ELIMÄKI Locus Is Required for Vertical Proprioceptive Response in Birch Trees

• Published in: Current biology 2020-02, Vol.30 (4), p.589-599.e5
• Main Authors: Alonso-Serra, Juan, Shi, Xueping, Peaucelle, Alexis, Rastas, Pasi, Bourdon, Matthieu, Immanen, Juha, Takahashi, Junko, Koivula, Hanna, Eswaran, Gugan, Muranen, Sampo, Help, Hanna, Smolander, Olli-Pekka, Su, Chang, Safronov, Omid, Gerber, Lorenz, Salojärvi, Jarkko, Hagqvist, Risto, Mähönen, Ari Pekka, Helariutta, Ykä, Nieminen, Kaisa
• Format: Article
• Language: English
• Subjects: Betula; Betula - genetics; Betula - growth & development; Botanik; Botany; Cambium - genetics; Cambium - growth & development; Development Biology; forward genetics; Genes, Plant; Life Sciences; mechanosensing; Morphogenesis; Mutation; Plant Stems - genetics; Plant Stems - growth & development; proprioception; Proprioception - genetics; radial growth; trees; Trees - genetics; Trees - growth & development; Vegetal Biology; wood formation
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2019.12.016

Tree architecture has evolved to support a top-heavy above-ground biomass, but this integral feature poses a weight-induced challenge to trunk stability. Maintaining an upright stem is expected to require vertical proprioception through feedback between sensing stem weight and responding with radial growth. Despite its apparent importance, the principle by which plant stems respond to vertical loading forces remains largely unknown. Here, by manipulating the stem weight of downy birch (Betula pubescens) trees, we show that cambial development is modulated systemically along the stem. We carried out a genetic study on the underlying regulation by combining an accelerated birch flowering program with a recessive mutation at the ELIMÄKI locus (EKI), which causes a mechanically defective response to weight stimulus resulting in stem collapse after just 3 months. We observed delayed wood morphogenesis in eki compared with WT, along with a more mechanically elastic cambial zone and radial compression of xylem cell size, indicating that rapid tissue differentiation is critical for cambial growth under mechanical stress. Furthermore, the touch-induced mechanosensory pathway was transcriptionally misregulated in eki, indicating that the ELIMÄKI locus is required to integrate the weight-growth feedback regulation. By studying this birch mutant, we were able to dissect vertical proprioception from the gravitropic response associated with reaction wood formation. Our study provides evidence for both local and systemic responses to mechanical stimuli during secondary plant development. [Display omitted] •Trees stems adjust their radial growth allometry in response to a weight increase•Fast-forward genetics by accelerated flowering reveals a Mendelian trait in birch•Vertical proprioception response in radial growth is linked to the ELIMÄKI locus•Timely tissue differentiation is critical for cambial growth under mechanical stress Alonso-Serra et al. use birch trees to explore vertical proprioception, the growth response of stems to changes in aerial body weight. They identify a genetic locus, which is required for this developmental response, and study the consequences of cambial growth under mechanical stress.