Gene Research for GO Annotation Review

Target

• Gene symbol: SPCH
• Organism: Arabidopsis thaliana

UniProt Context

=== UNIPROT METADATA ===
UniProt ID: Q700C7
Entry Name: SPCH_ARATH
Gene Name: SPCH
Locus Tag: At5g53210 {ECO:0000312|Araport:AT5G53210}
Gene Synonyms: BHLH98 {ECO:0000303|PubMed:12679534,
Protein Name: Transcription factor SPEECHLESS
Organism: Arabidopsis thaliana (Mouse-ear cress)
NCBI Taxonomy ID: 3702
Function: Transcription factor acting as an integration node for stomata and brassinosteroid (BR) signaling pathways to control stomatal initiation and development (PubMed:22466366, PubMed:28507175). Activates transcription when in the presence of SCRM/ICE1 (PubMed:28507175). Functions as a dimer with SCRM or SCRM2 during stomatal initiation (PubMed:18641265). Required for the initiation, the spacing and the formation of stomata, by promoting the first asymmetric cell divisions (PubMed:19008449, PubMed:25680231, PubMed:25843888). Together with FMA and MUTE, modulates the stomata formation. Involved in the regulation of growth reduction under osmotic stress (e.g. mannitol), associated with a quick decrease of meristemoid mother cells (MMCs) number lower stomatal index and density (PubMed:25381317).
Subcellular Location: Nucleus
Subunit: Homodimer (Probable). Forms dimers with SCRM and SCRM2 (PubMed:18641265, PubMed:28507175). May interact with CDKA-1 (PubMed:25680231).
======================

Research Objective

Prepare a comprehensive literature-backed research report for GO annotation review of the target gene.

Focus on:

1. The core biochemical activity of the gene product and any substrate specificity.
2. The activation or maturation mechanism of the protein, including proteolytic processing if relevant.
3. The best-supported subcellular localization and complexes where the active protein functions.
4. The strongest experimentally supported biological processes in the target organism, or in very close orthologs when transfer is justified.
5. Which annotations appear to reflect core function versus context-specific, pleiotropic, or over-extended roles.
6. Any evidence bearing on apoptosis, developmental cell death, neuronal roles, inflammatory signaling, pyroptosis, synaptic remodeling, protein processing, and localization to cytoplasm, cytosol, nucleus, or signaling complexes.

Output Requirements

Structure the report as:

1. Executive summary
2. Molecular function
3. Biological process roles
4. Cellular localization and complexes
5. Annotation-risk assessment
6. Key literature

Use citations for all substantive claims.

Executive summary

Gene/product: Arabidopsis thaliana SPCH (SPEECHLESS; UniProt Q700C7; At5g53210) encodes a basic helix–loop–helix (bHLH) sequence-specific transcription factor that is necessary and sufficient to initiate stomatal lineage entry and promote the asymmetric (amplifying/entry) cell divisions that generate stomatal precursors. The consensus view from recent authoritative synthesis (2024) is that SPCH is the master regulator of stomatal lineage initiation whose activity is tuned by peptide-receptor/MAPK signaling and multiple environmental inputs. (chua2024stomataldevelopmentin pages 1-2)

Core molecular function (GO MF focus): SPCH binds promoter cis-elements consistent with E-box/G-box class motifs and acts primarily as a transcriptional activator of stomatal-lineage regulators; direct binding/activation is supported by EMSA and reporter activation for at least the MUTE promoter, and by genome-scale association/motif enrichment from ChIP-seq. (cao2021arabidopsiscryptochrome1 pages 6-9, marcos2017amutationin pages 27-30, liu2024bhlhtranscriptionfactors pages 3-5)

Key complexes and localization (GO CC focus): SPCH functions in the nucleus, typically as an obligate heterodimer with bHLH partners SCREAM/ICE1 (SCRM/ICE1) and SCRM2. Nuclear protein–protein interaction data also support SPCH association with PP2A A subunits (stabilizing dephosphorylation) and with AGB1 (inhibitory binding to the bHLH DNA-binding domain). (bian2020proteinphosphatase2a pages 6-7, cao2021arabidopsiscryptochrome1 pages 6-9, chua2024stomataldevelopmentin pages 1-2)

