{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,5]],"date-time":"2026-09-05T05:53:22Z","timestamp":1788587602435,"version":"build-2803163510"},"reference-count":46,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,9,4]],"date-time":"2017-09-04T00:00:00Z","timestamp":1504483200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,9,4]],"date-time":"2017-09-04T00:00:00Z","timestamp":1504483200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Plant GDP-D-mannose epimerase (GME) converts GDP-D-mannose to GDP-L-galactose, a precursor of both L-ascorbate (vitamin C) and cell wall polysaccharides. However, the genetic functions of <jats:italic>GME<\/jats:italic> in <jats:italic>Arabidopsis<\/jats:italic> are unclear. In this study, we found that mutations in <jats:italic>Arabidopsis GME<\/jats:italic> affect pollen germination, pollen tube elongation, and transmission and development of the male gametophyte through analysis of the heterozygous <jats:italic>GME<\/jats:italic>\/<jats:italic>gme<\/jats:italic> plants and the homozygous <jats:italic>gme<\/jats:italic> plants. <jats:italic>Arabidopsis gme<\/jats:italic> mutants also exhibit severe growth defects and early leaf senescence. Surprisingly, the defects in male gametophyte in the <jats:italic>gme<\/jats:italic> plants are not restored by L-ascorbate, boric acid or GDP-L-galactose, though boric acid rescues the growth defects of the mutants, indicating that GME may regulate male gametophyte development independent of L-ascorbate and GDP-L-galactose. These results reveal key roles for <jats:italic>Arabidopsis GME<\/jats:italic> in reproductive development, vegetative growth and leaf senescence, and suggest that <jats:italic>GME<\/jats:italic> regulates plant growth and controls male gametophyte development in different manners.<\/jats:p>","DOI":"10.1038\/s41598-017-10765-5","type":"journal-article","created":{"date-parts":[[2017,8,29]],"date-time":"2017-08-29T09:46:29Z","timestamp":1503999989000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":24,"title":["GDP-D-mannose epimerase regulates male gametophyte development, plant growth and leaf senescence in Arabidopsis"],"prefix":"10.1038","volume":"7","author":[{"given":"Tiancong","family":"Qi","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhipeng","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meng","family":"Fan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haixia","family":"Tian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dewei","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hua","family":"Gao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunmei","family":"Ren","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Susheng","family":"Song","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daoxin","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,9,4]]},"reference":[{"key":"10765_CR1","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1080\/10409230008984166","volume":"35","author":"N Smirnoff","year":"2000","unstructured":"Smirnoff, N. & Wheeler, G. L. Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol \n                           35, 291\u2013314 (2000).","journal-title":"Crit Rev Biochem Mol Biol"},{"key":"10765_CR2","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1111\/j.1365-313X.2007.03266.x","volume":"52","author":"J Dowdle","year":"2007","unstructured":"Dowdle, J., Ishikawa, T., Gatzek, S., Rolinski, S. & Smirnoff, N. Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant J \n                           52, 673\u2013689, doi:10.1111\/j.1365-313X.2007.03266.x (2007).","journal-title":"Plant J"},{"key":"10765_CR3","doi-asserted-by":"publisher","first-page":"803","DOI":"10.1104\/pp.108.132324","volume":"149","author":"SO Kotchoni","year":"2009","unstructured":"Kotchoni, S. O., Larrimore, K. E., Mukherjee, M., Kempinski, C. F. & Barth, C. Alterations in the endogenous ascorbic acid content affect flowering time in Arabidopsis. Plant Physiol \n                           149, 803\u2013815, doi:10.1104\/pp.108.132324 (2009).","journal-title":"Plant Physiol"},{"key":"10765_CR4","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0061987","volume":"8","author":"C Zhang","year":"2013","unstructured":"Zhang, C. et al. Reducing AsA leads to leaf lesion and defence response in knock-down of the AsA biosynthetic enzyme GDP-D-mannose pyrophosphorylase gene in tomato plant. PLoS One \n                           8, e61987, doi:10.1371\/journal.pone.0061987 (2013).","journal-title":"PLoS