Autophagy-related direct membrane import from ER/cytoplasm into the vacuole or apoplast: a hidden gateway also for secondary metabolites and phytohormones?
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
PubMed
24786101
PubMed Central
PMC4057683
DOI
10.3390/ijms15057462
PII: ijms15057462
Knihovny.cz E-zdroje
- MeSH
- anthokyaniny metabolismus MeSH
- autofagie MeSH
- biologický transport MeSH
- cytoplazma metabolismus MeSH
- endoplazmatické retikulum metabolismus MeSH
- Golgiho aparát metabolismus MeSH
- regulátory růstu rostlin metabolismus MeSH
- rostlinné buňky metabolismus MeSH
- vakuoly metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- anthokyaniny MeSH
- regulátory růstu rostlin MeSH
Transportation of low molecular weight cargoes into the plant vacuole represents an essential plant cell function. Several lines of evidence indicate that autophagy-related direct endoplasmic reticulum (ER) to vacuole (and also, apoplast) transport plays here a more general role than expected. This route is regulated by autophagy proteins, including recently discovered involvement of the exocyst subcomplex. Traffic from ER into the vacuole bypassing Golgi apparatus (GA) acts not only in stress-related cytoplasm recycling or detoxification, but also in developmentally-regulated biopolymer and secondary metabolite import into the vacuole (or apoplast), exemplified by storage proteins and anthocyanins. We propose that this pathway is relevant also for some phytohormones' (e.g., auxin, abscisic acid (ABA) and salicylic acid (SA)) degradation. We hypothesize that SA is not only an autophagy inducer, but also a cargo for autophagy-related ER to vacuole membrane container delivery and catabolism. ER membrane localized enzymes will potentially enhance the area of biosynthetic reactive surfaces, and also, abundant ER localized membrane importers (e.g., ABC transporters) will internalize specific molecular species into the autophagosome biogenesis domain of ER. Such active ER domains may create tubular invaginations of tonoplast into the vacuoles as import intermediates. Packaging of cargos into the ER-derived autophagosome-like containers might be an important mechanism of vacuole and exosome biogenesis and cytoplasm protection against toxic metabolites. A new perspective on metabolic transformations intimately linked to membrane trafficking in plants is emerging.
Zobrazit více v PubMed
Robinson D.G., Jiang L., Schumacher K. The endosomal system of plants: Charting new and familiar territories. Plant Physiol. 2008;147:1482–1492. PubMed PMC
Frigerio L., Hinz G., Robinson D.G. Multiple vacuoles in plant cells: Rule or exception? Traffic. 2008;9:1564–1570. PubMed
Foresti O., Denecke J. Intermediate organelles of the plant secretory pathway: Identity and function. Traffic. 2008;9:1599–1612. PubMed
Zouhar J., Rojo E. Plant vacuoles: Where did they come from and where are they heading? Curr. Opin. Plant Biol. 2009;12:677–684. PubMed
Bottanelli F., Foresti O., Hanton S., Denecke J. Vacuolar transport in tobacco leaf epidermis cells involves a single route for soluble cargo and multiple routes for membrane cargo. Plant Cell. 2011;23:3007–3025. PubMed PMC
Liu Y., Bassham D.C. Autophagy: Pathways for self-eating in plant cells. Annu. Rev. Plant Biol. 2012;63:215–237. PubMed
Pourcel L., Irani N.G., Lu Y., Riedl K., Schwartz S., Grotewold E. The formation of anthocyanic vacuolar inclusions in Arabidopsis thaliana and implications for the sequestration of anthocyanin pigments. Mol. Plant. 2010;3:78–90. PubMed PMC
Inoue Y., Suzuki T., Hattori M., Yoshimoto K., Ohsumi Y., Moriyasu Y. AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells. Plant Cell Physiol. 2006;47:1641–1652. PubMed
Kulich I., Pečenková T., Sekereš J., Smetana O., Fendrych M., Foissner I., Höftberger M., Zárský V. Arabidopsis exocyst subcomplex containing subunit Exo70B1 is involved in autophagy-related transport to the vacuole. Traffic. 2013;14:1155–1165. PubMed
Viotti C., Krüger F., Krebs M., Neubert C., Fink F., Lupanga U., Scheuring D., Boutté Y., Frescatada-Rosa M., Wolfenstetter S., et al. The endoplasmic reticulum is the main membrane source for biogenesis of the lytic vacuole in Arabidopsis. Plant Cell. 2013;25:3434–3449. PubMed PMC
Stigliano E., Faraco M., Neuhaus J.M., Montefusco A., Dalessandro G., Piro G., di Sansebastiano G.P. Two glycosylated vacuolar GFPs are new markers for ER-to-vacuole sorting. Plant Physiol. Biochem. 2013;73:337–343. PubMed
Saslowsky D.E., Warek U., Winkel B.S.J. Nuclear localization of flavonoid enzymes in Arabidopsis. J. Biol. Chem. 2005;280:23735–23740. PubMed
Winkel-Shirley B. Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways. Physiol. Plant. 1999;107:142–149.
