Stomatal Development In Response Research Articles

TOR and SnRK1 fine tune SPEECHLESS transcription and protein stability to optimize stomatal development in response to exogenously supplied sugar.

In Arabidopsis, the differentiation of epidermal cells into stomata is regulated by endogenous and environmental signals. Sugar is required for plant epidermal cell proliferation and differentiation. However, it is unclear how epidermal cells maintain division and differentiation to generate proper amounts of stomata in response to different sugar availability. Here, we show that two evolutionarily conserved kinase Snf1-related protein kinase 1 (SnRK1) and Target of rapamycin (TOR) play critical roles in the regulation of stomatal development under different sugar availability. When plants are grown on a medium containing 1% sucrose, sucrose-activated TOR promotes the stomatal development by inducing the expression of SPEECHLESS (SPCH), a master regulator of stomatal development. SnRK1 promotes stomatal development through phosphorylating and stabilizing SPCH. However, under the high sucrose conditions, the highly accumulated trehalose-6-phosphate (Tre6P) represses the activity of KIN10, the catalytic α-subunit of SnRK1, by reducing the interaction between KIN10 and its upstream kinase, consequently promoting SPCH degradation and inhibiting stomatal development. Our findings revealed that TOR and SnRK1 finely regulate SPCH expression and protein stability to optimize the stomatal development in response to exogenously supplied sugar.

Transcriptome and Metabolomic Analyses Reveal Regulatory Networks Controlling Maize Stomatal Development in Response to Blue Light.

(1) Background: Blue light is important for the formation of maize stomata, but the signal network remains unclear. (2) Methods: We replaced red light with blue light in an experiment and provided a complementary regulatory network for the stomatal development of maize by using transcriptome and metabolomics analysis. (3) Results: Exposure to blue light led to 1296 differentially expressed genes and 419 differential metabolites. Transcriptome comparisons and correlation signaling network analysis detected 55 genes, and identified 6 genes that work in the regulation of the HY5 module and MAPK cascade, that interact with PTI1, COI1, MPK2, and MPK3, in response to the substitution of blue light in environmental adaptation and signaling transduction pathways. Metabolomics analysis showed that two genes involved in carotenoid biosynthesis and starch and sucrose metabolism participate in stomatal development. Their signaling sites located on the PHI1 and MPK2 sites of the MAPK cascade respond to blue light signaling. (4) Conclusions: Blue light remarkably changed the transcriptional signal transduction and metabolism of metabolites, and eight obtained genes worked in the HY5 module and MAPK cascade.

KIN10 promotes stomatal development through stabilization of the SPEECHLESS transcription factor

Stomata are epidermal structures that modulate gas exchanges between plants and the atmosphere. The formation of stomata is regulated by multiple developmental and environmental signals, but how these signals are coordinated to control this process remains unclear. Here, we showed that the conserved energy sensor kinase SnRK1 promotes stomatal development under short-day photoperiod or in liquid culture conditions. Mutation of KIN10, the catalytic α-subunit of SnRK1, results in the decreased stomatal index; while overexpression of KIN10 significantly induces stomatal development. KIN10 displays the cell-type-specific subcellular location pattern. The nuclear-localized KIN10 proteins are highly enriched in the stomatal lineage cells to phosphorylate and stabilize SPEECHLESS, a master regulator of stomatal formation, thereby promoting stomatal development. Our work identifies a module links connecting the energy signaling and stomatal development and reveals that multiple regulatory mechanisms are in place for SnRK1 to modulate stomatal development in response to changing environments.

Elevated CO2 promotes satellite stomata production in young cotyledons of Arabidopsis thaliana.

Stomata are tiny pores on plant leaves and stems surrounded by a pair of differentiated epidermal cells known as guard cells. Plants undergo guard cell differentiation in response to environmental cues, including atmospheric CO2 . To quantitatively evaluate stomatal development in response to elevated CO2 , imaging analysis of stomata was conducted using young cotyledons of Arabidopsis thaliana grown under ambient (380ppm) and elevated (1,000ppm) CO2 conditions. Our analysis revealed that treatment with 1,000ppm CO2 did not affect stomatal numbers on abaxial sides of cotyledons but increased cotyledon area, resulting in decreased stomatal density, 7days after germination. Interestingly, this treatment also perturbed the uniform distribution of stomata via excess satellite stomata and stomatal precursor cells. We used overexpression lines of the DNA replication licensing factor gene CDC6, a reported positive regulator of satellite stomata production. CDC6 overexpression decreased the speed of cotyledon expansion, even under treatment with 1,000ppm CO2 , possibly by suppressing pavement cell maturation. In contrast, treatment with 1,000ppm CO2 induced stomatal distribution changes in the overexpressor. These results suggest that treatment with 1,000ppm CO2 enhances both cotyledon expansion and satellite stomata production via independent pathways, at least in young cotyledons of A.thaliana.

