Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus

Abstract

SUMMARYMembers of the CENTRORADIALIS (CEN)/TERMINAL FLOWER 1 (TFL1) subfamily control shoot meristem identity, and loss-of-function mutations in both monopodial and sympodial herbaceous plants result in dramatic changes in plant architecture. We studied the degree of conservation between herbaceous and woody perennial plants in shoot system regulation by overexpression and RNA interference (RNAi)-mediated suppression of poplar orthologs of CEN, and the related gene MOTHER OF FT AND TFL 1 (MFT). Field study of transgenic poplars (Populus spp.) for over 6 years showed that downregulation of PopCEN1 and its close paralog, PopCEN2, accelerated the onset of mature tree characteristics, including age of first flowering, number of inflorescences and proportion of short shoots. Surprisingly, terminal vegetative meristems remained indeterminate in PopCEN1-RNAi trees, suggesting the possibility that florigen signals are transported to axillary mersitems rather than the shoot apex. However, the axillary inflorescences (catkins) of PopCEN1-RNAi trees contained fewer flowers than did wild-type catkins, suggesting a possible role in maintaining the indeterminacy of the inflorescence apex. Expression of PopCEN1 was significantly correlated with delayed spring bud flush in multiple years, and in controlled environment experiments, 35S::PopCEN1 and RNAi transgenics required different chilling times to release dormancy. Considered together, these results indicate that PopCEN1/PopCEN2 help to integrate shoot developmental transitions that recur during each seasonal cycle with the age-related changes that occur over years of growth.

EARLY BUD-BREAK 1 (EBB1) is a regulator of release from seasonal dormancy in poplar trees

“…CEN is known as TERMINAL FLOWER1 (TFL1) in Arabidopsis and is a repressor of flowering (33). Similar to Arabidopsis, PopCEN1 overexpression delayed flowering, whereas RNAi suppression of both paralogs (PopCEN1 and PopCEN2) accelerated flowering in poplar (34). In support of the growing body of evidence for a link between regulation of flowering and bud phenology in perennials (35), PopCEN1 overexpressors displayed delayed bud-break, whereas RNAi transgenics showed precocious bud flush (34).…”

Mutation inTERMINAL FLOWER1Reverses the Photoperiodic Requirement for Flowering in the Wild StrawberryFragaria vesca

“…Natural variation in TFL1 homologs has been important for the domestication and crop improvement of several annual crops (Turnbull, 2011), and our study shows the importance of TFL1 in the perennial context. As TFL1 homologs exist in all angiosperms (Karlgren et al, 2011) and their function as floral repressors is conserved between plant families (Shannon and Meeks-Wagner, 1991;Foucher et al, 2003;Kotoda et al, 2006;Mohamed et al, 2010;Imamura et al, 2011), our findings are of general significance for understanding the regulation of flowering-and perennial-specific traits in a wide range of economically important crops.…”

“…and F. vesca (Brown and Wareing, 1965;Iwata et al, 2012). Furthermore, TFL1 homologs have been shown to repress flowering and to control the length of the juvenile phase in apple (Malus domestica), Populus, and A. alpina (Kotoda et al, 2006;Mohamed et al, 2010;Wang et al, 2011).…”

Tracing a key player in the regulation of plant architecture: the columnar growth habit of apple trees (Malus × domestica)

“…For instance, Populus has several wuschel and shoot meristemless orthologs, which in addition to regulating stem cell maintenance in the SAM also play a similar role in the vascular cambium (Schrader et al 2004;Groover 2005;Groover et al 2006;Bao et al 2009). With regard to the regulation of flowering, Populus has two orthologs of FT (see below), TFL 1 (Mohamed et al 2010) and agamous (Brunner et al 2000), respectively, and in apple, two leafy orthologs with different expression patterns and thus possibly different functions can be detected (Wada et al 2002). Functional differences of certain genes in Arabidopsis and trees have been reported, especially in the case of heterologous transformation (Gocal et al 2001;Flachowsky et al 2010).…”

“…FT transcription gradually increases during the juvenile phase (Böhlenius et al 2006), and Populus plants overexpressing the FT homologs FT1 or FT2 as well as plum plants transformed with poplar FT1 show an early flowering phenotype (Böhlenius et al 2006;Hsu et al 2006Hsu et al , 2011Srinivasan et al 2012). Downregulation of the Populus TFL homologs Populus Centroradialis 1 (PopCEN1) and Populus Centroradialis 2 (PopCEN2) leads to precocious maturity (Mohamed et al 2010). In addition, miR156 and miR172 contribute to the control of vegetative phase change (reviewed in Huijser and Schmid 2011).…”