Abstract
Plant sugars serve to balance nutrition, regulate development, and respond to biotic and abiotic stresses, whereas non-structural carbohydrates (NSCs) are essential energy sources that facilitate plant growth, metabolism, and environmental adaptation. To better elucidate the mechanisms of NSCs in red maple, ultrahigh-performance liquid chromatograph Q extractive mass spectrometry (UHPLC-QE-MS) and high-throughput RNA-sequencing were performed on green, red, and yellow leaves from a selected red maple mutant. In green leaves, the fructose phosphorylation process exhibited greater flux. In yellow leaves, sucrose and starch had a stronger capacity for synthesis and degradation, whereas in red leaves, there was a greater accumulation of trehalose and manninotriose. ArTPS5 positively regulated amylose, which was negatively regulated by ArFBP2, whereas ArFRK2 and ArFBP13 played a positive role in the biosynthesis of Sucrose-6P. Sucrose-6P also regulated anthocyanins and abscisic acid in red maple by affecting transcription factors. The results of this paper can assist with the control and optimization of the biosynthesis of NSCs in red maple, which may ultimately provide the foundation for influencing sugar production in Acer.
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Data availability
The datasets generated and analyzed during the current study (SRA accession number PRJNA531583) has been released on NCBI (https://www.ncbi.nlm.nih.gov/). The metabolomics and metadata reported in this paper are available at www.ebi.ac.uk/metabolights/MTBLS903 study identifier MTBLS903.
References
Aghdasi M, Smeekens S, Schluepmanb H (2008) Microarray analysis of gene expression patterns in Arabidopsis seedlings under trehalose, sucrose and sorbitol. Int J Plant Prod 2
Araniti F, Lupini A, Mauceri A, Zumbo A, Sunseri F, Abenavoli MR (2018) The allelochemical trans-cinnamic acid stimulates salicylic acid production and galactose pathway in maize leaves: a potential mechanism of stress tolerance. Plant Physiol Biochem 128:32–40. https://doi.org/10.1016/j.plaphy.2018.05.006
Beauvoit B et al (2014) Model-assisted analysis of sugar metabolism throughout tomato fruit development reveals enzyme and carrier properties in relation to vacuole expansion. Plant Cell:26. https://doi.org/10.1105/tpc.114.127761
Benaroudj N, Lee DH, Goldberg AL (2001) Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem 276:24261–24267. https://doi.org/10.1074/jbc.M101487200
Bi W et al (2016) Traditional uses, phytochemistry, and pharmacology of the genus Acer (maple): a review. J Ethnopharmacol 189:31–60. https://doi.org/10.1016/j.jep.2016.04.021
Bläsing OE et al (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17:3257–3281. https://doi.org/10.1105/tpc.105.035261
Bonini BM, Van Dijck P, Thevelein JM (2004) Trehalose metabolism: enzymatic pathways and physiological functions. Biochemistry and Molecular Biology 3:291–332. https://doi.org/10.1007/978-3-662-06064-3_15
Cavill R, Jennen D, Kleinjans J, Briedé JJ (2016) Transcriptomic and metabolomic data integration. Brief Bioinform 17:891–901. https://doi.org/10.1093/bib/bbv090
Chang C-Y et al (2019) Identification of sugar response complex in the metallothionein OsMT2b gene promoter for enhancement of foreign protein production in transgenic rice. Plant Cell Rep 38. https://doi.org/10.1007/s00299-019-02411-3
Chardon F et al (2013) Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr Biol 23:697–702. https://doi.org/10.1016/j.cub.2013.03.021
Chen W et al (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574. https://doi.org/10.1105/tpc.010410
Chen Z, Lu X, Xuan Y, Tang F, Wang J, Shi D, Fu S, Ren J (2019) Transcriptome analysis based on a combination of sequencing platforms provides insights into leaf pigmentation in Acer rubrum. BMC Plant Biol 19:240. https://doi.org/10.1186/s12870-019-1850-7
