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Comprehensive Research Report: RIC7 (ROP-interactive CRIB motif-containing protein 7) in Arabidopsis thaliana

Gene and Protein Identity

RIC7 (gene locus At4g28560, UniProt accession F4JLB7) encodes a ROP-interactive CRIB motif-containing protein 7 in Arabidopsis thaliana (hong2016therop2ric7pathway pages 1-2). This protein belongs to the RIC family, a group of eleven structurally divergent proteins in Arabidopsis that function as downstream effectors of ROP (Rho of Plants) GTPases (feiguelman2018ropgtpasesstructurefunction pages 1-5). The identity of RIC7 has been confirmed through molecular studies showing it contains the characteristic CRIB (Cdc42/Rac-interactive binding) domain that mediates interaction with activated ROP proteins (hong2016therop2ric7pathway pages 1-2, feiguelman2018ropgtpasesstructurefunction pages 10-13).

Protein Family and Structural Features

The RIC Family in Arabidopsis

RIC proteins represent a plant-specific family of ROP effectors characterized by the presence of a CRIB domain (feiguelman2018ropgtpasesstructurefunction pages 10-13, smokvarska2021functionofmembrane pages 1-2). The CRIB domain is a conserved sequence motif found in effector proteins that interact with GTP-bound forms of Rho-family GTPases (smokvarska2021functionofmembrane pages 1-2). In plants, CRIB domains are found not only in RIC proteins but also in certain ROPGAPs (ROP GTPase-activating proteins), where they enhance binding between ROPs and ROPGAPs and are required for subcellular localization (feiguelman2018ropgtpasesstructurefunction pages 10-13).

Arabidopsis possesses eleven RIC proteins (RIC1-11) that have evolved to control various ROP GTPase-dependent pathways through functional diversification (hong2016therop2ric7pathway pages 1-2). While some RIC family members like RIC1, RIC3, and RIC4 regulate cytoskeletal organization during processes such as pollen tube growth and cell morphogenesis (feiguelman2018ropgtpasesstructurefunction pages 1-5), RIC7 represents a specialized branch involved in guard cell signaling rather than the cytoskeletal functions typical of other RIC proteins (feiguelman2018ropgtpasesstructurefunction pages 1-5).

Domain Architecture

The defining feature of RIC7 is its CRIB motif, which enables direct interaction with activated (GTP-bound) ROP proteins (hong2016therop2ric7pathway pages 1-2, feiguelman2018ropgtpasesstructurefunction pages 10-13). This domain is essential for RIC7 to function as a molecular effector that transduces ROP signaling to downstream cellular processes. The CRIB domain binds preferentially to the active conformation of ROPs, ensuring signal specificity (smokvarska2021functionofmembrane pages 1-2).

Primary Molecular Function

Role as a Negative Regulator of Stomatal Movement

The primary function of RIC7 is to negatively regulate stomatal movements in Arabidopsis guard cells (hong2016therop2ric7pathway pages 1-2, hong2016therop2ric7pathway pages 3-4). Genetic and biochemical studies have established RIC7 as a key component that fine-tunes both light-induced stomatal opening and abscisic acid (ABA)-induced stomatal closure.

Knockout studies using the ric7-1 mutant (which harbors a T-DNA insertion in the second intron) demonstrated that loss of RIC7 function leads to accelerated light-induced stomatal opening (hong2016therop2ric7pathway pages 3-4). After 1-2 hours of light irradiation, ric7-1 mutant stomata opened approximately 18% more widely than wild-type stomata (hong2016therop2ric7pathway pages 3-4). Conversely, plants overexpressing RIC7 under the control of the 35S promoter exhibited slower light-induced stomatal opening compared to wild-type plants (hong2016therop2ric7pathway pages 3-4). Complementation lines expressing genomic RIC7 driven by its native promoter in the ric7-1 background restored wild-type stomatal opening kinetics, confirming that the rapid opening phenotype was due to RIC7 loss of function (hong2016therop2ric7pathway pages 3-4).

RIC7 also suppresses ABA-induced stomatal closure. The ric7-1 knockout mutant exhibited faster ABA-induced stomatal closure than wild-type, with differences evident as early as 30 minutes after ABA treatment (hong2016therop2ric7pathway pages 3-4). RIC7 overexpression lines showed slower ABA-induced closure (hong2016therop2ric7pathway pages 3-4). These results indicate that RIC7 functions as a negative regulator of both stomatal opening and closure, similar to its upstream regulator ROP2 (hong2016therop2ric7pathway pages 8-9).

