Szymon Tylewicz, Hiroyuki Tsuji, Pál Miskolczi, Anna Petterle, Abdul Azeez, Kristoffer Jonsson, Ko Shimamoto, and Rishikesh P. Bhalerao

Significance

Perennial plants display seasonal cycles of growth. For example, in the trees of boreal temperate forests, growth must cease prior to the advent of winter and cold hardiness must be acquired to survive extreme low temperature. Growth cessation and activation of transcriptional programs underlying adaptive responses associated with cold hardiness are photoperiodically controlled. We show that the evolutionarily conserved protein FD implicated in the control of flowering mediates photoperiodic control of seasonal growth in trees by forming a complex with FLOWERING LOCUS T (FT) protein. FD genes of hybrid aspen display neofunctionalization and, in contrast to Arabidopsis, have evolved functions that are independent of their interaction with FT, such as transcriptional control of the adaptive response and bud maturation pathways in trees.

Abstract

A complex consisting of evolutionarily conserved FD, FLOWERING LOCUS T (FT) proteins is a regulator of floral transition. Intriguingly, FT orthologs are also implicated in developmental transitions distinct from flowering, such as photoperiodic control of bulbing in onions, potato tuberization, and growth cessation in trees. However, whether an FT–FD complex participates in these transitions and, if so, its mode of action, are unknown. We identified two closely related FD homologs, FD-like 1 (FDL1) and FD-like 2 (FDL2), in the model tree hybrid aspen. Using gain of function and RNAi-suppressed FDL1 and FDL2 transgenic plants, we show that FDL1 and FDL2 have distinct functions and a complex consisting of FT and FDL1 mediates in photoperiodic control of seasonal growth. The downstream target of the FT–FD complex in photoperiodic control of growth is Like AP1 (LAP1), a tree ortholog of the floral meristem identity gene APETALA1. Intriguingly, FDL1 also participates in the transcriptional control of adaptive response and bud maturation pathways, independent of its interaction with FT, presumably via interaction with ABSCISIC ACID INSENSITIVE 3 (ABI3) transcription factor, a component of abscisic acid (ABA) signaling. Our data reveal that in contrast to its primary role in flowering, FD has dual roles in the photoperiodic control of seasonal growth and stress tolerance in trees. Thus, the functions of FT and FD have diversified during evolution, and FD homologs have acquired roles that are independent of their interaction with FT.

See http://www.pnas.org/content/112/10/3140.abstract.html?etoc

PNAS March 10, 2015 vol. 112 no. 10 3140-3145

Fig. 1.

Bud formation in WT and FDL1oe (lines 3A and 5A) plants. A, D, and G represent plants growing in long days (LD). WT plants had ceased growth and developed buds (B and C), but the FDL1oe plants had not (E and H). (F and I) FDL1oe plants set buds after 10 wk (W) of SDs. Arrows indicate apical buds.