Effect of different rootstocks on the leaf metabolite profile of ‘Sugar Belle’ mandarin hybrid

Nabil Killiny; Maria Filomena Valim; Shelley E Jones; Faraj Hijaz

doi:10.1080/15592324.2018.1445934

. 2018 Mar 20;13(3):e1445934. doi: 10.1080/15592324.2018.1445934

Effect of different rootstocks on the leaf metabolite profile of ‘Sugar Belle’ mandarin hybrid

Nabil Killiny ^1,^✉, Maria Filomena Valim ¹, Shelley E Jones ¹, Faraj Hijaz ¹

PMCID: PMC5927713 PMID: 29485923

ABSTRACT

Currently, citrus greening is threatening the citrus industry worldwide. So far, there is no effective cure for this destructive disease and management mainly depends on the control of Diaphorina citri vector using insecticides. Although the use of different rootstocks could increase citrus scions' tolerance to biotic and abiotic stresses, little work has been conducted to investigate the effect of rootstocks on citrus tolerance to citrus greening pathogen. In this study, we investigated the effect of rootstock on the metabolite profile of ‘Sugar Belle’ mandarin hybrid using gas-chromatography mass spectrometry (GC-MS). The principle component analysis showed that the metabolite profiles of the ‘Sugar Belle’ mandarin hybrid on the three selected rootstocks were different from each other. These results indicated that rootstocks could affect the primary and secondary metabolites of citrus scions, and consequently could affect scion tolerance to pathogens.

KEYWORDS: Citrus, GC-MS, metabolites, rootstock, scion, trimethylsilylation

Until the middle of the 18^th century, citrus trees were mainly grown from seedlings. However, the spread of the Phytophthora foot rot in sweet oranges lead to the first use of sour orange (Citrus aurantium L.) as a rootstock.¹ In the early part of the 20th century, the devastation of citrus tristeza virus to sweet orange grafted on sour orange rootstock enhanced the use of alternate rootstocks by the citrus industry.¹ The use of rootstock brings many advantages to citrus trees; (1) it decreases growth time and increases tree's strength, (2) enhances various horticultural traits such as yield, fruit quality and size, (3) increases citrus resistance to pests and pathogens such as Phytophthora rots, root weevils, burrowing nematodes, and tristeza virus, and (4) enhances trees tolerance to abiotic stresses such as salinity, drought, flooding, cold, and high soil pH.¹ Even though rootstocks brings many advantages to citrus scions, each rootstock has one or more disadvantages.¹ Consequently, there is no universal or ideal citrus rootstock. Since the initial use of the first rootstock (sour orange), several other varieties have also been used including rough lemon, ‘Volkamer’ lemon, ‘Carrizo’ citrange, Citrus macrophylla, ‘Swingle’ citrumelo, and ‘Rangpur’ lime.¹

Many studies have been conducted to explain how rootstocks affect scion growth and cropping, and several hypotheses have been proposed.² Early studies suggested that the rootstocks produced their own effects on the scion by influencing translocation of water and assimilates between the scion and rootstock as well as by promoting and inhibiting circulation of endogenous hormones.² Recently, Liu et al., (2015)³ investigated the mechanisms behind the effect of rootstock on fruit size, and found that large fruit size was accompanied by high auxin levels in fruits as the result of AUX1 upregulation, whereas low fruit size was accompanied by high abscisic acid levels. Liu et al. (2015)³ suggested that rootstocks could modulate auxin signaling by affecting the transcription of several auxin response factor genes. Santos et al. (2017)⁴ also showed that citrus rootstock affects the levels of flavonoids and phytohormones in citrus plants subjected to dehydration/rehydration. Martinez-Cuenca et al. (2017)⁵ showed that the citrus rootstock regulates iron uptake by roots, as well as in leaves by affecting ferric chelate reductase activity and the foliar level of active iron.

