Integrated transcriptome and metabolism unravel critical roles of carbon metabolism and oxidoreductase in mushroom with Korshinsk peashrub substrates.
Lentinula edodes
Amino acids biosynthesis
Carbon metabolism
Korshinsk peashrub branches
Metabolism
Transcriptome
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
06 Aug 2024
06 Aug 2024
Historique:
received:
06
03
2024
accepted:
25
07
2024
medline:
7
8
2024
pubmed:
7
8
2024
entrez:
6
8
2024
Statut:
epublish
Résumé
Edible fungi cultivation serves as an efficient biological approach to transforming agroforestry byproducts, particularly Korshinsk peashrub (KP) branches into valuable mushroom (Lentinus edodes) products. Despite the widespread use of KP, the molecular mechanisms underlying its regulation of mushroom development remain largely unknown. In this study, we conducted a combined analysis of transcriptome and metabolism of mushroom fruiting bodies cultivated on KP substrates compared to those on apple wood sawdust (AWS) substrate. Our aim was to identify key metabolic pathways and genes that respond to the effects of KP substrates on mushrooms. The results revealed that KP induced at least a 1.5-fold increase in protein and fat content relative to AWS, with 15% increase in polysaccharide and total sugar content in mushroom fruiting bodies. There are 1196 differentially expressed genes (DEGs) between mushrooms treated with KP relative to AWS. Bioinformatic analysis show significant enrichments in amino acid metabolic process, oxidase activity, malic enzyme activity and carbon metabolism among the 698 up-regulated DEGs induced by KP against AWS. Additionally, pathways associated with organic acid transport and methane metabolism were significantly enriched among the 498 down-regulated DEGs. Metabolomic analysis identified 439 differentially abundant metabolites (DAMs) in mushrooms treated with KP compared to AWS. Consistent with the transcriptome data, KEGG analysis on metabolomic dataset suggested significant enrichments in carbon metabolism, alanine, aspartate and glutamate metabolism among the up-regulated DAMs by KP. In particular, some DAMs were enhanced by 1.5-fold, including D-glutamine, L-glutamate, glucose and pyruvate in mushroom samples treated with KP relative to AWS. Targeted metabolomic analysis confirmed the contents of DAMs related to glutamate metabolism and energy metabolism. In conclusion, our findings suggest that reprogrammed carbon metabolism and oxidoreductase pathways act critical roles in the enhanced response of mushroom to KP substrates.
Identifiants
pubmed: 39107700
doi: 10.1186/s12864-024-10666-8
pii: 10.1186/s12864-024-10666-8
doi:
Substances chimiques
Carbon
7440-44-0
Oxidoreductases
EC 1.-
Fungal Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
763Subventions
Organisme : Science and Technology Achievement Transformation Project of Qinghai Province
ID : 2023-NK-140
Organisme : Science and Technology Commissioner Project of Qinghai Province
ID : 2024-NK-P05
Informations de copyright
© 2024. The Author(s).
Références
Cheng X, Huang M, Si BC, Yu M, Shao M. The differences of water balance components of Caragana Korshinkii grown in homogeneous and layered soils in the desert–Loess Plateau transition zone. J arid Environ. 2013;11(98):10–9.
doi: 10.1016/j.jaridenv.2013.07.007
Huang H, Zhang Y. Growth suitability of Caragana Korshinkii in three water types afforested area in northern mountain of Lanzhou City. Sci Soil Water Conserv. 2013;2(11):72–6.
Mo B, Cai G, Lu J, Wang Z, Wang D, Qi J, Yang L, Dang H. Soil water use and balance characteristics in mature forest land profile of Caragana korshinskii in Semiarid Loess Area. Ying Yong Sheng Tai Xue bao. 2013;33(13):4011–20.
Guo Z, Shao M. Effect of artificial Caragana korshinskii forest on soil water in the semiarid area of Loess hilly region. Scientia Silvae Sinicae. 2010;46(12):1–7.