One"},{"key":"10765_CR5","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1007\/s12038-011-9000-x","volume":"36","author":"S Talla","year":"2011","unstructured":"Talla, S. et al. Ascorbic acid is a key participant during the interactions between chloroplasts and mitochondria to optimize photosynthesis and protect against photoinhibition. J Biosci \n                           36, 163\u2013173 (2011).","journal-title":"J Biosci"},{"key":"10765_CR6","doi-asserted-by":"publisher","first-page":"1784","DOI":"10.1104\/pp.103.032185","volume":"134","author":"C Barth","year":"2004","unstructured":"Barth, C., Moeder, W., Klessig, D. F. & Conklin, P. L. The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiol \n                           134, 1784\u20131792, doi:10.1104\/pp.103.032185 (2004).","journal-title":"Plant Physiol"},{"key":"10765_CR7","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1093\/jxb\/erp310","volume":"61","author":"C Barth","year":"2010","unstructured":"Barth, C., Gouzd, Z. A., Steele, H. P. & Imperio, R. M. A mutation in GDP-mannose pyrophosphorylase causes conditional hypersensitivity to ammonium, resulting in Arabidopsis root growth inhibition, altered ammonium metabolism, and hormone homeostasis. J Exp Bot \n                           61, 379\u2013394, doi:10.1093\/jxb\/erp310 (2010).","journal-title":"J Exp Bot"},{"key":"10765_CR8","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1093\/genetics\/154.2.847","volume":"154","author":"PL Conklin","year":"2000","unstructured":"Conklin, P. L., Saracco, S. A., Norris, S. R. & Last, R. L. Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics \n                           154, 847\u2013856 (2000).","journal-title":"Genetics"},{"key":"10765_CR9","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1104\/pp.103.028399","volume":"133","author":"AH Millar","year":"2003","unstructured":"Millar, A. H. et al. Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol \n                           133, 443\u2013447, doi:10.1104\/pp.103.028399 (2003).","journal-title":"Plant Physiol"},{"key":"10765_CR10","doi-asserted-by":"publisher","first-page":"18308","DOI":"10.1073\/pnas.0806168105","volume":"105","author":"C Qin","year":"2008","unstructured":"Qin, C. et al. GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana. Proc Natl Acad Sci USA \n                           105, 18308\u201318313, doi:10.1073\/pnas.0806168105 (2008).","journal-title":"Proc Natl Acad Sci USA"},{"key":"10765_CR11","doi-asserted-by":"publisher","first-page":"567","DOI":"10.1016\/j.tplants.2008.08.005","volume":"13","author":"CL Linster","year":"2008","unstructured":"Linster, C. L. & Clarke, S. G. L-Ascorbate biosynthesis in higher plants: the role of VTC2. Trends Plant Sci \n                           13, 567\u2013573, doi:10.1016\/j.tplants.2008.08.005 (2008).","journal-title":"Trends Plant Sci"},{"key":"10765_CR12","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1038\/30728","volume":"393","author":"GL Wheeler","year":"1998","unstructured":"Wheeler, G. L., Jones, M. A. & Smirnoff, N. The biosynthetic pathway of vitamin C in higher plants. Nature \n                           393, 365\u2013369, doi:10.1038\/30728 (1998).","journal-title":"Nature"},{"key":"10765_CR13","doi-asserted-by":"publisher","first-page":"14843","DOI":"10.1073\/pnas.011578198","volume":"98","author":"BA Wolucka","year":"2001","unstructured":"Wolucka, B. A. et al. Partial purification and identification of GDP-mannose 3\u2033, 5\u2033-epimerase of Arabidopsis thaliana, a key enzyme of the plant vitamin C pathway. Proc Natl Acad Sci USA \n                           98, 14843\u201314848, doi:10.1073\/pnas.011578198 (2001).","journal-title":"Proc Natl Acad Sci USA"},{"key":"10765_CR14","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1006\/abio.2001.5165","volume":"294","author":"BA Wolucka","year":"2001","unstructured":"Wolucka, B. A., Davey, M. W. & Boerjan, W. A high-performance liquid chromatography radio method for determination of L-ascorbic acid and guanosine 5\u2032-diphosphate-l-galactose, key metabolites of the plant vitamin C pathway. Anal Biochem \n                           294, 161\u2013168, doi:10.1006\/abio.2001.5165 (2001).","journal-title":"Anal Biochem"},{"key":"10765_CR15","doi-asserted-by":"publisher","first-page":"47483","DOI":"10.1074\/jbc.M309135200","volume":"278","author":"BA Wolucka","year":"2003","unstructured":"Wolucka, B. A. & Van Montagu, M. GDP-mannose 3\u2032,5\u2032-epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants. J Biol Chem \n                           278, 47483\u201347490, doi:10.1074\/jbc.M309135200 (2003).","journal-title":"J Biol Chem"},{"key":"10765_CR16","doi-asserted-by":"publisher","first-page":"2262","DOI":"10.1073\/pnas.051625798","volume":"98","author":"W Lukowitz","year":"2001","unstructured":"Lukowitz, W. et al. Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc Natl Acad Sci USA \n                           98, 2262\u20132267, doi:10.1073\/pnas.051625798 (2001).","journal-title":"Proc Natl Acad Sci USA"},{"key":"10765_CR17","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1007\/s00425-004-1205-x","volume":"219","author":"BL Reuhs","year":"2004","unstructured":"Reuhs, B. L. et al. l-Galactose replaces l-fucose in the pectic polysaccharide rhamnogalacturonan II synthesized by the l-fucose-deficient mur1 Arabidopsis mutant. Planta \n                           219, 147\u2013157, doi:10.1007\/s00425-004-1205-x (2004).","journal-title":"Planta"},{"key":"10765_CR18","doi-asserted-by":"publisher","first-page":"2602","DOI":"10.1016\/j.phytochem.2007.08.034","volume":"68","author":"BA Wolucka","year":"2007","unstructured":"Wolucka, B. A. & Van Montagu, M. The VTC2 cycle and the de novo biosynthesis pathways for vitamin C in plants: an opinion. Phytochemistry \n                           68, 2602\u20132613, doi:10.1016\/j.phytochem.2007.08.034 (2007).","journal-title":"Phytochemistry"},{"key":"10765_CR19","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1111\/j.1365-313X.2009.03972.x","volume":"60","author":"L Gilbert","year":"2009","unstructured":"Gilbert, L. et al. GDP-D-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and non-cellulosic cell-wall biosynthesis in tomato. Plant J \n                           60, 499\u2013508, doi:10.1111\/j.1365-313X.2009.03972.x (2009).","journal-title":"Plant J"},{"key":"10765_CR20","doi-asserted-by":"publisher","first-page":"338","DOI":"10.1016\/j.phytochem.2005.12.003","volume":"67","author":"K Watanabe","year":"2006","unstructured":"Watanabe, K., Suzuki, K. & Kitamura, S. Characterization of a GDP-D-mannose 3\u201d,5\u201d-epimerase from rice. Phytochemistry \n                           67, 338\u2013346, doi:10.1016\/j.phytochem.2005.12.003 (2006).","journal-title":"Phytochemistry"},{"key":"10765_CR21","doi-asserted-by":"publisher","first-page":"2331","DOI":"10.1007\/s10529-014-1598-y","volume":"36","author":"L Ma","year":"2014","unstructured":"Ma, L., Wang, Y., Liu, W. & Liu, Z. Overexpression of an alfalfa GDP-mannose 3, 5-epimerase gene enhances acid, drought and salt tolerance in transgenic Arabidopsis by increasing ascorbate accumulation. Biotechnol Lett \n                           36, 2331\u20132341, doi:10.1007\/s10529-014-1598-y (2014).","journal-title":"Biotechnol Lett"},{"key":"10765_CR22","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1111\/j.1399-3054.2009.01213.x","volume":"136","author":"T Imai","year":"2009","unstructured":"Imai, T., Ban, Y., Terakami, S., Yamamoto, T. & Moriguchi, T. L-Ascorbate biosynthesis in peach: cloning of six L-galactose pathway-related genes and their expression during peach fruit development. Physiol Plant \n                           136, 139\u2013149, doi:10.1111\/j.1399-3054.2009.01213.x (2009).","journal-title":"Physiol Plant"},{"key":"10765_CR23","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1146\/annurev.arplant.55.031903.141717","volume":"56","author":"H Ma","year":"2005","unstructured":"Ma, H. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol \n                           56, 393\u2013434 (2005).","journal-title":"Annu Rev Plant Biol"},{"key":"10765_CR24","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1007\/s004970050158","volume":"11","author":"P Sanders","year":"1999","unstructured":"Sanders, P. et al. RB Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod \n                           11, 297\u2013322 (1999).","journal-title":"Sex. Plant Reprod"},{"key":"10765_CR25","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1007\/s00497-010-0157-5","volume":"24","author":"D Twell","year":"2011","unstructured":"Twell, D. Male gametogenesis and germline specification in flowering plants. Sex Plant Reprod \n                           24, 149\u2013160 (2011).","journal-title":"Sex Plant Reprod"},{"issue":"Suppl","key":"10765_CR26","doi-asserted-by":"publisher","first-page":"S142","DOI":"10.1105\/tpc.016659","volume":"16","author":"S McCormick","year":"2004","unstructured":"McCormick, S. Control of male gametophyte development. Plant Cell \n                           16(Suppl), S142\u2013153, doi:10.1105\/tpc.016659 (2004).","journal-title":"Plant Cell"},{"key":"10765_CR27","doi-asserted-by":"publisher","first-page":"1458","DOI":"10.1126\/science.8197459","volume":"264","author":"D Preuss","year":"1994","unstructured":"Preuss, D., Rhee, S. Y. & Davis, R. W. Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science \n                           264, 1458\u20131460 (1994).","journal-title":"Science"},{"key":"10765_CR28","doi-asserted-by":"publisher","first-page":"8014","DOI":"10.1074\/jbc.M110.198614","volume":"286","author":"A Voxeur","year":"2011","unstructured":"Voxeur, A. et al. Silencing of the GDP-D-mannose 3,5-epimerase affects the structure and cross-linking of the pectic polysaccharide rhamnogalacturonan II and plant growth in tomato. J Biol Chem \n                           286, 8014\u20138020, doi:10.1074\/jbc.M110.198614 (2011).","journal-title":"J Biol Chem"},{"key":"10765_CR29","doi-asserted-by":"publisher","first-page":"1986","DOI":"10.1126\/science.270.5244.1986","volume":"270","author":"SS Gan","year":"1995","unstructured":"Gan, S. S. & Amasino, R. M. Inhibition of leaf senescence by autoregulated production of cytokinin. Science \n                           270, 1986\u20131988, doi:10.1126\/science.270.5244.1986 (1995).","journal-title":"Science"},{"key":"10765_CR30","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1111\/j.1399-3054.1994.tb05343.x","volume":"92","author":"KN Lohman","year":"1994","unstructured":"Lohman, K. N., Gan, S. S., John, M. C. & Amasino, R. M. Molecular Analysis of Natural Leaf Senescence in Arabidopsis thaliana. Physiol Plantarum \n                           92, 322\u2013328, doi:10.1034\/j.1399-3054.1994.920218.x (1994).","journal-title":"Physiol Plantarum"},{"key":"10765_CR31","doi-asserted-by":"publisher","first-page":"1015","DOI":"10.1104\/pp.120.4.1015","volume":"120","author":"JD Miller","year":"1999","unstructured":"Miller, J. D., Arteca, R. N. & Pell, E. J. Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol \n                           120, 1015\u20131024 (1999).","journal-title":"Plant Physiol"},{"key":"10765_CR32","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1023\/A:1005958300951","volume":"37","author":"JH Park","year":"1998","unstructured":"Park, J. H., Oh, S. A., Kim, Y. H., Woo, H. R. & Nam, H. G. Differential expression of senescence-associated mRNAs during leaf senescence induced by different senescence-inducing factors in Arabidopsis. Plant Mol Biol \n                           37, 445\u2013454 (1998).","journal-title":"Plant Mol Biol"},{"key":"10765_CR33","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1023\/A:1005934428906","volume":"37","author":"LM Weaver","year":"1998","unstructured":"Weaver, L. M., Gan, S., Quirino, B. & Amasino, R. M. A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol \n                           37, 455\u2013469 (1998).","journal-title":"Plant Mol Biol"},{"key":"10765_CR34","doi-asserted-by":"publisher","first-page":"4767","DOI":"10.1093\/jxb\/erw260","volume":"67","author":"L Mounet-Gilbert","year":"2016","unstructured":"Mounet-Gilbert, L. et al. Two tomato GDP-D-mannose epimerase isoforms involved in ascorbate biosynthesis play specific roles in cell wall biosynthesis and development. J Exp Bot \n                           67, 4767\u20134777, doi:10.1093\/jxb\/erw260 (2016).","journal-title":"J Exp Bot"},{"key":"10765_CR35","doi-asserted-by":"publisher","first-page":"1177","DOI":"10.1093\/aob\/mcu093","volume":"114","author":"M Dumont","year":"2014","unstructured":"Dumont, M. et al. The cell wall pectic polymer rhamnogalacturonan-II is required for proper pollen tube elongation: implications of a putative sialyltransferase-like protein. Ann Bot \n                           114, 1177\u20131188, doi:10.1093\/aob\/mcu093 (2014).","journal-title":"Ann Bot"},{"key":"10765_CR36","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1111\/nph.13200","volume":"206","author":"K Hoedemaekers","year":"2015","unstructured":"Hoedemaekers, K. et al. BURSTING POLLEN is required to organize the pollen germination plaque and pollen tube tip in Arabidopsis thaliana. New Phytol \n                           206, 255\u2013267, doi:10.1111\/nph.13200 (2015).","journal-title":"New Phytol"},{"key":"10765_CR37","doi-asserted-by":"publisher","first-page":"647","DOI":"10.1111\/j.1365-313X.2010.04452.x","volume":"65","author":"XL Liu","year":"2011","unstructured":"Liu, X. L. et