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. 2011 Jun 28;108(26):10756-61.
doi: 10.1073/pnas.1104713108. Epub 2011 Jun 8.

FLOWERING LOCUS T Duplication Coordinates Reproductive and Vegetative Growth in Perennial Poplar

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Free PMC article

FLOWERING LOCUS T Duplication Coordinates Reproductive and Vegetative Growth in Perennial Poplar

Chuan-Yu Hsu et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

Annual plants grow vegetatively at early developmental stages and then transition to the reproductive stage, followed by senescence in the same year. In contrast, after successive years of vegetative growth at early ages, woody perennial shoot meristems begin repeated transitions between vegetative and reproductive growth at sexual maturity. However, it is unknown how these repeated transitions occur without a developmental conflict between vegetative and reproductive growth. We report that functionally diverged paralogs FLOWERING LOCUS T1 (FT1) and FLOWERING LOCUS T2 (FT2), products of whole-genome duplication and homologs of Arabidopsis thaliana gene FLOWERING LOCUS T (FT), coordinate the repeated cycles of vegetative and reproductive growth in woody perennial poplar (Populus spp.). Our manipulative physiological and genetic experiments coupled with field studies, expression profiling, and network analysis reveal that reproductive onset is determined by FT1 in response to winter temperatures, whereas vegetative growth and inhibition of bud set are promoted by FT2 in response to warm temperatures and long days in the growing season. The basis for functional differentiation between FT1 and FT2 appears to be expression pattern shifts, changes in proteins, and divergence in gene regulatory networks. Thus, temporal separation of reproductive onset and vegetative growth into different seasons via FT1 and FT2 provides seasonality and demonstrates the evolution of a complex perennial adaptive trait after genome duplication.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Year-round normal expression of FT1 and FT2 in the same five above-ground tissues of mature P. deltoides. (A) Monthly high/low temperatures and day length in Mississippi, where experimental trees were grown. Error bars show SD about the mean. (B and C) Relative fold change in transcript levels of FT1 (B) or FT2 (C) relative to the lowest amount of expression within a tissue. (B) FT1 transcripts are abundant in all the analyzed tissues in winter. Dashed lines indicate missing samples. (C) FT2 transcripts are abundant in leaves and reproductive buds in spring and summer.
Fig. 2.
Fig. 2.
Regulation of FT1 and FT2 in P. deltoides. (A) FT1 transcript abundance increased in dormant trees (n = 12) at 4 °C under short-day conditions. When six trees were transferred to 25 °C after 90 d of 4 °C treatment, FT1 was undetectable. FT2 transcripts were undetectable in the identical tissues. (B) In winter, FT1 transcripts were more abundant in mature dormant trees in the field at ambient conditions (SM-A; n = 3), in mature dormant trees in pots at ambient conditions (M-A; n = 3), in mature dormant trees in pots at 4 °C in continuous darkness (M-4 °C-D; n = 3), or in mature dormant trees in pots at ambient conditions in long-day conditions (M-A-LD; n = 3) than in mature dormant trees in pots at 25 °C under short-day conditions (M-25 °C-SD; n = 3). FT2 transcripts were not detected in the identical tissues. (C) FT2 transcripts were more abundant in long-day than in short-day conditions at 25 °C. FT1 transcripts were undetectable in the identical tissues. (D) Treatment at 4 °C repressed FT2 transcription (n = 3) in trees grown for 14 d at 4 °C and 25 °C. In contrast, FT1 transcripts increased slightly in abundance at 4 °C. Error bars indicate SD. **P ≤ 0.005 and ***P ≤ 0.0005 within a treatment.
Fig. 3.
Fig. 3.
Functional and network analyses of FT1 and FT2 in poplar. (A) Trees (P. tremula × P. tremuloides 353) harboring ProHSP:FT1 and ProHSP:FT2 (n = 30) were treated at 37 °C and 40 °C under long-day conditions to determine reproductive onset. (Right) (Upper) Red arrows show terminal inflorescences. (Lower) Black arrows show axillary inflorescences. (Left) FT1 (Upper) and FT2 (Lower) transcript abundance was determined in leaves of trees (P. tremula x P. tremuloides 353) harboring ProHSP:FT1 and ProHSP:FT2, in leaves of trees (P. tremula × P. alba 717) harboring Pro35S:FT1 and Pro35S:FT2, and in leaves of normally growing mature P. deltoides (controls) in February and May. ***P ≤ 0.0001 within a treatment. (B) (Left) Heat maps showing year-round normal expression of genes downstream of FT1 and FT2 (Dataset S2) in mature P. deltoides. (Left) Clusters on the left represent modules. The column on the right shows up-regulated (red) and down-regulated (blue) genes downstream of FT1, downstream of FT2, or downstream of both FT1 and FT2 commonly expressed in Pro35S:FT1 and ProHSP:FT1, and Pro35S:FT2 and ProHSP:FT2. Months from September (S) to June (Jn) are identified below the heat maps. SDs are shown below the heat maps. (Right) Pie charts show functional categorization of similar Gene Ontology Biological Process terms. Numbers in parenthesis represent partitioning of overall percentages into up (↑) and down (↓) percentages. n, number of genes.
Fig. 4.
Fig. 4.
A schematic integrated model showing that FT1 and FT2 regulate cycles of reproductive and vegetative growth. When FT1 transcription is triggered by winter temperature, it induces reproductive onset through a network of downstream genes in a small number of axillary meristems in dormant buds, resulting in reproductive buds in the Floral Zone. Conversely, in response to warm temperatures, long days, and multiple stress factors in the following growing season, FT2, through its molecular networks, regulates vegetative growth.

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