Regulatory mechanism (activation/maturation): SPCH is not known to undergo proteolytic maturation; instead, its effective activity depends on phosphorylation state and protein stability. SPCH is regulated by CDKA;1 phosphorylation at Ser186 (positive) and by MAPK (YDA→MPK3/6) and BIN2 (BR pathway) phosphorylation (generally inhibitory/ destabilizing); PP2A dephosphorylation stabilizes SPCH and counteracts phosphorylation-dependent proteasome-mediated degradation, evidenced by MG132 rescue. (yang2015phosphorylationofserine pages 1-5, bian2020proteinphosphatase2a pages 6-7, bian2020proteinphosphatase2a pages 5-6)

Recent developments (prioritizing 2023–2024): A 2024 PLOS Biology study integrates scRNA-seq and ChIP-seq to propose that stomatal bHLH factors (including SPCH) act in a chromatin context where targets can be repressed prior to activation, and that bHLHs cooperate with chromatin regulators (SWI/SNF and HAC1 identified by proximity labeling) to enable fate transitions; importantly, SPCH is solidly supported as the initiator but its role as a “pioneer factor” remains unresolved. A 2024 Development review contextualizes SPCH as a central integrator of environmental plasticity of stomatal development under climate-relevant cues. (liu2024bhlhtranscriptionfactors pages 1-2, liu2024bhlhtranscriptionfactors pages 15-16, chua2024stomataldevelopmentin pages 1-2)

Annotation risk/exclusions: Across the retrieved evidence base, there is no support for annotations involving apoptosis/developmental cell death, neuronal roles, inflammatory signaling, pyroptosis, synaptic remodeling, or proteolytic processing/maturation. (cao2021arabidopsiscryptochrome1 pages 6-9, bian2020proteinphosphatase2a pages 7-9, chua2024stomataldevelopmentin pages 1-2)

Molecular function

Key concepts and definitions (current understanding)

1. bHLH transcription factor activity: bHLH proteins generally recognize E-box (CANNTG) / G-box (CACGTG)-class DNA elements via their basic region and dimerize via the HLH region. SPCH is widely described as a stomatal-lineage master bHLH regulator. (chua2024stomataldevelopmentin pages 1-2, marcos2017amutationin pages 1-5)

2. Sequence specificity and direct promoter binding: A Plant Physiology study analyzing SPCH genomic binding reports that SPCH binds proximal promoters genome-wide and that binding sites are enriched for an E-box motif variant “CDCGTG” (degenerate code: D=A/G/T), consistent with canonical bHLH preferences. (marcos2017amutationin pages 27-30)

3. Transcriptional activation with partner bHLHs: SPCH’s transcriptional activity is commonly modeled as requiring heterodimerization with SCRM/ICE1 family partners (SCRM/ICE1 and SCRM2), consistent with bHLH behavior and genetic requirement. (chua2024stomataldevelopmentin pages 1-2, chen2020speechlessspeaksloudly pages 1-2)

Core biochemical activity and substrate specificity

SPCH is best curated as:

• Sequence-specific DNA binding (E-box/G-box-like motifs), and
• RNA polymerase II transcription factor activity regulating stomatal-lineage gene expression.

Direct experimental support:

• EMSA: recombinant GST-SPCH binds the MUTE promoter DNA probe in a concentration-dependent manner. (cao2021arabidopsiscryptochrome1 pages 6-9)
• Dual-luciferase reporter: SPCH activates the MUTE promoter, and AGB1 can suppress this activation (functional readout of TF activity). (cao2021arabidopsiscryptochrome1 pages 6-9)

Partners influencing activity (expert/authoritative analyses)

• SCRM/ICE1 and SCRM2: SPCH acts with these bHLH partners to drive stomatal lineage transitions, with genetic evidence that loss of both SCRM/ICE1 and SCRM2 eliminates stomatal formation. (chen2020speechlessspeaksloudly pages 1-2, chua2024stomataldevelopmentin pages 1-2)
• AGB1 (G-protein β subunit): AGB1 physically binds SPCH via the N-terminal bHLH-containing region and inhibits SPCH’s DNA-binding and transcriptional output in vitro/in vivo assays, providing a mechanistic route for signaling crosstalk. (cao2021arabidopsiscryptochrome1 pages 6-9)

Biological process roles

Strongest experimentally supported roles in Arabidopsis

1. Stomatal lineage initiation / stomatal precursor cell formation:

2. The 2024 Development review emphasizes SPCH as a master TF essential for stomatal precursor formation; loss-of-function spch mutants lack stomatal precursors/stomata (seedling lethal), while increased activity (e.g., MAPK-insensitive SPCH) drives extra divisions. (chua2024stomataldevelopmentin pages 1-2)

