Drought Sensitivity and Involvement in Leaf Epidermal Development and Stomatal Closure

A Nck‐associated Protein 1‐like Protein Affects Drought Sensitivity by Its Involvement in Leaf Epidermal Development and Stomatal Closure in Rice

by Huang L., Chen L., Wang L., Yang Y., Rao Y., Ren D., Dai L., Gao Y., Zou W., Lu X., Zhang G., Zhu L., Hu J., Chen G., Shen L., Dong G., Gao Z., Guo L., Qian Q., Zeng D. (2019)

Lichao Huang, Long Chen, Lan Wang, Yaolong Yang, Yuchun Rao, Deyong Ren, Liping Dai, Yihong Gao; Weiwei Zou, Xueli Lu, Guangheng Zhang, Li Zhu, Jiang Hu, Guang Chen, Lan Shen, Guojun Dong, Zhenyu Gao, Longbiao Guo, Qian Qian, Dali Zeng,

In Plant Journ. – https://doi.org/10.1111/tpj.14288 – 

https://onlinelibrary.wiley.com/doi/abs/10.1111/tpj.14288?af=R

Abstract

Water deficit is a major environmental threat affecting crop yields worldwide.

In this study, a drought stress‐sensitive mutant drought sensitive 8 (ds8) was identified in rice (Oryza sativa L.). The DS8 gene was cloned using a map‐based approach. Further analysis revealed that DS8 encoded a Nck‐associated protein 1 (NAP1)‐like protein, a component of the SCAR/WAVE complex, which played a vital role in actin filament nucleation activity.

The mutant exhibited changes in leaf cuticle development. Functional analysis revealed that the mutation of DS8 increased stomatal density and impaired stomatal closure activity. The distorted actin filaments in the mutant led to a defect in abscisic acid (ABA)‐mediated stomatal closure and increased ABA accumulation.

All these resulted in excessive water loss in ds8 leaves. Notably, antisense transgenic lines also exhibited increased drought sensitivity, along with impaired stomatal closure and elevated ABA levels. These findings suggest that DS8 affects drought sensitivity by influencing actin filament activity.

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De novo protein synthesis contributes to the maintenance of long‐term Ca2+‐programmed stomatal closure

Working model for Ca2+ oscillation‐controlled gene expression and stomatal movements.
Increases and decreases in cytosolic Ca2+ concentration result in Ca2+oscillations. Cytosolic Ca2+ increases and/or Ca2+ oscillations in turn activate anion channels, eliciting cellular events leading to short‐term Ca2+‐reactive stomatal closure. Calcium oscillations modulate expression of a subset of genes that contribute to the maintenance of long‐term ‘Ca2+‐programmed’ stomatal closure. Long‐term Ca2+‐programmed stomatal closure may comprise H+‐pump inhibition and/or anion channel activation. AtGLRs are likely to play a role in Ca2+oscillation‐controlled gene expression and thus in long‐term Ca2+‐programmed stomatal closure.

De‐regulated expression of the plant glutamate receptor homolog AtGLR3.1impairs long‐term Ca2+‐programmed stomatal closure

by Cho D., Kim S. A., Murata Y., Lee S., Jae S.-K., Nam H. G., Kwak J. M. (2009)

Daeshik Cho, Sun A. Kim, Yoshiyuki Murata, Sangmee Lee, Seul‐Ki Jae, Hong Gil Nam, June M. Kwak,

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In Plant Journ. 58(3): – https://doi.org/10.1111/j.1365-313X.2009.03789.x – 

https://onlinelibrary.wiley.com/doi/full/10.1111/j.1365-313X.2009.03789.x

Abstract

Cytosolic Ca2+ ([Ca2+]cyt) mediates diverse cellular responses in both animal and plant cells in response to various stimuli. Calcium oscillation amplitude and frequency control gene expression.