Nowadays, Huanglongbing (HLB) has invaded most citrus producing areas in the world. So far, HLB has destroyed millions of citrus trees and resulted in a sharp decline in citrus production worldwide. In North America and Asia, HLB disease is caused by Candidatus Liberibacter asiaticus (CLas). The CLas pathogen is transmitted by the Asian citrus psyllid, Diaphorina citri Kuwayama.⁶ Field observations and greenhouse-controlled studies showed that D. citri favors some host plants more than others.⁷ In the same manner, field observations and greenhouse-controlled studies showed that some citrus cultivars are relatively more tolerant to the CLas pathogen than others.⁷ If the tolerance of these cultivars is confirmed, they could be used to replace susceptible cultivars.

During the last few years, most of the citrus research was dedicated to HLB disease. However, rootstock were not proposed as one of the possible solutions for the control of this disease.⁸ Recently, field observations indicated that some cultivars were more tolerant to HLB when grafted onto specific rootstocks.⁸ In our previous study, we investigated the metabolic profiles of ‘Sugar Belle’® ‘LB8-9’ mandarin hybrid and four of its ancestors in order to understand why this cultivar is relatively tolerant to HLB.⁷ Our results showed that leaves of ‘Sugar Belle’ were high in several metabolites such as thymol, β-elemene, and (E)-β-caryophyllene, and inositols, which were possibly implicated in its tolerance.⁷ In the current study, the objective is to investigate the effect of different rootstocks on the metabolic profile of ‘Sugar Belle’ mandarin hybrid leaves (the scion). Any rootstock effects on leaf biochemistry will be reflected in the metabolites present and potentially enhance the tolerance to HLB.

One-year old ‘Sugar Belle’® ‘LB8-9’ mandarin hybrid trees grafted onto ‘Carrizo’ citrange (Citrus sinensis (L.) Osb. x Poncirus trifoliata (L.) Raf.), ‘Swingle’ citrumelo [Citrus paradisi MacFaden × P. trifoliata (L.) Raf.], and UF-15 rootstocks were obtained from a commercial nursery in Florida. Trees were maintained under greenhouse conditions (16 h:8 h L:D photoperiod, 27 °C, 65% RH). One month later, several leaves were collected from each plant from three different locations (top, middle, and bottom). Twelve plants were sampled from each rootstock. Leaf metabolites were analyzed using gas-chromatography mass-spectrometry (GC-MS) as described by Killiny et al. (2017).⁷ Briefly, three leaves from each plant were pooled together and ground to a fine powder in liquid nitrogen using a mortar and pestle. About 0.1 g of the leaf powder was mixed with 1 mL methanol:water (1:1, v/v) and was extracted overnight at 8 °C. Samples were centrifuged at 5 °C for 5 min at 5000 rpm to precipitate the leaf debris. A 180-mL aliquot of the leaf extract was transferred to a 200 mL silanized vial insert, ribitol (10 mL of 1 mg∙mL⁻¹) was added as the internal standard, vortexed, and the sample was dried under a stream of nitrogen gas. Dried residues were derivatized using the trimethylsilylation (TMS) and analyzed by GC-MS.

Forty-two metabolites were identified and quantified in the leaf sample extracts (Table 1). Table 1 shows the concentration of polar metabolites in ‘Sugar Belle’ leaves from the three different rootstocks. Nineteen of the detected metabolites were not affected by the rootstock and slight differences were observed in the rest of the metabolites (Table 1). ‘Sugar Belle’ grafted on UF-15 was the highest in _L-threonine, and malic acid (Table 1). Whereas, ‘Sugar Belle’ on ‘Swingle’ citrumelo was highest in lactic acid, benzoic acid, phosphoric acid, _L-serine, aspartic acid, _L-asparagine, quinic acid, glucose, galactose, gluconic acid, saccharic acid, galactaric acid, and ferulic acid (Table 1). Of particular interest were the levels of phenolic compounds found in two of the three rootstocks. Phenolic compounds have been shown to have antimicrobial effects in many plants^9–13 and on many pathogens including Ca. Liberibacter solanacearum.¹¹^,¹⁴ Caffeic acid levels were similar between the three rootstocks (Table 1). However, significant differences between the rootsocks in ferulic acid and quinic acid were found. Quinic acid was higher in ‘Sugar Belle’ on ‘Carrizo’ citrange or ‘Swingle' citrumelo, compared to UF-15 while ferulic acid was highest in ‘Sugar Belle’ on ‘Swingle’ (Table 1). These results suggest that ‘Swingle’ citrumelo would be the optimal rootstock for providing enhanced disease resistance (of the three rootstocks studied) based on their phenolic content which exist in phloem.