3. Asymmetric cell division in stomatal lineage:

4. SPCH promotes the entry and amplifying asymmetric divisions that generate meristemoids and stomatal lineage ground cells. (chua2024stomataldevelopmentin pages 1-2, fung2025multiscaledynamicsinfluence pages 1-2)

5. Stomatal patterning/spacing via feedback to signaling:

6. SPCH is described as controlling spacing/patterning through direct regulation of EPF2–TMM–ERECTA-family signaling components (network-level feedback restricting excessive initiation). (chen2020speechlessspeaksloudly pages 2-4)

Environmental plasticity (recent authoritative synthesis)

The 2024 Development review frames stomatal development as climate-sensitive and highlights SPCH as a key node modulated by abiotic cues, with specific cited evidence including osmotic stress reducing SPCH protein abundance and ABA acting through EPF–SPCH-associated pathways. (chua2024stomataldevelopmentin pages 12-13)

A key mechanistic example of transcriptional control by temperature is provided by a primary study showing PIF4 directly binds the SPCH promoter and represses SPCH at warm temperatures, reducing stomatal production, positioning SPCH as an integration point for temperature signaling. (lau2018directcontrolof pages 1-3)

Chromatin and transcriptional-phase logic (2023–2024 research)

A 2024 PLOS Biology study integrating scRNA-seq/ChIP-seq/MNase-seq supports a model where stomatal fate transitions involve bHLH binding to targets that can be embedded in repressive chromatin prior to activation, and identifies candidate chromatin machinery (SWI/SNF, HAC1) that physically associates with stomatal bHLHs; knockdown of these factors disrupts activation of bHLH targets and causes stomatal defects. (liu2024bhlhtranscriptionfactors pages 1-2, liu2024bhlhtranscriptionfactors pages 3-5)

Notably, the same study indicates that while later bHLH complexes (e.g., MUTE-SCRM, FAMA-SCRM) show evidence consistent with accessing/restructuring repressive chromatin, whether SPCH itself has biochemical “pioneer-factor” activity remains unclear, so chromatin-remodeling annotations should be conservative. (liu2024bhlhtranscriptionfactors pages 15-16)

Cellular localization and complexes

Best-supported subcellular localization

Nucleus: Multiple orthogonal assays support SPCH function and physical interactions in the nucleus.

• PP2A-SPCH BiFC signals localize to nuclei in tobacco epidermal cells, supporting nuclear association of SPCH with PP2A A-subunits. (bian2020proteinphosphatase2a pages 6-7, bian2020proteinphosphatase2a media 4c45dadc)
• SPCH-AGB1 BiFC shows nuclear fluorescence using an RFP-H2B nuclear marker. (cao2021arabidopsiscryptochrome1 pages 6-9)
• In stomatal lineage cells, SPCH transcriptional reporters (nuclear) are broadly present, while SPCH translational fusions are restricted to specific precursor states, supporting nuclear function with strong protein-level regulation. (yang2015phosphorylationofserine pages 5-8)

Complexes

• SPCH–SCRM/ICE1 and SPCH–SCRM2 heterodimers: Widely supported as functional units in stomatal development; SPCH–ICE1 interaction is used as a positive control in BiFC assays. (chen2020speechlessspeaksloudly pages 1-2, bian2020proteinphosphatase2a pages 6-7)
• SPCH–PP2A (A subunit) nuclear complex: Supported by yeast two-hybrid, BiFC, and pull-down assays; functional data show PP2A stabilizes SPCH. (bian2020proteinphosphatase2a pages 6-7, bian2020proteinphosphatase2a pages 5-6)
• SPCH–AGB1 nuclear interaction: Supported by yeast two-hybrid, pull-down, split-LUC, BiFC, and co-IP; has functional consequence of inhibiting SPCH DNA binding and transcriptional activation. (cao2021arabidopsiscryptochrome1 pages 6-9)

Annotation-risk assessment

Core function vs context-specific roles

• Core, high-confidence: stomatal lineage initiation; stomatal precursor asymmetric divisions; nuclear bHLH transcription factor activity; partnership with SCRM/ICE1 family partners. (chua2024stomataldevelopmentin pages 1-2, chen2020speechlessspeaksloudly pages 1-2)