HY5 is not integral to light mediated stomatal development in Arabidopsis.

Light is a crucial signal that regulates many aspects of plant physiology and growth including the development of stomata, the pores in the epidermal surface of the leaf. Light signals positively regulate stomatal development leading to changes in stomatal density and stomatal index (SI; the proportion of cells in the epidermis that are stomata). Both phytochrome and cryptochrome photoreceptors are required to regulate stomatal development in response to light. The transcription factor ELONGATED HYPOCOTYL 5 (HY5) is a key regulator of light signalling, acting downstream of photoreceptors. We hypothesised that HY5 could regulate stomatal development in response to light signals due to the putative presence of HY5 binding sites in the promoter of the STOMAGEN (STOM) gene, which encodes a peptide regulator of stomatal development. Our analysis shows that HY5 does have the potential to regulate the STOM promoter in vitro and that HY5 is expressed in both the epidermis and mesophyll. However, analysis of hy5 and hy5 hyh double mutants (HYH; HY5-HOMOLOG), found that they had normal stomatal development under different light conditions and the expression of stomatal developmental genes was not perturbed following light shift experiments. Analysis of stable lines overexpressing HY5 also showed no change in stomatal development or the expression of stomatal developmental genes. We therefore conclude that whilst HY5 has the potential to regulate the expression of STOM, it does not have a major role in regulating stomatal development in response to light signals.

A Ca2+/CaM-regulated transcriptional switch modulates stomatal development in response to water deficit

Calcium (Ca2+) signals are decoded by the Ca2+-sensor protein calmodulin (CaM) and are transduced to Ca2+/CaM-binding transcription factors to directly regulate gene expression necessary for acclimation responses in plants. The molecular mechanisms of Ca2+/CaM signal transduction processes and their functional significance remains enigmatic. Here we report a novel Ca2+/CaM signal transduction mechanism that allosterically regulates DNA-binding activity of GT2-LIKE 1 (GTL1), a transrepressor of STOMATAL DENSITY AND DISTRIBUTION 1 (SDD1), to repress stomatal development in response to water stress. We demonstrated that Ca2+/CaM interaction with the 2nd helix of the GTL1 N-terminal trihelix DNA-binding domain (GTL1N) destabilizes a hydrophobic core of GTL1N and allosterically inhibits 3rd helix docking to the SDD1 promoter, leading to osmotic stress-induced Ca2+/CaM-dependent activation (de-repression) of SDD1 expression. This resulted in GTL1-dependent repression of stomatal development in response to water-deficit stress. Together, our results demonstrate that a Ca2+/CaM-regulated transcriptional switch on a trihelix transrepressor directly transduces osmotic stress to repress stomatal development to improve plant water-use efficiency as an acclimation response.

Drought induces alterations in the stomatal development program in Populus.

Much is known about the physiological control of stomatal aperture as a means by which plants adjust to water availability. By contrast, the role played by the modulation of stomatal development to limit water loss has received much less attention. The control of stomatal development in response to water deprivation in the genus Populus is explored here. Drought induced declines in stomatal conductance as well as an alteration in stomatal development in two genotypes of Populus balsamifera. Leaves that developed under water-deficit conditions had lower stomatal indices than leaves that developed under well-watered conditions. Transcript abundance of genes that could hypothetically underpin drought-responsive changes in stomatal development was examined, in two genotypes, across six time points, under two conditions, well-watered and with water deficit. Populus homologues of STOMAGEN, ERECTA (ER), STOMATA DENSITY AND DISTRIBUTION 1 (SDD1), and FAMA had variable transcript abundance patterns congruent with their role in the modulation of stomatal development in response to drought. Conversely, there was no significant variation in transcript abundance between genotypes or treatments for the Populus homologues of YODA (YDA) and TOO MANY MOUTHS (TMM). The findings highlight the role that could be played by stomatal development during leaf expansion as a longer term means by which to limit water loss from leaves. Moreover, the results point to the key roles played by the regulation of the homologues of STOMAGEN, ER, SDD1, and FAMA in the control of this response in poplar.

