Abstract
Key message
Our results from transcriptomics and metabolomics extend the understanding of the consequences of interspecific grafting to improve blueberry fruit quality.
Abstract
Grafting plays an important role in improving fruit quality and plant stress resistance. The effect of interspecific grafting on fruit quality in ‘O'Neal’ blueberry (Vaccinium corymbosum L.) was investigated with transcriptomics and non-targeted metabolomics. Fruits were collected from own-rooted ‘O'Neal’ (NO), ‘O'Neal’ grafted on ‘Tifblue’ (V. virgatum Ait.) (TO), and ‘Anna’ (V. corymbosum L.) (AO) bushes. The total soluble solids and anthocyanin concentrations, and solid:acid ratio in TO fruits were higher, while the vitamin C level was lower than AO and NO. The metabolic profiling showed that interspecific grafted blueberry had higher levels of sugars such as glucose, maltose, raffinose, myo-inositol, and galactinol, as well as glucose-6-phosphate and trehalose-6-phosphate as compared to intraspecific grafted blueberry. The fruits of TO also showed higher concentrations of secondary metabolites such as catechin, 5,7-dihydroxy-4'-methoxyisoflavone, glycyl tyrosine, and tocopherol, and lower concentrations of tryptophan and phenylalanine as compared to AO. Transcriptomic data showed that not only sugar metabolism-related enzymes such as trehalose-phosphate synthase and galactol synthase but also shikimate-derived metabolism-related enzymes such as flavonoid 3'-monooxygenase, anthocyanidin glucosyltransferase, isoflavone reductase, alcohol dehydrogenase, and aspartate aminotransferase were up-regulated in a comparison of TO/AO. Moreover, sugar signaling-related genes such as 6-phosphofructokinase, bHLHs, MYBs, 1-aminocyclopropane-1-carboxylate oxidase, 1-aminocyclopropane-1-carboxylate synthase, ABC transporter, and malate transporter were also up-regulated in a comparison of TO/AO. Finally, we proposed the hypothesis that sugar signals regulate the accumulation of sugars and organic acids and fruit ripening. These results will provide interesting insights into the interaction of scions on rootstocks and the promotion of blueberry genetic improvement.
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Availability of data
Sequencing data used in this study are available in the NCBI Sequence Read Archive database (accession numbers: PRJNA919406). Metabolome data are available in supplementary data (DLM20223305.tar). Supplementary Information are available at Trees Online.
References
Anders S, Huber W (2013) Differential expression of RNA-Seq data at the gene level—the DESeq package. EMBL. https://doi.org/10.1038/npre.2012.6837
Anders S, Pyl PT, Huber W (2015) HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169. https://doi.org/10.1093/bioinformatics/btu638
Balfagón D, Rambla JL, Granell A (2022) Grafting improves tolerance to combined drought and heat stresses by modifying metabolism in citrus scion. Environ Exp Bot 195:10479. https://doi.org/10.1007/s00299-021-02744-y
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bonner CA, Jensen RA, Gander JE, Keyhani NO (2004) A core catalytic domain of the TyrA protein family: arogenate dehydrogenase from Synechocystis. Biochem J 382:279–291. https://doi.org/10.1042/BJ20031809
Chen S, Li Y, Zhao Y, Li G, Zhang W, Wu Y, Huang L (2021) iTRAQ and RNA-Seq analyses revealed the effects of grafting on fruit development and ripening of oriental melon (Cucumis melo L. var. makuwa). Gene. 766:145142. https://doi.org/10.1016/j.gene.2020.145142
Corso M, Vannozzi A, Ziliotto F, Zouine M, Maza E, Nicolato T, Vitulo N, Meggio F, Valle G, Bouzayen M, Müller M, Munné-Bosch S, Lucchin M, Bonghi C (2016) Grapevine rootstocks differentially affect the rate of ripening and modulate auxin related genes in cabernet sauvignon berries. Front Plant Sci 7:69. https://doi.org/10.3389/fpls.2016.00069
Darnell RL, Casamali B, Williamson JG (2015) Nutrient assimilation in southern highbush blueberry and implications for the field. HortTechnology 25(4):460–463
Dong NQ, Lin HX (2021) Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions. J Integr Plant Biol 63:180–209. https://doi.org/10.1111/jipb.13054
Dong D, Shi YN, Mou ZM, Chen SY, Zhao DK (2022) Grafting: a potential method to reveal the differential accumulation mechanism of secondary metabolites. Hortic Res 9:uhac 050. https://doi.org/10.1093/hr/uhac050
Dubey AK, Sharma RM (2021) Long term performance of mango varieties on five polyembryonic rootstocks under subtropical conditions: effect on vigour, yield, fruit quality and nutrient acquisition. Sci Hortic 280:109944. https://doi.org/10.1016/j.scienta.2021.109944