• Well supported but network/context dependent: stomatal spacing/patterning via signaling feedback; environmental plasticity roles where SPCH is regulated by external cues (temperature via PIF4; osmotic stress via reduced SPCH protein; ABA-linked regulation discussed in 2024 review). These should typically be curated as regulation of stomatal development in response to stimulus, not as direct broad stress-response master roles. (lau2018directcontrolof pages 1-3, chua2024stomataldevelopmentin pages 12-13)

• Chromatin remodeling: Evidence supports cooperation of stomatal bHLHs with chromatin regulators for fate transitions, but direct assignment of SPCH to “chromatin remodeling” as a molecular function may be over-extended because SPCH’s pioneer capacity is explicitly described as unclear in the 2024 PLOS Biology work. (liu2024bhlhtranscriptionfactors pages 15-16, liu2024bhlhtranscriptionfactors pages 1-2)

Activation/maturation mechanism

• No proteolytic maturation: SPCH regulation is best described as phosphorylation-state control and proteasome-mediated degradation, not cleavage activation. MG132 rescues SPCH loss when PP2A is inhibited, supporting a phosphorylation→proteasome axis. (bian2020proteinphosphatase2a pages 6-7, bian2020proteinphosphatase2a media 4c45dadc)

Explicit exclusions requested

No retrieved evidence supports any role for SPCH in apoptosis, developmental cell death, neuronal biology, inflammatory signaling, pyroptosis, synaptic remodeling, or related animal processes. Such annotations should be avoided as biologically inappropriate and unsupported. (cao2021arabidopsiscryptochrome1 pages 6-9, bian2020proteinphosphatase2a pages 7-9)

Summary evidence table (for GO review)

Table: This table summarizes evidence-based GO annotation recommendations for Arabidopsis SPCH, distinguishing core stomatal-lineage functions from context-dependent regulatory roles and unsupported annotations. It is designed to support conservative, citation-traceable curation decisions.

Current applications and real-world implementations

While SPCH itself is a basic research target in Arabidopsis, its pathway is actively used as an engineering handle to tune stomatal density/patterning for climate resilience in crops. One recent example is cis-regulatory editing of SPCH orthologs (e.g., in tomato) to create alleles with altered stomatal development responses to environmental cues; this underscores translational interest in SPCH-centered developmental control modules, although these data are outside Arabidopsis GO annotation transfer without explicit orthology evidence. (nir2023targetingeditingof, not in evidence context; therefore not cited for claims beyond general translational framing)

Chemical biology also targets stomatal bHLH networks (e.g., perturbing bHLH heterodimers) to modulate development, suggesting future applications in controllable stomatal trait manipulation; however, detailed SPCH-specific chemical inhibitors were not directly evidenced in the retrieved SPCH primary sources used here. (nakagawa2024chemicalinhibitionof, not in evidence context)

Key literature (prioritizing 2023–2024, plus foundational mechanistic studies)

1. Chua LC, Lau OS. Stomatal development in the changing climate. Development. Oct 2024. https://doi.org/10.1242/dev.202681 (chua2024stomataldevelopmentin pages 1-2)
2. Liu A et al. bHLH transcription factors cooperate with chromatin remodelers to regulate cell fate decisions during Arabidopsis stomatal development. PLOS Biology. Aug 2024. https://doi.org/10.1371/journal.pbio.3002770 (liu2024bhlhtranscriptionfactors pages 1-2)
3. Cao X et al. Arabidopsis cryptochrome 1 promotes stomatal development through repression of AGB1 inhibition of SPEECHLESS DNA-binding activity. J Integr Plant Biol. Oct 2021. https://doi.org/10.1111/jipb.13168 (cao2021arabidopsiscryptochrome1 pages 6-9)
4. Bian C et al. Protein phosphatase 2A promotes stomatal development by stabilizing SPEECHLESS in Arabidopsis. PNAS. May 2020. https://doi.org/10.1073/pnas.1912075117 (bian2020proteinphosphatase2a pages 6-7)
5. Yang K-Z et al. Phosphorylation of Serine 186 of bHLH Transcription Factor SPEECHLESS Promotes Stomatal Development in Arabidopsis. Molecular Plant. May 2015. https://doi.org/10.1016/j.molp.2014.12.014 (yang2015phosphorylationofserine pages 1-5)
6. de Marcos A et al. A mutation in the bHLH domain of the SPCH transcription factor uncovers a BR-dependent mechanism for stomatal development. Plant Physiology. May 2017. https://doi.org/10.1104/pp.17.00615 (marcos2017amutationin pages 27-30)
7. Lau OS et al. Direct Control of SPEECHLESS by PIF4 in the High-Temperature Response of Stomatal Development. Current Biology. Apr 2018. https://doi.org/10.1016/j.cub.2018.02.054 (lau2018directcontrolof pages 1-3)

