Decoding the Lateral Expansion of Plant Stems
Developmental Biology
Plant Genetics and Genomics
Final Report Abstract
In contrast to most animals, including humans, plants grow continuously throughout their entire life. Especially thickening of plant shoots and roots is remarkable in this regard because these very rigid structures are able to expand constantly while maintaining their respective functions which are mechanical support of the plant body and long-distance transport of water, sugars and nutrients. The essential structures determining mechanical properties of plant tissues and organs are extracellular matrices called cell walls built by carbohydrates and distinct proteins. To characterize the cross-talk between the mechanical state of a plant organ and its constant growth, we investigated in this project the role of the cell wall in the process of plant shoot thickening. We assumed that the regulation of this major cellular compartment is fundamental for communicating and integrating mechanical constraints during plant growth processes. For monitoring mechanical cell wall properties we first established Brillouin spectroscopy as a tool for investigating subcellular structures in plant cells. Brillouin spectroscopy is an emerging technology in biological research and what makes it attractive is that it allows the non-contact analysis of mechanical properties with high spatial resolution. In this project, we could show that Brillouin spectroscopy is indeed suited for extracting biological relevant information about the cell wall state and that also internal structures and tissues are accessible by this technology. Considering that mechanical properties of wood are cell wall-dependent and that those properties determine the application of wood as a building material, Brillouin spectroscopy may allow a more profound and earlier analysis of this essential aspect of this natural product in comparison to more classical methods of material science. Because the change of cellular properties is crucial for any growth process, we were interested in identifying a clear case of cell fate change during lateral stem growth for investigating the role of cell wall regulation in a very distinct example. Interestingly, we found that starch sheath cells, usually important for sensing gravity in the plant shoot, transform into cambium cells, the stem cells responsible for shoot and root thickening, during the initiation of lateral stem growth. We also observed that a boost of the biosynthesis of the plant hormone auxin in those cells is sufficient for convincing starch sheath cells to change their identity into cambium cells. Thus, we identified auxin as a switch by which we were able to initiate this characteristic change of cell fate on demand. Exploiting this switch, we identified genes which change their activity at early stages of the starch sheath-to-cambium transition including a defined set of cell wallrelated genes. Future analyse will show whether this set is instrumental for regulating cell wall properties during lateral plant growth. Complementing this dataset, we established a comprehensive toolset for targeting individual plant stem tissues by genetic approaches. This toolset together with the elucidation of profiles of genes active in each of those individual tissues represent the most profound approach for investing lateral plant growth followed until now. We expect that these achievements will generate multiple opportunities for basic research as well as for modulating mechanical properties and long distance transport capacities in crop species potentially boosting crop production and resistance against abiotic stress.
Publications
- (2019) Mobile PEAR transcription factors integrate positional cues to prime cambial growth. Nature 565 (7740) 490–494
Miyashima, Shunsuke; Roszak, Pawel; Sevilem, Iris; Toyokura, Koichi; Blob, Bernhard; Heo, Jung-Ok; Mellor, Nathan; Help-Rinta-Rahko, Hanna; Otero, Sofia; Smet, Wouter; Boekschoten, Mark; Hooiveld, Guido; Hashimoto, Kayo; Smetana, Ondřej; Siligato, Riccard
(See online at https://doi.org/10.1038/s41586-018-0839-y) - (2016) Mapping the subcellular mechanical properties of live cells in tissues with fluorescence emission-Brillouin imaging. Sci Signal 9(435):RS5
Elsayad K, Werner S, Gallemi M, Guajardo ERS, Zhang L, Jaillais Y, Greb T, Belkhadir Y
(See online at https://doi.org/10.1126/scisignal.aaf6326) - (2017) Strigolactone and karrikinindependent SMXL proteins are central regulators of phloem formation. Curr Biol 27(8):1241– 1247
Wallner ES, López-Salmerón V, Belevich I, Poschet G, Jung I, Grünwald K, Sevilem I, Jokitalo E, Hell R, Helariutta Y, Agustí J, Lebovka I, Greb T
(See online at https://doi.org/10.1016/j.cub.2017.03.014) - (2018) A comprehensive toolkit for inducible, cell type-specific gene expression in Arabidopsis. Plant Phys 178(1):40-53
Schuerholz A-K, López-Salmerón V, Li Z, Forner J, Wenzl C, Gaillochet C, Augustin S, Vilches Barro A, Fuchs M, Gebert M, Lohmann JU, Greb T, Wolf S
(See online at https://doi.org/10.1104/pp.18.00463) - (2018) Spatial specificity of auxin responses coordinates wood formation. Nat Commun 9(1):875
Brackmann K, Qi J, Gebert M, Jouannet V, Schlamp T, Grünwald K, Wallner ES, Novikova DD, Levitsky VG, Agusti J, Sanchez P, Lohmann JU, Greb T
(See online at https://doi.org/10.1038/s41467-018-03256-2) - (2018) Translational control of phloem development by RNA G-quadruplex/zinc2 finger protein determines plant sink strength. Nat Plants 4:376–390
Cho H, Cho HS, Nam H, Jo H, Yoon J, Park C, Dang TVT, Kim E, Jeong J, Park S, Wallner ES, Youn H, Park J, Jeon J, Ryu H, Greb T, Choi K, Lee Y, Jang SK, Ban C, Hwang I
(See online at https://doi.org/10.1038/s41477-018-0157-2)
