Formation of the Stomatal Outer Cuticular Ledge Requires a Guard Cell Wall Proline-Rich Protein.

Lee Hunt,Mahsa Movahedi,Kamal Swarup,Thomas Denyer,Mana Afsharinafar,Alice Baillie,Andrew J Fleming,Samuel Amsbury,Ranjan Swarup,Jamie K Hobbs,Alice Mitchell,Julie E Gray

doi:10.1104/pp.16.01715

Lee Hunt, Mahsa Movahedi + Show 10 more

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https://doi.org/10.1104/pp.16.01715

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Abstract

Stomata are formed by a pair of guard cells which have thickened, elastic cell walls to withstand the large increases in turgor pressure that have to be generated to open the pore that they surround. We have characterized FOCL1, a guard cell-expressed, secreted protein with homology to Hyp-rich cell wall proteins. FOCL1-GFP localizes to the guard cell outer cuticular ledge and plants lacking FOCL1 produce stomata without a cuticular ledge. Instead the majority of stomatal pores are entirely covered over by a continuous fusion of the cuticle, and consequently plants have decreased levels of transpiration and display drought tolerance. The focl1 guard cells are larger and less able to reduce the aperture of their stomatal pore in response to closure signals suggesting that the flexibility of guard cell walls is impaired. FOCL1 is also expressed in lateral root initials where it aids lateral root emergence. We propose that FOCL1 acts in these highly specialized cells of the stomata and root to impart cell wall strength at high turgor and/or to facilitate interactions between the cell wall and the cuticle.

Highlights

Stomata are formed by a pair of guard cells which have thickened, elastic cell walls to withstand the large increases in turgor pressure that have to be generated to open the pore that they surround
There is currently no genetic evidence of a role for cell wall Hyp-rich glycoproteins (HRGPs) in stomatal function, individual polysaccharide moieties of the mature guard cell wall are known to be important for pore aperture control as removal of the arabinan component of the guard cell wall or modifying pectin methyl esterification impairs stomatal opening and closing (Jones et al, 2003; Amsbury et al, 2016)
FUSED OUTER CUTICULAR LEDGE1 (FOCL1) may be intermolecularly bonded by Tyr residues in a different sequence context, as seen for the HRGP, PRP10 (Chen et al, 2015)

Summary

Introduction

Stomata are formed by a pair of guard cells which have thickened, elastic cell walls to withstand the large increases in turgor pressure that have to be generated to open the pore that they surround. Plant cell walls typically consist of a network of cellulose, hemicellulose, pectin, and lignin, and contain many structural proteins of unknown function such as Hyp-rich glycoproteins (HRGPs; Lamport et al, 2011). This group of proteins includes Pro-rich proteins (PRPs), arabinogalactan proteins (AGPs), and extensins. HRGPs are sequentially posttranslationally modified by Pro 4-hydroxylases, converting Pro residues to Hyp, and by O-glycosyltransferases adding sugar moieties to Hyp residues These posttranslational modifications are thought to contribute to the structural and possibly to the intercellular communication properties of the cell wall. There is currently no genetic evidence of a role for cell wall HRGPs in stomatal function, individual polysaccharide moieties of the mature guard cell wall are known to be important for pore aperture control as removal of the arabinan component of the guard cell wall or modifying pectin methyl esterification impairs stomatal opening and closing (Jones et al, 2003; Amsbury et al, 2016)

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