Impact of scion/rootstock reciprocal effects on metabolomics of fruit juice and phloem sap in grafted Citrus reticulata

Autoři: Zipora Tietel aff001;  Snehil Srivastava aff002;  Aaron Fait aff002;  Noemi Tel-Zur aff002;  Nir Carmi aff001;  Eran Raveh aff001
Působiště autorů: Agricultural Research Organization, Gilat Research Center, Gilat, Israel aff001;  French Associates Institutes for Agriculture and Biotechnology of Drylands, J. Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev (BGU), Sede-Boqer Campus, Sede Boker, Israel aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article



Rootstock has a significant impact on plant growth and development, including fruit maturation. However, the existence of mutual interaction between scion and rootstock is often neglected. To explore the origin of different fruit quality traits in citrus, we studied the effect of rootstock and the reciprocal interaction between scion and rootstock of nine combinations; three mandarin varieties grafted on three different rootstocks. We analyzed the metabolic profile of juice via gas and liquid chromatography-mass spectrometry (GC-MS and LC-MS, respectively). Additionally, we profiled phloem sap composition in the scion and the rootstock. Quality traits of fruit and their physio-chemical characteristics were also evaluated.


For all three cultivars, rootstock was found to affect fruit yield and biochemical fruit quality parameters (sugar and acidity) in interactions with the scions. In mandarin juice, eight of 48 compounds (two primary and six secondary) were related directly to the rootstock, and another seven (one primary and six secondary) were interactively affected by scion and rootstock. In scion and rootstock sap, six and 14 of 53 and 55 primary metabolites, respectively, were directly affected by the rootstock, while 42 and 33 were affected by rootstock interactively with scion, respectively.


In this work, we show for the first time a reciprocal effect between rootstock and scion. Based on our results, the scion and rootstock interaction might be organ, distance or time dependent.

Klíčová slova:

Citrus – Fruits – Gas chromatography-mass spectrometry – Metabolites – Organic acids – Phloem – Plant biochemistry – vitamin C


1. Hanana M, Hamrouni L, Hamed K, Abdelly C (2015) Influence of the rootstock/scion combination on the grapevines behavior under salt stress. Journal of Plant Biochemistry & Physiology 3.

2. Naor A, Klein I, Doron I (1995) Stem water potential and apple size. Journal of the American Society for Horticultural Science 120: 577–582.

3. Raveh E, Levy Y (2005) Analysis of xylem water as an indicator of current chloride uptake status in citrus trees. Scientia Horticulturae 103: 317–327.

4. Raveh E, Saban T, Zipi H, Beit‐Yannai E (2009) Influence of rootstock and scion on antioxidant capacity of juice from new pomelo and mandarin varieties. Journal of the Science of Food and Agriculture 89: 1825–1830.

5. Shackel KA, Ahmadi H, Biasi W, Buchner R, Goldhamer D, et al. (1997) Plant water status as an index of irrigation need in deciduous fruit trees. HortTechnology 7: 23–29.

6. Gonçalves B, Santos A, Silva A, Moutinho-Pereira J, Torres-Pereira J (2003) Effect of pruning and plant spacing on the growth of cherry rootstocks and their influence on stem water potential of sweet cherry trees. The Journal of Horticultural Science and Biotechnology 78: 667–672.

7. Neilsen G, Kappel F (1996) Bing'sweet cherry leaf nutrition is affected by rootstock. HortScience 31: 1169–1172.

8. Raveh E, Levy Y (2011) Effect of KNO3 fertilization and rootstock on grapefruit response to reclaimed, salinized water. Israel Journal of Plant Sciences 59: 177–186.

9. Schmitt E, Duhme F, Schmid P (1989) Water relations in sweet cherries (Prunus avium L.) on sour cherry rootstocks (Prunus cerasus L.) of different compatibility. Scientia Horticulturae 39: 189–200.