Statistics and quantitative data highlights (from primary studies)

• PP2A inhibition reduces SPCH protein-positive cells: In seedlings with translational SPCHpro::SPCH-CFP, PP2A inhibitor cantharidin caused a reduction in SPCH-CFP-positive cells after 1 h (13.8% CT vs 19.7% DMSO) and a stronger reduction after 4 h (5.2% CT vs 19.7% DMSO), while transcriptional reporter expression remained stable—consistent with post-translational control. (bian2020proteinphosphatase2a pages 5-6)
• Proteasome dependence: MG132 co-treatment “almost fully” restored SPCH-CFP under PP2A inhibition, supporting proteasome-mediated degradation when SPCH is hyperphosphorylated. (bian2020proteinphosphatase2a pages 6-7, bian2020proteinphosphatase2a media 4c45dadc)

References

1. (chua2024stomataldevelopmentin pages 1-2): Li Cong Chua and On Sun Lau. Stomatal development in the changing climate. Development (Cambridge, England), Oct 2024. URL: https://doi.org/10.1242/dev.202681, doi:10.1242/dev.202681. This article has 38 citations.

2. (cao2021arabidopsiscryptochrome1 pages 6-9): Xiaoli Cao, Pengbo Xu, Yao Liu, Guangqiong Yang, Minqing Liu, Li Chen, Yingyu Cheng, Pengbo Xu, Langxi Miao, Zhilei Mao, Wenxiu Wang, Shuang Kou, Tongtong Guo, and Hongquan Yang. arabidopsis cryptochrome 1 promotes stomatal development through repression of agb1 inhibition of speechless dna‐binding activity. Oct 2021. URL: https://doi.org/10.1111/jipb.13168, doi:10.1111/jipb.13168. This article has 21 citations and is from a peer-reviewed journal.

3. (marcos2017amutationin pages 27-30): Alberto de Marcos, Anaxi Houbaert, Magdalena Triviño, Dolores Delgado, Mar Martín-Trillo, Eugenia Russinova, Carmen Fenoll, and Montaña Mena. A mutation in the bhlh domain of the spch transcription factor uncovers a br-dependent mechanism for stomatal development. Plant Physiology, 174:823-842, May 2017. URL: https://doi.org/10.1104/pp.17.00615, doi:10.1104/pp.17.00615. This article has 43 citations and is from a highest quality peer-reviewed journal.

4. (liu2024bhlhtranscriptionfactors pages 3-5): Ao Liu, Andrea Mair, Juliana L. Matos, Macy Vollbrecht, Shou-Ling Xu, and Dominique C. Bergmann. Bhlh transcription factors cooperate with chromatin remodelers to regulate cell fate decisions during arabidopsis stomatal development. PLOS Biology, 22:e3002770, Aug 2024. URL: https://doi.org/10.1371/journal.pbio.3002770, doi:10.1371/journal.pbio.3002770. This article has 20 citations and is from a highest quality peer-reviewed journal.

5. (bian2020proteinphosphatase2a pages 6-7): Chao Bian, Xiaoyu Guo, Yi Zhang, Lu Wang, Tongda Xu, Alison DeLong, and Juan Dong. Protein phosphatase 2a promotes stomatal development by stabilizing speechless in arabidopsis. Proceedings of the National Academy of Sciences, 117:13127-13137, May 2020. URL: https://doi.org/10.1073/pnas.1912075117, doi:10.1073/pnas.1912075117. This article has 49 citations and is from a highest quality peer-reviewed journal.

6. (yang2015phosphorylationofserine pages 1-5): Ke-Zhen Yang, Min Jiang, Ming Wang, Shan Xue, Ling-Ling Zhu, Hong-Zhe Wang, Jun-Jie Zou, Eun-Kyoung Lee, Fred Sack, and Jie Le. Phosphorylation of serine 186 of bhlh transcription factor speechless promotes stomatal development in arabidopsis. Molecular plant, 8 5:783-95, May 2015. URL: https://doi.org/10.1016/j.molp.2014.12.014, doi:10.1016/j.molp.2014.12.014. This article has 66 citations and is from a highest quality peer-reviewed journal.

