Golgi-localised manganese transporter PML3 regulates Arabidopsis growth through modulating Golgi glycosylation and cell wall biosynthesis.
Yang CH; Shanghai Center for Plant Stress Biology and National Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China.; University of the Chinese Academy of Sciences, Beijing, 100049, China.
Wang C; Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou, 510631, China.
Singh S; Shanghai Center for Plant Stress Biology and National Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China.
Fan N; Shanghai Center for Plant Stress Biology and National Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China.; University of the Chinese Academy of Sciences, Beijing, 100049, China.
Liu S; Shanghai Center for Plant Stress Biology and National Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China.
Zhao L; Shanghai Center for Plant Stress Biology and National Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China.
Cao H; Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou, 510631, China.
Xie W; Shanghai Center for Plant Stress Biology and National Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China.
Yang C; Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou, 510631, China.
Huang CF; Shanghai Center for Plant Stress Biology and National Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China.; University of the Chinese Academy of Sciences, Beijing, 100049, China.
The New phytologist [New Phytol] 2021 Jan 17. Date of Electronic Publication: 2021 Jan 17.
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Alejandro S, Cailliatte R, Alcon C, Dirick L, Domergue F, Correia D, Castaings L, Briat JF, Mari S, Curie C. 2017. Intracellular distribution of manganese by the trans-Golgi network Transporter NRAMP2 is critical for photosynthesis and cellular redox homeostasis. The Plant Cell 29: 3068-3084.
Alejandro S, Holler S, Meier B, Peiter E. 2020. Manganese in plants: from acquisition to subcellular allocation. Frontiers in Plant Science 11: 300.
Cailliatte R, Schikora A, Briat JF, Mari S, Curie C. 2010. High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. The Plant Cell 22: 904-917.
Castaings L, Caquot A, Loubet S, Curie C. 2016. The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision. Scientific Reports 6: 37222.
Delhaize E, Gruber BD, Pittman JK, White RG, Leung H, Miao YS, Jiang LW, Ryan PR, Richardson AE. 2007. A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. The Plant Journal 51: 198-210.
Demaegd D, Colinet AS, Deschamps A, Morsomme P. 2014. Molecular evolution of a novel family of putative calcium transporters. PLoS ONE 9: e100851.
Demaegd D, Foulquier F, Colinet AS, Gremillon L, Legrand D, Mariot P, Peiter E, Van Schaftingen E, Matthijs G, Morsomme P. 2013. Newly characterized Golgi- localized family of proteins is involved in calcium and pH homeostasis in yeast and human cells. Proceedings of the National Academy of Sciences, USA 110: 6859-6864.
Dulary E, Yu SY, Houdo M, de Bettignies G, Decool V, Potelle S, Duvet S, Krzewinski-Recchi MA, Garat A, Matthijs G et al. 2018. Investigating the function of Gdt1p in yeast Golgi glycosylation. Biochimica Et Biophysica Acta-General Subjects 1862: 394-402.
Durr G, Strayle J, Plemper R, Elbs S, Klee SK, Catty P, Wolf DH, Rudolph HK. 1998. The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum associated protein degradation. Molecular Biology of the Cell 9: 1149-1162.
Eisenhut M, Hoecker N, Schmidt SB, Basgaran RM, Flachbart S, Jahns P, Eser T, Geimer S, Husted S, Webers APM et al. 2018. The plastid envelope CHLOROPLAST MANGANESE TRANSPORTER1 is essential for manganese homeostasis in Arabidopsis. Molecular Plant 11: 955-969.
Eroglu S, Meier B, von Wiren N, Peiter E. 2016. The vacuolar manganese transporter MTP8 determines tolerance to iron deficiency-induced chlorosis in Arabidopsis. Plant Physiology 170: 1030-1045.
Foster CE, Martin TM, Pauly M. 2010. Comprehensive compositional analysis of plant cell walls (lignocellulosic biomass) part II: carbohydrates. Journal of Visualized Experiments 37: e1837.
Frank J, Happeck R, Meier B, Hoang MTT, Stribny J, Hause G, Ding H, Morsomme P, Baginsky S, Peiter E. 2019. Chloroplast-localized BICAT proteins shape stromal calcium signals and are required for efficient photosynthesis. New Phytologist 221: 866-880.
Gao HL, Xie WX, Yang CH, Xu JY, Li JJ, Wang H, Chen X, Huang CF. 2018. NRAMP2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. New Phytologist 217: 179-193.
