Abstract
With the rapid development of omics technologies during the last several decades, genomics, transcriptomics, and proteomics have been extensively used to characterize gene or protein functions in many organisms at the cell or tissue level. However, metabolomics has not been conducted in reproductive organs, with a focus on meiosis in plants. In this study, we adopted a nuclear magnetic resonance (NMR)-based metabolomics approach to reveal the metabolic profile of inflorescences from two Arabidopsis accessions, Columbia (Col) and Landsberg erecta (Ler), and several sterile mutants caused by meiosis defects. We identified 68 dominant metabolites in the samples. Col and Ler displayed distinct metabolite profiles. Interestingly, mutants with similar meiotic defects, such as Atrad51-3, Atrfc1-2, and Atpol2a-2, exhibited similar alterations in metabolites, including upregulation of energy metabolites and promotion of compounds related to maintenance of genomic stability, cytoplasmic homeostasis, and membrane integrity. The collective data reveal distinct changes in metabolites in Arabidopsis inflorescences between the Col and Ler wild type accessions. NMR-based metabolomics could be an effective tool for molecular phenotyping in studies of aspects of plant reproductive development such as meiosis.
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Data availability
The datasets generated for this study are available upon request from the corresponding authors.
Code availability
Not applicable.
Abbreviations
- DSBs:
-
Double-strand breaks
- COs:
-
Crossovers
- NCOs:
-
Non-crossovers
- Col-0:
-
Columbia-0
- Ler :
-
Landsberg erecta
- 1H-NMR:
-
Proton nuclear magnetic resonance
- LC–MS:
-
Liquid chromatography-mass spectrometry
- GC–MS:
-
Gas chromatography–mass spectrometry
- PCA:
-
Principal component analysis
- OPLS-DA:
-
Orthogonal projection to latent structure with discriminant analysis
- COSY:
-
Correlation spectroscopy
- TOCSY:
-
Total correlation spectroscopy
- JRES:
-
J-resolved spectroscopy
- HSQC:
-
Heteronuclear single quantum coherence spectroscopy
- HMBC:
-
Heteronuclear multiple-bond correlation
- Ala:
-
Alanine
- Arg:
-
Arginine
- α-KG:
-
α-Ketoglutarate
- cAA:
-
cis-Aconitic acid
- Cho:
-
Choline
- Cit:
-
Citrate
- DMA:
-
Dimethylamine
- EA:
-
Ethanolamine
- Eth:
-
Ethanol
- Fruc:
-
Fructose
- Fum:
-
Fumarate
- GABA:
-
4-Aminobutyrate
- Glc:
-
Glucose
- Glu:
-
Glutamate
- Gln:
-
Glutamine
- His:
-
Histidine
- Ile:
-
Isoleucine
- Lac:
-
Lactate
- Tyr:
-
Tyrosine
- Phe:
-
Phenylalanine
- Thr:
-
Threonine
- Suc:
-
Sucrose
- Succ:
-
Succinate
- Val:
-
Valine
- 6PGL:
-
6-Phosphogluconate
- E-4-P:
-
Erythrose-4-phosphate
- PRPP:
-
5-Phosphoribosyl diphosphate
- PEP:
-
Phosphoenolpyruvate
- Ici:
-
Isocitrate
- F-1,6-2P:
-
Fructose-1, 6-biphosphate
- TCA:
-
Tricarboxylic acid
- IMP:
-
Inosine monophosphate
- UMP:
-
Uridine monophosphate
- CMP:
-
Cytidine monophosphate
- DMA:
-
Dimethylamine
- SAM:
-
S-adenosylmethionine
- AMP:
-
Adenosine monophosphate
- ADP:
-
Adenosine diphosphate
- ATP:
-
Adenosine triphosphate
References
Abdullah MF, Borts RH (2001) Meiotic recombination frequencies are affected by nutritional states in Saccharomy cescerevisiae. Proc Natl Acad Sci USA 98(25):14524–14529. https://doi.org/10.1073/pnas.201529598
Andreuzza S, Nishal B, Singh A, Siddiqi I (2015) The chromatin protein DUET/MMD1 controls expression of the meiotic gene TDM1 during male meiosis in Arabidopsis. PLOS Genet 11(9):e1005396. https://doi.org/10.1371/journal.pgen.1005396
