2 College of Life Science, Northeast Forestry University, Harbin, 150040, China
3 The State Key Laboratory of Subtropical Silviculture, Zhejiang Agriculture and Forestry University, Lin’An, 311300, China
Author Correspondence author
Molecular Soil Biology, 2023, Vol. 14, No. 1 doi: 10.5376/msb.2023.14.0001
Received: 17 Jan., 2023 Accepted: 07 Apr., 2023 Published: 15 May, 2023
Zhang R.R., Cai M.L., Liu S.K., and Bu Y.Y., 2023, Research progress of plant Rab proteins, Molecular Soil Biology, 14(1): 1-7 (doi: 10.5376/msb.2023.14.0001)
Rab protein is one of the largest members in the superfamily of small G protein, which widely exists in animals, plants and microorganisms. Rab acts as a molecular switch for vesicle transport and regulates the budding, transport, tethering, docking and fusion of intracellular vesicles. The Rab protein family in plants is divided into eight branches, namely RabA, RabB, RabC, RabD, RabE, RabF, RabG and RabH. Rab protein has unique structure characteristics, which determines its functional specificity. Rab proteins have certain regulatory effects on pollen tube germination, fruit maturation, root hair development and nodule formation in plants. Rab proteins also has salt and drought-tolerance in plants. Therefore, the structure of Rab protein, its involvement in plant growth and development, and abiotic stress were discussed.
Small GTP-binding proteins are 20~40 kDa monomeric proteins, also known as small G proteins, small GTPases or Ras superfamily (Takai et al., 2001). The G protein involved in protein synthesis and the heterotrimeric G protein used as a membrane receptor transduction have two mutually convertible forms, namely the GDP-bound inactive form and the GTP-bound active form. The GDP-bound inactive form is converted into the GTP-bound active form through the GDP/GTP exchange reaction (Takai et al., 1992). At present, many small G proteins have been identified from eukaryotes such as yeast, plants and humans. They are divided into five families according to structure and function: Ras, Rho, Rab, Arf and Ran families. Ras family members are generally involved in signal transduction. Rho family members are usually involved in the regulation of cytoskeleton. Rab family members generally control vesicle transport. The functions of Arf family members partially overlap with Rabs and are generally involved in vesicle biogenesis and recycling, intracellular transport and cytoskeleton regulation. Ran controls nuclear localization and structure (Reiner and Lundquist, 2018).
Rab protein is the largest branch of the Ras superfamily of GTPases and plays an important role in the targeting and fusion of transport vesicles with their corresponding receptor membranes (Martinez and Goud, 1998). There are 57 Rab members in Arabidopsis thaliana (Vernoud et al., 2003), 52 Rab members in rice (Zhang et al., 2007), 60 Rab members in human (Pereira-Leal and Seabra, 2001), 11 Rab members in yeast (Segev, 2001), 29 Rab proteins in nematodes and 26 Rab proteins in Drosophila melanogaster (Bock et al., 2001). In addition, 17 members were identified in Marchantia polymorpha (Minamino et al., 2018), 23 genes encoding Rab proteins were identified in mango (Lawson et al., 2020), and 87 GrRabs, 169 GhRabs, 136 GbRabs and 80 GaRabs were obtained from four cotton varieties (G.raimondii, G.hirsutum acc. TM-1, G.barbadense acc. 3-79 and G.arboreum) (Li and Guo, 2017). Plant Rab GTPase family is divided into eight branches, namely RabA, RabB, RabC, RabD, RabE, RabF, RabG and RabH. These branches have been found to have high similarities with mammalian Rab1, Rab2, Rab5, Rab6, Rab7, Rab8, Rab11 and Rab18, respectively (Rutherford and Moore, 2002). This paper will review the structure of Rab protein and the role of Rab protein in plant growth and development and abiotic stress.
1 Rab Protein Structure
In eukaryotes, the connection between organelles is regulated by vesicle trafficking, which includes vesicle budding, transport, tethering, docking, and fusion. Rab protein is a ubiquitous component in vesicle transport and plays an important role in precise regulation of vesicle transport, which is related to its unique structural characteristics. Rab protein is similar to other GTPases in its overall core folding, consisting of a six-stranded β-fragment, five parallel chains and an anti-parallel chain, surrounded by five α-helixes. Similar to small G proteins, there are two switch elements called Switch I and Switch II (Pfeffer, 2005). Although Rab proteins have similar overall folding with the small G protein family, they have unique structural specificity. By constructing the 2.0Å crystal structure of the active form of Rab3A binding to the non-hydrolyzed GTP analogue GppNHp, it was found that the active conformation of Rab3A showed significant but localized structural differences compared with the small G protein. The α3-β5 ring in Rab3A is one residue shorter than the α3-β5 ring in the small G protein. All the main chain atoms in the putative Switch I and Switch II regions in the Rab3A structure adopt an ordered conformation. The amino acid sequence of the Rab protein has a highly variable N-terminal and C-terminal extension in length and sequence. The N-terminus of Rab3A contains a 19-residue extension, which is one of the longest extensions in the Rab family. The N-terminus is sensitive to proteolysis of both Lys-C and Glu-C. In addition, it was also found that Ser residues from the phosphate binding ring (P ring) and the putative Switch I region mediate new interactions with nucleotide γ-phosphates (Dumas et al., 1999). The unique structure of Rab3A provides a basis for us to further explore the molecular mechanism and function of Rab protein.
