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

Abstract

Plants are sessile and as such their reactions to environmental challenges differ from those of mobile organisms. Many adaptions involve growth responses and hence, growth regulation is one of the most crucial biological processes for plant survival and fitness. The plant-specific TEOSINTE BRANCHED 1, CYCLOIDEA, PCF1 (TCP) transcription factor family is involved in plant development from cradle to grave, i.e., from seed germination throughout vegetative development until the formation of flowers and fruits. TCP transcription factors have an evolutionary conserved role as regulators in a variety of plant species, including orchids, tomatoes, peas, poplar, cotton, rice and the model plant Arabidopsis. Early TCP research focused on the regulatory functions of TCPs in the development of diverse organs via the cell cycle. Later research uncovered that TCP transcription factors are not static developmental regulators but crucial growth regulators that translate diverse endogenous and environmental signals into growth responses best fitted to ensure plant fitness and health. I will recapitulate the research on TCPs in this review focusing on two topics: the discovery of TCPs and the elucidation of their evolutionarily conserved roles across the plant kingdom, and the variety of signals, both endogenous (circadian clock, plant hormones) and environmental (pathogens, light, nutrients), TCPs respond to in the course of their developmental roles.

Keywords: TCP; development; evolution; plant hormones; signaling; transcription factor.

FIGURE 1

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).

FIGURE 2

Hormonal pathways associated with Arabidopsis TCP transcription factors and orthologs. The proteins were plotted according to their phylogenetic similarity using PhyML and TreeDyne (Dereeper et al., 2008). AA, abscisic acid; AX, auxin; BR, brassinosteroids; CK, cytokinin; ET, ethylene; GA, gibberellic acid; JA, jasmonic acid; SA, salicylic acid; SL, strigolactones.

FIGURE 3

Interactions of TCP transcription factors with components of the circadian clock both within the central clock circuitry and in downstream processes. Class I and class II TCPs are depicted in green and blue, respectively. Known clock components are depicted in gray. Proteins are represented as circles, genes in squares. Dimers are depicted as overlapping circles. CCA1 inhibition by TCP21 is abolished by dimerization of TCP21 with TOC1. The CCA1/LHY dimer inhibits TCP21 expression (Pruneda-Paz et al., 2009). The effect of nine TCPs that bind to the CCA1 promoter in yeast one-hybrid studies is unknown (Pruneda-Paz et al., 2014). Downstream of the clock, TCP/clock component heterodimers regulate rhythmic expression of mitochondrial proteins depending on the number and arrangement of TCP binding sites in the mitochondrial gene promoters (Giraud et al., 2010).

FIGURE 4

Schematic figure depicting the diversity of environmental signals that affect TCP functions in plants (Mukhtar et al., 2011; Sugio et al., 2011; Balsemão-Pires et al., 2013; González-Grandío et al., 2013; Niwa et al., 2013; Viola et al., 2013, 2016; Guan et al., 2014; Hu et al., 2014; Kim et al., 2014; Mukhopadhyay et al., 2015; Nicolas et al., 2015; Kumar et al., 2016).