Feng GT (2016) Extraction, purification, component identification and antioxidant of blueberry anthocyanins. Guizhou Univ. https://doi.org/10.1002/mnfr.200900094
Feng Y, Gu DZ, Wang ZY, Lu CY, Fan JF, Zhou J, Wang RX, Su XR (2022) Comprehensive evaluation and analysis of the salinity stress response mechanisms based on transcriptome and metabolome of Staphylococcus aureus. Arch Microbiol 204(1):28. https://doi.org/10.1007/s00203-021-02624-9
FontiForcada C, Gogorcena Y, Moreno MA (2013) Fruit sugar profile and antioxidants of peach and nectarine cultivars on almond × peach hybrid rootstocks. Sci Hortic 164:563–572. https://doi.org/10.1016/j.scienta.2013.10.020
FontiForcada C, Reig G, Giménez R, Mignard P, Mestre L, Moreno MÁ (2019) Sugars and organic acids profile and antioxidant compounds of nectarine fruits influenced by different rootstocks. Sci Hortic 248:145–153. https://doi.org/10.1016/j.scienta.2018.12.010
Ge Q, Chen L, Tang M, Zhang S, Liu LL, Gao L, Ma SS, Kong M, Yao Q, Feng F, Chen KP (2018) Analysis of mulberry leaf components in the treatment of diabetes using network pharmacology. Eur J Pharmacol 833:50–62. https://doi.org/10.1016/j.ejphar.2018.05.021
Habibi F, Liu T, Folta K, Sarkhosh A (2022) Physiological, biochemical, and molecular aspects of grafting in fruit trees. Hortic Res 9:uhac032. https://doi.org/10.1093/hr/uhac032
Han QQ, Song HF, Yang CC, Zhang S, Korpelainen H, Li CY (2022) Intergrated DNA methylation, transcriptome and physiological analyses reveal new insights into the superiority of poplars formed by interspecific grafting. Tree Physiol 42:1481–1500. https://doi.org/10.1093/treephys/tpac013
Heller CR, Nunez GH, Williamson JG (2023) Effects of Vaccinium arboreum rootstocks on yield and fruit quality of ‘Patrecia’ southern highbush blueberry grown with minimum soil amendment. J Am Pomol Soc 77(2):103–109
Hu D, Sun C, Ma Q, You CX, Cheng L, Hao YJ (2016) MdMYB1 regulates anthocyanin and malate accumulation by directly facilitating their transport into vacuoles in apples. Plant Physiol 170:1315–1330. https://doi.org/10.1104/pp.15.01333
Hu D, Yu JQ, Han PL, Xie XB, Sun CH, Zhang QY, Wang JH, Hao YJ (2019) The regulatory module MdPUB29-MdbHLH3 connects ethylene biosynthesis with fruit quality in apple. New Phytol 221:1966–1982. https://doi.org/10.1111/nph.15511
Hu Z, Wang F, Yu H (2022) Effects of scion-rootstock interaction on citrus fruit quality related to differentially expressed small RNAs. Sci Hortic 298:110974. https://doi.org/10.1111/ppl.12395
Jiang X, Yan LJ (2022) Preliminary study on the fruit characters of 27 blueberry cultivars in Linhai, Zhejiang Province. South China Fruits 51:144–149
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360. https://doi.org/10.1038/nmeth.3317
Kokubo Y, Nishizaka M, Ube N, Yabuta Y, Tebayashi SI, Ueno K, Taketa S, Ishihara AD (2017) Distribution of the tryptophan pathway-derived defensive secondary metabolites gramine and benzoxazinones in Poaceae. Biosci Biotech Bioch 81:431–440. https://doi.org/10.1080/09168451.2016.1256758
Legrand P, Dumas R, Seux M, Rippert P, Ravelli R, Ferrer JL, Matringe M (2006) Biochemical characterization and crystal structure of Synechocystis arogenate dehydrogenase provide insights into catalytic reaction. Structure 14:767–776. https://doi.org/10.1016/j.str.2006.01.006
Li WJ, Meng R, Liu Y, Chen S, Jiang J, Wang L, Zhao S, Wang Z, Fang W, Chen F, Guan Z (2022) Heterografted chrysanthemums enhance salt stress tolerance by integrating reactive oxygen species, soluble sugar, and proline. Hortic Res 9:uhac073. https://doi.org/10.1093/hr/uhac073
Li Z, Wei X, Tong X, Zhao J, Liu X, Wang H, Tang L, Shu Y, Li G, Wang Y, Ying J, Jiao G, Hu H, Hu P, Zhang J (2022b) The OsNAC23-Tre6P-SnRK1a feed-forward loop regulates sugar homeostasis and grain yield in rice. Mol Plant 15:706–722. https://doi.org/10.1016/j.molp.2022.01.016
Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Meitzel T, Raduchuk R, McAdam EL, Thormählen I, Feil R, Munz E, Hilo A, Geigenberger P, Ross JJ, Lunn JE, Borisjuk L (2021) Trehalose 6-phosphate promotes seed filling by activating auxin biosynthesis. New Phytol 229:1553–1565. https://doi.org/10.1111/nph.16956
Morandi B, Manfrini L, Lugli S, Tugnoli A, Boini A, Perulli GD, Bresilla K, Venturi M, Corelli Grappadelli L (2019) Sweet cherry water relations and fruit production efficiency are affected by rootstock vigor. J Plant Physiol 237:43–50. https://doi.org/10.1016/j.jplph.2019.04.007