The key for Rab GTPases to function is to recruit effector molecules that specifically bind to their GTP binding forms. Rab effector proteins are a class of very heterogeneous proteins: some are coiled-coil proteins involved in membrane tethering or docking, and some are enzymes or cytoskeleton-related proteins. Rab proteins switch between GDP and GTP binding forms, and the conversion from GDP to GTP binding form is caused by nucleotide exchange and catalyzed by GDP/GTP exchange factor (GEF). Under the promotion of GTPase-activated protein (GAP), GTP hydrolysis occurs from GTP to GDP binding form. The GTP-bound form interacts with effector molecules, and the GDP-bound form interacts with Rab-associated protein (REP) and GDP dissociation inhibitor (GDI). Rab proteins interact with these effector proteins and play important roles in cell growth and development (Stenmark and Olkkonen, 2001). Rab protein is acylated at its C-terminus. Rab escort protein (REP) is an accessory protein of Rab geranylgeranoyl transferase (RGT) complex and an essential protein for Rab allylation. Studies have shown that the structural basis of plant REP-Rab binding is explored by hydrogen-deuterium exchange mass spectrometry (HDX-MS). It is found that the interaction between REP and Rabs is highly dynamic and related to specific structural changes of both sides. Compared with mammalian REP, the C-terminal truncation of plant REP has no obvious phenotypic changes in plants. On the contrary, REP mutations can lead to male sterility in Arabidopsis (Gutkowska et al., 2021). It has been found that EREX is a plant-specific PX domain-containing protein that acts as an effector of typical RAB5 and regulates specific aspects of vacuolar transport (Sakurai et al., 2016). Although many Rab GTPase effectors have been identified, the identification and functional characterization of Rab effectors need to be further explored.
2 The Role of Rab Protein in Plant Growth and Development
The growth mode of pollen tube is apical growth. During pollination, when pollen interacts with stigma, pollen cells grow a long tube to transport sperm to ovules. This growth mode depends largely on vesicle transport (Kato et al., 2010). The NtRab2 (Cheung et al., 2002) and NtRab11b (de Graaf et al., 2005) genes in Nicotiana tabacum are located in the Golgi apparatus in elongated pollen tubes and the apical transparent region of pollen tubes cultured in vitro, respectively, and are involved in the transport and growth of pollen tubes. AtRabD2b and AtRabD2c are highly expressed in pollen. In the transformed Arabidopsis plants of AtRabD2b/2c-GUS fusion gene, the two genes were expressed in pollen grains and germinated pollen. After the fusion expression of AtRabD2b/2c and GFP, it was found that it was located in the Golgi apparatus, and the pollen produced by AtRabD2b and AtRabD2c mutants was deformed, and the pollen tube was short, the top was enlarged and branched, indicating that AtRabD2b and AtRabD2c play an important role in pollen development, germination and pollen tube elongation (Peng et al., 2011). In addition, AtRab7 (Cui et al., 2017) and AtRabA4d (Szumlanski and Nielsen, 2009) are also essential for pollen development in Arabidopsis. Recent studies have also found that Arabidopsis amino phospholipid ALA3 (ATPASE 3) and RabA4d co-regulate the growth of pollen tubes. The loss of ALA3 function leads to a significant decrease in the vesicles at the top of YFP-RabA4b, RFP-RabA4d and FM4-64-labeled pollen tubes, an increase in the width of pollen tubes, and a loss of polar localization and distribution of PS (phosphatidylserine) at the top of pollen tubes, indicating that the top-located PS established by ALA3 plays an important role in the polar growth of RabA4d pollen tubes (Zhou et al., 2020).