Manavalan T, Manavalan A, Heese K. Characterization of lignocellulolytic enzymes from white-rot fungi. Curr Microbiol. 2015;70:485–98.
pubmed: 25487116
doi: 10.1007/s00284-014-0743-0
Montoya S, Sánchez ÓJ, Levin L. Production of lignocellulolytic enzymes from three white-rot fungi by solid-state fermentation and mathematical modeling. Afr J Biotechnol. 2015;14(15):1304–17.
doi: 10.5897/AJB2014.14331
Chang ST. Overview of mushroom cultivation and utilization as functional foods. John Wiley Sons, Ltd. New York, pp. 2008. 281 – 234.
Sánchez C. Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv. 2009;27(2):185–94.
pubmed: 19100826
doi: 10.1016/j.biotechadv.2008.11.001
Sun F, Xing Z. Research on advantage and new use of Korshinsk Peashrub resources. Agri Sci Technol. 2014;15(4):709.
Zou Y, Du F, Zhang H, Hu Q. Evaluation of Korshinsk Peashrub (Caragana korshinskii Kom.) As a substrate for the cultivation of Pleurotus Eryngii. Waste Biomass Valor. 2019;10:2879–85.
doi: 10.1007/s12649-018-0301-2
Yang C, Ma L, Xiao D, Liu X, Jiang X, Lin Y. Comparative transcriptomics reveals unique pine wood decay strategies in the Sparassis latifolia. Sci Rep. 2022;12(1):19875.
pubmed: 36400936
pmcid: 9674834
doi: 10.1038/s41598-022-24171-z
Du F, Qu J, Hu Q, Yuan X, Yin G, Wang L, Zou Y. Maximizing the value of Korshinsk peashrub branches by the integration of Pleurotus tuoliensis cultivation and anaerobic digestion of spent mushroom substrate. Renew Energy. 2021;179:679–86.
doi: 10.1016/j.renene.2021.07.053
Zhang J, Ren A, Chen H, Zhao M, Shi L, Chen M, Wang H, Feng Z. Transcriptome analysis and its application in identifying genes associated with fruiting body development in basidiomycete Hypsizygus Marmoreus. PLoS ONE. 2015;10(4):e0123025.
pubmed: 25837428
pmcid: 4383556
doi: 10.1371/journal.pone.0123025
Lee HJ, Suh DH, Jung ES, Park HM, Jung G-Y, Do S-G, Lee CH. Metabolomics of Lonicera caerulea fruit during ripening and its relationship with color and antioxidant activity. Food Res Int. 2015;78:343–51.
pubmed: 28433302
doi: 10.1016/j.foodres.2015.09.017
Jang YK, Jung ES, Lee H-A, Choi D, Lee CH. Metabolomic characterization of hot pepper (Capsicum annuum CM334) during fruit development. J agri food chem. 2015;63(43):9452–60.
doi: 10.1021/acs.jafc.5b03873
Harada A, Yoneyama S, Doi S, Aoyama M. Changes in contents of free amino acids and soluble carbohydrates during fruit-body development of Hypsizygus marmoreus. Food chem. 2003;83(3):343–7.
doi: 10.1016/S0308-8146(03)00093-1
Gao W, Sun H-X, Xiao H, Cui G, Hillwig ML, Jackson A, Wang X, Shen Y, Zhao N, Zhang L. Combining metabolomics and transcriptomics to characterize tanshinone biosynthesis in Salvia miltiorrhiza. BMC Genom. 2014;15:1–14.
doi: 10.1186/1471-2164-15-73
Kim HY, Heo DY, Park HM, Singh D, Lee CH. Metabolomic and transcriptomic comparison of solid-state and submerged fermentation of Penicillium Expansum KACC 40815. PLoS ONE. 2016;11(2):e0149012.
pubmed: 26863302
pmcid: 4749308
doi: 10.1371/journal.pone.0149012
Huang H, Yao Q, Xia E, Gao L. Metabolomics and transcriptomics analyses reveal nitrogen influences on the accumulation of flavonoids and amino acids in young shoots of tea plant (Camellia sinensis L.) associated with tea flavor. J agri food chem. 2018;66(37):9828–38.