Murch SJ, Krishnaraj S, Saxena PK (2000) Tryptophan is a precursor for melatonin and serotonin biosynthesis in in vitro regenerated St. John’s wort (Hypericum perforatum L. cv. Anthos) plants. Plant Cell Rep 19:698–704. https://doi.org/10.1007/s002990000206
O’Connor SE, Maresh JJ (2006) Chemistry and biology of monoterpene indole alkaloid biosynthesis. Nat Prod Rep 23:532–547. https://doi.org/10.1039/b512615k
Pertea M, Pertea GA, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33:290–295. https://doi.org/10.1038/nbt.3122
Roberts A, Trapnell C, Donaghey J, Roberts A, Trapnell C, Donaghey J, Rinn JL, Pachter L (2011) Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biol 12:R22. https://doi.org/10.1186/gb-2011-12-3-r22
Saini MK, Capalash N, Kaur C (2019) Comprehensive metabolic profiling to decipher the influence of rootstocks on fruit juice metabolome of Kinnow (C. nobilis × C. deliciosa). Sci Hortic. 257:108673. https://doi.org/10.1016/j.scienta.2019.108673
Scalzo J, Politi A, Pellegrini N, Mezzetti B, Battino M (2005) Plant genotype affects total antioxidant capacity and phenolic contents in fruit. Nutrition 21:207–213. https://doi.org/10.1016/j.nut.2004.03.025
Schenck CA, Maeda HA (2018) Tyrosine biosynthesis, metabolism, and catabolism in plant. Phytochemistry 149:82–102. https://doi.org/10.1016/j.phytochem.2018.02.003
Sherwin JE, Purves WK (1969) Tryptophan as an auxin precursor in cucumber seedlings. Plant Physiol 44:1303–1309. https://doi.org/10.1104/pp.44.9.1303
Stotz HU, Brown PD, Tokuhisa J (2015) Glucosinolate biosynthesis from amino acids. Amino Acids in Higher Plants, CAB International, Wallingford
Tietel Z, Srivastava S, Fait A, Tel-Zur N, Carmi N, Raveh E (2020) Impact of scion/ rootstock reciprocal effects on metabolomics of fruit juice and phloem sap in grafted Citrus reticulata. PLoS ONE 15:e0227192. https://doi.org/10.1371/journal.pone.0227192
Tomić J, Glišić I, Milošević N, Štampar F, Mikulič-Petkovšek M, Jakopič J (2022) Determination of fruit chemical contents of two plum cultivars grafted on four rootstocks. J Food Compos Anal 105:103944. https://doi.org/10.1016/j.jfca.2021.103944
Trapnell C, William BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. https://doi.org/10.1038/nbt.1621
Wang CK, Zhao YW, Sun CH (2022) Deciphering the impact of glucose signaling on fruit quality. Fruit Res 2:3. https://doi.org/10.48130/FruRes-2022-0003
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735. https://doi.org/10.1093/aob/mci083
Xu CX, Ma YP, Chen H (2014) Technique of grafting with Wufanshu (Vaccinium bracteatum Thunb.) and the effects on blueberry plant growth and development, fruit yield and quality. Sci Hortic 176:290–296. https://doi.org/10.1016/j.scienta.2014.07.021
Xu JJ, Fang X, Li CY, Yang L, Chen XY (2020) General and specialized tyrosine metabolism pathways in plants. Abiotech 1:97–105. https://doi.org/10.1007/s42994-019-00006-w
Yan QC, Jiang XM (2012) Determination of total acid and amino nitrogen in fruit juice by acidimeter continuous titration. Shandong J Anim Husb Vet 33(02):8–9
Zheng JP (2006) Determination of the vitamin C in fruits vegetables—discussion on UV spectrophotometry. Chin J Spectrosc Lab 23:731–735
Zhong H, Liu Z, Zhang F, Zhou X, Sun X, Li Y, Liu W, Xiao H, Wang N, Lu H, Pan M, Wu X, Zhou Y (2022) Metabolomic and transcriptomic analyses reveal the effects of self- and hetero-grafting on anthocyanin biosynthesis in grapevine. Hortic Res 9:103. https://doi.org/10.1093/hr/uhac103
Acknowledgements
We are grateful to Chun-Long Zhang for assistance with field-test establishment and plant material for the study.
Funding
This work was supported by the National Natural Science Foundation of China (32371927), Key Research and Development Program in Anhui Province(202204c06020029), and Anhui Provincial Financial Agricultural Germplasm Resources Protection and Utilization Project in 2022 (WNZH [2022] No.262 987).
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Study design, drafting the manuscript: BZ, P-PG, and J-XX. Data acquisition and analysis, manuscript preparation and editing: MS, YZ, FH, LY, and XG. Manuscript revision and final version approval: BZ, YH, and J-XX.
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Zhu, B., Guo, PP., Shen, M. et al. Transcriptome and metabolome analyses reveal improvement in blueberry fruit quality by interspecific grafting. Trees 38, 65–78 (2024). https://doi.org/10.1007/s00468-023-02466-6
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DOI: https://doi.org/10.1007/s00468-023-02466-6