Rab protein affects the growth and development of plant root hairs. In Arabidopsis thaliana, AtRabA4b was fused with an enhanced yellow fluorescent protein (EYFP) and located at the top of root hair cell growth, but EYFP-RabA4b disappeared in mature root hair cells that stopped growing. After the growth of root hair cells was inhibited, EYFP-RabA4b could not be localized at the top of root hair cells. When the inhibition was eliminated, EYFP-RabA4b localized at the top of root hair cells was rediscovered, and root hair cells were restored to normal growth. In addition, EYFP-RabA4b was not correctly localized or absent at the top of root hair cells in mutants with defective root hair morphology. It is indicated that AtRabA4b is involved in the vesicle transport process of the components required for root hair growth, which in turn affects the growth and development of root hair cells (Preuss et al., 2004). In addition, AtRabA4b and the interacting protein PI-4Kβ1 co-regulated the polar growth of root hair cells (Preuss et al., 2006). The PvRabA2 gene in Phaseolus vulgaris is expressed in roots, especially in root hairs, and is related to nodule formation. After the expression of PvRabA2 gene was inhibited, the number and length of root hairs were significantly reduced. On this basis, after further inoculation with Rhizobium venetum, it was found that the nodules were damaged, and the early gene expression of nodules was not detected, such as ERN1, ENOD40 and Hap5. Therefore, PvRabA2 plays an important role in the polar growth of root hairs and affects the direction of root hair growth (Blanco et al., 2009). The GFP-RabA1d fusion protein was specifically localized in the vesicle-like structure of the Golgi transmembrane region by transient expression in Allium porrum and Nicotiana benthamiana. BFA is a mycotoxin that inhibits exocytosis and endocytosis. Proteomic analysis of BFA-treated Arabidopsis roots showed that RabA1d protein levels were quantitatively up-regulated. During root meristem cell division, GFP-RabA1d was specifically accumulated on the cell plate deposition plane, and GFP-RabA1d was enriched at the root hair bulge and the top circle of the vigorously elongated root hair. However, in mature root hairs, this apical localization gradually disappeared. These results suggest that RabA1d is involved in both the formation of cell plates and the growth of root hairs, and has a certain correlation with vesicle transport (Berson et al., 2014).
Fruit ripening is a developmental process of cell wall synthesis and modification. During this process, the structure and composition of cell wall are changed. New cell wall polymers and enzymes are synthesized and transported to the plastid. Vesicle transport plays a key role in this process (Lawson et al., 2018). MiRab11 was strongly expressed in mature fruits of mango (Mangifera indica L.) (Zainal et al., 1996). MiRab5, another gene in mango, was also expressed in mature fruits. Real-time quantitative RT-PCR analysis showed that MiRab5 was widely expressed in different tissues of mango, but was up-regulated in the late stage of fruit ripening. In addition, MiRab5 is also generally up-regulated under various abiotic stresses, such as low temperature, salt and PEG treatment (Liu et al., 2014). The SLRab11a gene in tomato (Solanum lycopersicum) is highly expressed during fruit development and is related to cell wall deposition. After the SLRab11a gene was inhibited, the proportion of pectin in the cell wall decreased (Lunn et al., 2013).
In addition, Rab proteins also play an important role in plant embryonic development, nodule formation and xylem development. Rab protein geranylgeranyl transferase β1 subunit plays an important role in the embryonic development of Arabidopsis thaliana. Due to the defects before and after pollination, the seed setting rate of the mutant is low, and the guidance of pollen and pollen tube is reduced (Rojek et al., 2021). AtRAB8A, AtRAB8B and AtRAB8D, members of AtRAB8s in Arabidopsis, interact with several RTNLB proteins (membrane-bound reticular proteins) and participate in the process of Agrobacterium tumefaciens infection (Huang et al., 2021). The PagRabE1b gene is highly expressed in Populus stems, especially in phloem and xylem tissues. Overexpression of PagRabE1b enhanced programmed cell death (PCD) and increased growth rate, secondary cell wall (SCW) thickness and monosaccharide content, suggesting that PagRabE1b plays an active role in promoting xylem development in poplar (Liu et al., 2021).