Dong Q et al (2019) Overexpression of ZmbZIP22 gene alters endosperm starch content and composition in maize and rice. Plant Sci 283:407–415. https://doi.org/10.1016/j.plantsci.2019.03.001
Downie B et al (2003) Expression of a GALACTINOL SYNTHASE gene in tomato seeds is up-regulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented. Plant Physiol 131:1347–1359. https://doi.org/10.1104/pp.016386
Doyle EA, Lane AM, Sides JM, Mudgett MB, Monroe JD (2007) An alpha-amylase (At4g25000) in Arabidopsis leaves is secreted and induced by biotic and abiotic stress. Plant Cell Environ 30:388–398. https://doi.org/10.1111/j.1365-3040.2006.01624.x
Elsayed A, Rafudeen M, Golldack D (2013) Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol (Stuttgart, Germany) 16. https://doi.org/10.1111/plb.12053
Fan W, Zhang Z, Zhang Y (2009) Cloning and molecular characterization of fructose-1,6-bisphosphate aldolase gene regulated by high-salinity and drought in Sesuvium portulacastrum. Plant Cell Rep 28:975–984. https://doi.org/10.1007/s00299-009-0702-6
Fernandez O, Béthencourt L, Quero A, Sangwan RS, Clément C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417. https://doi.org/10.1016/j.tplants.2010.04.004
Gleiser G, Verdú M (2005) Repeated evolution of dioecy from androdioecy in Acer. New Phytol 165:633–640. https://doi.org/10.1111/j.1469-8137.2004.01242.x
González-Sarrías A, Li L, Seeram NP (2012) Effects of maple (Acer) plant part extracts on proliferation, apoptosis and cell cycle arrest of human tumorigenic and non-tumorigenic colon cells. Phytother Res 26:995–1002. https://doi.org/10.1002/ptr.3677
Gu L et al (2019) Maize HSFA2 and HSBP2 antagonistically modulate raffinose biosynthesis and heat tolerance in Arabidopsis. 100:128–142. https://doi.org/10.1111/tpj.14434
Han Q et al (2020) ZmDREB2A regulates ZmGH3.2 and ZmRAFS, shifting metabolism towards seed aging tolerance over seedling growth. Plant J. https://doi.org/10.1111/tpj.14922
Holger BD (2009) The mycota : a comprehensive treatise on fungi as experimental systems for basic and applied research. Springer Berlin Heidelberg, Berlin, Heidelberg
Jia H et al (2017) Abscisic acid, sucrose, and auxin coordinately regulate berry ripening process of the Fujiminori grape. Funct Integr Genomics 17:441–457. https://doi.org/10.1007/s10142-017-0546-z
Jin R (2013) Sugar regulate the physiology of potato under different level of phosphorus. Dissertation, Gansu Agricultural University
Jorge TF, Rodrigues JA, Caldana C, Schmidt R, van Dongen JT, Thomas-Oates J, António C (2016) Mass spectrometry-based plant metabolomics: metabolite responses to abiotic stress. Mass Spectrom Rev 35:620–649. https://doi.org/10.1002/mas.21449
Keunen E, Peshev D, Vangronsveld J, Van Den Ende W, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242–1255. https://doi.org/10.1111/pce.12061
Kim MS et al (2008) Galactinol is a signaling component of the induced systemic resistance caused by Pseudomonas chlororaphis O6 root colonization. Mol Plant Microbe Interact 21:1643–1653. https://doi.org/10.1094/mpmi-21-12-1643
Kunz S, Gardeström P, Pesquet E, Kleczkowski LA (2015) Hexokinase 1 is required for glucose-induced repression of bZIP63, At5g22920, and BT2 in Arabidopsis. Front Plant Sci 6:525. https://doi.org/10.3389/fpls.2015.00525
Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65:799–807. https://doi.org/10.1093/jxb/ert474
Legault J, Girard-Lalancette K, Grenon C, Dussault C, Pichette A (2010) Antioxidant activity, inhibition of nitric oxide overproduction, and in vitro antiproliferative effect of maple sap and syrup from Acer saccharum. J Med Food 13:460–468. https://doi.org/10.1089/jmf.2009.0029
Legay S et al (2011) Carbohydrate metabolism and cell protection mechanisms differentiate drought tolerance and sensitivity in advanced potato clones (Solanum tuberosum L.). Funct Integr Genomics 11:275–291. https://doi.org/10.1007/s10142-010-0206-z
Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opin Plant Biol 33:116–125. https://doi.org/10.1016/j.pbi.2016.06.018
Li T et al (2015) Comparative proteomic approaches to analysis of litchi pulp senescence after harvest. Food Res Int (Ottawa, Ont) 78:274–285. https://doi.org/10.1016/j.foodres.2015.09.033
Liu J, Fu S, Yang L, Luan M, Zhao F, Luan S, Lan W (2016) Vacuolar SPX-MSF transporters are essential for phosphate adaptation in plants. Plant Signal Behav 11. https://doi.org/10.1080/15592324.2016.1213474
Liu Y, Rose KN, DaSilva NA, Johnson SL, Seeram NP (2017) Isolation, identification, and biological evaluation of phenolic compounds from a traditional North American confectionery, maple sugar. 65:4289–4295. https://doi.org/10.1021/acs.jafc.7b01969
Liu ZY, Baoyin T, Li XL, Wang ZL (2019) How fall dormancy benefits alfalfa winter-survival? Physiologic and transcriptomic analyses of dormancy process. BMC Plant Biol 19:205. https://doi.org/10.1186/s12870-019-1773-3
Lu Y, Sharkey TD (2006) The importance of maltose in transitory starch breakdown. Plant Cell Environ 29:353–366. https://doi.org/10.1111/j.1365-3040.2005.01480.x
Lu S, Li T, Jiang J (2010) Effects of salinity on sucrose metabolism during tomato fruit development. Afr J Biotechnol 9:842–849. https://doi.org/10.5897/AJB09.1602
Lu X, Chen Z, Gao J, Fu S, Hu H, Ren J (2020) Combined metabolome and transcriptome analyses of photosynthetic pigments in red maple. Plant Physiol Biochem 154:476–490. https://doi.org/10.1016/j.plaphy.2020.06.025
Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose metabolism in plants. Plant J 79:544–567. https://doi.org/10.1111/tpj.12509
Martins MC et al (2013) Feedback inhibition of starch degradation in Arabidopsis leaves mediated by trehalose 6-phosphate. Plant Physiol 163:1142–1163. https://doi.org/10.1104/pp.113.226787
Matiolli CC et al (2011) The Arabidopsis bZIP gene AtbZIP63 is a sensitive integrator of transient abscisic acid and glucose signals. Plant Physiol 157:692–705. https://doi.org/10.1104/pp.111.181743
Mrva K, Wallwork M, Mares DJ (2006) Alpha-amylase and programmed cell death in aleurone of ripening wheat grains. J Exp Bot 57:877–885. https://doi.org/10.1093/jxb/erj072
Murakami PF, Schaberg PG, Shane JB (2008) Stem girdling manipulates leaf sugar concentrations and anthocyanin expression in sugar maple trees during autumn. Tree Physiol 28:1467–1473. https://doi.org/10.1093/treephys/28.10.1467
Neilson J et al (2017) Gene expression profiles predictive of cold-induced sweetening in potato. Funct Integr Genomics 17:459–476. https://doi.org/10.1007/s10142-017-0549-9
O'Leary B, Plaxton WC (2020) Multifaceted functions of post-translational enzyme modifications in the control of plant glycolysis. Curr Opin Plant Biol 55:28–37. https://doi.org/10.1016/j.pbi.2020.01.009
Park KH, Yoon KH, Yin J, Le TT, Ahn HS, Yoon SH, Lee MW (2017) Antioxidative and anti-inflammatory activities of galloyl derivatives and antidiabetic activities of Acer ginnala. 2017:6945912. https://doi.org/10.1155/2017/6945912
Perkins TD, van den Berg AK (2009) Maple syrup-production, composition, chemistry, and sensory characteristics. Adv Food Nutr Res 56:101–143. https://doi.org/10.1016/s1043-4526(08)00604-9
Pfister B, Zeeman SC (2016) Formation of starch in plant cells. Cell Mol Life Sci 73:2781–2807. https://doi.org/10.1007/s00018-016-2250-x
Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150. https://doi.org/10.1105/tpc.104.022616
Rai A, Saito K, Yamazaki M (2017) Integrated omics analysis of specialized metabolism in medicinal plants. Plant J 90:764–787
Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67. https://doi.org/10.1146/annurev-arplant-050213-040251
