Tree architecture: A strigolactone-deficient mutant reveals a connection between branching order and auxin gradient along the tree stem

Chang Su, Andrzej Kokosza, Xiaonan Xie, Aleš Pěnčík, Youjun Zhang, Pasi Raumonen, Xueping Shi, Sampo Muranen, Melis Kucukoglu Topcu, Juha Immanen, Risto Hagqvist, Omid Safronov, Juan Alonso-Serra, Gugan Eswaran, Mirko Pavicic Venegas, Karin Ljung, Sally Ward, Ari Pekka Mähönen, Kristiina Himanen, Jarkko SalojärviAlisdair R. Fernie, Ondřej Novák, Ottoline Leyser, Wojtek Pałubicki, Ykä Helariutta, Kaisa Nieminen

Research output: Contribution to journalArticlepeer-review

8 Scopus citations

Abstract

Due to their long lifespan, trees and bushes develop higher order of branches in a perennial manner. In contrast to a tall tree, with a clearly defined main stem and branching order, a bush is shorter and has a less apparent main stem and branching pattern. To address the developmental basis of these two forms, we studied several naturally occurring architectural variants in silver birch (Betula pendula). Using a candidate gene approach, we identified a bushy kanttarelli variant with a loss-of-function mutation in the BpMAX1 gene required for strigolactone (SL) biosynthesis. While kanttarelli is shorter than the wild type (WT), it has the same number of primary branches, whereas the number of secondary branches is increased, contributing to its bush-like phenotype. To confirm that the identified mutation was responsible for the phenotype, we phenocopied kanttarelli in transgenic BpMAX1::RNAi birch lines. SL profiling confirmed that both kanttarelli and the transgenic lines produced very limited amounts of SL. Interestingly, the auxin (IAA) distribution along the main stem differed between WT and BpMAX1::RNAi. In the WT, the auxin concentration formed a gradient, being higher in the uppermost internodes and decreasing toward the basal part of the stem, whereas in the transgenic line, this gradient was not observed. Through modeling, we showed that the different IAA distribution patterns may result from the difference in the number of higher-order branches and plant height. Future studies will determine whether the IAA gradient itself regulates aspects of plant architecture.

Original languageEnglish
Article numbere2308587120
JournalProceedings of the National Academy of Sciences of the United States of America
Volume120
Issue number48
DOIs
StatePublished - 2023