Mechanistic Basis: The ROP2-RIC7-Exo70B1 Signaling Module

RIC7 does not function as a substrate-specific enzyme or transporter. Instead, it operates as a signaling adaptor protein that links ROP2 GTPase activity to the vesicle trafficking machinery required for stomatal movement (hong2016therop2ric7pathway pages 8-9, hong2016therop2ric7pathway pages 9-10).

Interaction with ROP2: RIC7 functions downstream of ROP2, a plant Rho-type GTPase that negatively regulates stomatal movements (hong2016therop2ric7pathway pages 1-2, hong2016therop2ric7pathway pages 8-9). Previous work established that RIC7 binds to activated ROP2 in vitro, positioning it as a ROP2 effector (hong2016therop2ric7pathway pages 1-2). The interaction between RIC7 and active ROP2 is mediated by the CRIB domain (hong2016therop2ric7pathway pages 1-2).

Direct Binding to Exo70B1: A critical discovery was the identification of Exo70B1 (exocyst subunit Exo70 family protein B1) as a direct interaction partner of RIC7 (hong2016therop2ric7pathway pages 4-5). Multiple experimental approaches confirmed this interaction:

• Yeast two-hybrid assays demonstrated that RIC7 binds to Exo70B1 (hong2016therop2ric7pathway pages 4-5)
• In vitro pull-down assays showed that GST-fused Exo70B1 directly pulls down MBP-fused RIC7, whereas free GST does not (hong2016therop2ric7pathway pages 4-5)
• Bimolecular fluorescence complementation (BiFC) assays in tobacco leaves confirmed the RIC7-Exo70B1 interaction in vivo (hong2016therop2ric7pathway pages 4-5)

Importantly, BiFC assays revealed that Exo70B1 does not bind directly to ROP2 (hong2016therop2ric7pathway pages 4-5), indicating that RIC7 serves as a linker protein connecting ROP2 to the exocyst machinery. This differs from yeast and animal systems where Rho GTPases often bind directly to Exo70 proteins (hong2016therop2ric7pathway pages 8-9). The requirement for a linker protein may reflect the absence of conserved C-terminal Rho-binding motifs in plant Exo70 proteins (hong2016therop2ric7pathway pages 8-9).

Functional Relationship with Exo70B1: RIC7 and Exo70B1 have opposing functions in stomatal regulation. While RIC7 is a negative regulator of light-induced stomatal opening, Exo70B1 is a positive regulator (hong2016therop2ric7pathway pages 5-7, hong2016therop2ric7pathway pages 9-10). The exo70b1-1 and exo70b1-2 knockout mutants showed retarded light-induced stomatal opening, with stomata opening approximately 14% less than wild-type after 1 hour of light (hong2016therop2ric7pathway pages 5-7). Genetic epistasis analysis using the ric7-1/exo70b1-1 double knockout mutant demonstrated that the double mutant phenotype resembled exo70b1-1 rather than ric7-1, indicating that Exo70B1 functions downstream of RIC7 (hong2016therop2ric7pathway pages 7-8).

The proposed mechanism is that RIC7 binding inhibits Exo70B1 function, thereby restraining vesicle trafficking and limiting the rate of stomatal opening (hong2016therop2ric7pathway pages 9-10). This creates a brake mechanism that prevents excessive stomatal opening and associated water loss while still allowing efficient CO₂ uptake for photosynthesis (hong2016therop2ric7pathway pages 8-9, hong2016therop2ric7pathway pages 9-10).

Subcellular Localization and Dynamic Regulation

RIC7 exhibits stimulus-dependent subcellular localization, which is critical for its regulatory function (hong2016therop2ric7pathway pages 7-8, hong2016therop2ric7pathway pages 5-7).

Localization Under Dark Conditions: In guard cells maintained in darkness, CFP-tagged RIC7 localizes predominantly to the nucleus (hong2016therop2ric7pathway pages 7-8, hong2016therop2ric7pathway pages 5-7). Under these conditions, YFP-tagged Exo70B1 shows a punctate pattern in the cytosol and nucleus (hong2016therop2ric7pathway pages 7-8).