al. Male gametophyte defective 4 encodes a rhamnogalacturonan II xylosyltransferase and is important for growth of pollen tubes and roots in Arabidopsis. Plant J \n                           65, 647\u2013660, doi:10.1111\/j.1365-313X.2010.04452.x (2011).","journal-title":"Plant J"},{"key":"10765_CR38","doi-asserted-by":"publisher","first-page":"117","DOI":"10.3109\/10520296909063335","volume":"44","author":"MP Alexander","year":"1969","unstructured":"Alexander, M. P. Differential staining of aborted and nonaborted pollen. Stain Technol \n                           44, 117\u2013122 (1969).","journal-title":"Stain Technol"},{"key":"10765_CR39","doi-asserted-by":"publisher","first-page":"2191","DOI":"10.1105\/tpc.13.10.2191","volume":"13","author":"S Ishiguro","year":"2001","unstructured":"Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I. & Okada, K. The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. The Plant Cell \n                           13, 2191\u20132209 (2001).","journal-title":"The Plant Cell"},{"key":"10765_CR40","doi-asserted-by":"publisher","first-page":"570","DOI":"10.1111\/j.1365-313X.2007.03248.x","volume":"52","author":"LC Boavida","year":"2007","unstructured":"Boavida, L. C. & McCormick, S. Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J. \n                           52, 570\u2013582 (2007).","journal-title":"Plant J."},{"key":"10765_CR41","doi-asserted-by":"crossref","first-page":"3901","DOI":"10.1002\/j.1460-2075.1987.tb02730.x","volume":"6","author":"RA Jefferson","year":"1987","unstructured":"Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. Embo J \n                           6, 3901\u20133907 (1987).","journal-title":"Embo J"},{"key":"10765_CR42","doi-asserted-by":"publisher","first-page":"1795","DOI":"10.1105\/tpc.111.083261","volume":"23","author":"T Qi","year":"2011","unstructured":"Qi, T. et al. The jasmonate-ZIM-domain proteins interact with the WD-Repeat\/bHLH\/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. The Plant Cell \n                           23, 1795\u20131814 (2011).","journal-title":"The Plant Cell"},{"key":"10765_CR43","doi-asserted-by":"publisher","first-page":"1565","DOI":"10.1038\/nprot.2007.199","volume":"2","author":"SD Yoo","year":"2007","unstructured":"Yoo, S. D., Cho, Y. H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc \n                           2, 1565\u20131572 (2007).","journal-title":"Nat Protoc"},{"key":"10765_CR44","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1006\/abio.1995.1127","volume":"225","author":"K Kampfenkel","year":"1995","unstructured":"Kampfenkel, K., Van Montagu, M. & Inze, D. Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem \n                           225, 165\u2013167 (1995).","journal-title":"Anal Biochem"},{"key":"10765_CR45","doi-asserted-by":"publisher","first-page":"1634","DOI":"10.1105\/tpc.15.00110","volume":"27","author":"T Qi","year":"2015","unstructured":"Qi, T. et al. Regulation of jasmonate-induced leaf senescence by antagonism between bHLH subgroup IIIe and IIId factors in Arabidopsis. The Plant Cell \n                           27, 1634\u20131649, doi:10.1105\/tpc.15.00110 (2015).","journal-title":"The Plant Cell"},{"key":"10765_CR46","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1105\/tpc.113.120394","volume":"26","author":"S Song","year":"2014","unstructured":"Song, S. et al. Interaction between MYC2 and ETHYLENE INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis. The Plant Cell \n                           26, 263\u2013279 (2014).","journal-title":"The Plant Cell"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-10765-5","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-10765-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-10765-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,23]],"date-time":"2022-12-23T10:12:56Z","timestamp":1671790376000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-10765-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,9,4]]},"references-count":46,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,12]]}},"alternative-id":["10765"],"URL":"https:\/\/doi.org\/10.1038\/s41598-017-10765-5","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,9,4]]},"assertion":[{"value":"16 May 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 August 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 September 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that they have no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"10309"}}