Table 1.

Concentrations (µg/g) of the major metabolites detected in leaves of Sugar Belle mandarin in three different rootstocks.¹

Compound	RT²	LRI ³	Sugar Belle (Carrizo)	Sugar Belle (Swingle)	Sugar Belle (UF-15)
Pyruvic acid	4.23	1087	1.64 ± 0.04^a	1.66 ± 0.16^a	1.52 ± 0.02^a
Lactic acid	4.46	1098	1.70 ± 0.13^b	2.09 ± 0.38^a	1.47 ± 0.02^b
L-alanine ³	4.94	1123	1.29 ± 0.16^a	1.50 ± 0.07^a	1.44 ± 0.15^a
N-methyl-L-proline	5.80	1171	1.66 ± 0.33^a	1.66 ± 0.30^a	1.30 ± 0.21^a
L-valine	6.32	1203	1.17 ± 0.03^b	1.26 ± 0.13^b	1.44 ± 0.11^a
Benzoic acid	7.03	1251	2.00 ± 0.12^b	2.34 ± 0.19^a	1.99 ± 0.11^b
Phosphoric acid	7.10	1255	6.48 ± 0.98^ab	7.54 ± 1.07^a	3.01 ± 0.98^b
Glycerol	7.12	1257	2.12 ± 0.13^a	2.22 ± 0.14^a	2.12 ± 0.13^a
Glycine	7.50	1284	1.16 ± 0.09^a	1.15 ± 0.07^a	1.17 ± 0.07^a
L-proline⁴	7.58	1290	6.60 ± 1.41^b	12.40 ± 1.55^a	11.40 ± 1.41^ab
Propanoic acid, -1-oxo	7.81	1306	1.94 ± 0.20^a	2.18 ± 0.37^a	1.92 ± 0.32^a
L-serine⁴	8.21	1336	2.34 ± 0.21^b	2.88 ± 0.35^a	2.69 ± 0.42^ab
L-threonine⁴	8.52	1360	8.96 ± 1.46^b	14.35 ± 4.68^ab	14.78 ± 4.10^b
Malic acid⁴	10.05	1483	12.02 ± 1.96^b	19.26 ± 6.29^ab	19.84 ± 5.51^a
Aspartic acid⁴	10.41	1514	2.07 ± 0.03^b	2.26 ± 0.21^a	2.05 ± 0.03^b
γ-aminobutyric acid⁴	10.51	1522	2.63 ± 1.44^a	3.94 ± 1.52^a	3.27 ± 0.71^a
Arabinofuranose	10.61	1531	0.13 ± 0.01^a	0.13 ± 0.01^a	0.12 ± 0.01^a
Threonic acid	10.85	1552	14.06 ± 2.16^a	16.84 ± 4.99^a	12.55 ± 0.91^a
Xylose⁴	11.94; 12.02	1647; 1654	2.59 ± 0.68^a	2.56 ± 0.59^a	1.80 ± 0.34^a
Asparagine	12.40	1688	2.20 ± 0.07^ab	2.26 ± 0.07^a	2.16 ± 0.01^b
Unknown sugar	13.07	1749	2.87 ± 0.79^a	1.32 ± 0.11^b	3.01 ± 0.37^a
Ribonic acid	13.13	1755	5.65 ± 1.42^a	6.61 ± 1.40^a	5.21 ± 0.99^a
Citric acid⁴	13.59	1796	61.71 ± 18.28^a	90.99 ± 38.71^a	83.59 ± 19.08^a
Quinic acid	13.96	1831	224.42 ± 118.34^ab	298.31 ± 40.22^a	108.05 ± 63.23^b
Fructose	14.29; 14.38	1862; 1870	7.74 ± 1.95^a	7.50 ± 1.74^a	9.03 ± 2.21^a
Mannose⁴	14.47; 14.68	1878; 1898	2.36 ± 0.55^a	2.59 ± 0.88^a	2.25 ± 0.26^a
Glucose⁴	14.55; 14.71	1886; 1901	62.86 ± 34.70^ab	74.62 ± 30.50^a	20.72 ± 16.50^b
Galactose⁴	14.84	1913	14.87 ± 9.31^ab	18.98 ± 7.31^a	5.69 ± 4.58^b
Galactitol	14.65	1895	0.75 ± 0.02^a	0.76 ± 0.06^a	0.76 ± 0.01^a
chiro-Inositol	15.12	1939	3.80 ± 1.51^a	4.87 ± 1.01^a	3.32 ± 1.12^a
Gluconic acid	15.50	1975	0.92 ± 0.05^b	1.10 ± 0.17^a	0.83 ± 0.03^b
Saccharic acid⁴	15.67	1991	1.97 ± 0.48^b	5.27 ± 2.93^a	1.71 ± 0.44^b
scyllo-Inositol	15.82	2005	1.99 ± 0.26^a	1.90 ± 0.12^a	1.83 ± 0.16^a
Galactaric acid	15.95	2017	0.93 ± 0.10^b	1.16 ± 0.17^a	0.86 ± 0.02^b
Palmitic acid	16.10	2031	0.88 ± 0.07^a	0.82 ± 0.02^a	0.88 ± 0.05^a
myo-Inositol⁴	16.20	2041	2.82 ± 0.43^a	3.18 ± 0.74^a	2.53 ± 0.15^a
Ferulic acid	16.37	2056	5.60 ± 1.07^b	7.23 ± 0.67^a	3.83 ± 0.41^c
Arabino-hexaric acid	16.39	2058	6.94 ± 1.40^a	6.61 ± 1.17^a	6.95 ± 1.00^a
Caffeic acid	16.78	2095	3.16 ± 0.53^a	3.31 ± 0.14^a	2.83 ± 0.45^a
Stearic acid	18.33	2243	0.88 ± 0.04^a	0.87 ± 0.06^a	0.84 ± 0.04^a
Glycerol-glyceride	18.97	2304	1.14 ± 0.13^a	1.30 ± 0.14^a	1.13 ± 0.14^a
Sucrose⁴	22.0	2597	45.22 ± 15.59^a	51.44 ± 9.75^a	19.31 ± 5.33^b

