Characterization of the rice glup4 mutant suggests a role for the small GTPase Rab5 in the biosynthesis of carbon and nitrogen storage reserves in developing endosperm

Doroshenk, Kelly A.; Crofts, Andrew J.; Washida, Haruhiko; Satoh-Cruz, Mio; Crofts, Naoko; Sugino, Aya; Okita, Thomas W.; Morris, Robert T.; Wyrick, John J.; Fukuda, M; Kumamaru, Toshihiro; Satoh, Hiroyuki

doi:10.1270/jsbbs.60.556

Cited by 18 publications

(19 citation statements)

References 54 publications

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“…In situ reverse transcription-PCR studies using fluorescently labeled nucleotides show that glutelin RNAs are missorted in glup4 mutant lines. Instead of their normal distribution on the cisternal-ER, glutelin RNAs are found distributed on PB-I as well as to the PMBs (Doroshenk et al, 2010). Similar to that seen for glup4, glutelin RNAs are also mislocalized in glup6, where they are seen on both PB-I and PMBs (Crofts et al, 2005).…”

Section: Secretion Of Proglutelinmentioning

confidence: 60%

A Guanine Nucleotide Exchange Factor for Rab5 Proteins Is Essential for Intracellular Transport of the Proglutelin from the Golgi Apparatus to the Protein Storage Vacuole in Rice Endosperm

et al. 2013

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Rice (Oryza sativa) glutelins are synthesized on the endoplasmic reticulum as a precursor, which are then transported via the Golgi to protein storage vacuoles (PSVs), where they are proteolytically processed into acidic and basic subunits. The glutelin precursor mutant6 (glup6) accumulates abnormally large amounts of proglutelin. Map-base cloning studies showed that glup6 was a loss-offunction mutant of guanine nucleotide exchange factor (GEF), which activates Rab GTPase, a key regulator of membrane trafficking. Immunofluorescence studies showed that the transport of proglutelins and a-globulins to PSV was disrupted in glup6 endosperm. Secreted granules of glutelin and a-globulin were readily observed in young glup6 endosperm, followed by the formation of large dilated paramural bodies (PMBs) containing both proteins as the endosperm matures. The PMBs also contained membrane biomarkers for the Golgi and prevacuolar compartment as well as the cell wall component, b-glucan. Direct evidence was gathered showing that GLUP6/GEF activated in vitro GLUP4/Rab5 as well as several Arabidopsis (Arabidopsis thaliana) Rab5 isoforms to the GTP-bound form. Therefore, loss-of-function mutations in GEF or Rab5 disrupt the normal transport of proglutelin from the Golgi to PSVs, resulting in the initial extracellular secretion of these proteins followed, in turn, by the formation of PMBs. Overall, our results indicate that GLUP6/GEF is the activator of Rab5 GTPase and that the cycling of GTP-and GDP-bound forms of this regulatory protein is essential for the intracellular transport of proglutelin and a-globulin from the Golgi to PSVs and in the maintenance of the general structural organization of the endomembrane system in rice seeds.

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Section: Secretion Of Proglutelinmentioning

confidence: 60%

A Guanine Nucleotide Exchange Factor for Rab5 Proteins Is Essential for Intracellular Transport of the Proglutelin from the Golgi Apparatus to the Protein Storage Vacuole in Rice Endosperm

et al. 2013

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“…In addition to reorganizing the endomembrane system, the loss of Rab5a function results in the mislocalization of glutelin RNAs from the cisternal ER to the PB-ER as well as to the PMBs (Doroshenk et al, 2010). By contrast, prolamin RNAs are correctly targeted to the PB-ER in glup4-rab5a.…”

Section: Discussionmentioning

confidence: 99%

“…Figure 11 depicts a model that accounts for the cellular events that are likely responsible for PMB formation. Mislocalized glutelin RNAs are translated on the PB-ER, where the protein is exported to the Golgi apparatus, where it is packaged into dense vesicles (Doroshenk et al, 2010). Because of the loss of Rab5a activity in the glup4 mutant, most dense vesicles are not transported to the PSV but are secreted as electron-dense granules to the extracellular space.…”

Section: Discussionmentioning

confidence: 99%

The Small GTPase Rab5a Is Essential for Intracellular Transport of Proglutelin from the Golgi Apparatus to the Protein Storage Vacuole and Endosomal Membrane Organization in Developing Rice Endosperm

