FT-like proteins induce transposon silencing in the shoot apex during floral induction in rice

Abstract

Floral induction is a crucial developmental step in higher plants. Florigen, a mobile floral activator that is synthesized in the leaf and transported to the shoot apex, was recently identified as a protein encoded by FLOWERING LOCUS T (FT) and its orthologs; the rice florigen is Heading date 3a (Hd3a) protein. The 14-3-3 proteins mediate the interaction of Hd3a with the transcription factor OsFD1 to form a ternary structure called the florigen activation complex on the promoter of OsMADS15, a rice APETALA1 ortholog. However, crucial information, including the spatiotemporal overlap among FT-like proteins and the components of florigen activation complex and downstream genes, remains unclear. Here, we confirm that Hd3a coexists, in the same regions of the rice shoot apex, with the other components of the florigen activation complex and its transcriptional targets. Unexpectedly, however, RNA-sequencing analysis of shoot apex from wild-type and RNA-interference plants depleted of florigen activity revealed that 4,379 transposable elements (TEs; 58% of all classifiable rice TEs) were expressed collectively in the vegetative and reproductive shoot apex. Furthermore, in the reproductive shoot apex, 214 TEs were silenced by florigen. Our results suggest a link between floral induction and regulation of TEs.floral transition | FT-like proteins | shoot apical meristem | transposable elements | rice F loral induction has been studied extensively over the years, and the use of molecular genetics in the model species Arabidopsis thaliana has been particularly successful in identifying genes and genetic pathways that are involved in flower development (1-3). Several key flowering genes sense environmental conditions and activate the proper expression of genes that are essential for floral induction. Once floral induction occurs, further key genes positively and negatively regulate each other in the shoot apex and activate flower identity genes, eventually leading to the formation of flowers (1-3).One of the critical molecules for floral induction is florigen, a mobile floral activator that is produced in leaves and transported to the shoot apex. Many studies now indicate that proteins encoded by Arabidopsis FLOWERING LOCUS T (FT) and its orthologs in other species are florigens (4-8). Transcription of florigen genes is tightly regulated by environmental conditions, and florigen protein is transported from leaves to the shoot apex where it induces the expression of downstream genes to ensure proper flower development. Despite its important role in floral induction, many questions about florigen remain unresolved. They include its molecular function, mechanism of transport, localization in the shoot apex, and the identities of its downstream genes.Rice is a short-day (SD) plant and has two florigens, Heading date 3a (Hd3a) and RICE FLOWERING LOCUS T1 (RFT1), which predominate, respectively, under SD and long-day (LD) conditions (7, 9). When GFP fusions of Hd3a and RFT1 are expressed under their own promoters, GFP fluorescence...

Regulation of Histone Methylation and Reprogramming of Gene Expression in the Rice Inflorescence Meristem

“…This is consistent with previous data showing that many TE genes are transcriptionally active in maize shoot meristems (Ohtsu et al, 2007;Li et al, 2010;Martínez and Slotkin, 2012). In particular, a recent work showed that many TEs are transcribed in rice vegetative and reproductive shoot apex (Tamaki et al, 2015). The mechanism of release of the TE silencing in meristems is not clear.…”

Antagonistic Transcription Factor Complexes Modulate the Floral Transition in Rice

“…Under inductive photoperiods, both Hd3a and RFT1 are transcribed, and their protein products are essential for flowering to the extent that artificial reduction of their mRNA expression results in never-flowering plants (Komiya et al, 2008;Tamaki et al, 2015). However, transcription of RFT1 can be induced also under long days (LDs), and its floral promotive activity under these conditions contributes to the facultative nature of the photoperiodic flowering response of rice (Gómez-Ariza et al, 2015;Komiya et al, 2009).…”

“…Transcription of Ehd1, Hd3a, and RFT1 thus correlates under SD in leaves, showing a transient induction that persists only for the time required to irreversibly commit flowering at the SAM (Galbiati et al, 2016;Doi et al, 2004;Cho et al, 2016;Komiya et al, 2008). Once a sufficient amount of Hd3a and/or RFT1 proteins reaches the SAM, expression of target genes that promote inflorescence formation is induced (Taoka et al, 2011;Tamaki et al, 2015).…”

“…The rice FAC is a transcriptional activation complex assembled in cells of the SAM by Hd3a or RFT1, a Gf14 protein and OsFD1, and its primary targets include members of the OsMADS transcription factor family (Kojima et al, 2002;Taoka et al, 2011;Tsuji et al, 2013;Tamaki et al, 2015;Kobayashi et al, 2012). It has been proposed that FAC complexes control a wide range of developmental processes in distinct tissues of several plant species, but to which extent a FAC might function outside of the SAM and in rice leaf tissues is unclear.…”

A Universal Positive-Negative Selection System for Gene Targeting in Plants Combining an Antibiotic Resistance Gene and Its Antisense RNA

“…In earlier studies in higher plants, most transferred DNA (T-DNA) containing sequences homologous to the endogenous target gene was found to have integrated randomly into the plant genome through the nonhomologous end joining (NHEJ) pathway, leading to decreased GT frequency (0.01%-0.1% compared with random integration; Paszkowski et al, 1988;Offringa et al, 1990;Puchta et al, 1996). More recently, GT has developed to become a reproducible and general approach, at least in rice (Oryza sativa), through the use of a positive-negative selection system with the hygromycin resistance gene as a positive selection marker and the diphtheria toxin A subunit (DT-A) gene as a negative selection marker (Terada et al, 2002(Terada et al, , 2007Yamauchi et al, 2009;Moritoh et al, 2012;Ono et al, 2012;Ozawa et al, 2012;Dang et al, 2013;Tamaki et al, 2015). Toxic to rice plants, expression of DT-A is also toxic in some dicots, such as Arabidopsis (Arabidopsis thaliana; Czakó et al, 1992; Thorsness et al, 1993;Day et al, 1995;Nilsson et al, 1998;Tsugeki and Fedoroff, 1999;Weijers et al, 2003), tobacco (Nicotiana tabacum; Czakó et al, 1992;Day et al, 1995;Twell, 1995;Uk Kim et al, 1998), and Brassica campestris (Lee et al, 2003).…”