FLOWERING LOCUS T paralogs control the annual growth cycle in Populus trees

Abstract

In temperate and boreal regions, perennials adapt their annual growth cycle to the change of seasons. These adaptations ensure survival in harsh environmental conditions, allowing growth at different latitudes and altitudes, and are therefore tightly regulated. Populus tree species cease growth and form terminal buds in autumn when photoperiod falls below a certain threshold.1Böhlenius H. Huang T. Charbonnel-Campaa L. Brunner A.M. Jansson S. Strauss S.H. Nilsson O. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees.Science. 2006; 312: 1040-1043https://doi.org/10.1126/science.1126038Crossref PubMed Scopus (768) Google Scholar This is followed by establishment of dormancy and cold hardiness over the winter. At the center of the photoperiodic pathway in Populus is the gene FLOWERING LOCUS T2 (FT2), which is expressed during summer and harbors significant SNPs in its locus associated with timing of bud set.1Böhlenius H. Huang T. Charbonnel-Campaa L. Brunner A.M. Jansson S. Strauss S.H. Nilsson O. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees.Science. 2006; 312: 1040-1043https://doi.org/10.1126/science.1126038Crossref PubMed Scopus (768) Google Scholar, 2Hsu C.-Y. Liu Y. Luthe D.S. Yuceer C. Poplar FT2 shortens the juvenile phase and promotes seasonal flowering.Plant Cell. 2006; 18: 1846-1861https://doi.org/10.1105/tpc.106.041038Crossref PubMed Scopus (249) Google Scholar, 3Hsu C.-Y. Adams J.P. Kim H. No K. Ma C. Strauss S.H. Drnevich J. Vandervelde L. Ellis J.D. Rice B.M. et al.FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar.Proc. Natl. Acad. Sci. USA. 2011; 108: 10756-10761https://doi.org/10.1073/pnas.1104713108Crossref PubMed Scopus (306) Google Scholar, 4Wang J. Ding J. Tan B. Robinson K.M. Michelson I.H. Johansson A. Nystedt B. Scofield D.G. Nilsson O. Jansson S. et al.A major locus controls local adaptation and adaptive life history variation in a perennial plant.Genome Biol. 2018; 19: 1-17https://doi.org/10.1186/s13059-018-1444-yCrossref PubMed Scopus (41) Google Scholar The paralogous gene FT1, on the other hand, is hyper-induced in chilling buds during winter.3Hsu C.-Y. Adams J.P. Kim H. No K. Ma C. Strauss S.H. Drnevich J. Vandervelde L. Ellis J.D. Rice B.M. et al.FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar.Proc. Natl. Acad. Sci. USA. 2011; 108: 10756-10761https://doi.org/10.1073/pnas.1104713108Crossref PubMed Scopus (306) Google Scholar,5Rinne P.L. Welling A. Vahala J. Ripel L. Ruonala R. Kangasjärvi J. van der Schoot C. Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1, 3-β-glucanases to reopen signal conduits and release dormancy in Populus.Plant Cell. 2011; 23: 130-146https://doi.org/10.1105/tpc.110.081307Crossref PubMed Scopus (303) Google Scholar Even though its function is so far unknown, it has been suggested to be involved in the regulation of flowering and the release of winter dormancy.3Hsu C.-Y. Adams J.P. Kim H. No K. Ma C. Strauss S.H. Drnevich J. Vandervelde L. Ellis J.D. Rice B.M. et al.FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar.Proc. Natl. Acad. Sci. USA. 2011; 108: 10756-10761https://doi.org/10.1073/pnas.1104713108Crossref PubMed Scopus (306) Google Scholar,5Rinne P.L. Welling A. Vahala J. Ripel L. Ruonala R. Kangasjärvi J. van der Schoot C. Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1, 3-β-glucanases to reopen signal conduits and release dormancy in Populus.Plant Cell. 2011; 23: 130-146https://doi.org/10.1105/tpc.110.081307Crossref PubMed Scopus (303) Google Scholar In this study, we employ CRISPR-Cas9-mediated gene editing to individually study the function of the FT-like genes in Populus trees. We show that while FT2 is required for vegetative growth during spring and summer and regulates the entry into dormancy, expression of FT1 is absolutely required for bud flush in spring. Gene expression profiling suggests that this function of FT1 is linked to the release of winter dormancy rather than to the regulation of bud flush per se. These data show how FT duplication and sub-functionalization have allowed Populus trees to regulate two completely different and major developmental control points during the yearly growth cycle.

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