The<i>Arabidopsis</i>GTL1 Transcription Factor Regulates Water Use Efficiency and Drought Tolerance by Modulating Stomatal Density via Transrepression of<i>SDD1</i>

Yoo, Chan Yul; Pence, Heather E.; Jin, Jing Bo; Miura, Kenji; Gosney, Michael J.; Hasegawa, Paul M.; Mickelbart, Michael V.

doi:10.1105/tpc.110.078691

Cited by 311 publications

(348 citation statements)

References 67 publications

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“…Gains in WUE have been found to be associated with trade-offs in growth potential (8)(9)(10). WUE is controlled by genes regulating stomatal density and size (11)(12)(13). Stomatal aperture is, in turn, controlled by abscisic acid (ABA) signaling (14).…”

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confidence: 99%

Leveraging abscisic acid receptors for efficient water use in Arabidopsis

Yang

Liu

Tischer

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

113

141

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Plant growth requires the influx of atmospheric CO 2 through stomatal pores, and this carbon uptake for photosynthesis is inherently associated with a large efflux of water vapor. Under water deficit, plants reduce transpiration and are able to improve carbon for water exchange leading to higher water use efficiency (WUE). Whether increased WUE can be achieved without trade-offs in plant growth is debated. The signals mediating the WUE response under water deficit are not fully elucidated but involve the phytohormone abscisic acid (ABA). ABA is perceived by a family of related receptors known to mediate acclimation responses and to reduce transpiration. We now show that enhanced stimulation of ABA signaling via distinct ABA receptors can result in plants constitutively growing at high WUE in the model species Arabidopsis. WUE was assessed by three independent approaches involving gravimetric analyses, 13 C discrimination studies of shoots and derived cellulose fractions, and by gas exchange measurements of whole plants and individual leaves. Plants expressing the ABA receptors RCAR6/PYL12 combined up to 40% increased WUE with high growth rates, i.e., are water productive. Water productivity was associated with maintenance of net carbon assimilation by compensatory increases of leaf CO 2 gradients, thereby sustaining biomass acquisition. Leaf surface temperatures and growth potentials of plants growing under well-watered conditions were found to be reliable indicators for water productivity. The study shows that ABA receptors can be explored to generate more plant biomass per water transpired, which is a prime goal for a more sustainable water use in agriculture.carbon assimilation | drought resistance | water deficit | water productivity | water use efficiency P lants are ferocious consumers of water, and plant transpiration is the dominant vector for water mobilization from terrestrial surfaces to the atmosphere (1). Plant transpiration is sustained by efficient water uptake through the root systems, which can comprise 500 m 2 of root surface and 500 km in combined length even in a single barley plant. Water is the major factor limiting crop productivity in the field (2). Thus, more than two-thirds of the fresh water resources used globally are channeled into agriculture, thereby contributing to potential social conflicts over water (3).Whereas the gas exchange of CO 2 and water vapor at the stomatal pore is a physical process controlled by both the ratio in partial pressure gradients and gas diffusivities (4, 5), terrestrial plants are able to capture carbon more efficiently under water deficit. Both short-term leaf gas exchange measurements and 13 C isotope discrimination analyses revealed increases of the instantaneous water use efficiency (insWUE) and intrinsic WUE (iWUE), respectively, by a factor of 1.5-2.5 in wheat and other species (6, 7). The underlying mechanisms, however, are not fully elucidated. Gains in WUE have been found to be associated with trade-offs in growth potential (8-10). WUE is control...

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mentioning

confidence: 99%

Leveraging abscisic acid receptors for efficient water use in Arabidopsis

Yang

Liu

Tischer

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

113

141

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“…For example, transcriptional analysis of guard cells from epidermal fragments (Wang et al, 2012) or microdisection of individual guard cells (Gandotra et al, 2013), along with single-cell metabolic profiling (Burrell et al, 2007), have greatly assisted in our understanding of the metabolic signaling and response pathways within guard cells. The identification of highly specific guard cell promoters (Müller-Röber et al, 1994;Cominelli et al, 2005) and transcription factors (Cominelli et al, 2010;Yoo et al, 2010), the production of guard cell enhancer trap lines (Gardner et al, 2009), and the ability to induce transient expression in guard cells (Rusconi et al, 2013) open up new exciting potential approaches to not only fully understand signaling and transduction pathways in guard cells but also to provide us with the tools to manipulate guard cell metabolism in order to improve plant WUE. Such tools have greatly improved our understanding of the molecular networks that control guard cell perception of and response to internal and external environmental cues and have provided possible candidates for manipulation (Galbiati et al, 2008;Rusconi et al, 2013).…”

Section: Resultsmentioning

confidence: 99%

“…GTL1 is a transcription factor that regulates trichome and stomatal development through its interaction with SDD1 expression (Breuer et al, 2009). Physiological analysis of these plants revealed no difference in photosynthetic rates over a range of light levels but reduced g s and transpiration (Yoo et al, 2009(Yoo et al, , 2010, illustrating that manipulating one gene related to stomatal development can "fine-tune" WUE.…”

Section: Stomatal Anatomymentioning

confidence: 99%

Stomatal Size, Speed, and Responsiveness Impact on Photosynthesis and Water Use Efficiency

