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      Age-dependent seasonal growth cessation in Populus

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          In natural forests, juvenile seedlings display different seasonal growth patterns to adult trees. We characterize the genetic and molecular base of this age-dependent seasonal growth in Populus trees. We show a regulatory aspect of the miR156-SPL3/5s module in perennial trees that is very different from its mechanism in annual plants. Our study reveals a genetic mechanism for an important climate adaptation, establishment, and survival strategy for trees of different ages in natural forests.

          Abstract

          In temperate and boreal regions, perennial plants adapt their annual growth cycle to the change of seasons. In natural forests, juvenile seedlings usually display longer growth seasons compared to adult trees to ensure their establishment and survival under canopy shade. However, how trees adjust their annual growth according to their age is not known. In this study, we show that age-dependent seasonal growth cessation is genetically controlled and found that the miR156-SPL3/5 module, a key regulon of vegetative phase change (VPC), also triggers age-dependent growth cessation in Populus trees. We show that miR156 promotes shoot elongation during vegetative growth, and its targets SPL3/5s function in the same pathway but as repressors. We find that the miR156-SPL3/5s regulon controls growth cessation in both leaves and shoot apices and through multiple pathways, but with a different mechanism compared to how the miR156-SPL regulon controls VPC in annual plants. Taken together, our results reveal an age-dependent genetic network in mediating seasonal growth cessation, a key phenological process in the climate adaptation of perennial trees.

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          Most cited references55

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          miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana.

          The FT gene integrates several external and endogenous cues controlling flowering, including information on day length. A complex of the mobile FT protein and the bZIP transcription factor FD in turn has a central role in activating genes that execute the switch from vegetative to reproductive development. Here we reveal that microRNA156-targeted SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes not only act downstream of FT/FD, but also define a separate endogenous flowering pathway. High levels of miR156 in young plants prevent precocious flowering. A subsequent day length-independent decline in miR156 abundance provides a permissive environment for flowering and is paralleled by a rise in SPL levels. At the shoot apex, FT/FD and SPLs converge on an overlapping set of targets, with SPLs directly activating flower-promoting MADS box genes, providing a molecular substrate for both the redundant activities and the feed-forward action of the miR156/SPL and FT/FD modules in flowering control.
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            Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3.

            SPL3, SPL4 and SPL5 (SPL3/4/5) are closely related members of the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE family of transcription factors in Arabidopsis, and have a target site for the microRNA miR156 in their 3' UTR. The phenotype of Arabidopsis plants constitutively expressing miR156-sensitive and miR156-insensitive forms of SPL3/4/5 revealed that all three genes promote vegetative phase change and flowering, and are strongly repressed by miR156. Constitutive expression of miR156a prolonged the expression of juvenile vegetative traits and delayed flowering. This phenotype was largely corrected by constitutive expression of a miR156-insensitive form of SPL3. The juvenile-to-adult transition is accompanied by a decrease in the level of miR156 and an increase in the abundance of SPL3 mRNA. The complementary effect of hasty on the miR156 and SPL3 transcripts, as well as the miR156-dependent temporal expression pattern of a 35S::GUS-SPL3 transgene, suggest that the decrease in miR156 is responsible for the increase in SPL3 expression during this transition. SPL3 mRNA is elevated by mutations in ZIPPY/AGO7, RNA DEPENDENT RNA POLYMERASE 6 (RDR6) and SUPPRESSOR OF GENE SILENCING 3 (SGS3), indicating that it is directly or indirectly regulated by RNAi. However, our results indicate that RNAi does not contribute to the temporal expression pattern of this gene. We conclude that vegetative phase change in Arabidopsis is regulated by an increase in the expression of SPL3 and probably also SPL4 and SPL5, and that this increase is a consequence of a decrease in the level of miR156.
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              CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees.

              Forest trees display a perennial growth behavior characterized by a multiple-year delay in flowering and, in temperate regions, an annual cycling between growth and dormancy. We show here that the CO/FT regulatory module, which controls flowering time in response to variations in daylength in annual plants, controls flowering in aspen trees. Unexpectedly, however, it also controls the short-day-induced growth cessation and bud set occurring in the fall. This regulatory mechanism can explain the ecogenetic variation in a highly adaptive trait: the critical daylength for growth cessation displayed by aspen trees sampled across a latitudinal gradient spanning northern Europe.
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                Author and article information

                Contributors
                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                22 November 2023
                28 November 2023
                22 May 2024
                : 120
                : 48
                : e2311226120
                Affiliations
                [1] aNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry, Huazhong Agricultural University , Wuhan 430070, China
                [2] bHubei Hongshan Laboratory , Wuhan 430070, China
                [3] cHubei Engineering Technology Research Center for Forestry Information, College of Horticulture and Forestry, Huazhong Agricultural University , Wuhan 430070, China
                [4] dDepartment of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences , Umeå 901 83, Sweden
                Author notes
                2To whom correspondence may be addressed. Email: Ove.Nilsson@ 123456slu.se or jihuading@ 123456mail.hzau.edu.cn .

                Edited by George Coupland, Max-Planck-Institut fur Pflanzenzuchtungsforschung, Cologne, Germany; received July 3, 2023; accepted October 17, 2023

                1X.L., Y.S., M.K., and Y.L. contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-1033-1909
                https://orcid.org/0000-0002-5127-0129
                Article
                202311226
                10.1073/pnas.2311226120
                10691234
                37991940
                c0d749a8-b5d2-4906-a781-179d7c0114e8
                Copyright © 2023 the Author(s). Published by PNAS.

                This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                : 03 July 2023
                : 17 October 2023
                Page count
                Pages: 10, Words: 7393
                Funding
                Funded by: National Natural Science Foundation of China;
                Award ID: 32271824
                Award Recipient : Ove Nilsson Award Recipient : Jihua Ding
                Funded by: Fundamental Research Funds for the Central Universities;
                Award ID: 266019PY007
                Award Recipient : Ove Nilsson Award Recipient : Jihua Ding
                Funded by: Swedish Research Council;
                Award ID: 2013-04943
                Award Recipient : Ove Nilsson Award Recipient : Jihua Ding
                Funded by: Knut och Alice Wallenbergs Stiftelse (Knut and Alice Wallenberg Foundation), FundRef 501100004063;
                Award ID: 2019.0277
                Award Recipient : Ove Nilsson
                Funded by: VINNOVA (Swedish Governmental Agency for Innovation Systems), FundRef 501100001858;
                Award ID: 2016.00504
                Award Recipient : Ove Nilsson
                Categories
                dataset, Dataset
                research-article, Research Article
                plant-bio, Plant Biology
                428
                Biological Sciences
                Plant Biology

                tree phenology,age-dependency,bud set,bud break,climate adaptation

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