3 The Role of Rab Protein in Abiotic Stress
Because plants are inherent, they are often exposed to various adverse environmental conditions, so environmental stress will have a negative impact on plant growth and development. The AtRabG3e (original AtRab7) gene was cloned into a 35S cauliflower mosaic virus promoter and introduced into Arabidopsis thaliana by Agrobacterium-mediated transformation. The transgenic plants showed accelerated endocytosis in roots, leaves and protoplasts, and the sodium content in vacuoles and buds was higher. Transgenic plants were less sensitive to salt and sorbitol stress than wild type, and reduced the accumulation of reactive oxygen species under salt stress, indicating that vesicle transport plays an important role in plant adaptation to stress (Mazel et al., 2004). AtRabA1 in Arabidopsis contains four members, AtRABA1a, AtRABA1b, AtRABA1c and AtRABA1d, which are located in the mobile dot structure adjacent to the trans-Golgi network. The membrane structure of AtRabA1 showed actin-dependent dynamic movement, and the vesicles labeled with GFP-RABA1b fusion protein moved dynamically along the actin filament formation queue. The mutants of the four members of AtRabA1 showed extremely serious growth defects under salt stress, reduced fresh weight, and died at the cotyledon stage. These results suggest that AtRabA1 members play a mediating role in the transport between the trans-Golgi network and the plasma membrane and are required for salt tolerance (Asaoka et al., 2013). The AtRabF1OE (overexpression), mutant AtRabF1Q93L (constitutive activity) and AtRabF1S47N (dominant negative) of AtRabF1 (AtARA6) gene in Arabidopsis thaliana showed longer root growth under salt stress than wild type, rabF1 and AtRabF1Δ1−29 (loss of N-sericinylation) complementary overexpression mutants. AtRabF1OE was more resistant to dark-induced senescence (DIS) than wild type and AtRabF1, indicating that N-sericinylation of AtRabF1 gene is indispensable in salt tolerance and is highly expressed during senescence (Yin et al., 2017). OsRab7 was transferred into rice by Agrobacterium-mediated method to obtain overexpression transgenic plants. Under salt stress, overexpression OsRab7 plants and wild-type plants were inhibited, but compared with wild-type plants, overexpression OsRab7 plants were less sensitive to salt stress, grew faster, and had more lateral roots. After the release of salt stress, the overexpression of OsRab7 seedlings recovered at the same time, while the wild-type seedlings did not recover. Proline plays an important role in improving abiotic stress tolerance. The proline content of OsRab7 overexpression seedlings was higher than that of wild type seedlings after salt stress. In addition, the vesicles in the root tip of OsRab7 overexpressing rice increased, and the vesicle transport speed was accelerated. These results indicate that vesicle transport is very important for plant salt tolerance (Peng et al., 2014). A total of 67 PtRabs were identified in Populus trichocarpa, and PtRabE1b was significantly induced by salt stress. PtRabE1b (Q74L), a constitutively active mutant of PtRabE1b, was found to reduce the number of roots and inhibit the root length of wild-type poplar under salt stress, while PtRabE1b transgenic lines maintained good root growth status, indicating that PtRabE1b (Q74L) improved the salt tolerance of poplar (Zhang et al., 2018).
The rice OsRab7 gene was cloned and transformed into rice plants. The survival rate, relative water content, chlorophyll content, gas exchange characteristics, soluble protein content, soluble sugar content, proline content and antioxidant enzyme (CAT, SOD, APX, POD) activity of transgenic rice were significantly higher than those of wild type. Hydrogen peroxide, electrolyte leakage and malondialdehyde levels were significantly lower than wild type. It was significantly up-regulated in reactive oxygen scavenging enzyme genes and abiotic stress tolerance genes compared with wild type. These results indicate that OsRab7 can improve the stress resistance of rice (El-Esawi and Alayafi, 2019). The N-terminus of AtRabA2b was fused with GFP and overexpressed in Arabidopsis wild-type plants. Under drought stress, AtRabA2b overexpression showed strong drought tolerance compared with wild type. The co-localization between AtRabA2b and PM marker PIP2 is very strong in subcellular localization. Overexpression of AtRabA2b leads to changes in PM proteome structure. The permeability of the leaf cuticle was tested by toluidine blue (TB) test. Compared with the wild type, the TB staining in the leaves of AtRabA2b overexpression was very weak and highly dispersed, and the permeability of the leaf surface was significantly lower than that of the wild type, showing stronger water retention performance. It shows that increasing AtRabA2b-mediated PM transport can affect PM proteome and improve AtRabA2b drought tolerance (Ambastha et al., 2021).
4 Prospect
Rab proteins are abundant and widely distributed in plants, which play an important role in plant growth and development. The effector of Rab protein is the key to Rab function, so the identification and functional characterization of Rab effector need to be further explored. With the in-depth study of Rab function, it is found that Rab not only plays the basic function of vesicle transport in cells, but also participates in many specific biological processes, such as polar growth of pollen tubes and root hairs, cell division, embryonic development, hormone regulation, etc. The mechanism of regulating plant growth and development through Rab protein needs further study. Rab proteins can resist various biotic and abiotic stresses such as salinity, high temperature and dehydration by regulating the signal cascades of vesicle transport, cytoskeleton organization, upstream receptors, regulatory proteins and downstream effectors. Therefore, the involvement of Rab proteins in biotic and abiotic stresses is an area that needs to be studied in detail, which is conducive to improving plant resistance.
Authors’ contributions
ZRR drafted the manuscript. CML compiled the literatures. BYY was the director of the project and revised the manuscript. LSK supervised and critically revised the manuscript. All authors read and approved the final manuscript.
Acknowledgments
This work was jointly supported by Heilongjiang Province Government Postdoctoral Science Foundation (LBH-Q18008) awarded to Yuanyuan Bu and the Program for Changjiang Scholars and Innovative Research Team in University (No. IRT17R99) awarded to Shenkui Liu.
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