Dual Role of Tree Florigen Activation Complex Component FD in Photoperiodic Growth Control and Adaptive Response Pathways

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Dual Role of Tree Florigen Activation Complex Component FD in Photoperiodic Growth Control and Adaptive Response Pathways Dual role of tree florigen activation complex component FD in photoperiodic growth control and adaptive response pathways Szymon Tylewicza,1, Hiroyuki Tsujib,1, Pál Miskolczia,1, Anna Petterlea, Abdul Azeeza, Kristoffer Jonssona, Ko Shimamotob,2, and Rishikesh P. Bhaleraoa,c,3 aUmea Plant Science Center, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, S-901 87 Umea, Sweden; bLaboratory of Plant Molecular Genetics, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0192, Japan; and cCollege of Science, King Saud University, Riyadh 11362, Saudi Arabia Edited by Ronald R. Sederoff, North Carolina State University, Raleigh, NC, and approved January 27, 2015 (received for review December 9, 2014) A complex consisting of evolutionarily conserved FD, FLOWERING functionality. However, the mechanisms underlying the functional LOCUS T (FT) proteins is a regulator of floral transition. Intriguingly, diversity of the FT complexes and how they can participate in the FT orthologs are also implicated in developmental transitions dis- control of developmental pathways distinct from flowering are not tinct from flowering, such as photoperiodic control of bulbing in well understood because, in contrast to FT, FD or BRC1 (or other onions, potato tuberization, and growth cessation in trees. How- interactors of FT), which provide DNA binding ability to the ever, whether an FT–FD complex participates in these transitions complexes of FT and thus are crucial for the function of these and, if so, its mode of action, are unknown. We identified two complexes, have not been well characterized in pathways distinct closely related FD homologs, FD-like 1 (FDL1)andFD-like 2 (FDL2), from flowering. Thus, the role of complexes of FT and their mode in the model tree hybrid aspen. Using gain of function and RNAi- of action in these pathways remain poorly understood. suppressed FDL1 and FDL2 transgenic plants, we show that FDL1 Cessation of growth before the onset of winter is essential for and FDL2 have distinct functions and a complex consisting of FT and the survival of trees growing in temperate and boreal forests FDL1 mediates in photoperiodic control of seasonal growth. The during subsequent periods of low temperatures (12, 13). Growth downstream target of the FT–FD complex in photoperiodic control cessation is a photoperiodically controlled process (14, 15). In PLANT BIOLOGY “short days” (SDs), when day length falls below the critical of growth is Like AP1 (LAP1), a tree ortholog of the floral meristem threshold allowing growth, elongation growth ceases (14–16). identity gene APETALA1. Intriguingly, FDL1 also participates in the Moreover, the lamina of the last leaf primordia formed before transcriptional control of adaptive response and bud maturation the perception of SDs is aborted, and its stipules develop into pathways, independent of its interaction with FT, presumably via bud scales that enclose the embryonic leaves inside a bud at the interaction with ABSCISIC ACID INSENSITIVE 3 (ABI3) transcription apex (17). Thus, bud set results in termination of the emergence factor, a component of abscisic acid (ABA) signaling. Our data reveal of new leaves. SDs also concomitantly induce transcriptional FD that in contrast to its primary role in flowering, has dual roles in changes resulting in the so-called “adaptive response,” a meta- the photoperiodic control of seasonal growth and stress tolerance in bolic shift toward the accumulation of vegetative proteins and trees. Thus, the functions of FT and FD have diversified during evo- acquisition of cold hardiness that protect the shoot apical mer- lution, and FD homologs have acquired roles that are independent istem and embryonic leaves (18). of their interaction with FT. Significance growth cessation | bud set | seasonal growth | adaptive response | hybrid aspen Perennial plants display seasonal cycles of growth. For exam- ple, in the trees of boreal temperate forests, growth must he evolutionarily conserved protein FLOWERING LOCUS cease prior to the advent of winter and cold hardiness must be TT (FT) plays a key role in the control of flowering in plants acquired to survive extreme low temperature. Growth cessa- (1). Because FT lacks DNA binding activity, its interaction with tion and activation of transcriptional programs underlying – transcription factors, such as FD (2 4) and more recently iden- adaptive responses associated with cold hardiness are photo- tified BRANCHED1 (BRC1) (5), is critical for the formation of periodically controlled. We show that the evolutionarily con- protein complexes to control flowering via transcriptional con- served protein FD implicated in the control of flowering trol of downstream targets [e.g., floral meristem identity genes, mediates photoperiodic control of seasonal growth in trees by transcription factors