The roots of olive cultivars differing in tolerance to Verticillium dahliae show quantitative differences in phenolic and triterpenic profiles

References

• Al-Warhi T, Elmaidomy AH, Maher SA, Abu-Baih DH, Selim S, Albqmi M, et al. 2022. The wound-healing potential of Olea europaea L. cv. Arbequina leaves extract: an integrated in vitro, in silico, and in vivo investigation. Metabolites. 12:791. doi:10.3390/metabo12090791.
   PubMed Web of Science ®Google Scholar
• Ayele AG, Wheeler TA, Dever JK. 2020. Impacts of Verticillium wilt on photosynthesis rate, lint production, and fiber quality of greenhouse-grown cotton (Gossypium hirsutum). Plants. 9:857. doi:10.3390/plants9070857.
   Google Scholar
• Báidez AG, Gómez P, Del Río JA, Ortuño A. 2006. Antifungal capacity of major phenolic compounds of Olea europaea L. against Phytophthora megasperma Drechsler and Cylindrocarpon destructans (Zinssm.) Scholten. Physiol Mol Plant Pathol. 69:224–229. doi:10.1016/j.pmpp.2007.05.001.
   Web of Science ®Google Scholar
• Báidez AG, Gómez P, Del Río JA, Ortuño A. 2007. Dysfunctionality of the xylem in Olea europaea L. plants associated with the infection process by Verticillium dahliae Kleb. role of phenolic compounds in plant defense mechanism. J Agric Food Chem. 55:3373–3377. doi:10.1021/jf063166d.
   PubMed Web of Science ®Google Scholar
• Boskou D. 2006. Chemistry and technology. In: Dimitrios Boskou editor. Olive oil. 2nd ed. New York: AOCS Publishing; p. 288. doi:10.4324/9781003040217.
   Google Scholar
• Bubici G, Cirulli M. 2012. Control of Verticillium wilt of olive by resistant rootstocks. Plant Soil. 352:363–376. doi:10.1007/s11104-011-1002-9.
   Web of Science ®Google Scholar
• Cádiz-Gurrea MdlL, Pinto D, Delerue-Matos C, Rodrigues F. 2021. Olive fruit and leaf wastes as bioactive ingredients for cosmetics: a preliminary study. Antioxidants. 10:1–18. doi:10.3390/antiox10020245.
   Web of Science ®Google Scholar
• Cardoni M, Gómez-Lama Cabanás C, Valverde-Corredor A, Villar R, Mercado-Blanco J. 2022a. Unveiling differences in root defense mechanisms between tolerant and susceptible olive cultivars to Verticillium dahliae. Front Plant Sci. 13:1–19. doi:10.3389/fpls.2022.863055.
   Web of Science ®Google Scholar
• Cardoni M, Mercado-Blanco J, Villar R. 2021. Functional traits of olive varieties and their relationship with the tolerance level towards Verticillium wilt. Plants. 10: 1079. doi:10.3390/plants10061079.
   Google Scholar
• Cardoni M, Quero JL, Villar R, Mercado-Blanco J. 2022b. Physiological and structural responses of olive leaves related totolerance/susceptibility to Verticillium dahliae. Plants. 11:2302. doi:10.3390/plants11172302.
   Google Scholar
• Cayuela JA, Rada M, Rios JJ, Albi T, Guinda A. 2006. Changes in phenolic composition induced by Pseudomonas savastanoi pv. savastanoi infection in olive tree: presence of large amounts of verbascoside in nodules of tuberculosis disease. J Agric Food Chem. 54:5363–5368. doi:10.1021/jf060807w.
   PubMed Web of Science ®Google Scholar
• Chung PY, Navaratnam P, Chung LY. 2011. Synergistic antimicrobial activity between pentacyclic triterpenoids and antibiotics against Staphylococcus aureus strains. Ann Clin Microbiol Antimicrob. 10:1–6. doi:10.1186/1476-0711-10-25.
   PubMed Web of Science ®Google Scholar
• Del Río JA, Báidez AG, Botía JM, Ortuño A. 2003. Enhancement of phenolic compounds in olive plants (Olea europaea L.) and their influence on resistance against Phytophthora sp. Food Chem. 83:75–78. doi:10.1016/S0308-8146(03)00051-7.
   Web of Science ®Google Scholar
• De Mendiburu F, Simon R. 2015. Agricolae – Ten years of an open source statistical tool for experiments in breeding, agriculture and biology. PeerJ Pre Prints. 3:0–17. doi:10.7287/peerj.preprints.1404.