Bauschjurken MT, Sabina RL (1995) Divergent N-terminal regions in AMP deaminase and isoform-specific catalytic properties of the enzyme. Arch Biochem Biophys 321(2):372–380. https://doi.org/10.1006/abbi.1995.1407
Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9(3):110. https://doi.org/10.1016/j.tplants
Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, Yashiro K, Chawengsaksophak K, Wilson MJ, Rossant J, Hamada H, Koopman P (2006) Retinoid signaling determines germ cell fate in mice. Science 312(5773):596–600. https://doi.org/10.1126/science.1125691
Cao X, Jacobsen SE (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12(13):1138–1144. https://doi.org/10.1016/S0960-9822(02)00925-9
Chen C, Farmer AD, Langley RJ, Mudge J, Crow JA, May GD, Huntley J, Smith AG, Retzel EF (2010) Meiosis-specific gene discovery in plants: RNA-Seq applied to isolated Arabidopsis male meiocytes. BMC Plant Biol 10:280. https://doi.org/10.1186/1471-2229-10-280
Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335(6065):207. https://doi.org/10.1126/science.1213351
Choi YH, Tapias EC, Kim HK, Lefeber AW, Erkelens C, Verhoeven JT, Brzin J, Zel J, Verpoorte R (2004) Metabolic discrimination of Catharanthus roseus leaves infected by phytoplasma using 1H-NMR spectroscopy and multivariate data analysis. Plant Physiol 135(4):2398–2410. https://doi.org/10.1104/pp.104.041012
Cloarec O, Dumas ME, Trygg J, Craig A, Barton RH, Lindon JC, Nicholson JK, Holmes E (2005) Evaluation of the orthogonal projection on latent structure model limitations caused by chemical shift variability and improved visualization of biomarker changes in 1H NMR spectroscopic metabonomic studies. Anal Chem 77(2):517–526. https://doi.org/10.1021/ac048803i
Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant cell 11(9):1623–1634. https://doi.org/10.1105/tpc.11.9.1623
Cui Q, Lewis IA, Hegeman AD, Anderson ME, Li J, Schulte CF, Westler WM, Eghbalnia HR, Sussman MR, Markley JL (2008) Metabolite identification via the madison metabolomics consortium database. Nat Biotechnol 26(2):162–164. https://doi.org/10.1038/nbt0208-162
Dai H, Xiao C, Liu H, Hao F, Tang H (2010a) Combined NMR and LC-DAD-MS analysis reveals comprehensive metabonomic variations for three phenotypic cultivars of Salvia Miltiorrhiza Bunge. J Proteome Res 9(3):1565–1578. https://doi.org/10.1021/pr901045c
Dai H, Xiao C, Liu H, Tang H (2010b) Combined NMR and LC-MS analysis reveals the metabonomic changes in Salvia miltiorrhiza bunge induced by water depletion. J Proteome Res 9(3):1460–1475. https://doi.org/10.1021/pr900995m
Downs SM (1994) Induction of meiotic maturation In vivo in the mouse by IMP dehydrogenase inhibitors: effects on the developmental capacity of Ova. Mol Reprod Dev 38:293–302. https://doi.org/10.1002/mrd.1080380310
Drouaud J, Khademian H, Giraut L, Zanni V, Bellalou S, Henderson IR, Falque M, Mézard C (2013) Contrasted patterns of crossover and non-crossover at Arabidopsis thaliana meiotic recombination hotspots. PLoS Genet 9(11):e1003922. https://doi.org/10.1371/journal.pgen.1003922
Fan WMT (1996) Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog Nucl Mag Res Sp 28:161–219. https://doi.org/10.1016/0079-6565(95)01017-3
Fan WM, Lane AN (2008) Structure-based profiling of metabolites and isotopomers by NMR. Prog Nucl Mag Res Sp 52(2):69–117. https://doi.org/10.1016/j.pnmrs.2007.03.002
Francini A, Romeo S, Cifelli M, Gori D, Domenici V, Sebastiani L (2017) 1H NMR and PCA-based analysis revealed variety dependent changes in phenolic contents of apple fruit after drying. Food Chem 221:1206–1213. https://doi.org/10.1016/j.foodchem.2016.11.038