APETALA1 (AP1)andOsMADS1]. Whereas forming a complex with FLOWERING LOCUS T (FT) protein. FD the FT–FD complex promotes flowering at the shoot apical genes of hybrid aspen display neofunctionalization and, in meristem (4), BRC1 appears to delay floral transition at the ax- contrast to Arabidopsis, have evolved functions that are in- illary meristem (5). These findings indicate that depending upon dependent of their interaction with FT, such as transcriptional its interaction partner, FT-containing complexes can have dis- control of the adaptive response and bud maturation path- tinct roles. The structure of FT–FD complex elucidated in rice ways in trees. has shown that a 14-3-3 protein mediates the interaction between rice FT homolog HEADING DATE 3a (Hd3a) and FD homolog Author contributions: K.S. and R.P.B. designed research; S.T., H.T., P.M., A.P., A.A., and K.J. OsFD1 via the C-terminally located SAP (serine alanine proline) performed research; S.T., H.T., P.M., A.P., A.A., K.J., K.S., and R.P.B. analyzed data; and S.T. and R.P.B. wrote the paper. motif in OsFD1 to generate the active nuclear localized florigen activation complex (3). The authors declare no conflict of interest. Interestingly, FT homologs are also involved in the control of This article is a PNAS Direct Submission. diverse developmental transitions distinct from flowering, such as 1S.T., H.T., and P.M. contributed equally to this work. tuberization in potatoes (6), bulb formation in onions (7), stomatal 2Deceased September 28, 2013. opening (8), and photoperiodic control of seasonal growth in trees 3To whom correspondence should be addressed. Email: [email protected]. – (9 11). These observations suggest that complexes of FT are not This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. only important to the control of flowering but have a broader 1073/pnas.1423440112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1423440112 PNAS Early Edition | 1of6 Downloaded by guest on September 25, 2021 Several studies have shown that the tree ortholog of Arabidopsis FT plays an important role in photoperiodic control of growth cessation (9–11). For example, down-regulation of FT2 expres- sion by SDs is a key early event in the induction of growth ces- sation (9). Importantly, functional studies have shown that overexpression of FT2 or its paralog FT1 in hybrid aspen (P. tremula × tremuloides) attenuates SD responses and abolishes growth cessation, whereas suppression of FT expression leads to earlier growth cessation than in WT plants (9–11). The MADS box transcription factor LAP1 (Like-APETALA1), a tree homolog of AP1, has been recently identified as a target of SDs down- stream of FT (19). Like FT, LAP1 overexpression delays SD- mediated growth cessation, whereas its down-regulation causes early growth cessation in SDs (19). These findings clearly dem- onstrate that as in flowering, FT plays a central role in photope- riodic control of seasonal growth in trees. In addition to FT, FD is a key component of the FT–FD complex, given its role in selection of downstream targets by the FT–FD complex. However, in contrast to FT, there are few studies addressing the role of FD other than in flowering (8, 20). Therefore, to improve understanding of the photoperiodic con- trol of seasonal growth, we initiated analysis of FD homologs in the model tree hybrid aspen. Functional analyses in hybrid aspen of the two closely related FD homologs FD-like 1 (FDL1)and A D FD-like 1 (FDL2) show that they have distinct roles. We show that Fig. 1. Bud formation in WT and FDL1oe (lines 3A and 5A) plants. , ,and G represent plants growing in long days (LD). WT plants had ceased growth FDL1 interacts with FT2 to form a complex that mediates in pho- B C E H toperiodic control of seasonal growth. Most previously published and developed buds ( and ), but the FDL1oe plants had not ( and ). – (F and I) FDL1oe plants set buds after 10 wk (W) of SDs. Arrows indicate data suggest that FD functions primarily in a complex with FT (2 4, apical buds. 20). However, we show that FDL1 has additional roles in trees, inde- pendent of its interaction with FT. Thus, the function of the FT–FD complex has diversified during evolution, and FD homologs have stems from differences in their ability to interact with FT or, al- acquired novel roles that are independent of its interaction with FT. ternatively, whether both FDLs can interact with FT but the FDL1–FT complex differs in function from the FDL2–FT com- Results plex. To differentiate between these two possibilities, we used two FDL1 and FDL2 Have Distinct Functions. We cloned full-length approaches. First, we used bimolecular fluorescence complemen- cDNAs for two highly similar FD-like genes, FDL1 and FDL2,from tation (BiFC) (21) to investigate interaction between hybrid aspen hybrid aspen, which encode 168-aa and 302-aa proteins, re- FT and FDL proteins (Fig. S5). BiFC assays indicate that YFP spectively. The larger size of FDL2 is due to an insertion at the C fluorescence is observed only when FT1 or FT2 fused to C-ter- terminus (Fig.
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