   Google Scholar
• Deng J, Wang H, Mu X, He X, Zhao F, Meng Q. 2021. Advances in research on the preparation and biological activity of maslinic acid, in Mini reviews in medicinal chemistry. Sharjah, UAE: Bentham Science Publishers, 79–89.
   Google Scholar
• Dzubak P, Hajduch M, Vydra D, Hustova A, Kvasnica M, Biedermann D, et al. 2006. Pharmacological activities of natural triterpenoids and their therapeutic implications. Nat Prod Rep. 23:394–411. doi:10.1039/b515312n.
   PubMed Web of Science ®Google Scholar
• Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM, et al. 2007. The role of plant defence proteins in fungal pathogenesis. Mol Plant Pathol. 8:677–700. doi:10.1111/j.1364-3703.2007.00419.x.
   PubMed Web of Science ®Google Scholar
• García-Ruiz GM, Trapero C, Del Río C, López-Escudero FJ. 2014. Evaluation of resistance of Spanish olive cultivars to Verticillium dahliae in inoculations conducted in greenhouse. Phytoparasitica. 42:205–212. doi:10.1007/s12600-013-0353-6.
   Web of Science ®Google Scholar
• Gharbi Y, Barkallah M, Bouazizi E, Gdoura R, Triki MA. 2017. Differential biochemical and physiological responses of two olive cultivars differing by their susceptibility to the hemibiotrophic pathogen Verticillium dahliae. Physiol Mol Plant Pathol. 97:30–39. doi:10.1016/j.pmpp.2016.12.001.
   Web of Science ®Google Scholar
• Gómez-Lama Cabanás C, Schilirò E, Valverde-Corredor A, Mercado-Blanco J. 2015. Systemic responses in a tolerant olive (Olea europaea L.) cultivar upon root colonization by the vascular pathogen Verticillium dahliae. Front Microbiol. 6:1–13. doi:10.3389/fmicb.2015.00928.
   PubMed Web of Science ®Google Scholar
• Guinda Á, Rada M, Delgado T, Gutiérrez-Adánez P, Castellano JM. 2010. Pentacyclic triterpenoids from olive fruit and leaf. J Agric Food Chem. 58:9685–9691. doi:10.1021/jf102039t.
   PubMed Web of Science ®Google Scholar
• Jäger S, Trojan H, Kopp T, Laszczyk MN, Scheffler A. 2009. Pentacyclic triterpene distribution in various plants, rich sources for a new group of multi-potent plant extracts. Molecules. 14:2016–2031. doi:10.3390/molecules14062016.
   PubMed Web of Science ®Google Scholar
• Jamkhande PG, Pathan SK, Wadher SJ. 2016. In silico PASS analysis and determination of antimycobacterial, antifungal, and antioxidant efficacies of maslinic acid in an extract rich in pentacyclic triterpenoids. Int J Mycobacteriology. 5:417–425. doi:10.1016/j.ijmyco.2016.06.020.
   PubMed Web of Science ®Google Scholar
• Johnson G, Schaal LA. 1952. Relation of chlorogenic acid to scab resistance in potatoes. Science. 80(115):627–629. doi:10.1126/science.115.2997.627.
   Google Scholar
• Juven B, Henis Y. 1970. Studies on the antimicrobial activity of ovotransferrin. J. Appl Bacteriol. 33:721–732.
   PubMedGoogle Scholar
• Kanakis P, Termentzi A, Michel T, Gikas E, Halabalaki M, Skaltsounis AL. 2013. From olive drupes to olive oil. An HPLC-orbitrap-based qualitative and quantitative exploration of olive key metabolites. Planta Med. 79:1576–1587. doi:10.1055/s-0033-1350823.
   PubMed Web of Science ®Google Scholar
• Karygianni L, Cecere M, Argyropoulou A, Hellwig E, Skaltsounis AL, Wittmer A, et al. 2019. Compounds from Olea europaea and Pistacia lentiscus inhibit oral microbial growth. BMC Complement Altern Med. 19:1–10. doi:10.1186/s12906-019-2461-4.
   PubMed Web of Science ®Google Scholar
• Kassambara A. 2016. Practical guide to principal component methods in R: PCA, M (CA), FAMD, MFA, HCPC, factoextra. Vol. 2. Sthda.
   Google Scholar
• Kolde R. 2018. Package pheatmap. R package 1.10.
   Google Scholar
• Kunej U, Mikulič-Petkovšek M, Radišek S, Štajner N. 2020. Changes in the phenolic compounds of hop (Humulus lupulus l.) induced by infection with Verticillium nonalfalfae, the causal agent of hop Verticillium wilt. Plants. 9:841. doi:10.3390/plants9070841.