Sakr S, Wang M, Dédaldéchamp F, Perez-Garcia MD, Ogé L, Hamama L, Atanassova R (2018) The sugar-signaling hub: overview of regulators and interaction with the hormonal and metabolic network. Int J Mol Sci 19. https://doi.org/10.3390/ijms19092506
Schmölzer K, Gutmann A, Diricks M, Desmet T, Nidetzky B (2016) Sucrose synthase: a unique glycosyltransferase for biocatalytic glycosylation process development. Biotechnol Adv 34:88–111. https://doi.org/10.1016/j.biotechadv.2015.11.003
Schneider T, Keller F (2009) Raffinose in chloroplasts is synthesized in the cytosol and transported across the chloroplast envelope. Plant Cell Physiol 50:2174–2182. https://doi.org/10.1093/pcp/pcp151
Sengupta S, Mukherjee S, Basak P, Majumder AL (2015) Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Front Plant Sci 6:656. https://doi.org/10.3389/fpls.2015.00656
Shin DH et al (2013) HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis. FEBS Lett 587:1543–1547. https://doi.org/10.1016/j.febslet.2013.03.037
Slewinski TL (2012) Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production. J Exp Bot 63:4647–4670. https://doi.org/10.1093/jxb/ers124
Smirnova J, Fernie AR, Spahn CMT, Steup M (2017) Photometric assay of maltose and maltose-forming enzyme activity by using 4-alpha-glucanotransferase (DPE2) from higher plants. Anal Biochem 532:72–82. https://doi.org/10.1016/j.ab.2017.05.026
Stein O, Granot D (2018) Plant fructokinases: evolutionary, developmental, and metabolic aspects in sink tissues. Front Plant Sci 9:339. https://doi.org/10.3389/fpls.2018.00339
Stettler M, Eicke S, Mettler T, Messerli G, Hörtensteiner S, Zeeman SC (2009) Blocking the metabolism of starch breakdown products in Arabidopsis leaves triggers chloroplast degradation. Mol Plant 2:1233–1246. https://doi.org/10.1093/mp/ssp093
Strand A, Zrenner R, Trevanion S, Stitt M, Gustafsson P, Gardeström P (2000) Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J 23:759–770. https://doi.org/10.1046/j.1365-313x.2000.00847.x
Sun J, Zhang J, Larue CT, Huber SC (2015) Decrease in leaf sucrose synthesis leads to increased leaf starch turnover and decreased RuBP regeneration-limited photosynthesis but not Rubisco-limited photosynthesis in Arabidopsis null mutants of SPSA1. Plant Cell Environ 34:592–604
Takasaki H et al (2015) SNAC-As, stress-responsive NAC transcription factors, mediate ABA-inducible leaf senescence. Plant J 84:1114–1123. https://doi.org/10.1111/tpj.13067
Tamoi M, Nagaoka M, Miyagawa Y, Shigeoka S (2006) Contribution of Fructose-1,6-bisphosphatase and sedoheptulose-1,7-bisphosphatase to the photosynthetic rate and carbon flow in the calvin cycle in transgenic plants. Plant Cell Physiol 47:380–390. https://doi.org/10.1093/pcp/pcj004
Teng S, Keurentjes J, Bentsink L, Koornneef M, Smeekens S (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol 139:1840–1852. https://doi.org/10.1104/pp.105.066688
Tomasella M, Petrussa E, Petruzzellis F, Nardini A, Casolo V (2019) The possible role of non-structural carbohydrates in the regulation of tree hydraulics. Int J Mol Sci 21. https://doi.org/10.3390/ijms21010144
Valluru R, Van den Ende W (2011) Myo-inositol and beyond--emerging networks under stress. Plant Sci 181:387–400. https://doi.org/10.1016/j.plantsci.2011.07.009
Wan H, Wu L, Yang Y, Zhou G, Ruan YL (2018) Evolution of sucrose metabolism: the dichotomy of invertases and beyond trends. Plant Sci 23:163–177. https://doi.org/10.1016/j.tplants.2017.11.001
Wang W, Hao Q, Tian F, Li Q, Wang W (2016) Cytokinin-regulated sucrose metabolism in stay-green wheat phenotype. PLoS One 11:e0161351. https://doi.org/10.1371/journal.pone.0161351
Wingler A (2018) Transitioning to the next phase: the role of sugar signaling throughout the plant life cycle. Plant Physiol 176:1075–1084. https://doi.org/10.1104/pp.17.01229
Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Biochem Mol Biol 35:253–289. https://doi.org/10.1080/10409230008984165