Light-Induced Relocalization: Upon light irradiation (2 hours of white light), a subset of RIC7 relocates from the nucleus to the plasma membrane region, where it co-localizes with Exo70B1 (hong2016therop2ric7pathway pages 7-8, hong2016therop2ric7pathway pages 5-7). Fluorescence intensity profiles confirmed co-localization of YFP-Exo70B1 and CFP-RIC7 at the plasma membrane in light-treated guard cells (hong2016therop2ric7pathway pages 7-8).

ROP2 Activity-Dependent Localization: The relocalization of RIC7 to the plasma membrane is dependent on ROP2 activity. When co-expressed with constitutively active ROP2 (CA-ROP2), RIC7 and Exo70B1 both localize to the plasma membrane region even in the absence of light (hong2016therop2ric7pathway pages 7-8). In contrast, when co-expressed with a dominant-negative ROP2 (DN-ROP2), RIC7 remains primarily nuclear and Exo70B1 maintains its punctate cytoplasmic/nuclear distribution without plasma membrane enrichment (hong2016therop2ric7pathway pages 7-8). These findings indicate that light-mediated ROP2 activation triggers the recruitment of both RIC7 and Exo70B1 to the plasma membrane, where RIC7 can then modulate Exo70B1 function (hong2016therop2ric7pathway pages 7-8, hong2016therop2ric7pathway pages 9-10).

Biological Processes and Signaling Pathways

Guard Cell Function and Gas Exchange

RIC7 is highly expressed in stomatal guard cells, as demonstrated by RIC7 promoter::β-glucuronidase reporter analysis (hong2016therop2ric7pathway pages 3-4). Guard cells regulate stomatal apertures to balance CO₂ uptake for photosynthesis against water loss through transpiration. Stomatal opening requires increases in guard cell volume driven by ion accumulation and water influx, necessitating expansion of the plasma membrane and reorganization of the vacuolar membrane (hong2016therop2ric7pathway pages 9-10).

The ROP2 Signaling Pathway in Guard Cells

ROP2 (also known as RAC2) is a member of the plant-specific ROP subfamily of Rho GTPases and functions as a negative regulator of stomatal movements (hong2016therop2ric7pathway pages 1-2, feiguelman2018ropgtpasesstructurefunction pages 1-5). Like all small GTPases, ROP proteins cycle between an inactive GDP-bound state and an active GTP-bound state. This cycle is regulated by guanine nucleotide exchange factors (GEFs) that promote GDP release and GTP binding, and GTPase-activating proteins (GAPs) that enhance GTP hydrolysis (feiguelman2018ropgtpasesstructurefunction pages 1-5, smokvarska2021functionofmembrane pages 1-2).

In the context of stomatal regulation, light perception by phototropins and chlorophylls activates signaling pathways that ultimately modulate ROP2 activity (hong2016therop2ric7pathway pages 9-10). The current model proposes that light-induced stomatal opening activates positive regulatory pathways but simultaneously engages negative regulatory mechanisms, including the ROP2-RIC7-Exo70B1 pathway, to prevent excessive opening (hong2016therop2ric7pathway pages 8-9, hong2016therop2ric7pathway pages 9-10).

Vesicle Trafficking and Membrane Remodeling

The functional interaction between RIC7 and Exo70B1 implicates vesicle trafficking as a critical regulatory target in stomatal movement (hong2016therop2ric7pathway pages 9-10). Exo70B1 is a component of the exocyst complex, an eight-subunit complex (Sec3, Sec5, Sec6, Sec8, Sec10, Sec15, Exo70, and Exo84) that mediates tethering and spatial targeting of post-Golgi vesicles to the plasma membrane prior to fusion (hong2016therop2ric7pathway pages 1-2, hong2016therop2ric7pathway pages 2-3).

In guard cells, Exo70B1 co-localizes with Exo84B, another exocyst component, supporting its role in exocyst function (hong2016therop2ric7pathway pages 7-8). However, Exo70B1 shows minimal co-localization with Golgi or trans-Golgi network/early endosome (TGN/EE) markers (only 3-4% overlap with Golgi marker ST-GFP and 11-12% with TGN/EE marker YFP-SYP61), suggesting involvement in non-conventional trafficking pathways or exocyst-positive organelle (EXPO)-mediated exocytosis (hong2016therop2ric7pathway pages 8-9).

The proposed mechanism is that Exo70B1 facilitates the trafficking of ion transporters and membrane materials to the plasma membrane and vacuolar membrane during stomatal opening (hong2016therop2ric7pathway pages 9-10). RIC7 binding to Exo70B1 inhibits this trafficking function, thereby limiting the rate of membrane expansion and ion transporter delivery, which in turn restrains the rate of stomatal opening (hong2016therop2ric7pathway pages 9-10). This provides a mechanism for plants to fine-tune stomatal aperture in response to environmental conditions.