Geldner N, Denervaud-Tendon V, Hyman DL, Mayer U, Stierhof YD, Chory J. 2009. Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. The Plant Journal 59: 169-178.
Hebbern CA, Pedas P, Schjoerring JK, Knudsen L, Husted S. 2005. Genotypic differences in manganese efficiency: field experiments with winter barley (Hordeum vulgare L.). Plant and Soil 272: 233-244.
Hoecker N, Honke A, Frey K, Leister D, Schneider A. 2020. Homologous proteins of the manganese transporter PAM71 are localized in the Golgi apparatus and Endoplasmic Reticulum. Plants 9: 239.
Hull CC, Crofts NC. 1996. Determination of the total attenuation coefficient for six contact lens materials using the Beer-Lambert law. Ophthalmic and Physiological Optics 16: 150-157.
Huttner S, Veit C, Vavra U, Schoberer J, Liebminger E, Maresch D, Grass J, Altmann F, Mach L, Strasser R. 2014. Arabidopsis class I alpha-mannosidases MNS4 and MNS5 are involved in Endoplasmic Reticulum-associated degradation of misfolded glycoproteins. The Plant Cell 26: 1712-1728.
Kocsis L, Herman P, Eke A. 2006. The modified Beer-Lambert law revisited. Physics in Medicine & Biology 51: N91-98.
Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB. 1999. The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Molecular Biology 40: 37-44.
Lane DR, Wiedemeier A, Peng LC, Hofte H, Vernhettes S, Desprez T, Hocart CH, Birch RJ, Baskin TI, Burn JE et al. 2001. Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1,4-β-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiology 126: 278-288.
Lanquar V, Ramos MS, Lelievre F, Barbier-Brygoo H, Krieger-Liszkay A, Kramer U, Thomine S. 2010. Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiology 152: 1986-1999.
Li XY, Chanroj S, Wu ZY, Romanowsky SM, Harper JF, Sze H. 2008. A distinct endosomal Ca2+/Mn2+ pump affects root growth through the secretory process. Plant Physiology 147: 1675-1689.
Liebminger E, Huttner S, Vavra U, Fischl R, Schoberer J, Grass J, Blaukopf C, Seifert GJ, Altmann F, Mach L et al. 2009. Class I alpha-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana. The Plant Cell 21: 3850-3867.
Liu CF, Niu GT, Zhang HC, Sun YF, Sun SB, Yu FG, Lu S, Yang YH, Li JM, Hong Z. 2018. Trimming of N-glycans by the Golgi-localized alpha-1,2-Mannosidases, MNS1 and MNS2, is crucial for maintaining RSW2 protein abundance during salt stress in Arabidopsis. Molecular Plant 11: 678-690.
Maeda H, Ishida N. 1967. Specificity of binding of hexopyranosyl polysaccharides with fluorescent brightener. Journal of Biochemistry 62: 276-278.
Marschner H. 1995. Mineral nutrition of higher plants. London, UK: Academic Press.
Mills RF, Doherty ML, Lopez-Marques RL, Weimar T, Dupree P, Palmgren MG, Pittman JK, Williams LE. 2008. ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiology 146: 116-128.
Nguema-Ona E, Vicre-Gibouin M, Gotte M, Plancot B, Lerouge P, Bardor M, Driouich A. 2014. Cell wall O-glycoproteins and N-glycoproteins: aspects of biosynthesis and function. Frontiers in Plant Science 5: 499.
Nunan KJ, Scheller HV. 2003. Solubilization of an arabinan arabinosyltransferase activity from mung bean hypocotyls. Plant Physiology 132: 331-342.
Pallotta MA, Graham RD, Langridge P, Sparrow DHB, Barker SJ. 2000. RFLP mapping of manganese efficiency in barley. Theoretical and Applied Genetics 101: 1100-1108.
Peiter E, Montanini B, Gobert A, Pedas P, Husted S, Maathuis FJM, Blaudez D, Chalot M, Sanders D. 2007. A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. Proceedings of the National Academy of Sciences, USA 104: 8532-8537.
Potelle S, Morelle W, Dulary E, Duvet S, Vicogne D, Spriet C, Krzewinski-Recchi MA, Morsomme P, Jaeken J, Matthijs G et al. 2016. Glycosylation abnormalities in Gdt1p/TMEM165 deficient cells result from a defect in Golgi manganese homeostasis. Human Molecular Genetics 25: 1489-1500.
Romero PA, Herscovics A. 1989. Glycoprotein biosynthesis in Saccharomycescerevisiae - Characterization of alpha-1,6-mannosyltransferase which initiates outer chain formation. Journal of Biological Chemistry 264: 1946-1950.
