scholarly journals Pathogen-Mediated Stomatal Opening: A Previously Overlooked Pathogenicity Strategy in the Oomycete Pathogen Phytophthora infestans

2021 ◽  
Vol 12 ◽  
Author(s):  
Li-Na Yang ◽  
Hao Liu ◽  
Yan-Ping Wang ◽  
Jenifer Seematti ◽  
Laura J. Grenville-Briggs ◽  
...  

Phytophthora infestans, the most damaging oomycete pathogen of potato, is specialized to grow sporangiophore through opened stomata for secondary inoculum production. However, it is still unclear which metabolic pathways in potato are manipulated by P. infestans in the guard cell–pathogen interactions to open the stomata. Here microscopic observations and cell biology were used to investigate antagonistic interactions between guard cells and the oomycete pathogen. We observed that the antagonistic interactions started at the very beginning of infection. Stomatal movement is an important part of the immune response of potato to P. infestans infection and this occurs through guard cell death and stomatal closure. We observed that P. infestans appeared to manipulate metabolic processes in guard cells, such as triacylglycerol (TAG) breakdown, starch degradation, H2O2 scavenging, and NO catabolism, which are involved in stomatal movement, to evade these stomatal defense responses. The signal transduction pathway of P. infestans-induced stomatal opening likely starts from H2O2 and NO scavenging, along with TAG breakdown while the subsequent starch degradation reinforces the opening process by strengthening guard cell turgor and opening the stomata to their maximum aperture. These results suggest that stomata are a barrier stopping P. infestans from completing its life cycle, but this host defense system can be bypassed through the manipulation of diverse metabolic pathways that may be induced by P. infestans effector proteins.

2020 ◽  
Vol 32 (7) ◽  
pp. 2325-2344 ◽  
Author(s):  
Sabrina Flütsch ◽  
Yizhou Wang ◽  
Atsushi Takemiya ◽  
Silvere R. M. Vialet-Chabrand ◽  
Martina Klejchová ◽  
...  

2019 ◽  
Vol 20 (11) ◽  
pp. 2753
Author(s):  
Xin Li ◽  
Min Diao ◽  
Yanan Zhang ◽  
Guanlin Chen ◽  
Shanjin Huang ◽  
...  

The actin cytoskeleton is involved in regulating stomatal movement, which forms distinct actin arrays within guard cells of stomata with different apertures. How those actin arrays are formed and maintained remains largely unexplored. Elucidation of the dynamic behavior of differently oriented actin filaments in guard cells will enhance our understanding in this regard. Here, we initially developed a program called ‘guard cell microfilament analyzer’ (GCMA) that enables the selection of individual actin filaments and analysis of their orientations semiautomatically in guard cells. We next traced the dynamics of individual actin filaments and performed careful quantification in open and closed stomata. We found that de novo nucleation of actin filaments occurs at both dorsal and ventral sides of guard cells from open and closed stomata. Interestingly, most of the nucleated actin filaments elongate radially and longitudinally in open and closed stomata, respectively. Strikingly, radial filaments tend to form bundles whereas longitudinal filaments tend to be removed by severing and depolymerization in open stomata. By contrast, longitudinal filaments tend to form bundles that are severed less frequently in closed stomata. These observations provide insights into the formation and maintenance of distinct actin arrays in guard cells in stomata of different apertures.


2021 ◽  
Vol 12 ◽  
Author(s):  
Wenxiu Ye ◽  
Shota Koya ◽  
Yuki Hayashi ◽  
Huimin Jiang ◽  
Takaya Oishi ◽  
...  

Stomatal guard cells (GCs) are highly specialized cells that respond to various stimuli, such as blue light (BL) and abscisic acid, for the regulation of stomatal aperture. Many signaling components that are involved in the stomatal movement are preferentially expressed in GCs. In this study, we identified four new such genes in addition to an aluminum-activated malate transporter, ALMT6, and GDSL lipase, Occlusion of Stomatal Pore 1 (OSP1), based on the expression analysis using public resources, reverse transcription PCR, and promoter-driven β-glucuronidase assays. Some null mutants of GC-specific genes evidenced altered stomatal movement. We further investigated the role played by ALMT6, a vacuolar malate channel, in stomatal opening. Epidermal strips from an ALMT6-null mutant exhibited defective stomatal opening induced by BL and fusicoccin, a strong plasma membrane H+-ATPase activator. The deficiency was enhanced when the assay buffer [Cl–] was low, suggesting that malate and/or Cl– facilitate efficient opening. The results indicate that the GC-specific genes are frequently involved in stomatal movement. Further detailed analyses of the hitherto uncharacterized GC-specific genes will provide new insights into stomatal regulation.


2020 ◽  
Vol 32 (4) ◽  
pp. 984-999 ◽  
Author(s):  
Jin-Ge Li ◽  
Min Fan ◽  
Wenbo Hua ◽  
Yanchen Tian ◽  
Lian-Ge Chen ◽  
...  