10. Benjamin G, Tietel Z, Porat R (2013) Effects of rootstock/scion combinations on the flavor of citrus fruit. Journal of Agricultural and Food Chemistry 61: 11286–11294. doi: 10.1021/jf402892p 24219601

11. Gonçalves B, Moutinho-Pereira J, Santos A, Silva AP, Bacelar E, et al. (2006) Scion–rootstock interaction affects the physiology and fruit quality of sweet cherry. Tree Physiology 26: 93–104. doi: 10.1093/treephys/26.1.93 16203719

12. Vazifeshenas M, Khayyat M, Jamalian S, Samadzadeh A (2009) Effects of different scion-rootstock combinations on vigor, tree size, yield and fruit quality of three Iranian cultivars of pomegranate. Fruits 64: 343–349.

13. FAO (2012) Food and Agricultural Organization of the United Nations.

14. Goldenberg L, Yaniv Y, Kaplunov T, Doron-Faigenboim A, Porat R, et al. (2014) Genetic diversity among mandarins in fruit-quality traits. Journal of Agricultural and Food Chemistry 62: 4938–4946. doi: 10.1021/jf5002414 24828369

15. Grosser JW, Medina-Urrutia V, Ananthakrishnan G, Serrano P (2004) Building a replacement sour orange rootstock: somatic hybridization of selected mandarin+ pummelo combinations. Journal of the American Society for Horticultural Science 129: 530–534.

16. Castle WS (2010) A career perspective on citrus rootstocks, their development, and commercialization. HortScience 45: 11–15.

17. Dinant S, Bonnemain J-L, Girousse C, Kehr J (2010) Phloem sap intricacy and interplay with aphid feeding. Comptes Rendus Biologies 333: 504–515. doi: 10.1016/j.crvi.2010.03.008 20541162

18. Komor E, Orlich G, Weig A, Köckenberger W (1996) Phloem loading—not metaphysical, only complex: towards a unified model of phloem loading. Journal of Experimental Botany: 1155–1164. doi: 10.1093/jxb/47.Special_Issue.1155 21245244

19. Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, et al. (2013) Source-to-sink transport of sugar and regulation by environmental factors. Frontiers in Plant Science 4: 272. doi: 10.3389/fpls.2013.00272 23898339

20. Jia W, Zhang J (2008) Stomatal movements and long-distance signaling in plants. Plant Signaling & Behavior 3: 772–777.

21. Keller M, Kummer M, Vasconcelos MC (2001) Reproductive growth of grapevines in response to nitrogen supply and rootstock. Australian Journal of Grape and Wine Research 7: 12–18.

22. Ruhl E (1989) Effect of potassium and nitrogen supply on the distribution of minerals and organic acids and the composition of grape juice of Sultana vines. Australian Journal of Experimental Agriculture 29: 133–137.

23. Wallis CM, Wallingford AK, Chen J (2013) Grapevine rootstock effects on scion sap phenolic levels, resistance to Xylella fastidiosa infection, and progression of Pierce's disease. Frontiers in Plant Science 4: 502. doi: 10.3389/fpls.2013.00502 24376452

24. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry–based metabolite profiling in plants. Nature Protocols 1: 387. doi: 10.1038/nprot.2006.59 17406261

25. Fiehn O, Kopka J, Dörmann P, Altmann T, Trethewey RN, et al. (2000) Metabolite profiling for plant functional genomics. Nature biotechnology 18: 1157. doi: 10.1038/81137 11062433

26. Hochberg U, Degu A, Toubiana D, Gendler T, Nikoloski Z, et al. (2013) Metabolite profiling and network analysis reveal coordinated changes in grapevine water stress response. BMC Plant Biology 13: 184. doi: 10.1186/1471-2229-13-184 24256338

27. Xia J, Sinelnikov IV, Han B, Wishart DS (2015) MetaboAnalyst 3.0—making metabolomics more meaningful. Nucleic Acids Research 43: W251–W257. doi: 10.1093/nar/gkv380 25897128

28. Weckwerth W, Wenzel K, Fiehn O (2004) Process for the integrated extraction, identification and quantification of metabolites, proteins and RNA to reveal their co‐regulation in biochemical networks. Proteomics 4: 78–83. doi: 10.1002/pmic.200200500 14730673