   Google Scholar
• Kutchan T. 2001. Ecological arsenal and developmental dispatcher. The Paradigm of Secondary Metabolism. Plant Physiol. 125:58–60. doi:10.1104/pp.125.1.58
   PubMed Web of Science ®Google Scholar
• Lattanzio V, Cardinali A. 2006. Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. Phytochem Adv Res. 661:23–67.
   Google Scholar
• Leyva-Pérez MdlO, Jiménez-Ruiz J, Gómez-Lama Cabanás C, Valverde-Corredor A, Barroso JB, Luque F, et al. 2018. Tolerance of olive (Olea europaea) cv Frantoio to Verticillium dahliae relies on both basal and pathogen-induced differential transcriptomic responses. New Phytol. 217:671–686. doi:10.1111/nph.14833
   PubMed Web of Science ®Google Scholar
• Li Y, Wang J, Li L, Song W, Li M, Hua X, et al. 2022. Natural products of pentacyclic triterpenoids: from discovery to heterologous biosynthesis. Nat Prod Rep. doi:10.1039/d2np00063f.
   Web of Science ®Google Scholar
• Link K, Walker JC. 1933. The isolation of catechol from pigmented onion scales and its significance in relation to disease resistance in Onions. J Biol Chem. 100:2.
   Google Scholar
• Lins FSV, de Souza TA, Opretzka LCF, e Silva JPR, Pereira LCO, Abreu LS, et al. 2022. New pregnane glycosides from Mandevilla dardanoi and their anti-inflammatory activity. Molecules. 27:1–16. doi:10.3390/molecules27185992.
   Web of Science ®Google Scholar
• Liu S, Liu H, Zhang L, Ma C, Abd El-Aty AM. 2022. Edible pentacyclic triterpenes: a review of their sources, bioactivities, bioavailability, self-assembly behavior, and emerging applications as functional delivery vehicles. Crit Rev Food Sci Nutr. 1–17. doi:10.1080/10408398.2022.2153238.
   Web of Science ®Google Scholar
• López-Escudero FJ, Del Río C, Caballero JM, Blanco-López MA. 2004. Evaluation of olive cultivars for resistance to Verticillium dahliae. Eur J Plant Pathol. 110:79–85. doi:10.1023/B:EJPP.0000010150.08098.2d.
   Web of Science ®Google Scholar
• López-Escudero FJ, Mercado-Blanco J. 2011. Verticillium wilt of olive: a case study to implement an integrated strategy to control a soil-borne pathogen. Plant Soil. 344:1–50. doi:10.1007/s11104-010-0629-2.
   Web of Science ®Google Scholar
• Markakis EA, Tjamos SE, Antoniou PP, Roussos PA, Paplomatas EJ, Tjamos EC. 2010. Phenolic responses of resistant and susceptible olive cultivars induced by defoliating and non-defoliating Verticillium dahliae pathotypes. Plant Dis. 94:1156–1162. doi:10.1094/PDIS-94-9-1156.
   PubMed Web of Science ®Google Scholar
• Marsilio V, Lanza B. 1998. Characterisation of an oleuropein degrading strain of Lactobacillus plantarum. Combined effects of compounds present in olive fermenting brines (phenols, glucose and NaCl) on bacterial activity. J Sci Food Agric. 76:520–524. doi:10.1002/(SICI)1097-0010(199804)76:4 <; 520::AID-JSFA982 > 3.0.CO;2-I.
   Web of Science ®Google Scholar
• Mechri B, Tekaya M, Attia F, Hammami M, Chehab H. 2020. Drought stress improved the capacity of Rhizophagus irregularis for inducing the accumulation of oleuropein and mannitol in olive (Olea europaea) roots. Plant Physiol Biochem. 156:178–191. doi:10.1016/j.plaphy.2020.09.011.
   PubMed Web of Science ®Google Scholar
• Mechri B, Tekaya M, Hammami M, Chehab H. 2019. Root verbascoside and oleuropein are potential indicators of drought resistance in olive trees (Olea europaea L.). Plant Physiol Biochem. 141:407–414. doi:10.1016/j.plaphy.2019.06.024.
   PubMed Web of Science ®Google Scholar
• Michel T, Khlif I, Kanakis P, Termentzi A, Allouche N, Halabalaki M, et al. 2015. UHPLC-DAD-FLD and UHPLC-HRMS/MS based metabolic profiling and characterization of different Olea europaea organs of Koroneiki and Chetoui varieties. Phytochem Lett. 11:424–439. doi:10.1016/j.phytol.2014.12.020.
   Web of Science ®Google Scholar
• Montes-Osuna N, Mercado-Blanco J. 2020. Verticillium wilt of olive and its control: what did we learn during the last decade? Plants. 9:735. doi:10.3390/plants9060735.