2000 ◽  
Vol 28 (4) ◽  
pp. 476-481 ◽  
Author(s):  
M. R. McAinsh ◽  
J. E. Gray ◽  
A. M. Hetherington ◽  
C. P. Leckie ◽  
C. Ng

Ca2+ is a ubiquitous second messenger in the signal transduction pathway(s) by which stomatal guard cells respond to external stimuli. Increases in guard-cell cytosolic free Ca2+ concentration ([Ca2+]cyt) have been observed in response to stimuli that cause both stomatal opening and closure. In addition, several important components of Ca2+-based signalling pathways have been identified in guard cells, including the cADP-ribose and phospholipase C/Ins(1,4,5)P3-mediated Ca2+-mobilizing pathways. The central role of stimulus-induced increases in [Ca2+]cyt in guard-cell signal transduction has been clearly demonstrated in experiments examining the effects of modulating increases in [Ca2+]cyt on alterations in guard-cell turgor or the activity of ion channels that act as effectors in the guard-cell turgor response. In addition, the paradox that Ca2+ is involved in the transduction of signals that result in opposite end responses (stomatal opening and closure) might be accounted for by the generation of stimulus-specific Ca2+ signatures, such that increases in [Ca2+]cyt exhibit unique spatial and temporal characteristics.


2014 ◽  
Vol 37 (9) ◽  
pp. 2201-2210 ◽  
Author(s):  
SHU-WEI WANG ◽  
YING LI ◽  
XIAO-LU ZHANG ◽  
HAI-QIANG YANG ◽  
XUE-FEI HAN ◽  
...  

1988 ◽  
Vol 92 (5) ◽  
pp. 667-683 ◽  
Author(s):  
J I Schroeder

Electrical properties of the plasma membrane of guard cell protoplasts isolated from stomates of Vicia faba leaves were studied by application of the whole-cell configuration of the patch-clamp technique. The two types of K+ currents that have recently been identified in guard cells may allow efflux of K+ during stomatal closing, and uptake of K+ during stomatal opening (Schroeder et al., 1987). A detailed characterization of ion transport properties of the inward-rectifying (IK+,in) and the outward-rectifying (IK+,out) K+ conductance is presented here. The permeability ratios of IK+,in and IK+,out currents for K+ over monovalent alkali metal ions were determined. The resulting permeability sequences (PK+ greater than PRb+ greater than PNa+ greater than PLi+ much greater than PCs+) corresponded closely to the ion specificity of guard cell movements in V. faba. Neither K+ currents exhibited significant inactivation when K+ channels were activated for prolonged periods (greater than 10 min). The absence of inactivation may permit long durations of K+ fluxes, which occur during guard cell movements. Activation potentials of inward K+ currents were not shifted when external K+ concentrations were changed. This differs strongly from the behavior of inward-rectifying K+ channels in animal tissue. Blue light and fusicoccin induce hyperpolarization by stimulation of an electrogenic pump. From slow-whole-cell recordings it was concluded that electrogenic pumps require cytoplasmic substrates for full activation and that the magnitude of the pump current is sufficient to drive K+ uptake through IK+,in channels. First, direct evidence was gained for the hypothesis that IK+,in channels are a molecular pathway for K+ accumulation by the finding that IK+,in was blocked by Al3+ ions, which are known to inhibit stomatal opening but not closing. The results presented in this study strongly support a prominent role for IK+,in and IK+,out channels in K+ transport across the plasma membrane of guard cells.


2021 ◽  
Vol 22 (8) ◽  
pp. 4174
Author(s):  
Kai-Ting Fan ◽  
Yang Hsu ◽  
Ching-Fang Yeh ◽  
Chi-Hsin Chang ◽  
Wei-Hung Chang ◽  
...  

Late blight (LB) disease is a major threat to potato and tomato production. It is caused by the hemibiotrophic pathogen, Phytophthora infestans. P. infestans can destroy all of the major organs in plants of susceptible crops and result in a total loss of productivity. At the early pathogenesis stage, this hemibiotrophic oomycete pathogen causes an asymptomatic biotrophic infection in hosts, which then progresses to a necrotrophic phase at the later infection stage. In this study, to examine how the tomato proteome is regulated by P. infestans at different stages of pathogenesis, a data-independent acquisition (DIA) proteomics approach was used to trace the dynamics of the protein regulation. A comprehensive picture of the regulation of tomato proteins functioning in the immunity, signaling, defense, and metabolism pathways at different stages of P. infestans infection is revealed. Among the regulated proteins, several involved in mediating plant defense responses were found to be differentially regulated at the transcriptional or translational levels across different pathogenesis phases. This study increases understanding of the pathogenesis of P. infestans in tomato and also identifies key transcriptional and translational events possibly targeted by the pathogen during different phases of its life cycle, thus providing novel insights for developing a new strategy towards better control of LB disease in tomato.


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