doi: 10.1021/acs.jafc.8b01995
Song H-Y, Kim D-H, Kim J-M. Comparative transcriptome analysis of dikaryotic mycelia and mature fruiting bodies in the edible mushroom Lentinula edodes. Sci rep. 2018;8(1):8983.
pubmed: 29895888
pmcid: 5997629
doi: 10.1038/s41598-018-27318-z
Wang Y, Zeng X, Liu W. De novo transcriptomic analysis during Lentinula edodes fruiting body growth. Gene. 2018;641:326–34.
pubmed: 29066302
doi: 10.1016/j.gene.2017.10.061
Yan D, Gao Q, Rong C, Liu Y, Song S, Yu Q, Zhou K, Liao Y. Comparative transcriptome analysis of abnormal cap and healthy fruiting bodies of the edible mushroom Lentinula edodes. Fungal Genet Biol. 2021;156:103614.
pubmed: 34400332
doi: 10.1016/j.fgb.2021.103614
Sambucetti M, Zuleta A. Resistant starch in dietary fiber values measured by the AOAC method in different cereals. Cereal Chem. 1996;73(6):759–61.
Thiex N. Evaluation of analytical methods for the determination of moisture, crude protein, crude fat, and crude fiber in distillers dried grains with solubles. J AOAC int. 2009;92(1):61–73.
pubmed: 19382563
doi: 10.1093/jaoac/92.1.61
Fu X, Zhou X, Deng B, Shang X, Fang S. Seasonal and genotypic variation of water-soluble polysaccharide content in leaves of Cyclocarya paliurus. South for. 2015;77(3):231–6.
doi: 10.2989/20702620.2015.1010698
McCready R, Guggolz J, Siliviera V, Owens H. Biochemical methods. Anal Chem. 1950;22:1156.
doi: 10.1021/ac60045a016
Jiang C, Bi Y, Mo J, Zhang R, Qu M, Feng S, Essemine J. Proteome and transcriptome reveal the involvement of heat shock proteins and antioxidant system in thermotolerance of Clematis florida. Sci Rep. 2020;10(1):8883.
pubmed: 32483281
pmcid: 7264250
doi: 10.1038/s41598-020-65699-2
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21.
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Chen F, Zheng G, Qu M, Wang Y, Lyu M-JA, Zhu X-G. Knocking out NEGATIVE REGULATOR OF PHOTOSYNTHESIS 1 increases rice leaf photosynthesis and biomass production in the field. J Exp Bot. 2021;72(5):1836–49.
pubmed: 33258954
doi: 10.1093/jxb/eraa566
Hamdani S, Wang H, Zheng G, Perveen S, Qu M, Khan N, Khan W, Jiang J, Li M, Liu X. Genome-wide association study identifies variation of glucosidase being linked to natural variation of the maximal quantum yield of photosystem II. Physiol Plant. 2019;166(1):105–19.
pubmed: 30834537
doi: 10.1111/ppl.12957
Qu M, Chen G, Bunce JA, Zhu X, Sicher RC. Systematic biology analysis on photosynthetic carbon metabolism of maize leaf following sudden heat shock under elevated CO2. Sci Rep. 2018;8(1):7849.
pubmed: 29777170
pmcid: 5959914
doi: 10.1038/s41598-018-26283-x
Li J, Essemine J, Shang C, Zhang H, Zhu X, Yu J, Chen G, Qu M, Sun D. Combined proteomics and metabolism analysis unravels prominent roles of antioxidant system in the prevention of alfalfa (Medicago sativa L.) against salt stress. Int J Mol Sci. 2020;21(3):909.
pubmed: 32019165
pmcid: 7037825
doi: 10.3390/ijms21030909
Yang Y, Li C, Nie J, Xing H, Li Z, Wang Z. Study on substrate formula including Korshinsk peashrub and corncobs for Pleurotus ostreatus cultivation. Edible Fungi. 2011;4:20–2.