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Values represent means ± SD (n = 12). Different superscript letters on values in the same row indicate significant difference using Tukey's honestly significant difference test (HSD; p > 0.05), while means with the same superscript letters are not significantly different from each other.

RT: Retention time

LRI: Linear retention indices, generated by injecting n-alkanes (C₈-C₂₄) on ZB-5ms column under the same chromatographic conditions as samples.

⁴

Concentrations in µg/g calculated based on calibration curves made from authentic standards.

Our observations are in agreement with the previous studies, which showed that rootstocks affect citrus tree metabolites. For example, early studies showed that the inorganic composition of the citrus trees and fruits were highly affected by the rootstock.¹⁵ Scora et al. (1981)¹⁶ also showed that rootstock could affect some of the components of citrus leaf oil by interacting with the citrus scion. Scora et al. (1981)¹⁶ suggested that the rootstocks should be identified when the composition of essential oils of citrus leaf is reported. In a recent study, Santos et al. (2017)⁴ also showed that scion/rootstock combinations can affect phytohormones, flavonoids, and tree's growth under different soil water system. On the other hand, Verzera et al. (2003)¹⁷ found that the compositions of bergamot essential oils obtained from plants grafted on six different rootstocks were similar. The previous results together suggested that rootstock effect depends on the scion/rootstock combinations.

Rootstock choices which enhance the strength and disease resistance of HLB-susceptible varieties could help the citrus industry recover from citrus greening disease as it did with Phytophthora foot rot and citrus tristeza virus. However, little work has been done to investigate the effect of rootstock on scion tolerance to citrus greening. In a field study, Albrecht et al. (2012)¹⁸ found that citrus rootstocks did not decrease HLB incidence and damage, however scion tolerance to HLB was improved in trees grafted onto trifoliate hybrid rootstock. In another field study, Boava et al. (2015)¹⁹ suggested that citrandarin rootstock (Citrus reticulata var. austera x P. trifoliata) could improve citrus scions’ tolerance to HLB, however the authors suggested further work be done to confirm this result. Field observations in Florida also suggested that HLB incidence is less common in some citrus cultivars when grown on specific rootstocks.⁸ Since most of these observations are tentative, these rootstocks need further testing under controlled conditions to confirm their tolerance to HLB.

