Evolution of molecular mechanisms that control stomatal closure
Final Report Abstract
The development of stomata is likely to have been a key event during the evolution of land plants, as these pores enable plants to regulate their transpiration. Stomata are found in almost all land plants with the exception of liverworts and some clades of mosses. However, the function of stomata differs between extant bryophytes and vascular plants. Stomata of mosses and hornworts are only found on spore capsules, where they enable the desiccation of spores during maturation. In contrast, stomata occur in predominantly in vegetative tissues of vascular plants and close at unfavorable environmental conditions to protect these plants from excessive loss of water, or the entry of microorganisms. To get insights into the evolution of stomata we obtained the guard cell specific transcriptome of two ferns and two seed plants and analyzed these data in combination with nine other species that cover the complete phylogenetic tree of green plants. Our data show that genes, which existed early evolution, were recruited for guard cell specific functions, either before the development of ferns and seed plants, or specifically in one of both divisions. A main role could be assigned to genes encoding protein kinases, such as the MAP3K and MAP kinases involved in CO2 responses of stomata. Apparently, guard cells obtained the ability to respond to CO2 early in evolution and this signaling pathway was conserved in ferns and seed plants. Despite of many common elements, ferns have diverged considerably from seed plants, with regard to the way they control stomatal movements. We focused on the BK channels that have been lost during the evolution of seed plants, but are found in bryophytes, lycophytes and ferns. Plant BK channels genes are expressed in guard cells of ferns and encode voltagedependent K+ channels. It is likely that BK channels enable stomatal function in ferns at an expanded window of extracellular conditions, as can be mastered by K+ release channels of seed plants. Drought-induced stomatal closure in Arabidopsis thaliana depends on the protein kinase OST1, which activates the plasma membrane anion channel SLAC1 and thereby provokes the release of monovalent anions from guard cells. We found that the extrusion of monovalent anions from guard cells is sufficient to close stomata, using an optogenetic tool; the lightactivated anion channel GtCAR1. In line with the result, the OST1/SLAC1 module has a major role in provoking stomatal closure during drought, infestation by microorganisms and high atmospheric CO2 concentrations. Functional OST1-SLAC1-like modules are likely to have developed early in evolution, as they are found in mosses, hornworts as well as seed plants. However, SLAC1-like channels of ferns have lost the ability to interact with OST1, as well as Ca2+-dependent Protein Kinases. In line with these results, fern stomata appear to lack the ability to close response to ABA application. The analysis of ferns and seed plant transcriptomes revealed clear differences between guard cells of both divisions, which matches the observed differences of stomatal responses to light and drought. Apparently, ferns and seed plants have evolved alternative strategies to control the fluxes of CO2 and water vapor with the atmosphere. Future experiments may reveal further details of the signaling pathways and transport mechanisms that control stomatal movements in both divisions. Moreover, such studies may help to understand the advantages and downsides of fern-specific stomatal responses to environmental signals.
Publications
- 2019. Acquiring control: The evolution of stomatal signalling pathways. Trends in Plant Science 24(4): 342-351
Sussmilch FC, Schultz J, Hedrich R, Roelfsema MRG
(See online at https://doi.org/10.1016/j.tplants.2019.01.002) - 2019. On the origins of osmotically driven stomatal movements. New Phytologist 222(1): 84-90
Sussmilch FC, Roelfsema MRG, Hedrich R
(See online at https://doi.org/10.1111/nph.15593) - 2020. How to grow a tree: Plant voltage-dependent cation channels in the spotlight of evolution. Trends in Plant Science 26(1): 41-52
Dreyer I, Sussmilch FC, Fukushima K, Riadi G, Becker D, Schultz J, Hedrich R
(See online at https://doi.org/10.1016/j.tplants.2020.07.011) - 2020. The calcium-permeable channel OSCA1.3 regulates plant stomatal immunity. Nature 585(7826): 569-573
Thor K, Jiang SS, Michard E, George J, Scherzer S, Huang SG, Dindas J, Derbyshire P, Leitao N, DeFalco TA, Koster P, Hunter K, Kimura S, Gronnier J, Stransfeld L, Kadota Y, Bucherl CA, Charpentier M, Wrzaczek M, MacLean D, Oldroyd GED, Menke FLH, Roelfsema MRG, Hedrich R, Feijo J, Zipfel C
(See online at https://doi.org/10.1038/s41586-020-2702-1) - 2021. A voltage-dependent Ca2+ homeostat operates in the plant vacuolar membrane. New Phytologist 230(4): 1449-1460
Dindas J, Dreyer I, Huang S, Hedrich R, Roelfsema MRG
(See online at https://doi.org/10.1111/nph.17272) - 2021. Gaining or cutting SLAC: the evolution of plant guard cell signalling pathways
Sussmilch FC, Maierhofer T, Herrmann J, Voss LJ, Lind C, Messerer M, Mueller HM, Buenner MS, Ache P, Mayer KFX, Becker D, Roelfsema MRG, Geiger D, Schultz J and Hedrich R
(See online at https://doi.org/10.1101/2021.05.26.445736) - 2021. The liverwort Marchantia polymorpha operates a depolarizationactivated Slowpoke (SLO) K+ channel that recognises pH changes in the environment
Sussmilch FC, Böhm J, Gessner G, Maierhofer T, Müller TD, Heinemann SH, Becker D, Hedrich R
(See online at https://doi.org/10.1101/2021.06.01.446568)