Integration with ABA Signaling

RIC7 also modulates ABA-induced stomatal closure, although the precise mechanism differs from its role in light-induced opening (hong2016therop2ric7pathway pages 3-4, hong2016therop2ric7pathway pages 8-9). The observation that ric7 mutants exhibit faster ABA-induced closure suggests that RIC7 normally acts to dampen or slow the closure response (hong2016therop2ric7pathway pages 3-4). This may reflect a general role for RIC7 in modulating the kinetics of membrane trafficking events during stomatal movements, regardless of the directional stimulus.

Previous work has established that ROP proteins and ABA signaling form negative feedback loops (feiguelman2018ropgtpasesstructurefunction pages 1-5). ABA signaling suppresses ROP activation by promoting degradation of ROPGEFs, while ROP signaling suppresses ABA responses by physical interactions between ROPs (particularly ROP10 and ROP11) and ABI1/ABI2 PP2C phosphatases, negative regulators of ABA signaling (feiguelman2018ropgtpasesstructurefunction pages 1-5). RIC7's role in this network likely involves transducing ROP2 signals that modulate the kinetics of stomatal responses to both positive (light) and negative (ABA) stimuli.

Experimental Evidence

The characterization of RIC7 is supported by multiple lines of experimental evidence employing diverse methodologies:

Genetic Evidence:
- T-DNA insertion mutant ric7-1 (GK_062G02) with insertion in the second intron (hong2016therop2ric7pathway pages 1-2, hong2016therop2ric7pathway pages 3-4)
- RIC7 overexpression lines (OX1, OX3, OX8) under 35S promoter control (hong2016therop2ric7pathway pages 3-4)
- Complementation lines expressing genomic RIC7 under native promoter in ric7-1 background (hong2016therop2ric7pathway pages 3-4)
- Double mutant ric7-1/exo70b1-1 for epistasis analysis (hong2016therop2ric7pathway pages 7-8)

Biochemical Evidence:
- Yeast two-hybrid screens identifying Exo70B1 as RIC7-interacting protein (hong2016therop2ric7pathway pages 4-5)
- In vitro GST pull-down assays demonstrating direct RIC7-Exo70B1 interaction (hong2016therop2ric7pathway pages 4-5)
- Quantitative RT-PCR confirming gene expression levels in mutants and transgenics (hong2016therop2ric7pathway pages 2-3)

Cell Biological Evidence:
- Bimolecular fluorescence complementation (BiFC) assays in Nicotiana benthamiana confirming RIC7-Exo70B1 interaction in vivo (hong2016therop2ric7pathway pages 4-5)
- Transient expression of fluorescently tagged proteins in Vicia faba guard cells via particle bombardment (hong2016therop2ric7pathway pages 2-3, hong2016therop2ric7pathway pages 7-8)
- Confocal microscopy analysis of subcellular localization under different conditions (dark, light, with CA-ROP2, with DN-ROP2) (hong2016therop2ric7pathway pages 7-8, hong2016therop2ric7pathway pages 5-7)
- Co-localization studies with organelle markers (hong2016therop2ric7pathway pages 8-9)

Physiological Evidence:
- Stomatal aperture measurements showing altered light-induced opening kinetics in ric7 mutants and overexpression lines (hong2016therop2ric7pathway pages 3-4)
- ABA-induced stomatal closure assays demonstrating RIC7's role in closure kinetics (hong2016therop2ric7pathway pages 3-4)
- Promoter::β-glucuronidase reporter analysis revealing RIC7 expression patterns (hong2016therop2ric7pathway pages 3-4)

Comparison with Other RIC Family Members

The RIC family exhibits functional diversification, with different members regulating distinct cellular processes (feiguelman2018ropgtpasesstructurefunction pages 1-5). While RIC7 is specialized for guard cell signaling and vesicle trafficking regulation, other RIC proteins have well-characterized roles in cytoskeletal regulation:

• RIC1 regulates microtubule-mediated cell morphogenesis and localizes to the pollen tube tip (hong2016therop2ric7pathway pages 1-2, feiguelman2018ropgtpasesstructurefunction pages 1-5)
• RIC3 and RIC4 regulate cortical actin filament organization in growing pollen tubes (hong2016therop2ric7pathway pages 1-2, feiguelman2018ropgtpasesstructurefunction pages 1-5)
• RIC171 in barley (a RIC family ortholog) is involved in pathogen defense responses, where it accumulates at sites of fungal attack (feiguelman2018ropgtpasesstructurefunction pages 20-23)

This functional diversity reflects the evolution of the RIC family to mediate different downstream outputs of ROP signaling in different cellular contexts, despite sharing the common CRIB domain that enables ROP interaction (feiguelman2018ropgtpasesstructurefunction pages 1-5).

