Stomatal Opening Involves Polar, Not Radial, Stiffening Of Guard Cells

被引:74
作者
Carter, Ross [1 ,2 ,3 ]
Woolfenden, Hugh [3 ]
Baillie, Alice [1 ]
Amsbury, Sam [1 ]
Carroll, Sarah [1 ]
Healicon, Eleanor [1 ]
Sovatzoglou, Spyros [2 ]
Braybrook, Sioban [4 ]
Gray, Julie E. [5 ]
Hobbs, Jamie [2 ]
Morris, Richard J. [3 ]
Fleming, Andrew J. [1 ]
机构
[1] Univ Sheffield, Dept Anim & Plant Sci, Sheffield, S Yorkshire, England
[2] Univ Sheffield, Dept Phys & Astron, Sheffield, S Yorkshire, England
[3] John Innes Ctr, Computat & Syst Biol, Norwich, Norfolk, England
[4] Univ Cambridge, Sainsbury Lab, Cambridge, England
[5] Univ Sheffield, Dept Mol Biol & Biotechnol, Sheffield, S Yorkshire, England
基金
英国生物技术与生命科学研究理事会;
关键词
WALL; MECHANICS; PHOTOSYNTHESIS; CELLULOSE; GROWTH; VOLUME;
D O I
10.1016/j.cub.2017.08.006
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
It has long been accepted that differential radial thickening of guard cells plays an important role in the turgor-driven shape changes required for stomatal pore opening to occur [1-4]. This textbook description derives from an original interpretation of structure rather than measurement of mechanical properties. Here we show, using atomic force microscopy, that although mature guard cells display a radial gradient of stiffness, this is not present in immature guard cells, yet young stomata show a normal opening response. Finite element modeling supports the experimental observation that radial stiffening plays a very limited role in stomatal opening. In addition, our analysis reveals an unexpected stiffening of the polar regions of the stomata complexes, both in Arabidopsis and other plants, suggesting a widespread occurrence. Combined experimental data (analysis of guard cell wall epitopes and treatment of tissue with cell wall digesting enzymes, coupled with bioassay of guard cell function) plus modeling lead us to propose that polar stiffening reflects a mechanical, pectin-based pinning down of the guard cell ends, which restricts increase of stomatal complex length during opening. This is predicted to lead to an improved response sensitivity of stomatal aperture movement with respect to change of turgor pressure. Our results provide new insight into the mechanics of stomatal function, both negating an established view of the importance of radial thickening and providing evidence for a significant role for polar stiffening. Improved stomatal performance via altered cell-wall-mediated mechanics is likely to be of evolutionary and agronomic significance.
引用
收藏
页码:2974 / +
页数:12
相关论文
共 36 条
[1]   Understanding plant cell morphogenesis requires real-time monitoring of cell wall polymers [J].
Altartouri, Bara ;
Geitmann, Anja .
CURRENT OPINION IN PLANT BIOLOGY, 2015, 23 :76-82
[2]   Stomatal Function Requires Pectin De-methyl-esterification of the Guard Cell Wall [J].
Amsbury, Sam ;
Hunt, Lee ;
Elhaddad, Nagat ;
Baillie, Alice ;
Lundgren, Marjorie ;
Verhertbruggen, Yves ;
Scheller, Henrik V. ;
Knox, J. Paul ;
Fleming, Andrew J. ;
Gray, Julie E. .
CURRENT BIOLOGY, 2016, 26 (21) :2899-2906
[3]   STOMATAL MECHANICS [J].
AYLOR, DE ;
PARLANGE, JY ;
KRIKORIAN, AD .
AMERICAN JOURNAL OF BOTANY, 1973, 60 (02) :163-171
[4]   Shifting foundations: the mechanical cell wall and development [J].
Braybrook, Siobhan A. ;
Joensson, Henrik .
CURRENT OPINION IN PLANT BIOLOGY, 2016, 29 :115-120
[5]   Mechano-Chemical Aspects of Organ Formation in Arabidopsis thaliana: The Relationship between Auxin and Pectin [J].
Braybrook, Siobhan A. ;
Peaucelle, Alexis .
PLOS ONE, 2013, 8 (03)
[6]  
COOKE JR, 1976, T ASAE, V19, P1107, DOI 10.13031/2013.36186
[7]   Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes [J].
Cosgrove, Daniel J. .
JOURNAL OF EXPERIMENTAL BOTANY, 2016, 67 (02) :463-476
[8]   An integrated model of stomatal development and leaf physiology [J].
Dow, Graham J. ;
Bergmann, Dominique C. ;
Berry, Joseph A. .
NEW PHYTOLOGIST, 2014, 201 (04) :1218-1226
[9]  
Esau K., 1967, Plant anatomy
[10]   The mechanical diversity of stomata and its significance in gas-exchange control [J].
Franks, Peter J. ;
Farquhar, Graham D. .
PLANT PHYSIOLOGY, 2007, 143 (01) :78-87