Altering arabinans increases Arabidopsis guard cell flexibility and stomatal opening
Sarah Carroll, Sam Amsbury, Clinton H. Durney, Richard S. Smith, Richard J. Morris, Julie E. Gray, Andrew J. Fleming
Abstract
Stomata regulate plant water use and photosynthesis by controlling leaf gas exchange. They do this by reversibly opening the pore formed by two adjacent guard cells, with the limits of this movement ultimately set by the mechanical properties of the guard cell walls and surrounding epidermis.1Franks P.J. Farquhar G.D. The mechanical diversity of stomata and its significance in gas-exchange control.Plant Physiol. 2007; 143: 78-87https://doi.org/10.1104/pp.106.089367Crossref PubMed Scopus (368) Google Scholar,2Woolfenden H.C. Baillie A.L. Gray J.E. Hobbs J.K. Morris R.J. Fleming A.J. Models and mechanisms of stomatal mechanics.Trends Plant Sci. 2018; 23: 822-832https://doi.org/10.1016/j.tplants.2018.06.003Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar A body of evidence demonstrates that the methylation status and cellular patterning of pectin wall polymers play a core role in setting the guard cell mechanical properties, with disruption of the system leading to poorer stomatal performance.3Amsbury S. Hunt L. Elhaddad N. Baillie A. Lundgren M. Verhertbruggen Y. Scheller H.V. Knox J.P. Fleming A.J. Gray J.E. Stomatal function requires pectin de-methyl-esterification of the guard cell wall.Curr. Biol. 2016; 26: 2899-2906https://doi.org/10.1016/j.cub.2016.08.021Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar, 4Chen Y. Li W. Turner J.A. Anderson C.T. PECTATE LYASE LIKE12 patterns the guard cell wall to coordinate turgor pressure and wall mechanics for proper stomatal function in Arabidopsis.Plant Cell. 2021; 33: 3134-3150https://doi.org/10.1093/plcell/koab161Crossref PubMed Scopus (8) Google Scholar, 5Carter R. Woolfenden H. Baillie A. Amsbury S. Carroll S. Healicon E. Sovatzoglou S. Braybrook S. Gray J.E. Hobbs J. Morris R.J. Fleming A.J. Stomatal opening involves polar, not radial, stiffening of guard cells.Curr. Biol. 2017; 27: 2974-2983.e2https://doi.org/10.1016/j.cub.2017.08.006Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar, 6Rui Y. Xiao C. Yi H. Kandemir B. Wang J.Z. Puri V.M. Anderson C.T. POLYGALACTURONASE INVOLVED IN EXPANSION3 functions in seedling development, rosette growth, and stomatal dynamics in Arabidopsis thaliana.Plant Cell. 2017; 29: 2413-2432https://doi.org/10.1105/tpc.17.00568Crossref PubMed Scopus (62) Google Scholar Here we present genetic and biochemical data showing that wall arabinans modulate guard cell flexibility and can be used to engineer stomata with improved performance. Specifically, we show that a short-chain linear arabinan epitope associated with the presence of rhamnogalacturonan I in the guard cell wall is required for full opening of the stomatal pore. Manipulations leading to the novel accumulation of longer-chain arabinan epitopes in guard cell walls led to an increase in the maximal pore aperture. Using computational modeling combined with atomic force microscopy, we show that this phenotype reflected a decrease in wall matrix stiffness and, consequently, increased flexing of the guard cells under turgor pressure, generating larger, rounder stomatal pores. Our results provide theoretical and experimental support for the conclusion that arabinan side chains of pectin modulate guard cell wall stiffness, setting the limits for cell flexing and, consequently, pore aperture, gas exchange, and photosynthetic assimilation.