Ruiz-May E, Kim SJ, Brandizzi F, Rose JK. 2012. The secreted plant N-glycoproteome and associated secretory pathways. Frontiers in Plant Science 3: 117.
Schmidt SB, Jensen PE, Husted S. 2016. Manganese deficiency in plants: the impact on photosystem II. Trends in Plant Science 21: 622-632.
Schneider A, Steinberger I, Herdean A, Gandini C, Eisenhut M, Kurz S, Morper A, Hoecker N, Ruhle T, Labs M et al. 2016. The evolutionarily conserved protein PHOTOSYNTHESIS AFFECTED MUTANT71 is required for efficient manganese uptake at the thylakoid membrane in Arabidopsis. The Plant Cell 28: 892-910.
Scott TA, Melvin EH. 1953. Determination of Dextran with Anthrone. Analytical Chemistry 25: 1656-1661.
Shen JR. 2015. The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annual Review of Plant Biology 66: 23-48.
Strasser R, Altmann F, Mach L, Glossl J, Steinkellner H. 2004. Generation of Arabidopsis thaliana plants with complex N-glycans lacking beta 1,2-linked xylose and core alpha 1,3-linked fucose. FEBS Letters 561: 132-136.
Thines L, Deschamps A, Sengottaiyan P, Savel O, Stribny J, Morsomme P. 2018. The yeast protein Gdt1p transports Mn2+ ions and thereby regulates manganese homeostasis in the Golgi. Journal of Biological Chemistry 293: 8048-8055.
Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. The Plant Cell 14: 1223-1233.
Wang C, Xu WT, Jin HL, Zhang TJ, Lai JB, Zhou X, Zhang SC, Liu SJ, Duan XW, Wang HB et al. 2016. A putative chloroplast-localized Ca2+/H+ antiporter CCHA1 is involved in calcium and pH homeostasis and required for PSII function in Arabidopsis. Molecular Plant 9: 1183-1196.
White AR, Xin Y, Pezeshk V. 1993. Xyloglucan glucosyltransferase in Golgi membranes from Pisum sativum (Pea). Biochemical Journal 294: 231-238.
Wilson IBH, Harthill JE, Mullin NP, Ashford DA, Altmann F. 1998. Core alpha 1,3-fucose is a key part of the epitope recognized by antibodies reacting against plant N-linked oligosaccharides and is present in a wide variety of plant extracts. Glycobiology 8: 651-661.
Zhang B, Zhang C, Liu CG, Jing YP, Wang Y, Jin L, Yang L, Fu AG, Shi JS, Zhao FG et al. 2018. Inner envelope CHLOROPLAST MANGANESE TRANSPORTER 1 supports manganese homeostasis and phototrophic growth in Arabidopsis. Molecular Plant 11: 943-954.
Grant Information :
National Key Laboratory of Plant Molecular Genetics; Shanghai Center for Plant Stress Biology, Chinese Academy of Sciences; 31670286 National Natural Science Foundation of China
Contributed Indexing :
Keywords: Arabidopsis thaliana; Golgi glycosylation; PML3; cell wall; manganese transporter; manganese utilisation
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Date Created: 20210117 Latest Revision: 20210211
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Golgi is a critical compartment for both the reutilisation of the essential micronutrient manganese (Mn) and its detoxification. However, whether Mn plays a role in the Golgi remains to be demonstrated in plants. We characterised the function of PML3, a member of the Unknown Protein Family UPF0016, in Mn transport and the regulation of plant growth, Golgi glycosylation and cell wall biosynthesis in Arabidopsis. We also investigated the relationship of PML3 with NRAMP2, a trans-Golgi network localised Mn transporter. PML3-GFP is preferentially localised in the cis-Golgi. PML3 can transport Mn to rescue the hypersensitivity of yeast mutant Δpmr1 to excess Mn. Two mutant alleles of PML3 displayed reduced plant growth and impaired seed development under Mn-deficient conditions. The pml3 mutants also showed impaired Golgi glycosylation and cell wall biosynthesis under Mn deficiency. Double mutations of PML3 and NRAMP2 showed improved plant growth compared with that of single mutants under Mn deficiency, implying that PML3 and NRAMP2 play opposite roles in the regulation of Golgi Mn levels. Our results suggest that PML3 mediates Mn uptake into the Golgi compartments, which is required for proper protein glycosylation and cell wall biosynthesis under Mn-deficient conditions.
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