Distinct Regulatory Changes Underlying Differential Expression of TEOSINTE BRANCHED1-CYCLOIDEA-PROLIFERATING CELL FACTOR Genes Associated with Petal Variations in Zygomorphic Flowers of Petrocosmea spp. of the Family Gesneriaceae  

Abstract

CYCLOIDEA (CYC)-like genes, belonging to the plant-specific TCP transcription factor family that is named after TEOSINTE BRANCHED1 (TB1) from maize (Zea mays), CYC from Antirrhinum majus, and the PROLIFERATING CELL FACTORS (PCF) from rice (Oryza sativa), have conserved dorsal identity function in patterning floral zygomorphy mainly through specific expression in dorsal petals of a flower. Their expression changes are usually related to morphological diversity of zygomorphic flowers. However, it is still a challenge to elucidate the molecular mechanism underlying their expression differentiation. It is also unknown whether CINCINNATA (CIN )-like TCP genes, locally controlling cell growth and proliferation, are involved in the evolution of floral zygomorphy. To address these questions, we selected two closely related species, i.e. Petrocosmea glabristoma and Petrocosmea sinensis, with distinct petal morphology to conduct expression, hybridization, mutant, and allele-specific expression analyses. The results show that the size change of the dorsal petals between the two species is mainly mediated by the expression differentiation of CYC1C and CYC1D, while the shape variation of all petals is related to the expression change of CIN1. In reciprocal F1 hybrids, the expression of CYC1C, CYC1D, and CIN1 conforms to an additive inheritance mode, consistent with the petal phenotypes of hybrids. Through allele-specific expression analyses, we find that the expression differentiation of these TCP genes is underlain by distinctly different types of regulatory changes. We suggest that highly redundant paralogs with identical expression patterns and interspecific expression differentiation may be controlled by remarkably different regulatory pathways because natural selection may favor different regulatory modifications rather than coding sequence changes of key developmental genes in generating morphological diversity.

Temporal, but not spatial, changes in expression patterns of petal identity genes are associated with loss of papillate conical cells and the shift to bird pollination in Macaronesian Lotus (Leguminosae)

“…; Yang et al . ). To our knowledge, this is the first report of an association between changes of CYCLOIDEA genes and modifications to petal micromorphology and identity.…”

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

“… 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).…”

Evolving Tale of TCPs: New Paradigms and Old Lacunae

“…Characterization of TB1 orthologs from monocots, such as rice ( Fine culm1 / OsTB1 ), barley ( INTERMEDIUM-C ), Sorghum ( SbTB1 ), and switchgrass ( PvTB1 ) and dicots, such as Arabidopsis ( BRC1 and BRC2 ), pea ( PsBRC1 ), and tomato ( SlBRC1 ) indicate conserved role of this gene in negatively regulating axillary bud outgrowth across both the lineages of angiosperms (Takeda et al, 2003; Kebrom et al, 2006; Aguilar-Martínez et al, 2007; Ramsay et al, 2011; Braun et al, 2012; Nicolas et al, 2015; Xu et al, 2016). Duplication and differential expression of CYC2 genes have played a key role in the evolution of symmetry across different lineages of the angiosperms (Luo et al, 1996; Reeves and Olmstead, 2003; Specht and Howarth, 2015; Yang et al, 2015). CYC ortholog of rice, RETARDED PALEA 1 ( REP1 ), also played a key role in regulating floral zygomorphy (Yuan et al, 2009).…”

“…Genes belonging to CIN clade ( TCP2 – 5, 10, 13, 17 , and 24 ) of class II have been mainly implicated in regulating flowering time, floral organ development, leaf development and senescence, and morphogenesis of lateral organs (Nath et al, 2003; Palatnik et al, 2003; Koyama et al, 2007; Schommer et al, 2008; Ballester et al, 2015; Yang et al, 2015). Some of the more recent roles reported include regulation of secondary cell wall thickening in roots and floral organs of Arabidopsis (Wang H. et al, 2015) and ovule development in Phalaenopsis equestris (Lin et al, 2016).…”