Garcia-Perez I, Posma JM, Serrano-Contreras JI, Boulange CL, Chan Q, Frost G, Stamler J, Elliott P, Lindon JC, Holmes E, Nicholson JK (2020) Identifying unknown metabolites using NMR-based metabolic profiling techniques. Nat Protoc 15(8):2538–2567. https://doi.org/10.1038/s41596-020-0343-3
Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. Embo J 20(3):589–600. https://doi.org/10.1093/emboj/20.3.589
Hale CJ, Potok ME, Lopez J, Do T, Liu A, Gallego-Bartolome J, Michaels SD, Jacobsen SE (2016) Identification of multiple proteins coupling transcriptional gene silencing to genome stability in Arabidopsis thaliana. PLOS Genet 12(6):e1006092. https://doi.org/10.1371/journal.pgen.1006092
Hamant O, Ma H, Cande WZ (2006) Genetics of meiotic prophase I in plants. Annu Rev Plant Biol 57:267–302. https://doi.org/10.1146/annurev.arplant.57.032905.105255
Hartung F, Wurz-Wildersinn R, Fuchs J, Schubert I, Suer S, Puchta H (2007) The catalytically active tyrosine residues of both SPO11-1 and SPO11-2 are required for meiotic double-strand break induction in Arabidopsis. Plant Cell 19(10):3090–3099. https://doi.org/10.1105/tpc.107.054817
Herrick JR, Brad AM, Krisher RL (2006) Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 131(2):289–298. https://doi.org/10.1530/rep.1.00835
Hopper AK, Magee PT, Welch SK, Friedman M, Hall BD (1974) Macromolecule synthesis and breakdown in relation to sporulation and meiosis in yeast. J Bacteriol 119(2):619–628. https://doi.org/10.1128/JB.119.2.619-628.1974
Huang J, Cheng Z, Wang C, Hong Y, Su H, Wang J, Copenhaver GP, Ma H, Wang Y (2015) Formation of interference-sensitive meiotic cross-overs requires sufficient DNA leading-strand elongation. Proc Natl Acad Sci USA 112(40):12534–12539. https://doi.org/10.1073/pnas.1507165112
Huang JY, Copenhaver GP, Ma H, Wang YX (2016) New insights into the role of DNA synthesis in meiotic recombination. Sci Bull 61(16):1260–1269. https://doi.org/10.1007/s11434-016-1126-7
Huo Y, Kamal GM, Wang J, Liu H, Zhang G, Hu Z, Anwar F, Du H (2017) 1H NMR-based metabolomics for discrimination of rice from different geographical origins of China. J Cereal Sci 76:243–252. https://doi.org/10.1016/j.jcs
Kalitsis P, Zhang T, Marshall KM, Nielsen CF, Hudson DF (2017) Condensin, master organizer of the genome. Chromosome Res 25(1):61–76. https://doi.org/10.1007/s10577-017-9553-0
Koubova J, Hu YC, Bhattacharyya T, Soh YQ, Gill ME, Goodheart ML, Hogarth CA, Griswold MD, Page DC (2014) Retinoic acid activates two pathways required for meiosis in mice. PLOS Genet 10(8):e1004541. https://doi.org/10.1371/journal.pgen.1004541
Kumar Y, Zhang L, Panigrahi P, Dholakia BB, Dewangan V, Chavan SG, Kunjir SM, Wu X, Li N, Rajmohanan PR, Kadoo NY, Giri AP, Tang H, Gupta VS (2016) Fusarium oxysporum mediates systems metabolic reprogramming of chickpea roots as revealed by a combination of proteomics and metabolomics. Plant Biotechnol J 14(7):1589–1603. https://doi.org/10.1111/pbi.12522
Kusano M, Yang Z, Okazaki Y, Nakabayashi R, Fukushima A, Saito K (2015) Using metabolomic approaches to explore chemical diversity in rice. Mol Plant 8(1):58–67. https://doi.org/10.1016/j.molp.2014.11.010
Le Gall G, Colquhoun IJ, Davis AL, Collins GJ, Verhoeyen ME (2003) Metabolite profiling of tomato (Lycopersicon esculentum) using 1H NMR spectroscopy as a tool to detect potential unintended effects following a genetic modification. J Agric Food Chem 51(9):2447–2456. https://doi.org/10.1021/jf0259967
Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E, Ma H, Reiss B (2004) The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc Natl Acad Sci USA 101(29):10596–10601. https://doi.org/10.1073/pnas.0404110101
Li L, Zhu S, Shu W, Guo Y, Guan Y, Zeng J, Wang H, Han L, Zhang J, Liu X, Li C, Hou X, Gao M, Ge J, Ren C, Zhang H, Schedl T, Guo X, Chen M, Wang Q (2020) Characterization of Metabolic Patterns in Mouse Oocytes during Meiotic Maturation. Mol Cell 80 (3):525–540 e529. doi:https://doi.org/10.1016/j.molcel.2020.09.022
Lima MR, Felgueiras ML, Graça G, Rodrigues JE, Barros A, Gil AM, Dias AC (2010) NMR metabolomics of esca disease-affected Vitis vinifera cv. Alvarinho leaves J Exp Bot 61(14):4033–4042. https://doi.org/10.1093/jxb/erq214
Liu C, Du B, Hao F, Lei H, Wan Q, He G, Wang Y, Tang H (2017) Dynamic metabolic responses of brown planthoppers towards susceptible and resistant rice plants. Plant Biotechnol J 15(10):1346–1357. https://doi.org/10.1111/pbi.12721
Melamedbessudo C, Levy AA (2012) Deficiency in DNA methylation increases meiotic crossover rates in euchromatic but not in heterochromatic regions in Arabidopsis. Proc Natl Acad Sci USA 109(16):5932–5933. https://doi.org/10.1073/pnas.1120742109
Meng J, Wang L, Wang J, Zhao X, Cheng J, Yu W, Jin D, Li Q, Gong Z (2018) Methionine adenosyltransferase 4 mediates DNA and histone methylation. Plant Physiol. https://doi.org/10.1104/pp.18.00183
Mercier R, Mezard C, Jenczewski E, Macaisne N, Grelon M (2015) The molecular biology of meiosis in plants. Annu Rev Plant Biol 66:297–327. https://doi.org/10.1146/annurev-arplant-050213-035923
Mirouze M, Aversano R, Bucher E, Nicolet J, Reinders J, Paszkowski J (2012) Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc Natl Acad Sci USA 109(15):5880–5885. https://doi.org/10.1073/pnas.1120841109
Osman K, Roitinger E, Yang J, Armstrong S, Mechtler K, Franklin FCH (2013) Analysis of meiotic protein complexes from Arabidopsis and brassica using affinity-based proteomics. Methods in molecular biology (Clifton, NJ) 990:215–226. https://doi.org/10.1007/978-1-62703-333-6_21
Poisson LM, Munkarah A, Madi H, Datta I, Hensley-Alford S, Tebbe C, Buekers T, Giri S, Rattan R (2015) A metabolomic approach to identifying platinum resistance in ovarian cancer. J Ovarian Res 8(1):13. https://doi.org/10.1186/s13048-015-0140-8
Popov VN, Eprintsev AT, Fedorin DN, Oiu F, Igamberdiev AU (2007) Role of transamination in the mobilization of respiratory substrates in germinating seeds of castor oil plants. Appl Biochem Micro 43(3):341–346. https://doi.org/10.1104/pp.44.6.789
Pradillo M, Lopez E, Linacero R, Romero C, Cunado N, Sanchez-Moran E, Santos JL (2012) Together yes, but not coupled: new insights into the roles of RAD51 and DMC1 in plant meiotic recombination. Plant J 69(6):921–933. https://doi.org/10.1111/j.1365-313X.2011.04845.x
Rato L, Alves MG, Socorro S, Duarte AI, Cavaco JE, Oliveira PF (2012) Metabolic regulation is important for spermatogenesis. Nat Rev Urol 9(6):330–338. https://doi.org/10.1038/nrurol.2012.77
Ray D, Ye P (2013) Characterization of the metabolic requirements in yeast meiosis. PLoS ONE 8(5):e63707. https://doi.org/10.1371/journal.pone.0063707
Ren Y, Wang T, Peng Y, Xia B, Qu L-J (2009) Distinguishing transgenic from non-transgenic Arabidopsis plants by 1H NMR-based metabolic fingerprinting. J Genet Genomics 36(10):621–628. https://doi.org/10.1016/s1673-8527(08)60154-x