Xiao W, Sheen J, Jang JC (2000) The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol Biol 44:451–461. https://doi.org/10.1023/a:1026501430422
Yadav UP et al (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot 65:1051–1068. https://doi.org/10.1093/jxb/ert457
Yang J et al (2018) Increased activity of MdFRK2, a high-affinity fructokinase, leads to upregulation of sorbitol metabolism and downregulation of sucrose metabolism in apple leaves. 5:71. https://doi.org/10.1038/s41438-018-0099-x
Yang J, Wariss HM, Tao L, Zhang R, Yun Q, Hollingsworth P, Dao Z, Luo G, Guo H, Ma Y, Sun W (2019) De novo genome assembly of the endangered Acer yangbiense, a plant species with extremely small populations endemic to Yunnan Province, China. GigaScience 8. https://doi.org/10.1093/gigascience/giz085
Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401:13–28. https://doi.org/10.1042/bj20061393
Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234. https://doi.org/10.1146/annurev-arplant-042809-112301
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Anhui Provincial Natural Science Foundation (1908085QC113), supported Zhu Chen; Major Research and Development Projects in Anhui Province (202004a06020019), supported Jie Ren; Study on Breeding and Cultivation Techniques of Sugar Maple (AHLYCX-2019-16), supported Songling Fu; Ningbo Scientific and Technological Innovation 2025 Major Projects (2019B10012), supported Zhiyong Zhu; National Natural Science Foundation of China (31600543), supported Jie Ren.
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Conceptualization: Jie Ren and Songling Fu. Methodology: Xiaoyu Lu and Zhu Chen. Formal analysis and investigation: Xiaoyu Lu and Zhu Chen. Writing-original draft preparation: Xiaoyu Lu. Writing-review and editing: Xinyi Deng and Mingyuan Gu. Funding acquisition: Jie Ren, Zhu Chen, Songling Fu, and Zhiyong Zhu. Resources: Songling Fu and Zhiyong Zhu.
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Fig. S1
Flowchart of informatics analysis and processing of sequencing data (PNG 12117 kb)
Fig. S2
Statistical analysis of transcriptome. GO (a) and KEGG (b) annotation of red maple transcripts. c. Venn diagram of number of transcripts annotated by BLASTx against protein databases. Volcano plots of DEGs in RL vs. GL (d), YL vs. GL (e), and RL vs. YL (f) comparative groups (PNG 106488 kb)
Fig. S3
PCA score plots of GL-RL (a), GL-YL (b) and RL-YL (c) in positive mode. PLS-DA of GL-RL (d), GL-YL (e) and RL-YL (f) in negative mode (PNG 32442 kb)
Fig. S4
OPLS-DA score plots of GL-RL (a), GL-YL (b) and RL-YL (c) in positive mode. PLS-DA of GL-RL (d), GL-YL (e) and RL-YL (f) in negative mode (PNG 344215 kb)
Fig. S5
Expression level of ArZIP22 (PNG 546 kb)
Fig. S6
Expression level of ArMEX1 (PNG 544 kb)
Fig. S7
Content of ABA in red maple (PNG 366 kb)
Fig. S8
Content of total anthocyanins determined by HPLC in red maple (PNG 339 kb)
Table. S1
Gradient elution in HPLC analysis (XLSX 8 kb)
Table. S1
FPKM value of NSC-related genes in red maple (XLSX 28 kb)
Table. S2
Integral quantitative value of NSC-related metabolites in red maple (XLSX 9 kb)
Table. S3
Genes-metabolites Spearman correlation test in NSC pathways (XLSX 14 kb)
Table. S4
FPKM value of sugar-responsive transcription factors in red maple (XLSX 9 kb)
Table. S5
Integral quantitative value of hormone metabolites in red maple (XLSX 9 kb)
Table. S6
NSC-SRTF-Hormones Spearman correlation test in red maple (XLSX 13 kb)
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Lu, X., Chen, Z., Deng, X. et al. Transcriptomic and metabolomic analyses of non-structural carbohydrates in red maple leaves. Funct Integr Genomics 21, 265–281 (2021). https://doi.org/10.1007/s10142-021-00776-x
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DOI: https://doi.org/10.1007/s10142-021-00776-x