Funding Statement

This work was supported by the National Institute of Food and Agriculture (2016–70016–24824) This work was funded by grant #2016–70016–24824 from USDA-NIFA for NK.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

Acknowledgment

We thank our laboratory members for the helpful discussions and technical assistance.

References

1.Castle WS. A Career perspective on citrus rootstocks, their development, and commercialization. Hort Sci. 2010;45(1):11–15. [Google Scholar]
2.Webster AD. 1995. Rootstock and interstock effects on deciduous fruit tree vigour, precocity, and yield productivity. N. Z. J. Crop Hortic Sci. 1995;23(4):373–82. doi: 10.1080/01140671.1995.9513913. [DOI] [Google Scholar]
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4.Santos ICD, Almeida AF, Pirovani CP, Costa MGC, Silva MFDGFD, Bellete BS, Freschi L, Soares Filho W, Coelho Filho MA, Gesteira ADS. Differential accumulation of flavonoids and phytohormones resulting from the canopy/rootstock interaction of citrus plants subjected to dehydration/rehydration. Plant Physiol Biochem. 2017;119:147–58. doi: 10.1016/j.plaphy.2017.08.019. [DOI] [PubMed] [Google Scholar]
5.Martinez-Cuenca M, Primo-Capella A, Quiñones A, Bermejo A, Forner-Giner MA. Rootstock influence on iron uptake responses in Citrus leaves and their regulation under the Fe paradox effect. PeerJ. 2017;5:e3553. doi: 10.7717/peerj.3553. [DOI] [PMC free article] [PubMed] [Google Scholar]
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8.Castle WS, Bowman KD, Grosser JW, Futch SH, Graham JH. 2016. Florida citrus rootstock selection guide, 3rd Edition http://edis.ifas.ufl.edu/pdffiles/HS/HS126000.pdf.
9.Ishihara M, Hasegawa M, Taira T, Toyama S. Isolation and antimicrobial activity of feruloyl oligosaccharide ester from pineapple stem residues. J Jpn Soc Food Sci Technol. 2000;47:23–29. doi: 10.3136/nskkk.47.23. [DOI] [Google Scholar]
10.Proestos C, Sereli D, Komaitis M. Determination of phenolic compounds in aromatic plants by RP-HPLC and GC-MS. Food Chem. 2006;95:44–52. doi: 10.1016/j.foodchem.2004.12.016. [DOI] [Google Scholar]
11.Plyuta V, Zaitseva J, Lobakova E, Zagoskina N, Kuznetsov A, Khmel I. Effect of plant phenolic compounds on biofilm formation by Pseudomonas aeruginosa. Apmis. 2013;121:1073–81. doi: 10.1111/apm.12083. [DOI] [PubMed] [Google Scholar]
12.Wallis CM, Wallingford AK, Chen JC. Grapevine rootstock effects on scion sap phenolic levels, resistance to Xylella fastidiosa infection, and progression of Pierce's disease. Front Plant Sci. 2013;4. doi: 10.3389/fpls.2013.00502. [DOI] [PMC free article] [PubMed] [Google Scholar]
13.Mhlongo MI, Piater LA, Steenkamp PA, Madala NE, Dubery IA. Priming agents of plant defence stimulate the accumulation of mono- and di-acylated quinic acids in cultured tobacco cells. Physiol Mol Plant Path. 2014;88:61–66. doi: 10.1016/j.pmpp.2014.09.002. [DOI] [Google Scholar]
14.Wallis CM, Rashed A, Chen J, Paetzold L, Workneh F, Rush CM. Effects of Potato-Psyllid-Vectored ‘Candidatus Liberibacter solanacearum’ Infection on potato leaf and stem physiology. Phytopathology. 2015;105:189–98. doi: 10.1094/PHYTO-04-14-0113-R. [DOI] [PubMed] [Google Scholar]
15.Haas ARC. Effect of the rootstock on the composition of citrus trees and fruit. Plant Physiol. 1948;23(3):309–30. doi: 10.1104/pp.23.3.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
16.Scora RW, Kumamoto J, Clerx WA. Variations of leaf oil composition of citrus budded on different rootstocks. Syst Bot. 1981;6:31–7. doi: 10.2307/2418633. [DOI] [Google Scholar]
17.Verzera A, Trozzi A, Gazea F, Cicciarello G, Cotroneo A. Effects of rootstock on the composition of bergamot (Citrus bergamia Risso et Poiteau) essential oil. J Agric Food Chem. 2003;51:206–10. doi: 10.1021/jf0206872. [DOI] [PubMed] [Google Scholar]
18.Albrecht U, McCollum G, Bowman KD. Influence of rootstock variety on huanglongbing disease development in field-grown sweet orange (Citrus sinensis [L.] Osbeck) trees. Sci Hortic. 2012;138:210–20. doi: 10.1016/j.scienta.2012.02.027. [DOI] [Google Scholar]
19.Boava LP, Sagawa CH, Cristofani-Yaly M, Machado MA. Incidence of ‘Candidatus Liberibacter asiaticus’-infected plants among citrandarins as rootstock and scion under field conditions. Phytopathol. 2015;105(4):518–24. doi: 10.1094/PHYTO-08-14-0211-R. [DOI] [PubMed] [Google Scholar]