Sotelo-Silveira M, Chauvin A-L, Marsch-Martínez N, Winkler R, de Folter S (2015) Metabolic fingerprinting of Arabidopsis thaliana accessions. Front Plant Sci 6:365–365. https://doi.org/10.3389/fpls.2015.00365
Stacey NJ, Kuromori T, Azumi Y, Roberts G, Breuer C, Wada T, Maxwell A, Roberts K, Sugimoto-Shirasu K (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J 48(2):206–216. https://doi.org/10.1111/j.1365-313X.2006.02867.x
Stechow L, Ruiz-Aracama A, van de Water B, Peijnenburg A, Danen E, Lommen A (2013) Identification of cisplatin-regulated metabolic pathways in pluripotent stem cells. PLOS One 8 (10):e76476. doi:https://doi.org/10.1371/journal.pone.0076476
Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 15(8):462–470
Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8(4):735. https://doi.org/10.1105/tpc.8.4.735
Vrielynck N (2016) A DNA topoisomerase VI–like complex initiates meiotic recombination. Science 351(6276):939–943. https://doi.org/10.1126/science.aad5196
Walther T, Letisse F, Peyriga L, Alkim C, Liu Y, Lardenois A, Martin-Yken H, Portais JC, Primig M, Francois J (2014) Developmental stage dependent metabolic regulation during meiotic differentiation in budding yeast. BMC Biol 12:60. https://doi.org/10.1186/s12915-014-0060-x
Wang Y, Copenhaver GP (2018) Meiotic recombination: mixing it up in plants. Annu Rev Plant Biol 69 (1):13.11–13.33. doi:https://doi.org/10.1146/annurev-arplant-042817-040431
Wang Y, Holmes E, Tang H, Lindon JC, Sprenger N, Turini ME, Bergonzelli G, Fay LB, Kochhar S, Nicholson JK (2006) Experimental metabonomic model of dietary variation and stress interactions. J Proteome Res 5(7):1535–1542. https://doi.org/10.1021/pr0504182
Wang YL, Lawler D, Larson B, Ramadan Z, Kochhar S, Holmes E, Nicholson JK (2007) Metabonomic investigations of aging and caloric restriction in a life-long dog study. J Proteome Res 6(5):1846–1854. https://doi.org/10.1021/pr060685n
Wang Y, Cheng Z, Huang J, Shi Q, Hong Y, Copenhaver GP, Gong Z, Ma H (2012) The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana. PLoS Genet 8(11):e1003039. https://doi.org/10.1371/journal.pgen.1003039
Wang Y, Xiao R, Wang H, Cheng Z, Li W, Zhu G, Wang Y, Ma H (2014) The Arabidopsis RAD51 paralogs RAD51B, RAD51D and XRCC2 play partially redundant roles in somatic DNA repair and gene regulation. New Phytol 201(1):292–304. https://doi.org/10.1111/nph.12498
Wang J, Niu B, Huang J, Wang H, Yang X, Dong A, Makaroff C, Ma H, Wang Y (2016) The PHD finger protein MMD1/DUET ensures the progression of male meiotic chromosome condensation and directly regulates the expression of the condensin gene CAP-D3. Plant Cell 28(8):1894–1909. https://doi.org/10.1105/tpc.16.00040
Wang C, Huang J, Zhang J, Wang H, Han Y, Copenhaver GP, Ma H, Wang Y (2019) The largest subunit of DNA polymerase delta is required for normal formation of meiotic type I crossovers. Plant Physiol 179(2):446–459. https://doi.org/10.1104/pp.18.00861
Ward J, Harris C, Lewis J, Beale M (2003) Assessment of 1H NMR spectroscopy and multivariate analysis as a technique for metabolite fingerprinting of Arabidopsis thaliana. Phytochemistry 62:949–957. https://doi.org/10.1016/S0031-9422(02)00705-7
Wen W, Li K, Alseekh S, Omranian N, Zhao L, Zhou Y, Xiao Y, Jin M, Yang N, Liu H, Florian A, Li W, Pan Q, Nikoloski Z, Yan J, Fernie AR (2015) Genetic determinants of the network of primary metabolism and their relationships to plant performance in a maize recombinant inbred line population. Plant Cell 27(7):1839–1856. https://doi.org/10.1105/tpc.15.00208