In stomatal guard cells, [Ca2+]cyt has been shown to regulate stomatal movements, and a defined window of Ca2+ oscillation kinetic parameters encodes necessary information for long‐term stomatal movements. However, it remains unknown how the encrypted information in the cytosolic Ca2+ signature is decoded to maintain stomatal closure.

Here we report that the Arabidopsis glutamate receptor homolog AtGLR3.1 is preferentially expressed in guard cells compared to mesophyll cells. Furthermore, over‐expression of AtGLR3.1 using a viral promoter resulted in impaired external Ca2+‐induced stomatal closure.

Cytosolic Ca2+ activation of S‐type anion channels, which play a central role in Ca2+‐reactive stomatal closure, was normal in the AtGLR3.1 over‐expressing plants. Interestingly, AtGLR3.1 over‐expression did not affect Ca2+‐induced Ca2+oscillation kinetics, but resulted in a failure to maintain long‐term ‘Ca2+‐programmed’ stomatal closure when Ca2+ oscillations containing information for maintaining stomatal closure were imposed.

By contrast, prompt short‐term Ca2+‐reactive closure was not affected in AtGLR3.1 over‐expressing plants. In wild‐type plants, the translational inhibitor cyclohexamide partially inhibited Ca2+‐programmed stomatal closure induced by experimentally imposed Ca2+ oscillations without affecting short‐term Ca2+‐reactive closure, mimicking the guard cell behavior of the AtGLR3.1 over‐expressing plants.

Our results suggest that over‐expression of AtGLR3.1 impairs Ca2+ oscillation‐regulated stomatal movements, and that de novo protein synthesis contributes to the maintenance of long‐term Ca2+‐programmed stomatal closure.

L-Met regulates stomatal movement

L-Met Activates Arabidopsis GLR Ca2+ Channels Upstream of ROS Production and Regulates Stomatal Movement

by Kong D., Hu H.-C., Okuma E., Lee Y., Lee H. S., Munemasa S., Cho D., Ju C., Pedoeim L., Rodriguez B., Wang J., Im W., Murata Y., Pei Z.-M., Kwak J. (2016)

In Cell Reports 17(10): 2553-2561 – DOI:https://doi.org/10.1016/j.celrep.2016.11.015 –

https://www.cell.com/cell-reports/fulltext/S2211-1247(16)31556-X?_returnURL=https%3A%2F%2Flinkinghub.elsevier.com%2Fretrieve%2Fpii%2FS221112471631556X%3Fshowall%3Dtrue

Highlights

  • •GLR3.1 and GLR3.5 form guard cell Ca2+ channels specifically activated by L-Met
  • •GLR3.1/3.5 Ca2+ channels contribute to maintenance of basal cytosolic Ca2+ levels
  • •GLR3.1/3.5 Ca2+ channels act upstream of reactive oxygen species
  • •GLR3.1/3.5 Ca2+ channels play a role in plant growth and stomatal movement

Summary

Plant glutamate receptor homologs (GLRs) have long been proposed to function as ligand-gated Ca2+ channels, but no in planta evidence has been provided.

Here, we present genetic evidence that Arabidopsis GLR3.1 and GLR3.5 form Ca2+ channels activated by L-methionine (L-Met) at physiological concentrations and regulate stomatal apertures and plant growth. The glr3.1/3.5 mutations resulted in a lower cytosolic Ca2+level, defective Ca2+-induced stomatal closure, and Ca2+-deficient growth disorder, all of which involved L-Met. Patch-clamp analyses of guard cells showed that GLR3.1/3.5 Ca2+ channels are activated specifically by L-Met, with the activation abolished in glr3.1/3.5. Moreover, GLR3.1/3.5 Ca2+ channels are distinct from previously characterized ROS-activated Ca2+ channels and act upstream of ROS, providing Ca2+transients necessary for the activation of NADPH oxidases.

Our data indicate that GLR3.1/3.5 constitute L-Met-activated Ca2+ channels responsible for maintaining basal [Ca2+]cyt, play a pivotal role in plant growth, and act upstream of ROS, thereby regulating stomatal aperture.

