huang and Irish, 2015; Ma et al, 2016) (green dots), respectively. The phylogenetic tree was created using Phylotree and iTOL (Letunic and Bork, 2016).…”

Letter to the 21st century botanist: “What is a flower?” 6. The evo-devo of floral symmetry

“…Nicolas and Cubas 2016). More precisely, they belong to the class II CYC/TB1 subclade that seems to originate in the ancestor of angiosperms (Horn et al 2015). RADIALIS (RAD) and DIVARICATA (DIV) belong to another family of transcription factor genes, the MYB family.…”

“…Second from the genetic and molecular standpoints, a CYC/TB1-based candidate gene approach has been implemented over the past 25 years, exploring the orders Piperales (Magnoliidae), Zingiberales, Commelinales and Poales (Monocotyledonae), Ranunculales and Proteales (basal eudicots), Malpighiales, Fabales and Brassicales (Rosidae), and Lamiales, Dipsacales and Asterales (Asteridae) (Hileman 2014 for review; Citerne et al 2017;Horn et al 2015). These studies have revealed a complex history of duplications in the CYC/TB1 gene lineage.…”

“…While very few data are available on the expression pattern of CYC/TB1 genes in ancestrally actinomorphic species (Horn et al 2015), various alterations have been associated with reversals from zygomorphy to actinomorphy. First, absent or downregulated expression (often with residual expression early in development as in Bournea leiophylla (W.T.…”