2014

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The control of gaseous exchange between the leaf and bulk atmosphere by stomata governs CO 2 uptake for photosynthesis and transpiration, determining plant productivity and water use efficiency. The balance between these two processes depends on stomatal responses to environmental and internal cues and the synchrony of stomatal behavior relative to mesophyll demands for CO 2 . Here we examine the rapidity of stomatal responses with attention to their relationship to photosynthetic CO 2 uptake and the consequences for water use. We discuss the influence of anatomical characteristics on the velocity of changes in stomatal conductance and explore the potential for manipulating the physical as well as physiological characteristics of stomatal guard cells in order to accelerate stomatal movements in synchrony with mesophyll CO 2 demand and to improve water use efficiency without substantial cost to photosynthetic carbon fixation. We conclude that manipulating guard cell transport and metabolism is just as, if not more likely to yield useful benefits as manipulations of their physical and anatomical characteristics. Achieving these benefits should be greatly facilitated by quantitative systems analysis that connects directly the molecular properties of the guard cells to their function in the field.In order for plants to function efficiently, they must balance gaseous exchange between inside and outside the leaf to maximize CO 2 uptake for photosynthetic carbon assimilation (A) and to minimize water loss through transpiration. Stomata are the "gatekeepers" responsible for all gaseous diffusion, and they adjust to both internal and external environmental stimuli governing CO 2 uptake and water loss. The pathway for CO 2 uptake from the bulk atmosphere to the site of fixation is determined by a series of diffusional resistances, which start with the layer of air immediately surrounding the leaf (the boundary layer). Stomatal pores provide a major resistance to flux from the atmosphere to the substomatal cavity within the leaf. Further resistance is encountered by CO 2 across the aqueous and lipid boundaries into the mesophyll cell and chloroplasts (mesophyll resistance). Water leaving the leaf largely follows the same pathway in reverse, but without the mesophyll resistance component. Guard cells surround the stomatal pore. They increase or decrease in volume in response to external and internal stimuli, and the resulting changes in guard cell shape adjust stomatal aperture and thereby affect the flux of gases between the leaf internal environment and the bulk atmosphere. Stomatal behavior, therefore, controls the volume of CO 2 entering the intercellular air spaces of the leaf for photosynthesis. It also plays a key role in minimizing the amount of water lost. Transpiration, by virtue of the concentration differences, is an order of magnitude greater than CO 2 uptake, which is an inevitable consequence of free diffusion across this pathway. Although the cumulative area of stomatal pores only represents a small fraction...

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“…Thus, the drought tolerance phenotype of the cych;1 RNAi mutant may be due to lower transpiration rates. To confirm this, we investigated the transpiration rate by means of gravimetric analyses over diurnal light/ dark periods (Yoo et al, 2010). The cych;1 RNAi plants exhibited a lower transpiration rate than the wild type during the light period, but transpiration rates were similar in mutant and wild-type plants during the dark period (Fig.…”

Section: Morphological Phenotypes Of the Cych;1 Rnai Mutantsmentioning

confidence: 99%

“…Water loss rate was calculated as (initial fresh weight-final fresh weight)/initial fresh weight 3 100%. Wild-type and mutant plants grown for 5 weeks in a growth room with 10-h light/14-h dark were subjected to a transpiration rate assay as described previously (Yoo et al, 2010).…”

Section: Water Lossmentioning

confidence: 99%

CYCLIN H;1 Regulates Drought Stress Responses and Blue Light-Induced Stomatal Opening by Inhibiting Reactive Oxygen Species Accumulation in Arabidopsis

Zhou

Jin

Yoo³

et al. 2013

Plant Physiology

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Arabidopsis (Arabidopsis thaliana) CYCLIN-DEPENDENT KINASE Ds (CDKDs) phosphorylate the C-terminal domain of the largest subunit of RNA polymerase II. Arabidopsis CYCLIN H;1 (CYCH;1) interacts with and activates CDKDs; however, the physiological function of CYCH;1 has not been determined. Here, we report that CYCH;1, which is localized to the nucleus, positively regulates blue light-induced stomatal opening. Reduced-function cych;1 RNA interference (cych;1 RNAi ) plants exhibited a drought tolerance phenotype. CYCH;1 is predominantly expressed in guard cells, and its expression was substantially down-regulated by dehydration. Transpiration of intact leaves was reduced in cych;1 RNAi plants compared with the wild-type control in light but not in darkness. CYCH;1 down-regulation impaired blue light-induced stomatal opening but did not affect guard cell development or abscisic acid-mediated stomatal closure. Microarray and real-time polymerase chain reaction analyses indicated that CYCH;1 did not regulate the expression of abscisic acid-responsive genes or light-induced stomatal opening signaling determinants, such as MYB60, MYB61, Hypersensitive to red and blue1, and Protein phosphatase7. CYCH;1 down-regulation induced the expression of redox homeostasis genes, such as LIPOXYGENASE3 (LOX3), LOX4, ARABIDOPSIS GLUTATHIONE PEROXIDASE 7 (ATGPX7), EARLY LIGHT-INDUCIBLE PROTEIN1 (ELIP1), and ELIP2, and increased hydrogen peroxide production in guard cells. Furthermore, loss-of-function mutations in CDKD;2 or CDKD;3 did not affect responsiveness to drought stress, suggesting that CYCH;1 regulates the drought stress response in a CDKD-independent manner. We propose that CYCH;1 regulates blue light-mediated stomatal opening by controlling reactive oxygen species homeostasis.

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TheArabidopsisGTL1 Transcription Factor Regulates Water Use Efficiency and Drought Tolerance by Modulating Stomatal Density via Transrepression ofSDD1

Cited by 311 publications

References 67 publications

Leveraging abscisic acid receptors for efficient water use in Arabidopsis

Leveraging abscisic acid receptors for efficient water use in Arabidopsis

Stomatal Size, Speed, and Responsiveness Impact on Photosynthesis and Water Use Efficiency

CYCLIN H;1 Regulates Drought Stress Responses and Blue Light-Induced Stomatal Opening by Inhibiting Reactive Oxygen Species Accumulation in Arabidopsis

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