7. (bian2020proteinphosphatase2a pages 5-6): Chao Bian, Xiaoyu Guo, Yi Zhang, Lu Wang, Tongda Xu, Alison DeLong, and Juan Dong. Protein phosphatase 2a promotes stomatal development by stabilizing speechless in arabidopsis. Proceedings of the National Academy of Sciences, 117:13127-13137, May 2020. URL: https://doi.org/10.1073/pnas.1912075117, doi:10.1073/pnas.1912075117. This article has 49 citations and is from a highest quality peer-reviewed journal.

8. (liu2024bhlhtranscriptionfactors pages 1-2): Ao Liu, Andrea Mair, Juliana L. Matos, Macy Vollbrecht, Shou-Ling Xu, and Dominique C. Bergmann. Bhlh transcription factors cooperate with chromatin remodelers to regulate cell fate decisions during arabidopsis stomatal development. PLOS Biology, 22:e3002770, Aug 2024. URL: https://doi.org/10.1371/journal.pbio.3002770, doi:10.1371/journal.pbio.3002770. This article has 20 citations and is from a highest quality peer-reviewed journal.

9. (liu2024bhlhtranscriptionfactors pages 15-16): Ao Liu, Andrea Mair, Juliana L. Matos, Macy Vollbrecht, Shou-Ling Xu, and Dominique C. Bergmann. Bhlh transcription factors cooperate with chromatin remodelers to regulate cell fate decisions during arabidopsis stomatal development. PLOS Biology, 22:e3002770, Aug 2024. URL: https://doi.org/10.1371/journal.pbio.3002770, doi:10.1371/journal.pbio.3002770. This article has 20 citations and is from a highest quality peer-reviewed journal.

10. (bian2020proteinphosphatase2a pages 7-9): Chao Bian, Xiaoyu Guo, Yi Zhang, Lu Wang, Tongda Xu, Alison DeLong, and Juan Dong. Protein phosphatase 2a promotes stomatal development by stabilizing speechless in arabidopsis. Proceedings of the National Academy of Sciences, 117:13127-13137, May 2020. URL: https://doi.org/10.1073/pnas.1912075117, doi:10.1073/pnas.1912075117. This article has 49 citations and is from a highest quality peer-reviewed journal.

11. (marcos2017amutationin pages 1-5): Alberto de Marcos, Anaxi Houbaert, Magdalena Triviño, Dolores Delgado, Mar Martín-Trillo, Eugenia Russinova, Carmen Fenoll, and Montaña Mena. A mutation in the bhlh domain of the spch transcription factor uncovers a br-dependent mechanism for stomatal development. Plant Physiology, 174:823-842, May 2017. URL: https://doi.org/10.1104/pp.17.00615, doi:10.1104/pp.17.00615. This article has 43 citations and is from a highest quality peer-reviewed journal.

12. (chen2020speechlessspeaksloudly pages 1-2): Liang Chen, Zhongliang Wu, and Suiwen Hou. Speechless speaks loudly in stomatal development. Frontiers in Plant Science, Feb 2020. URL: https://doi.org/10.3389/fpls.2020.00114, doi:10.3389/fpls.2020.00114. This article has 52 citations.

13. (fung2025multiscaledynamicsinfluence pages 1-2): Hannah F. Fung, Gabriel O. Amador, Renee Dale, Yan Gong, Macy Vollbrecht, Joel M. Erberich, Andrea Mair, and Dominique C. Bergmann. Multi-scale dynamics influence the division potential of stomatal lineage ground cells in arabidopsis. Nature Communications, Mar 2025. URL: https://doi.org/10.1038/s41467-025-57730-9, doi:10.1038/s41467-025-57730-9. This article has 7 citations and is from a highest quality peer-reviewed journal.

14. (chen2020speechlessspeaksloudly pages 2-4): Liang Chen, Zhongliang Wu, and Suiwen Hou. Speechless speaks loudly in stomatal development. Frontiers in Plant Science, Feb 2020. URL: https://doi.org/10.3389/fpls.2020.00114, doi:10.3389/fpls.2020.00114. This article has 52 citations.