Stomatal aperture observed by low-temperature scanning electron microscopy

Variation in stomatal aperture in leaves of Avena fatua L. observed by low-temperature scanning electron microscopy

by van Gardingen P. R., Jeffree C. E., Grace J. (1989)

P. R. van Gardingen, Christopher E Jeffree, John Grace,

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In Plant, Cell and Environment 12: 887-888 – https://doi.org/10.1111/j.1365-3040.1989.tb01968.x – 

https://onlinelibrary.wiley.com/doi/full/10.1111/j.1365-3040.1989.tb01968.x

Abstract

A novel technique to record the variability of stomatal aperture over the leaf surface is described. This combines observations of leaf surfaces using low‐temperature scanning electron microscopy (LTSEM), with digital image analysis to produce the most accurate aperture measurements obtained to date.

Leaf samples are rapidly immobilized by cryo‐fixation in liquid nitrogen and stored in a purpose‐built cryo‐storage system. Specimens can be collected in the field, remote from the cryopreparation system, and stored for up to several weeks before being examined on the LTSEM. The advantages of this method are that the time frame of the measurements is accurately known, and is identical for all stomatal apertures in a sample, and the precision of the measurements is not limited by the resolving power of the microscope.

Measurements of stomatal aperture were obtained from leaves of field grown Avena fatua using the above procedure.

Leaf surface conductance (gsur) was determined by porometry immediately before cryo‐fixation of the same region of the leaf.

Measurements of aperture size showed a high degree of variability within each specimen, with coefficients of variation similar to those found in previous studies.

Stomatal conductance (gs) was calculated from stomatal dimensions using formulae derived elsewhere. A linear regression between the computed values of gsand porometric estimates of gsur showed good agreement with the regression line passing through the origin with a slope of 1.0 (R2=0.96). Applications of the experimental system are discussed.

Photosynthetic and stomatal responses of potatoes grown under elevated CO2 and/or O3

Photosynthetic and stomatal responses of potatoes grown under elevated CO2and/or O3 – results from the European CHIP-programme

by Vandermeiren K., Black C., Lawson T., Casanova M. A., Ojanperä K. (2002)

K. Vandermeiren, a, C. Black, b, T. Lawson, b, 1, M. A. Casanova, c, K. Ojanperä, d, 

Veterinary and Agrochemical Research Centre, B-3080 Tervuren, Belgium

School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK

Institute for Plant Ecology of the Justus-Liebig-University, D-35392 Giessen, Germany

dInstitute of Resource Management, Agricultural Research Centre of Finland, FIN-31600 Jokioinen, Finland

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In Eur. J. Agron. 17: 337-352 – https://doi.org/10.1016/S1161-0301(02)00070-9 – 

https://www.sciencedirect.com/science/article/abs/pii/S1161030102000709

Abstract

The physiological effects of elevated CO2 and/or O3 on Solanum tuberosum cv. Bintje were examined in Open-Top Chambers during 1998 and 1999 at experimental sites across Europe as part of the EU ‘Changing Climate and Potential Impacts on Potato Yield and Quality’ programme (CHIP).

At tuber initiation (≈20 days after emergence, DAE) elevated CO2 (680 μl l−1) induced a 40% increase in the light saturated photosynthetic rate (Asat) of fully expanded leaves in the upper canopy. This was 16% less than expected from short-term exposures of plants grown under ambient CO2 (360 μl l−1) to elevated CO2, indicating that photosynthetic acclimation began at an early stage of crop growth. This effect resulted from a combination of a 12% reduction in stomatal conductance (gs) and a decline in photosynthetic capacity, as indicated by the significant reductions in the maximum carboxylation rate of Rubisco (Vcmax) and light-saturated rate of electron transport (Jmax) under elevated CO2.

The seasonal decline in the promotion of photosynthesis by elevated CO2 reflected the concurrent decrease in gsVcmax and Jmax were both reduced in plants grown under elevated CO2 until shortly after maximum leaf area (MLA) was attained. Although non-photorespiratory mitochondrial respiration in the light (Rd) increased during the later stages of the season, net photosynthesis was consistently increased by elevated CO2 during the main part of the season.