Funding

Author affiliations: aOrganismal and Evolutionary Biology Research Program, Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki 00014, Finland; b\u9600nstitute of Biotechnology, Helsinki \u9600nstitute of Life Science, University of Helsinki, Helsinki 00014, Finland; cMathematics and Computer Science, Adam Mickiewicz University, Pozna\u0144 61-614, Poland; dCenter for Bioscience Research and Education, Utsunomiya University, Utsunomiya 321-8505, Japan; eLaboratory of Growth Regulators, \u9600nstitute of Experimental Botany of the Czech Academy of Sciences, Faculty of Science of Palack\u00FD University, Olomouc CZ-78371, Czech Republic; fMax-Planck-\u9600nstitute of Molecular Plant Physiology, Potsdam-Golm 14476, Germany; gCenter of Plant Systems Biology and Biotechnology, 4000 Plovdiv, Bulgaria; hMathematics, Tampere University, Tampere 33720, Finland; iKey Laboratory of Horticultural Plant Biology of Ministry of Education, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, China; jProduction Systems, Natural Resources \u9600nstitute Finland (Luke), Helsinki 00790, Finland; kMolecular and \u9600ntegrative Biosciences Research Program, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Centre, University of Helsinki, Helsinki 00014, Finland; lLaboratoire de Reproduction et D\u00E9veloppement des Plantes, \u00C9cole Normale Sup\u00E9rieure de Lyon, \u9600nstitut National de la Recherche Agronomique, Lyon 69342, France; mBiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37830; nNational Plant Phenotyping \u9600nfrastructure, Helsinki \u9600nstitute of Life Science, University of Helsinki, Biocenter Finland, Helsinki 00014, Finland; oDepartment of Forest Genetics and Plant Physiology, Ume\u00E5 Plant Science Centre, Swedish University of Agricultural Sciences, 90183 Ume\u00E5, Sweden; pSainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, United Kingdom; qSchool of Biological Sciences, Nanyang Technological University, Singapore 637551, Singapore; and rCentre of the Region Han\u00E1 for Biotechnological and Agricultural Research, Faculty of Science, Palack\u00FD University and \u9600nstitute of Experimental Botany of the Academy of Sciences of the Czech Republic, Olomouc 78371, Czech Republic Author contributions: C.S., Y.H., and K.N. designed research; C.S., A.K., X.X., A.P., Y.Z., P.R., X.S., S.M., M.K.T., J. \u9600., R.H., O.S., J.AS..-, G.E., and M.P.V. performed research; C.S. contributed new reagents/analytic tools; C.S., A.K., P.R., X.S., K.L., S.W., A.P.M., K.H., J.S., A.R.F., O.N., O.L., and W.P. analyzed data; K.L. and O.N. supervision of auxin measurement; S.W. supervision of PAT measurement; A.P.M. interpretation of experiments; K.H. supervision of NaPP \u9600 measurement; J.S. supervision of bioinformatics analysis; A.R.F. supervision of sugar measurement and manuscript revision; O.L. interpretation of experiments and manuscript revision; W.P. supervision of auxin dynamics computational model generation, manuscript preparation, and revision; C.S., Y.H., and K.N. study conception and design, analysis and interpretation of experiments, manuscript preparation and revision; and C.S. wrote the paper. We thank Katja Kainulainen, Leena Gr\u00F6nholm, Puk Klamer, Clemens Raths, Aruto Nakada, Wafaa Kanash, and Elias P\u00E4ivinen for the excellent technical assistance. Additionally, we thank Thomas Lilja for finding the scanned commercial stands, Nina Heiska for 3D terrestrial laser-scanning and providing the scanning details, and Marco Pisanu for digital analysis support. The work was funded by the European Research Council (ERC SYMDEV 323052, ERC-CoG CORKtheCAMBIA 819422), Academy of Finland Center of Excellence in Molecular Biology of Primary Producers (AoF CoE 271832) and CoE in Tree Biology (TreeBio AoF CoE 346139; 346141), University of Helsinki award (799992091), Gatsby Foundation (GAT3395/PR3 and GAT3272C), Academy Professor (AoF 345137), Jane and Aatos Erkko Foundation (200003), Bill & Melinda Gates Foundation (OPP1207956), Academy Project Funding (AoF 286404 and 322690, Chinese Government Scholarship (201506600037), European Union\u2019s Horizon 2020 project PlantaSYST (SGA-CSA No 664621 and No 739582 under FPA No. 664620), European Regional Development Fund-Project (CZ.02.1.01/0.0/0.0/1 6_019/0000827), Academy of Finland Postdoctoral Researcher (AoF 326036), Academy Research Fellow (AoF 347130 and 353537), Suomen Luonnonvarain tutkimuss\u00E4\u00E4ti\u00F6 (SLTS 20220013/20230059), Knut and Alice Wallenberg Foundation (KAW 2016.0352 and KAW 2020.0240), and Swedish Governmental Agency for Innovation Systems (VINNOVA 2016-00504). ACKNOWLEDGMENTS. We thank Katja Kainulainen, Leena Gr\u00F6nholm, Puk Klamer, Clemens Raths, Aruto Nakada, Wafaa Kanash, and Elias P\u00E4ivinen for the excellent technical assistance.Additionally,we thank Thomas Lilja for finding the scanned commercial stands, Nina Heiska for 3D terrestrial laser-scanning and providing the scanning details, and Marco Pisanu for digital analysis support. The work was funded by the European Research Council (ERC SYMDEV 323052, ERC-CoG CORKtheCAMBIA819422),Academy of Finland Center of Excellence in Molecular Biology of Primary Producers (AoF CoE 271832) and CoE in Tree Biology (TreeBio AoF CoE 346139; 346141), University of Helsinki award (799992091), Gatsby Foundation (GAT3395/PR3 and GAT3272C), Academy Professor (AoF 345137), Jane and Aatos Erkko Foundation (200003), Bill & Melinda Gates Foundation (OPP1207956),Academy Project Funding (AoF 286404 and 322690, Chinese Government Scholarship (201506600037), European Union\u2019s Horizon 2020 project PlantaSYST (SGA-CSA No 664621 and No 739582 under FPA No. 664620), European Regional Development Fund-Project (CZ.02.1.01/0.0/0.0/1 6_019/0000827), Academy of Finland Postdoctoral Researcher (AoF 326036), Academy Research Fellow (AoF 347130 and 353537),Suomen Luonnonvarain tut-kimuss\u00E4\u00E4ti\u00F6 (SLTS 20220013/20230059), Knut and Alice Wallenberg Foundation (KAW 2016.0352 and KAW 2020.0240), and Swedish Governmental Agency for Innovation Systems (VINNOVA 2016-00504).

Keywords

  • Betula pendula
  • auxin distribution
  • branching modeling
  • strigolactones
  • tree architecture

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