Poustka F., Irani N.G., Feller A., Lu Y., Pourcel L., Frame K., Grotewold E. A trafficking pathway for anthocyanins overlaps with the endoplasmic reticulum-to-vacuole protein-sorting route in Arabidopsis and contributes to the formation of vacuolar inclusions. Plant Physiol. 2007;145:1323–1335. PubMed PMC
Sun Y., Li H., Huang J.R. Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts. Mol. Plant. 2012;5:387–400. PubMed
Conn S., Franco C., Zhang W. Characterization of anthocyanic vacuolar inclusions in Vitis vinifera L. cell suspension cultures. Planta. 2010;231:1343–1360. PubMed
Gomez C., Conejero G., Torregrosa L., Cheynier V., Terrier N., Ageorges A. In vivo grapevine anthocyanin transport involves vesicle-mediated trafficking and the contribution of anthoMATE transporters and GST. Plant J. 2011;67:960–970. PubMed
Irani N.G., Grotewold E. Light-induced morphological alteration in anthocyanin-accumulating vacuoles of maize cells. BMC Plant Biol. 2005;5 doi: 10.1186/1471-2229-5-7. PubMed DOI PMC
Zhang H., Wang L., Deroles S., Bennett R., Davies K. New insight into the structures and formation of anthocyanic vacuolar inclusions in flower petals. BMC Plant Biol. 2006;6 doi: 10.1186/1471-2229-6-29. PubMed DOI PMC
Markham K.R., Gould K.S., Winefield C.S., Mitchell K.A., Bloor S.J., Boase M.R. Anthocyanic vacuolar inclusions—Their nature and significance in flower colouration. Phytochemistry. 2000;55:327–336. PubMed
Bae R.N., Kim K.W., Kim T.C., Lee S.K. Anatomical observations of anthocyanin rich cells in apple skins. HortScience. 2006;41:733–736.
Müller O., Sattler T., Flötenmeyer M., Schwarz H., Plattner H., Mayer A. Autophagic tubes vacuolar invaginations involved in lateral membrane sorting and inverse vesicle budding. J. Cell Biol. 2000;151:519–528. PubMed PMC
Thompson A.R., Doelling J.H., Suttangkakul A., Vierstra R.D. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 2005;138:2097–2110. PubMed PMC
Yamamoto Y., Nishimura M., Hara-Nishimura I., Noguchi T. Behavior of vacuoles during microspore and pollen development in Arabidopsis thaliana. Plant Cell Physiol. 2003;44:1192–1201. PubMed
Saito C., Ueda T., Abe H., Wada Y., Kuroiwa T., Hisada A., Furuya M., Nakano A. A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J. 2002;29:245–255. PubMed
Sattler T., Mayer A. Cell-free reconstitution of microautophagic vacuole invagination and vesicle formation. J. Cell Biol. 2000;151:529–538. PubMed PMC
Kunz J.B., Schwarz H., Mayer A. Determination of four sequential stages during Microautophagy in Vitro. J. Biol. Chem. 2004;279:9987–9996. PubMed
Zhao Y., Liu J., Yang C., Capraro B.R., Baumgart T., Bradley R.P., Ramakrishnan N., Xu X., Radhakrishnan R., Svitkina T., et al. Exo70 generates membrane curvature for morphogenesis and cell migration. Dev. Cell. 2013;26:266–278. PubMed PMC
Liu Y., Burgos J.S., Deng Y., Srivastava R., Howell S.H., Bassham D.C. Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis. Plant Cell. 2012;24:4635–4651. PubMed PMC
Lin Y., Irani N.G., Grotewold E. Sub-cellular trafficking of phytochemicals explored using auto-fluorescent compounds in maize cells. BMC Plant Biol. 2003;3 doi: 10.1186/1471-2229-3-10. PubMed DOI PMC
Yoshimoto K., Jikumaru Y., Kamiya Y., Kusano M., Consonni C., Panstruga R., Ohsumi Y., Shirasu K. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell. 2009;21:2914–2927. PubMed PMC
Métraux J.P. Recent breakthroughs in the study of salicylic acid biosynthesis. Trends Plant Sci. 2002;7:332–334. PubMed
Brillouet J.M., Romieu C., Schoefs B., Solymosi K., Cheynier V., Fulcrand H., Verdeil J.L., Conéjéro G. The tannosome is an organelle forming condensed tannins in the chlorophyllous organs of Tracheophyta. Ann. Bot. 2013;112:1003–1014. PubMed PMC
Dixon R., Paiva N. Stress-induced phenylpropanoid metabolism. Plant Cell. 1995;7:1085–1097. PubMed PMC
Fritz C., Palacios-Rojas N., Feil R., Stitt M. Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: Nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J. Cell Mol. Biol. 2006;46:533–548. PubMed
De Geyter N., Gholami A., Goormachtig S., Goossens A. Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci. 2012;17:349–359. PubMed
Alcantara J., Bird D.A., Franceschi V.R., Facchini P.J. Sanguinarine biosynthesis is associated with the endoplasmic reticulum in cultured opium poppy cells after elicitor treatment. Plant Physiol. 2005;138:173–183. PubMed PMC
Ralston L., Yu O. Metabolons involving plant cytochrome P450s. Phytochem. Rev. 2006;5:459–472.