[cit0001] 1.Castle WS. A Career perspective on citrus rootstocks, their development, and commercialization. Hort Sci. 2010;45(1):11–15. [Google Scholar]

[cit0002] 2.Webster AD. 1995. Rootstock and interstock effects on deciduous fruit tree vigour, precocity, and yield productivity. N. Z. J. Crop Hortic Sci. 1995;23(4):373–82. doi: 10.1080/01140671.1995.9513913. [DOI] [Google Scholar]

[cit0003] 3.Liu X, Li J, Huang M, Chen J. Mechanisms for the influence of citrus rootstocks on fruit size. J Agric Food Chem. 2015;63:2618–27. doi: 10.1021/jf505843n. [DOI] [PubMed] [Google Scholar]

[cit0004] 4.Santos ICD, Almeida AF, Pirovani CP, Costa MGC, Silva MFDGFD, Bellete BS, Freschi L, Soares Filho W, Coelho Filho MA, Gesteira ADS. Differential accumulation of flavonoids and phytohormones resulting from the canopy/rootstock interaction of citrus plants subjected to dehydration/rehydration. Plant Physiol Biochem. 2017;119:147–58. doi: 10.1016/j.plaphy.2017.08.019. [DOI] [PubMed] [Google Scholar]

[cit0005] 5.Martinez-Cuenca M, Primo-Capella A, Quiñones A, Bermejo A, Forner-Giner MA. Rootstock influence on iron uptake responses in Citrus leaves and their regulation under the Fe paradox effect. PeerJ. 2017;5:e3553. doi: 10.7717/peerj.3553. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0006] 6.Tatineni S, Sagaram US, Gowda S, Robertson CJ, Dawson WO, Iwanami T, Wang N. In planta distribution of “Candidatus Liberibacter asiaticus” as revealed by polymerase chain reaction (PCR) and real-time P5CR. Phytopathol. 2008;98:592–9. doi: 10.1094/PHYTO-98-5-0592. [DOI] [PubMed] [Google Scholar]

[cit0007] 7.Killiny N, Valim MF, Jones SE, Omar AA, Hijaz F, Gmitter Jr FG, Grosser JW. Metabolically speaking: possible reasons behind the tolerance of ‘Sugar Belle’ mandarin hybrid to huanglongbing. Plant Physiol Biochem. 2017;116:36–47. doi: 10.1016/j.plaphy.2017.05.001. [DOI] [PubMed] [Google Scholar]

[cit0008] 8.Castle WS, Bowman KD, Grosser JW, Futch SH, Graham JH. 2016. Florida citrus rootstock selection guide, 3rd Edition http://edis.ifas.ufl.edu/pdffiles/HS/HS126000.pdf.