29. Doerfler H, Lyon D, Nägele T, Sun X, Fragner L, et al. (2013) Granger causality in integrated GC–MS and LC–MS metabolomics data reveals the interface of primary and secondary metabolism. Metabolomics 9: 564–574. doi: 10.1007/s11306-012-0470-0 23678342

30. Hijaz F, Killiny N (2014) Collection and chemical composition of phloem sap from Citrus sinensis L. Osbeck (sweet orange). PloS One 9: e101830. doi: 10.1371/journal.pone.0101830 25014027

31. Xia J, Psychogios N, Young N, Wishart DS (2009) MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Research 37: W652–W660. doi: 10.1093/nar/gkp356 19429898

32. Ramin A-A, Alirezanezhad A (2005) Effects of citrus rootstocks on fruit yield and quality of Ruby Red and Marsh grapefruit. Fruits 60: 311–317.

33. Davies FS, Albrigo LG (1994) Citrus. CAB International. Wallingford, UK: 30–33.

34. Zhao C, Wang F, Lian Y, Xiao H, Zheng J (2018) Biosynthesis of citrus flavonoids and their health effects. Critical Reviews in Food Science and Nutrition: 1–18.

35. Ghosh S, Chisti Y, Banerjee UC (2012) Production of shikimic acid. Biotechnology Advances 30: 1425–1431. doi: 10.1016/j.biotechadv.2012.03.001 22445787

36. Tohge T, Alseekh S, Fernie AR (2014) On the regulation and function of secondary metabolism during fruit development and ripening. Journal of Experimental Botany 65: 4599–4611. doi: 10.1093/jxb/ert443 24446507

37. Manners GD (2007) Citrus Limonoids: Analysis, Bioactivity, and Biomedical Prospects. Journal of Agricultural and Food Chemistry 55: 8285–8294. doi: 10.1021/jf071797h 17892257

38. Pál M, Tajti J, Szalai G, Peeva V, Végh B, et al. (2018) Interaction of polyamines, abscisic acid and proline under osmotic stress in the leaves of wheat plants. Scientific Reports 8: 12839. doi: 10.1038/s41598-018-31297-6 30150658

39. Hasegawa S, Berhow MA, Manners GD (2000) Citrus limonoid research: an overview. In: Hasegawa S, Berhow MA, Manners GD, editors. Citrus Limonoids: ACS Publications. pp. 1–8.

40. Rennie EA, Turgeon R (2009) A comprehensive picture of phloem loading strategies. Proceedings of the National Academy of Sciences 106: 14162–14167.

41. Batushansky A, Kirma M, Grillich N, Pham PA, Rentsch D, et al. (2015) The transporter GAT1 plays an important role in GABA-mediated carbon-nitrogen interactions in Arabidopsis. Frontiers in Plant Science 6: 785. doi: 10.3389/fpls.2015.00785 26483804

42. DeBolt S, Cook DR, Ford CM (2006) L-Tartaric acid synthesis from vitamin C in higher plants. Proceedings of the National Academy of Sciences 103: 5608–5613.

43. Gillaspy GE (2011) The cellular language of myo‐inositol signaling. New Phytologist 192: 823–839. doi: 10.1111/j.1469-8137.2011.03939.x 22050576

44. Gregory PJ, Atkinson CJ, Bengough AG, Else MA, Fernández-Fernández F, et al. (2013) Contributions of roots and rootstocks to sustainable, intensified crop production. Journal of Experimental Botany 64: 1209–1222. doi: 10.1093/jxb/ers385 23378378

45. Koepke T, Dhingra A (2013) Rootstock scion somatogenetic interactions in perennial composite plants. Plant Cell Reports 32: 1321–1337. doi: 10.1007/s00299-013-1471-9 23793453

46. Martínez-Ballesta MC, Alcaraz-López C, Muries B, Mota-Cadenas C, Carvajal M (2010) Physiological aspects of rootstock–scion interactions. Scientia Horticulturae 127: 112–118.

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