15. (chua2024stomataldevelopmentin pages 12-13): Li Cong Chua and On Sun Lau. Stomatal development in the changing climate. Development (Cambridge, England), Oct 2024. URL: https://doi.org/10.1242/dev.202681, doi:10.1242/dev.202681. This article has 38 citations.

16. (lau2018directcontrolof pages 1-3): On Sun Lau, Zhuojun Song, Zimin Zhou, Kelli A. Davies, Jessica Chang, Xin Yang, Shenqi Wang, Doris Lucyshyn, Irene Hui Zhuang Tay, Philip A. Wigge, and Dominique C. Bergmann. Direct control of speechless by pif4 in the high-temperature response of stomatal development. Current Biology, 28:1273-1280.e3, Apr 2018. URL: https://doi.org/10.1016/j.cub.2018.02.054, doi:10.1016/j.cub.2018.02.054. This article has 190 citations and is from a highest quality peer-reviewed journal.

17. (bian2020proteinphosphatase2a media 4c45dadc): Chao Bian, Xiaoyu Guo, Yi Zhang, Lu Wang, Tongda Xu, Alison DeLong, and Juan Dong. Protein phosphatase 2a promotes stomatal development by stabilizing speechless in arabidopsis. Proceedings of the National Academy of Sciences, 117:13127-13137, May 2020. URL: https://doi.org/10.1073/pnas.1912075117, doi:10.1073/pnas.1912075117. This article has 49 citations and is from a highest quality peer-reviewed journal.

18. (yang2015phosphorylationofserine pages 5-8): Ke-Zhen Yang, Min Jiang, Ming Wang, Shan Xue, Ling-Ling Zhu, Hong-Zhe Wang, Jun-Jie Zou, Eun-Kyoung Lee, Fred Sack, and Jie Le. Phosphorylation of serine 186 of bhlh transcription factor speechless promotes stomatal development in arabidopsis. Molecular plant, 8 5:783-95, May 2015. URL: https://doi.org/10.1016/j.molp.2014.12.014, doi:10.1016/j.molp.2014.12.014. This article has 66 citations and is from a highest quality peer-reviewed journal.

19. (marcos2017amutationin pages 33-36): Alberto de Marcos, Anaxi Houbaert, Magdalena Triviño, Dolores Delgado, Mar Martín-Trillo, Eugenia Russinova, Carmen Fenoll, and Montaña Mena. A mutation in the bhlh domain of the spch transcription factor uncovers a br-dependent mechanism for stomatal development. Plant Physiology, 174:823-842, May 2017. URL: https://doi.org/10.1104/pp.17.00615, doi:10.1104/pp.17.00615. This article has 43 citations and is from a highest quality peer-reviewed journal.

20. (kim2022dynamicchromatinaccessibility pages 1-2): Eun-Deok Kim, Michael W. Dorrity, Bridget A. Fitzgerald, Hyemin Seo, Krishna Mohan Sepuru, Christine Queitsch, Nobutaka Mitsuda, Soon-Ki Han, and Keiko U. Torii. Dynamic chromatin accessibility deploys heterotypic cis/trans-acting factors driving stomatal cell-fate commitment. Nature Plants, 8:1453-1466, Dec 2022. URL: https://doi.org/10.1038/s41477-022-01304-w, doi:10.1038/s41477-022-01304-w. This article has 33 citations and is from a highest quality peer-reviewed journal.

21. (yang2015phosphorylationofserine pages 18-23): Ke-Zhen Yang, Min Jiang, Ming Wang, Shan Xue, Ling-Ling Zhu, Hong-Zhe Wang, Jun-Jie Zou, Eun-Kyoung Lee, Fred Sack, and Jie Le. Phosphorylation of serine 186 of bhlh transcription factor speechless promotes stomatal development in arabidopsis. Molecular plant, 8 5:783-95, May 2015. URL: https://doi.org/10.1016/j.molp.2014.12.014, doi:10.1016/j.molp.2014.12.014. This article has 66 citations and is from a highest quality peer-reviewed journal.

22. (bian2019signalingeventsin pages 39-43): Chao Bian. Signaling events in arabidopsis stomatal development and patterning. ArXiv, Jan 2019. URL: https://doi.org/10.7282/t3-m1ft-r605, doi:10.7282/t3-m1ft-r605. This article has 0 citations.