[cit0009] 9.Ishihara M, Hasegawa M, Taira T, Toyama S. Isolation and antimicrobial activity of feruloyl oligosaccharide ester from pineapple stem residues. J Jpn Soc Food Sci Technol. 2000;47:23–29. doi: 10.3136/nskkk.47.23. [DOI] [Google Scholar]

[cit0010] 10.Proestos C, Sereli D, Komaitis M. Determination of phenolic compounds in aromatic plants by RP-HPLC and GC-MS. Food Chem. 2006;95:44–52. doi: 10.1016/j.foodchem.2004.12.016. [DOI] [Google Scholar]

[cit0011] 11.Plyuta V, Zaitseva J, Lobakova E, Zagoskina N, Kuznetsov A, Khmel I. Effect of plant phenolic compounds on biofilm formation by Pseudomonas aeruginosa. Apmis. 2013;121:1073–81. doi: 10.1111/apm.12083. [DOI] [PubMed] [Google Scholar]

[cit0012] 12.Wallis CM, Wallingford AK, Chen JC. Grapevine rootstock effects on scion sap phenolic levels, resistance to Xylella fastidiosa infection, and progression of Pierce's disease. Front Plant Sci. 2013;4. doi: 10.3389/fpls.2013.00502. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0013] 13.Mhlongo MI, Piater LA, Steenkamp PA, Madala NE, Dubery IA. Priming agents of plant defence stimulate the accumulation of mono- and di-acylated quinic acids in cultured tobacco cells. Physiol Mol Plant Path. 2014;88:61–66. doi: 10.1016/j.pmpp.2014.09.002. [DOI] [Google Scholar]

[cit0014] 14.Wallis CM, Rashed A, Chen J, Paetzold L, Workneh F, Rush CM. Effects of Potato-Psyllid-Vectored ‘Candidatus Liberibacter solanacearum’ Infection on potato leaf and stem physiology. Phytopathology. 2015;105:189–98. doi: 10.1094/PHYTO-04-14-0113-R. [DOI] [PubMed] [Google Scholar]

[cit0015] 15.Haas ARC. Effect of the rootstock on the composition of citrus trees and fruit. Plant Physiol. 1948;23(3):309–30. doi: 10.1104/pp.23.3.309. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0016] 16.Scora RW, Kumamoto J, Clerx WA. Variations of leaf oil composition of citrus budded on different rootstocks. Syst Bot. 1981;6:31–7. doi: 10.2307/2418633. [DOI] [Google Scholar]

[cit0017] 17.Verzera A, Trozzi A, Gazea F, Cicciarello G, Cotroneo A. Effects of rootstock on the composition of bergamot (Citrus bergamia Risso et Poiteau) essential oil. J Agric Food Chem. 2003;51:206–10. doi: 10.1021/jf0206872. [DOI] [PubMed] [Google Scholar]

[cit0018] 18.Albrecht U, McCollum G, Bowman KD. Influence of rootstock variety on huanglongbing disease development in field-grown sweet orange (Citrus sinensis [L.] Osbeck) trees. Sci Hortic. 2012;138:210–20. doi: 10.1016/j.scienta.2012.02.027. [DOI] [Google Scholar]

[cit0019] 19.Boava LP, Sagawa CH, Cristofani-Yaly M, Machado MA. Incidence of ‘Candidatus Liberibacter asiaticus’-infected plants among citrandarins as rootstock and scion under field conditions. Phytopathol. 2015;105(4):518–24. doi: 10.1094/PHYTO-08-14-0211-R. [DOI] [PubMed] [Google Scholar]

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Effect of different rootstocks on the leaf metabolite profile of ‘Sugar Belle’ mandarin hybrid

Nabil Killiny

Maria Filomena Valim

Shelley E Jones

Faraj Hijaz

ABSTRACT

Table 1.

Funding Statement

Disclosure of potential conflicts of interest

Acknowledgment

References

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Effect of different rootstocks on the leaf metabolite profile of ‘Sugar Belle’ mandarin hybrid

Nabil Killiny

Maria Filomena Valim

Shelley E Jones

Faraj Hijaz

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