Current Understanding and Knowledge Gaps

The characterization of RIC7 published by Hong et al. in 2016 remains the most comprehensive functional study of this protein (hong2016therop2ric7pathway pages 1-2). Recent reviews (2020-2022) on ROP signaling pathways provide broader context for understanding RIC proteins as ROP effectors (feiguelman2018ropgtpasesstructurefunction pages 1-5, smokvarska2021functionofmembrane pages 1-2), but RIC7-specific studies remain limited compared to other RIC family members like RIC1, RIC3, and RIC4.

Key remaining questions include:
1. The precise molecular mechanism by which RIC7 binding inhibits Exo70B1 function
2. Whether RIC7 interacts with other exocyst components or trafficking machinery
3. The structural basis of RIC7-Exo70B1 interaction
4. Potential roles of RIC7 in other cell types beyond guard cells
5. The evolutionary origin and conservation of RIC7 function in other plant species

Summary

Table: This table compiles the verified identity, molecular function, localization, pathway role, and supporting evidence for Arabidopsis RIC7. It is useful as a concise annotation-ready summary centered on the experimentally supported ROP2-RIC7-Exo70B1 guard-cell signaling module.

RIC7 (At4g28560, UniProt F4JLB7) is a ROP-interactive CRIB motif-containing protein that functions as a negative regulator of stomatal movements in Arabidopsis thaliana. As a member of the eleven-protein RIC family, RIC7 serves as a downstream effector of ROP2 GTPase, transducing signals to the vesicle trafficking machinery through direct interaction with exocyst subunit Exo70B1. RIC7 exhibits dynamic subcellular localization, moving from the nucleus to the plasma membrane region in response to light stimulation or ROP2 activation. By binding to and inhibiting Exo70B1, RIC7 restrains excessive stomatal opening, providing a brake mechanism that balances CO₂ uptake against water loss. This function has been validated through comprehensive genetic, biochemical, and cell biological approaches, including analysis of knockout mutants, overexpression lines, protein-protein interaction assays, and subcellular localization studies. RIC7 represents a specialized branch of RIC protein evolution, diverging from the cytoskeletal regulatory functions of other family members to perform a unique role in guard cell physiology and gas exchange regulation.

Primary Reference: Hong, D., Jeon, B.W., Kim, S.Y., Hwang, J.-U., & Lee, Y. (2016). The ROP2-RIC7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit Exo70B1 in Arabidopsis. New Phytologist, 209(2), 624-635. doi:10.1111/nph.13625

Publication Date: October 2015 (published online), January 2016 (print)

DOI/URL: https://doi.org/10.1111/nph.13625

References

1. (hong2016therop2ric7pathway pages 1-2): Daewoong Hong, Byeong Wook Jeon, Soo Young Kim, Jae‐Ung Hwang, and Youngsook Lee. The rop2-ric7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit exo70b1 in arabidopsis. The New phytologist, 209 2:624-35, Oct 2016. URL: https://doi.org/10.1111/nph.13625, doi:10.1111/nph.13625. This article has 72 citations.

2. (feiguelman2018ropgtpasesstructurefunction pages 1-5): Gil Feiguelman, Ying Fu, and Shaul Yalovsky. Rop gtpases structure-function and signaling pathways1[open]. Plant Physiology, 176:57-79, Nov 2018. URL: https://doi.org/10.1104/pp.17.01415, doi:10.1104/pp.17.01415. This article has 227 citations and is from a highest quality peer-reviewed journal.

3. (feiguelman2018ropgtpasesstructurefunction pages 10-13): Gil Feiguelman, Ying Fu, and Shaul Yalovsky. Rop gtpases structure-function and signaling pathways1[open]. Plant Physiology, 176:57-79, Nov 2018. URL: https://doi.org/10.1104/pp.17.01415, doi:10.1104/pp.17.01415. This article has 227 citations and is from a highest quality peer-reviewed journal.

