Rab geranylgeranyl transferase β subunit is essential for male fertility and tip growth in Arabidopsis

Gutkowska, Małgorzata; Wnuk, Marta; Nowakowska, Julita; Lichocka, Małgorzata; Stronkowski, Michal M.; Świeżewska, Ewa

doi:10.1093/jxb/eru412

Cited by 22 publications

(36 citation statements)

References 50 publications

(85 reference statements)

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“…In yeast, loss of either of the single-copy Rab-GGT subunits leads to lethality (37). In Arabidopsis and P. patens, in which RGTB is duplicated, the rgtb1 and rgtb2 single knock-out mutants are viable, whereas the rgtb1 rgtb2 double mutants are non-viable, indicating genetic redundancy between the duplicated RGTB genes (38,39). The duplicated RGTB genes appear to be completely redundant in P. patens, because neither single rgtb knock-out shows a detectable phenotype (39).…”

Section: Discussionmentioning

confidence: 99%

“…In the Arabidopsis genome, genes encoding two putative ␣ subunits, RGTA1 and RGTA2, and two putative ␤ subunits, RGTB1 and RGTB2, of Rab-GGT were annotated (36). rgtb1 mutants show a series of defects in shoot morphology, shoot gravitropism, tip growth of root hairs and pollen tubes, and light response (37,38). rgtb2 mutants are broadly indistinguishable from wild-type plants under normal conditions but are also defective in tip growth (38).…”

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confidence: 99%

“…rgtb1 mutants show a series of defects in shoot morphology, shoot gravitropism, tip growth of root hairs and pollen tubes, and light response (37,38). rgtb2 mutants are broadly indistinguishable from wild-type plants under normal conditions but are also defective in tip growth (38). The rgtb1 rgtb2 double mutants are pollen-lethal, suggesting that they are at least partially genetically redundant (38).…”

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confidence: 99%

“…rgtb2 mutants are broadly indistinguishable from wild-type plants under normal conditions but are also defective in tip growth (38). The rgtb1 rgtb2 double mutants are pollen-lethal, suggesting that they are at least partially genetically redundant (38). The effects of mutations in either RGTA1 or RGTA2 have not been reported.…”

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confidence: 99%

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Arabidopsis Rab Geranylgeranyltransferases Demonstrate Redundancy and Broad Substrate Specificity in Vitro

Shi

Zeng

Kunkel

et al. 2016

Journal of Biological Chemistry

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Posttranslational lipid modifications mediate the membrane attachment of Rab GTPases, facilitating their function in regulating intracellular vesicular trafficking. In Arabidopsis, most Rab GTPases have two C-terminal cysteines and potentially can be double-geranylgeranylated by heterodimeric Rab geranylgeranyltransferases (Rab-GGTs). Genes encoding two putative ␣ subunits and two putative ␤ subunits of Rab-GGTs have been annotated in the Arabidopsis thaliana genome, but little is known about Rab-GGT activity in Arabidopsis. In this study, we demonstrate that four different heterodimers can be formed between putative Arabidopsis Rab-GGT ␣ subunits RGTA1/ RGTA2 and ␤ subunits RGTB1/RGTB2, but only RGTA1⅐ RGTB1 and RGTA1⅐RGTB2 exhibit bona fide Rab-GGT activity, and they are biochemically redundant in vitro. We hypothesize that RGTA2 function might be disrupted by a 12-amino acid insertion in a conserved motif. We present evidence that Arabidopsis Rab-GGTs may have preference for prenylation of C-terminal cysteines in particular positions. We also demonstrate that Arabidopsis Rab-GGTs can not only prenylate a great variety of Rab GTPases in the presence of Rab escort protein but, unlike Rab-GGT in yeast and mammals, can also prenylate certain non-Rab GTPases independently of Rab escort protein. Our findings may help to explain some of the phenotypes of Arabidopsis protein prenyltransferase mutants.Small GTPases serve as molecular switches that shuttle between active GTP-bound and inactive GDP-bound forms, providing transient signals to downstream effectors (1, 2). In plants, many membrane-localized small GTPases are important regulators of vesicular trafficking (1). They are typically anchored to membranes via posttranslational lipid modifications (3).Rab GTPases constitute the largest family of the Ras superfamily of small GTPases (3-5). They are involved in regulating trafficking processes, such as vesicle formation, transport, membrane targeting, and docking (1, 5). The diversity and specific localization of Rab GTPases not only determine membrane identity, but also reflect the complexity of vesicle trafficking (1, 6).Phylogenetic analysis suggests that the 57 Arabidopsis Rabencoding sequences fall into just eight subfamilies (3, 6), in contrast to ϳ40 Rab subfamilies in mammals (7). Accordingly, the size of each Arabidopsis Rab subfamily is expanded. The distinct composition of the Arabidopsis Rab GTPase family suggests plant-specific functions (1, 6). Of these 57 members, 54 include two cysteines that are near the C terminus and are candidate prenylation sites (Table 1). At least one of the non-prenylated Rabs, RABF1/ARA6, is N-myristoylated and palmitoylated (8).Protein prenylation irreversibly adds one 15-carbon isoprenoid (farnesylation), one 20-carbon isoprenoid (geranylgeranylation), or two 20-carbon isoprenoids (double geranylgeranylation) to one or two C-terminal cysteine residues of target proteins, by forming thioether bonds (9, 10). These three types of prenylation are respectively catalyzed by thre...