St-Pierre B., Luca V.D. A cytochrome P-450 monooxygenase catalyzes the first step in the conversion of tabersonine to vindoline in Catharanthus roseus. Plant Physiol. 1995;109:131–139. PubMed PMC
Wagner G.J., Hrazdina G. Endoplasmic reticulum as a site of phenylpropanoid and flavonoid metabolism in hippeastrum. Plant Physiol. 1984;74:901–906. PubMed PMC
Hrazdina G., Zobel A.M., Hoch H.C. Biochemical, Immunological, And immunocytochemical evidence for the association of chalcone synthase with endoplasmic reticulum membranes. Proc. Natl. Acad. Sci. USA. 1987;84:8966–8970. PubMed PMC
Jones P., Vogt T. Glycosyltransferases in secondary plant metabolism: Tranquilizers and stimulant controllers. Planta. 2001;213:164–174. PubMed
Vlot A.C., Dempsey D.A., Klessig D.F. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 2009;47:177–206. PubMed
Burla B., Pfrunder S., Nagy R., Francisco R.M., Lee Y., Martinoia E. Vacuolar transport of abscisic acid glucosyl ester is mediated by ATP-binding cassette and proton-antiport mechanisms in Arabidopsis. Plant Physiol. 2013;163:1446–1458. PubMed PMC
Lee K.H., Piao H.L., Kim H.Y., Choi S.M., Jiang F., Hartung W., Hwang I., Kwak J.M., Lee I.J., Hwang I. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell. 2006;126:1109–1120. PubMed
Okita T.W., Li X., Roberts M.W. Targeting of mRNAs to domains of the endoplasmic reticulum. Trends Cell Biol. 1994;4:91–96. PubMed
Sirikantaramas S., Yamazaki M., Saito K. Mutations in topoisomerase I as a self-resistance mechanism coevolved with the production of the anticancer alkaloid camptothecin in plants. Proc. Natl. Acad. Sci. USA. 2008;105:6782–6786. PubMed PMC
Mravec J., Skupa P., Bailly A., Hoyerová K., Krecek P., Bielach A., Petrásek J., Zhang J., Gaykova V., Stierhof Y.D., et al. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature. 2009;459:1136–1140. PubMed
Brooks D.A., Bader C., Ng Y.S., Brooks R.D., Borlace G.N., Shandal T. At the intersection of the pathways for exocytosis and autophagy. In: Roberto W., editor. Crosstalk and Integration of Membrane Trafficking Pathways. InTech; Rijeka, Croatia: 2012. pp. 109–136.
Pfeffer S.R. Unconventional secretion by autophagosome exocytosis. J. Cell Biol. 2010;188:451–452. PubMed PMC
Ding Y., Wang J., Wang J., Stierhof Y.D., Robinson D.G., Jiang L. Unconventional protein secretion. Trends Plant Sci. 2012;17:606–615. PubMed
Markham K.R., Ryan K.G., Gould K.S., Rickards G.K. Cell wall sited flavonoids in lisianthus flower petals. Phytochemistry. 2000;54:681–687. PubMed
Žárský V., Kulich I., Fendrych M., Pečenková T. Exocyst complexes multiple functions in plant cells secretory pathways. Curr. Opin. Plant Biol. 2013;16:726–733. PubMed
Zhao J., Dixon R.A. MATE transporters facilitate vacuolar uptake of epicatechin 3′-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell. 2009;21:2323–2340. PubMed PMC
Ting H.M., Wang B., Rydén A.M., Woittiez L., van Herpen T., Verstappen F.W.A., Ruyter-Spira C., Beekwilder J., Bouwmeester H.J., van der Krol A. The metabolite chemotype of Nicotiana benthamiana transiently expressing artemisinin biosynthetic pathway genes is a function of CYP71AV1 type and relative gene dosage. New Phytol. 2013;199:352–366. PubMed
Tabata M. The mechanism of shikonin biosynthesis in Lithospermum cell cultures. Plant Tissue Cult. Lett. 1996;13:117–125.
Yazaki K. Transporters of secondary metabolites. Curr. Opin. Plant Biol. 2005;8:301–307. PubMed
Agati G., Azzarello E., Pollastri S., Tattini M. Flavonoids as antioxidants in plants: Location and functional significance. Plant Sci. 2012;196:67–76. PubMed
Meyer D., Pajonk S., Micali C., O’Connell R., Schulze-Lefert P. Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J. 2009;57:986–999. PubMed
Roepke J., Salim V., Wu M., Thamm A.M.K., Murata J., Ploss K., Boland W., Luca V.D. Vinca drug components accumulate exclusively in leaf exudates of Madagascar periwinkle. Proc. Natl. Acad. Sci. USA. 2010;107:15287–15292. PubMed PMC
Marty F. Cytochemical studies on GERL, Provacuoles, and vacuoles in root meristematic cells of Euphorbia. Proc. Natl. Acad. Sci. USA. 1978;75:852–856. PubMed PMC
Constitutive Negative Regulation of R Proteins in Arabidopsis also via Autophagy Related Pathway?