Politowicz J, Lech K, Lipan L, Figiel A, Carbonell-Barrachina ÁA. Volatile composition and sensory profile of shiitake mushrooms as affected by drying method. J Sci Food Agri. 2018;98(4):1511–21.
doi: 10.1002/jsfa.8622
Zhu Z-Y, Liu X-C, Dong F-Y, Guo M-Z, Wang X-T, Wang Z, Zhang Y-M. Influence of fermentation conditions on polysaccharide production and the activities of enzymes involved in the polysaccharide synthesis of Cordyceps Militaris. Appl Microbiol Biotechnol. 2016;100:3909–21.
pubmed: 26685672
doi: 10.1007/s00253-015-7235-4
Tang Y-J, Zhong J-J. Exopolysaccharide biosynthesis and related enzyme activities of the medicinal fungus, Ganoderma Lucidum, grown on lactose in a bioreactor. Biotechnol lett. 2002;24:1023–6.
doi: 10.1023/A:1015677313598
Degn H, Wohlrab H. Measurement of steady-state values of respiration rate and oxidation levels of respiratory pigments at low oxygen tensions. A new technique. Biochim Biophys Acta. 1971;245(2):347–55.
pubmed: 4334350
doi: 10.1016/0005-2728(71)90153-8
Lin Y, Lin H, Chen Y, Wang H, Lin M, Ritenour MA, Lin Y. The role of ROS-induced change of respiratory metabolism in pulp breakdown development of longan fruit during storage. Food chem. 2020;305:125439.
pubmed: 31499287
doi: 10.1016/j.foodchem.2019.125439
Han M, Xu M, Su T, Wang S, Wu L, Feng J, Ding C. Transcriptome analysis reveals critical genes and pathways in carbon metabolism and ribosome biogenesis in poplar fertilized with glutamine. Int J Mol Sci. 2022;23(17):9998.
pubmed: 36077396
pmcid: 9456319
doi: 10.3390/ijms23179998
Lee YH, Foster J, Chen J, Voll LM, Weber AP, Tegeder M. AAP1 transports uncharged amino acids into roots of Arabidopsis. Plant J. 2007;50(2):305–19.
pubmed: 17419840
doi: 10.1111/j.1365-313X.2007.03045.x
Baier M, Dietz K-J. Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J exp bot. 2005;56(416):1449–62.
pubmed: 15863449
doi: 10.1093/jxb/eri161
Chen X, Yang B, Huang W, Wang T, Li Y, Zhong Z, Yang L, Li S, Tian J. Comparative proteomic analysis reveals elevated capacity for photosynthesis in polyphenol oxidase expression-silenced Clematis terniflora DC. Leaves. Int J Mol Sci. 2018;19(12):3897.
pubmed: 30563128
pmcid: 6321541
doi: 10.3390/ijms19123897
Zhao Z, Assmann SM. The glycolytic enzyme, phosphoglycerate mutase, has critical roles in stomatal movement, vegetative growth, and pollen production in Arabidopsis thaliana. J exp bot. 2011;62(14):5179–89.
pubmed: 21813794
pmcid: 3193020
doi: 10.1093/jxb/err223
Rosa-Téllez S, Anoman AD, Flores-Tornero M, Toujani W, Alseek S, Fernie AR, Nebauer SG, Muñoz-Bertomeu J, Segura J, Ros R. Phosphoglycerate kinases are co-regulated to adjust metabolism and to optimize growth. Plant Physiol. 2018;176(2):1182–98.
pubmed: 28951489
doi: 10.1104/pp.17.01227
Kim JY, Kim DY, Park Y-J, Jang M-J. Transcriptome analysis of the edible mushroom Lentinula edodes in response to blue light. PLoS ONE. 2020;15(3):e0230680.
pubmed: 32218597
pmcid: 7100940
doi: 10.1371/journal.pone.0230680