Widarto HT, Van DME, Lefeber AW, Erkelens C, Kim HK, Choi YH, Verpoorte R (2006) Metabolomic differentiation of Brassica rapa following herbivory by different insect instars using two-dimensional nuclear magnetic resonance spectroscopy. J Chem Ecol 32(11):2417–2428. https://doi.org/10.1007/s10886-006-9152-6
Xiao C, Dai H, Liu H, Wang Y, Tang H (2008) Revealing the metabonomic variation of rosemary extracts using 1H NMR spectroscopy and multivariate data analysis. J Agric Food Chem 56(21):10142–10153. https://doi.org/10.1021/jf8016833
Xie HL, Wang YB, Jiao GZ, Kong DL, Li Q, Li H, Zheng LL, Tan JH (2016) Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes. Sci Rep 6:20764. https://doi.org/10.1038/srep20764
Xu J, Zhang HY, Xie CH, Xue HW, Dijkhuis P, Liu CM (2005) EMBRYONIC FACTOR 1 encodes an AMP deaminase and is essential for the zygote to embryo transition in Arabidopsis. Plant J 42(5):743–756. https://doi.org/10.1111/j.1365-313X.2005.02411.x
Yang Y, Bedford MT (2013) Protein arginine methyltransferases and cancer. Nat Rev Cancer 13(1):37. https://doi.org/10.1038/nrc3409
Yang X, Makaroff CA, Ma H (2003) The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell 15(6):1281–1295. https://doi.org/10.1105/tpc.010447
Yang H, Lu P, Wang Y, Ma H (2011) The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J 65(4):503–516. https://doi.org/10.1111/j.1365-313X.2010.04439.x
Yao Y, Li X, Chen W, Liu H, Mi L, Ren D, Mo A, Lu P (2020) ATM promotes RAD51-mediated meiotic DSB repair by inter-sister-chromatid recombination in Arabidopsis. Front Plant Sci 11:839. https://doi.org/10.3389/fpls.2020.00839
Yuan Y, Zhao Y, Yang J, Jiang Y, Lu F, Jia Y, Yang B (2017) Metabolomic analyses of banana during postharvest senescence by 1H-high resolution-NMR. Food Chem 218:406–412. https://doi.org/10.1016/j.foodchem.2016.09.080
Zhang J, Zhang Y, Du Y, Chen S, Tang H (2011) Dynamic metabonomic responses of tobacco (Nicotiana tabacum) plants to salt stress. J Proteome Res 10(4):1904–1914. https://doi.org/10.1021/pr101140n
Zhao L, Huang Y, Hu J, Zhou H, Adeleye AS, Keller AA (2016) 1H NMR and GC-MS based metabolomics reveal defense and detoxification mechanism of cucumber plant under nano-Cu stress. Environ Sci Technol 50(4):2000–2010. https://doi.org/10.1021/acs.est.5b05011
Zhu G, Wang S, Huang Z, Zhang S, Liao Q, Zhang C, Lin T, Qin M, Peng M, Yang C (2018) Rewiring of the fruit metabolome in tomato breeding. Cell 172(1–2):249–261. https://doi.org/10.1016/j.cell
Acknowledgments
We thank Dr. Yanpeng An at the School of Life Sciences of Fudan University for helpful discussions regarding the experimental data.
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This work was supported by grants from the National Science Foundation of China (31570314 and 31925005) and by funds from the State Key Laboratory of Genetic Engineering at Fudan University.
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YXW and LMZ designed the research; YXW, LMZ and YW performed the experiments; XL, HKW, YXW and LMZ analyzed the data; and XL and HKW drafted the manuscript. YXW and LMZ have revised the manuscript. All authors read and approved the final manuscript.
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Li, X., Wang, H., Wang, Y. et al. Comparison of Metabolic Profiling of Arabidopsis Inflorescences Between Landsberg erecta and Columbia, and Meiosis-Defective Mutants by 1H-NMR Spectroscopy. Phenomics 1, 73–89 (2021). https://doi.org/10.1007/s43657-021-00012-3
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DOI: https://doi.org/10.1007/s43657-021-00012-3