et al. 2011

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Rice (Oryza sativa) glutelins are synthesized on the endoplasmic reticulum as larger precursors, which are then transported via the Golgi to the protein storage vacuole (PSV), where they are processed into acidic and basic subunits. Three independent glutelin precursor mutant4 (glup4) rice lines, which accumulated elevated levels of proglutelin over the wild type, were identified as loss-of-function mutants of Rab5a, the small GTPase involved in vesicular membrane transport. In addition to the plasma membrane, Rab5a colocalizes with glutelins on the Golgi apparatus, Golgi-derived dense vesicles, and the PSV, suggesting that Rab5a participates in the transport of the proglutelin from the Golgi to the PSV. This spatial distribution pattern was dramatically altered in the glup4 mutants. Numerous smaller protein bodies containing glutelin and a-globulin were evident, and the proteins were secreted extracellularly. Moreover, all three independent glup4 allelic lines displayed the novel appearance of a large dilated, structurally complex paramural body containing proglutelins, a-globulins, membrane biomarkers for the Golgi apparatus, prevacuolar compartment, PSV, and the endoplasmic reticulum luminal chaperones BiP and protein disulfide isomerase as well as b-glucan. These results indicate that the formation of the paramural bodies in glup4 endosperm was due to a significant disruption of endocytosis and membrane vesicular transport by Rab5a loss of function. Overall, Rab5a is required not only for the intracellular transport of proglutelins from the Golgi to the PSV in rice endosperm but also in the maintenance of the general structural organization of the endomembrane system in developing rice seeds.Developing plant seeds accumulate large quantities of storage proteins that are coded by two superfamilies of genes, globulins and prolamins (Shewry et al., 1995). Rice (Oryza sativa) is unique in that it accumulates major quantities of both storage protein types in the form of glutelins and prolamins as well as a third minor species, a-globulins (Tanaka et al., 1980;Krishnan and White, 1995). Glutelin, the dominant storage protein in rice, is homologous to leguminous 11S globulins and is packaged in a protein storage vacuole (PSV;Zhao et al., 1983). Unlike the saline-soluble 11S globulins, however, rice glutelins are only soluble in dilute acid and alkali solutions. During seed development, rice glutelin polypeptides are initially synthesized on the endoplasmic reticulum (ER) membrane as 57-kD proglutelin (Yamagata et al., 1982), which is then transported to the PSVs (Krishnan et al., 1986;Yamagata and Tanaka, 1986), where the precursors are cleaved to acidic and basic subunits (Yamagata et al., 1982). The rice a-globulin, a member of the prolamin superfamily, is also packaged in the PSV, where to-

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“…Upon export from the nucleus, the RNP complex is remodeled, where RBPs are removed and others added, enabling transport to selective intracellular sites where further remodeling enables anchoring to specific intracellular locations, activation for translation, storage, or processing (Aronov et al, 2007;Crofts et al, 2010;Doroshenk et al, 2010).…”

mentioning

confidence: 99%

“…The cis-zip code sequences of the two regulated mRNA transport and localization pathways have been defined (Washida et al, 2009a(Washida et al, , 2009b and are hierarchal, as the glutelin mRNA transport pathway is dominant over the prolamine transport pathway that, in turn, is dominant over the default pathway (Crofts et al, 2005;Doroshenk et al, 2011). The three pathways, however, are interrelated, as mutations in the glutelin mRNA transport pathway redirect glutelin mRNAs from the cisternal-ER to the PB-ER (Crofts et al, 2005;Doroshenk et al, 2010), while a mutation in the prolamine mRNA transport pathway mislocalizes prolamine mRNAs from the PB-ER to the cisternal-ER (Crofts et al, 2005;Fukuda et al, 2016). In addition to zip code-specific trans-factors, other ancillary factors are required for mRNA transport and localization, as suggested for the rice OsTudorStaphylococcus nuclease (SN; Wang et al, 2008).…”

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confidence: 99%

Multifunctional RNA Binding Protein OsTudor-SN in Storage Protein mRNA Transport and Localization

et al. 2017

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The multifunctional RNA-binding protein Tudor-SN plays multiple roles in transcriptional and posttranscriptional processes due to its modular domain structure, consisting of four tandem Staphylococcus nuclease (SN)-like domains (4SN), followed by a carboxyl-terminal Tudor domain, followed by a fifth partial SN sequence (Tsn). In plants, it confers stress tolerance, is a component of stress granules and P-bodies, and may participate in stabilizing and localizing RNAs to specific subdomains of the cortical-endoplasmic reticulum in developing rice (Oryza sativa) endosperm. Here, we show that, in addition to the intact rice OsTudor-SN protein, the 4SN and Tsn modules exist as independent polypeptides, which collectively may coassemble to form a complex population of homodimer and heteroduplex species. The 4SN and Tsn modules exhibit different roles in RNA binding and as a protein scaffold for stress-associated proteins and RNA-binding proteins. Despite their distinct individual properties, mutations in both the 4SN and Tsn modules mislocalize storage protein mRNAs to the cortical endoplasmic reticulum. These results indicate that the two modular peptide regions of OsTudor-SN confer different cellular properties but cooperate in mRNA localization, a process linking its multiple functions in the nucleus and cytoplasm.mRNA localization is readily evident in structurally polarized somatic cells

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Characterization of the rice glup4 mutant suggests a role for the small GTPase Rab5 in the biosynthesis of carbon and nitrogen storage reserves in developing endosperm

Cited by 18 publications

References 54 publications

A Guanine Nucleotide Exchange Factor for Rab5 Proteins Is Essential for Intracellular Transport of the Proglutelin from the Golgi Apparatus to the Protein Storage Vacuole in Rice Endosperm

A Guanine Nucleotide Exchange Factor for Rab5 Proteins Is Essential for Intracellular Transport of the Proglutelin from the Golgi Apparatus to the Protein Storage Vacuole in Rice Endosperm

The Small GTPase Rab5a Is Essential for Intracellular Transport of Proglutelin from the Golgi Apparatus to the Protein Storage Vacuole and Endosomal Membrane Organization in Developing Rice Endosperm

Multifunctional RNA Binding Protein OsTudor-SN in Storage Protein mRNA Transport and Localization

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