Photosynthetic rate declined more rapidly in response to elevated O3 under ambient CO2, and the detrimental impact of O3 was most obvious after MLA was attained (DAE 40–50). Several exposure indices were compared, with the objective of determining the critical ozone level required to induce physiological effects.

The critical O3 exposure above which a 5% reduction in light saturated photosynthetic rate may be expected (expressed in terms of cumulative exposure above 0 nl l−1 O3 between emergence and specific dates during the season (AOT0-cum)) was 11 μl l−1 h; however this value should only be extrapolated beyond the CHIP dataset with caution.

The interaction between O3 and stomatal behaviour was more complex, as it was influenced by both long-term and daily exposure levels. Elevated CO2 counteracted the adverse effect of O3 on photosynthesis, perhaps because the observed reduction in stomatal conductance decreased O3 fluxes into the leaves.

The results are discussed in the context of nitrogen deficiency, carbohydrate accumulation and yield.

Effect of elevated CO2 concentration on stomatal parameters

Effect of elevated carbon dioxide concentration on the stomatal parameters of rice cultivars

by Uprety D. C., Dwivedi N., Jain V., Mohan R. (2002)

  • D.C. Uprety,
  • N. Dwivedi,
  • V. Jain,
  • R. Mohan,

Division of Plant Physiology, Indian Agricultural Research Institute, New Delhi-India

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In Photosynthetica 40: 315–319 – https://doi.org/10.1023/A:1021322513770

https://link.springer.com/article/10.1023/A:1021322513770

Abstract

The response of stomatal parameters of four rice cultivars to atmospheric elevated CO2concentration (EC) was studied using open top chambers.

EC brought about reduction in stomatal conductance and increase in stomatal index, size of stomatal guard cells, stroma, and epidermal cells.

Such acclimation helped the regulation of photosynthesis to EC. These changes in stomatal characters made rice cultivars adjustable to EC environment,

Changes in stomatal conductance and net photosynthesis

Changes in stomatal conductance and net photosynthesis during phenological development in spring wheat: Implications for gas exchange modelling

by Uddling J., Pleijel H. (2006)

Johan Uddling, H. Pleijel,

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In International Journal of Biometeorology 51: 37–48 – DOI: 10.1007/s00484-006-0039-6 – 

https://www.ncbi.nlm.nih.gov/pubmed/16733690

Abstract

Gas exchange was measured from 1 month before the onset of anthesis until the end of grain filling in field-grown spring wheat, Triticum aestivum L., cv. Vinjett, in southern Sweden.

Two g ( s ) models were parameterised using these data:

one Jarvis-type multiplicative g ( s ) model (J-model),

and one combined stomatal-photosynthesis model (L-model).

In addition, the multiplicative g ( s ) model parameterisation for wheat used within the European Monitoring and Evaluation Programme (EMEP-model) was tested and evaluated. The J-model performed well (R (2)=0.77), with no systematic pattern of the residuals plotted against the driving variables. The L-model explained a larger proportion of the variation in g ( s ) data when observations of A (n) were used as input data (R (2)=0.71) compared to when A (n) was modelled (R (2)=0.53).

In both cases there was a systematic model failure, with g (s) being over- and underestimated before and after anthesis, respectively.

This pattern was caused by the non-parallel changes in g ( s ) and A (n) during plant phenological development, with A (n) both peaking and starting to decline earlier as compared to g ( s ). The EMEP-model accounted for 41% of the variation in g ( s ) data, with g ( s ) being underestimated after anthesis.

We conclude that, under the climatic conditions prevailing in southern Scandinavia, the performance of the combined stomatal-photosynthesis approach is hampered by the non-parallel changes in g ( s ) and A (n), and that the phenology function of the EMEP-model, having a sharp local maximum at anthesis, should be replaced by a function with a broad non-limiting period after anthesis.