4. (smokvarska2021functionofmembrane pages 1-2): Marija Smokvarska, Yvon Jaillais, and Alexandre Martinière. Function of membrane domains in rho-of-plant signaling. Plant Physiology, 185:663-681, Jan 2021. URL: https://doi.org/10.1093/plphys/kiaa082, doi:10.1093/plphys/kiaa082. This article has 54 citations and is from a highest quality peer-reviewed journal.

5. (hong2016therop2ric7pathway pages 3-4): Daewoong Hong, Byeong Wook Jeon, Soo Young Kim, Jae‐Ung Hwang, and Youngsook Lee. The rop2-ric7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit exo70b1 in arabidopsis. The New phytologist, 209 2:624-35, Oct 2016. URL: https://doi.org/10.1111/nph.13625, doi:10.1111/nph.13625. This article has 72 citations.

6. (hong2016therop2ric7pathway pages 8-9): Daewoong Hong, Byeong Wook Jeon, Soo Young Kim, Jae‐Ung Hwang, and Youngsook Lee. The rop2-ric7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit exo70b1 in arabidopsis. The New phytologist, 209 2:624-35, Oct 2016. URL: https://doi.org/10.1111/nph.13625, doi:10.1111/nph.13625. This article has 72 citations.

7. (hong2016therop2ric7pathway pages 9-10): Daewoong Hong, Byeong Wook Jeon, Soo Young Kim, Jae‐Ung Hwang, and Youngsook Lee. The rop2-ric7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit exo70b1 in arabidopsis. The New phytologist, 209 2:624-35, Oct 2016. URL: https://doi.org/10.1111/nph.13625, doi:10.1111/nph.13625. This article has 72 citations.

8. (hong2016therop2ric7pathway pages 4-5): Daewoong Hong, Byeong Wook Jeon, Soo Young Kim, Jae‐Ung Hwang, and Youngsook Lee. The rop2-ric7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit exo70b1 in arabidopsis. The New phytologist, 209 2:624-35, Oct 2016. URL: https://doi.org/10.1111/nph.13625, doi:10.1111/nph.13625. This article has 72 citations.

9. (hong2016therop2ric7pathway pages 5-7): Daewoong Hong, Byeong Wook Jeon, Soo Young Kim, Jae‐Ung Hwang, and Youngsook Lee. The rop2-ric7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit exo70b1 in arabidopsis. The New phytologist, 209 2:624-35, Oct 2016. URL: https://doi.org/10.1111/nph.13625, doi:10.1111/nph.13625. This article has 72 citations.

10. (hong2016therop2ric7pathway pages 7-8): Daewoong Hong, Byeong Wook Jeon, Soo Young Kim, Jae‐Ung Hwang, and Youngsook Lee. The rop2-ric7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit exo70b1 in arabidopsis. The New phytologist, 209 2:624-35, Oct 2016. URL: https://doi.org/10.1111/nph.13625, doi:10.1111/nph.13625. This article has 72 citations.

11. (hong2016therop2ric7pathway pages 2-3): Daewoong Hong, Byeong Wook Jeon, Soo Young Kim, Jae‐Ung Hwang, and Youngsook Lee. The rop2-ric7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit exo70b1 in arabidopsis. The New phytologist, 209 2:624-35, Oct 2016. URL: https://doi.org/10.1111/nph.13625, doi:10.1111/nph.13625. This article has 72 citations.

12. (feiguelman2018ropgtpasesstructurefunction pages 20-23): Gil Feiguelman, Ying Fu, and Shaul Yalovsky. Rop gtpases structure-function and signaling pathways1[open]. Plant Physiology, 176:57-79, Nov 2018. URL: https://doi.org/10.1104/pp.17.01415, doi:10.1104/pp.17.01415. This article has 227 citations and is from a highest quality peer-reviewed journal.

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Citations

1. feiguelman2018ropgtpasesstructurefunction pages 1-5
2. smokvarska2021functionofmembrane pages 1-2
3. feiguelman2018ropgtpasesstructurefunction pages 10-13
4. feiguelman2018ropgtpasesstructurefunction pages 20-23
5. open
6. https://doi.org/10.1111/nph.13625
7. https://doi.org/10.1111/nph.13625,
8. https://doi.org/10.1104/pp.17.01415,
9. https://doi.org/10.1093/plphys/kiaa082,