A view from the top: new ligands controlling stomatal development in Arabidopsis

A view from the top: new ligands controlling stomatal development in Arabidopsis

Phytochrome B and PIF4 regulate stomatal development in response to light quantity

Stomata are pores on the surfaces of leaves that regulate gas exchange between the plant interior and the atmosphere [1]. Plants adapt to changing environmental conditions in the short term by adjusting the aperture of the stomatal pores, whereas longer-term changes are accomplished by altering the proportion of stomata that develop on the leaf surface [2, 3]. Although recent work has identified genes involved in the control of stomatal development [4], we know very little about how stomatal development is modulated by environmental signals, such as light. Here, we show that mature leaves of Arabidopsis grown at higher photon irradiances show significant increases in stomatal index (S.I.) [5] compared to those grown at lower photon irradiances. Light quantity-mediated changes in S.I. occur in red light, suggesting that phytochrome photoreceptors [6] are involved. By using a genetic approach, we demonstrate that this response is dominated by phytochrome B and also identify a role for the transcription factor, PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) [7]. In sum, we identify a photoreceptor and downstream signaling protein involved in light-mediated control of stomatal development, thereby establishing a tractable system for investigating how an environmental signal modulates stomatal development.

The missing link? Arabidopsis SPCH is a MAPK specificity factor that controls entry into the stomatal lineage

Mitogen activated protein kinase (MAPK) signaling modules that incorporate AtMPK3 and AtMPK6 control critical aspects of Arabidopsis biology including stress responses, development, cell division and cell death. Arabidopsis stomatal development is negatively regulated by the YDA-MKK4/5-MPK3/6 MAPK module and follows a three step pathway of asymmetric and symmetric divisions followed by terminal differentiation. We have identified the bHLH transcription factor SPCH, which controls entry into the stomatal lineage as a substrate of AtMPK3 and AtMPK6. These findings suggest that SPCH activity may be directly affected by environmental conditions to enable the plant to modify stomatal development in response to suboptimal climates.

Phytochrome B and PIF4 Regulate Stomatal Development in Response to Light Quantity

Stomata are pores on the surfaces of leaves that regulate gas exchange between the plant interior and the atmosphere [1]. Plants adapt to changing environmental conditions in the short term by adjusting the aperture of the stomatal pores, whereas longer-term changes are accomplished by altering the proportion of stomata that develop on the leaf surface [2, 3]. Although recent work has identified genes involved in the control of stomatal development [4], we know very little about how stomatal development is modulated by environmental signals, such as light. Here, we show that mature leaves of Arabidopsis grown at higher photon irradiances show significant increases in stomatal index (S.I.) [5] compared to those grown at lower photon irradiances. Light quantity-mediated changes in S.I. occur in red light, suggesting that phytochrome photoreceptors [6] are involved. By using a genetic approach, we demonstrate that this response is dominated by phytochrome B and also identify a role for the transcription factor, PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) [7]. In sum, we identify a photoreceptor and downstream signaling protein involved in light-mediated control of stomatal development, thereby establishing a tractable system for investigating how an environmental signal modulates stomatal development.

Stomatal Pore Density

As atmospheric CO 2 concentration increases, the density of stomatal pores on the leaf surface decreases to prevent loss of water during transpiration. An analysis of mutants by Gray et al. reveals that a gene in the plant Arabidposis thaliana called high carbon dioxide ( HIC ) may be responsible for regulating stomatal development in response to CO 2 . HIC , expressed exclusively in guard cells that flank stomatal pores, encodes a putative 3-keto acyl coenzyme A synthase, an enzyme involved in synthesizing long-chain fatty acids that comprise components of the extracellular matrix found at the surface of guard cells. When HIC expression is disrupted, plants can no longer respond to increases in CO 2 . The authors propose that absence of the HIC -encoded enzyme could alter the composition of the extracellular matrix and thus affect diffusion of CO 2 -regulated morphogens that regulate stomatal development. Gray, J.E., Holroyd, G.H., Van der Lee, F.M., Bahrami, A.R., Sijmons, P.C., Woodward, F.I., Schuch, W., and Hetherington, A.M. (2000) The HIC signalling pathway links CO 2 perception to stomatal development. Nature 408 : 713-716. [Online Journal]