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Arabidopsis Rab Geranylgeranyltransferases Demonstrate Redundancy and Broad Substrate Specificity in Vitro

Shi

Zeng

Kunkel

et al. 2016

Journal of Biological Chemistry

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“…Staining of pollen anthers with Alexander stain and microscopy observations were performed as described earlier (Gutkowska et al, 2015).…”

Section: Staining Of Pollen Anthers With Alexander Stainmentioning

confidence: 99%

POLYPRENOL REDUCTASE2 Deficiency Is Lethal in Arabidopsis Due to Male Sterility

et al. 2015

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Dolichol is a required cofactor for protein glycosylation, the most common posttranslational modification modulating the stability and biological activity of proteins in all eukaryotic cells. We have identified and characterized two genes, PPRD1 and -2, which are orthologous to human SRD5A3 (steroid 5a reductase type 3) and encode polyprenol reductases responsible for conversion of polyprenol to dolichol in Arabidopsis thaliana. PPRD1 and -2 play dedicated roles in plant metabolism. PPRD2 is essential for plant viability; its deficiency results in aberrant development of the male gametophyte and sporophyte. Impaired protein glycosylation seems to be the major factor underlying these defects although disturbances in other cellular dolicholdependent processes could also contribute. Shortage of dolichol in PPRD2-deficient cells is partially rescued by PPRD1 overexpression or by supplementation with dolichol. The latter has been discussed as a method to compensate for deficiency in protein glycosylation. Supplementation of the human diet with dolichol-enriched plant tissues could allow new therapeutic interventions in glycosylation disorders. This identification of PPRD1 and -2 elucidates the factors mediating the key step of the dolichol cycle in plant cells which makes manipulation of dolichol content in plant tissues feasible.

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Male functions and malfunctions: the impact of phosphoinositides on pollen development and pollen tube growth

Heilmann

Ischebeck

2015

Plant Reprod

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Phosphoinositides in pollen. In angiosperms, sexual reproduction is a series of complex biological events that facilitate the distribution of male generative cells for double fertilization. Angiosperms have no motile gametes, and the distribution units of generative cells are pollen grains, passively mobile desiccated structures, capable of delivering genetic material to compatible flowers over long distances and in an adverse environment. The development of pollen (male gametogenesis) and the formation of a pollen tube after a pollen grain has reached a compatible flower (pollen tube growth) are important aspects of plant developmental biology. In recent years, a wealth of information has been gathered about the molecular control of cell polarity, membrane trafficking and cytoskeletal dynamics underlying these developmental processes. In particular, it has been found that regulatory membrane phospholipids, such as phosphoinositides (PIs), are critical regulatory players, controlling key steps of trafficking and polarization. Characteristic features of PIs are the inositol phosphate headgroups of the lipids, which protrude from the cytosolic surfaces of membranes, enabling specific binding and recruitment of numerous protein partners containing specific PI-binding domains. Such recruitment is globally an early event in polarization processes of eukaryotic cells and also of key importance to pollen development and tube growth. Additionally, PIs serve as precursors of other signaling factors with importance to male gametogenesis. This review highlights the recent advances about the roles of PIs in pollen development and pollen function.

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Rab geranylgeranyl transferase β subunit is essential for male fertility and tip growth in Arabidopsis

Abstract: SummaryRab proteins are post-translationally geranylgeranylated by Rab geranylgeranyl transferase (RGT) αβ. Mutations in each of the RGTB genes cause a tip growth defect whereas the double mutant is male sterile.

Cited by 22 publications

References 50 publications

Arabidopsis Rab Geranylgeranyltransferases Demonstrate Redundancy and Broad Substrate Specificity in Vitro

Arabidopsis Rab Geranylgeranyltransferases Demonstrate Redundancy and Broad Substrate Specificity in Vitro

POLYPRENOL REDUCTASE2 Deficiency Is Lethal in Arabidopsis Due to Male Sterility

Male functions and malfunctions: the impact of phosphoinositides on pollen development and pollen tube growth

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