   Google Scholar
• Olmo-García L, Bajoub A, Fernández-Gutiérrez A, Carrasco-Pancorbo A. 2016. Evaluating the potential of LC coupled to three alternative detection systems (ESI-IT, APCI-TOF and DAD) for the targeted determination of triterpenic acids and dialcohols in olive tissues. Talanta. 150:355–366. doi:10.1016/j.talanta.2015.12.042.
   PubMed Web of Science ®Google Scholar
• Olmo-García L, Carrasco-Pancorbo A. 2021. Chromatography-MS based metabolomics applied to the study of virgin olive oil bioactive compounds: characterization studies, agro-technological investigations and assessment of healthy properties. TrAC - Trends Anal Chem. 135:116153. doi:10.1016/j.trac.2020.116153.
   Web of Science ®Google Scholar
• Olmo-García L, Kessler N, Neuweger H, Wendt K, Olmo-Peinado JM, Fernández-Gutiérrez A, et al. 2018. Unravelling the distribution of secondary metabolites in Olea europaea L.: exhaustive characterization of eight olive-tree derived matrices by complementary platforms (LC-ESI/APCI-MS and GC-APCI-MS). Molecules. 23:1–16. doi:10.3390/molecules23102419.
   Web of Science ®Google Scholar
• Ortega-García F, Peragón J. 2009. The response of phenylalanine ammonia-lyase, polyphenol oxidase and phenols to cold stress in the olive tree (Olea europaea L. cv. Picual). J Sci Food Agric. 89:1565–1573. doi:10.1002/jsfa.3625.
   Web of Science ®Google Scholar
• Ortega-García F, Peragón J. 2010. HPLC analysis of oleuropein, hydroxytyrosol, and tyrosol in stems and roots of Olea europaea L. cv. picual during ripening. J Sci Food Agric. 90:2295–2300. doi:10.1002/jsfa.4085.
   PubMed Web of Science ®Google Scholar
• Petridis A, Therios I, Samouris G, Tananaki C. 2012. Salinity-induced changes in phenolic compounds in leaves and roots of four olive cultivars (Olea europaea L.) and their relationship to antioxidant activity. Environ Exp Bot. 79:37–43. doi:10.1016/j.envexpbot.2012.01.007.
   Web of Science ®Google Scholar
• Pichersky E, Gang DR. 2000. Genetics and biochemistry of secondary metabolites in plants: An evolutionary perspective. Trends Plant Sci. 5:439–445. doi:10.1016/S1360-1385(00)01741-6.
   PubMed Web of Science ®Google Scholar
• Ruiz-Barba JL, Garrido-Fernández A, Jiménez-Díaz R. 1991. Bactericidal action of oleuropein extracted from green olives against Lactobacillus plantarum. Lett Appl Microbiol. 12:65–68. doi:10.1111/j.1472-765X.1991.tb00505.x.
   Web of Science ®Google Scholar
• Ryan D, Robards K. 1998. Phenolic compounds in olives. Analyst. 123:31–44. doi:10.1039/a708920a.
   PubMed Web of Science ®Google Scholar
• Sabella E, Luvisi A, Aprile A, Negro C, Vergine M, Nicolì F, et al. 2018. Xylella fastidiosa induces differential expression of lignification related-genes and lignin accumulation in tolerant olive trees cv. Leccino. J Plant Physiol. 220:60–68. doi:10.1016/j.jplph.2017.10.007.
   PubMed Web of Science ®Google Scholar
• Seepe HA, Ramakadi TG, Lebepe CM, Amoo SO, Nxumalo W. 2021. Antifungal activity of isolated compound from the leaves of Combretum erythrophyllum (Burch.) Sond. and Withania somnifera (L.) Dunal against Fusarium pathogens. Molecules. 26:4732.
   Web of Science ®Google Scholar
• Serrano A, Rodríguez-Jurado D, López-Escudero FJ, Román B, Belaj A, De la Rosa R, Luque F, Ramírez-Tejero JA, León L. 2020. Verticillium wilt response of an olive core collection. Poster session presented at: The 7th international horticulture research conference; July 1–30; Northwest A&F University; China.
   Google Scholar
• Serrano A, Rodríguez-Jurado D, Ramírez-Tejero JA, Luque F, López-Escudero FJ, Belaj A, Román B, León L. 2023. Response to Verticillium dahliae infection in a genetically diverse set of olive cultivars. Sci Hortic. 316:112008. doi:10.1016/j.scienta.2023.112008
   Web of Science ®Google Scholar
• Serrano-García I, Olmo-García L, Polo-Megías D, Serrano A, León L, de la Rosa R, et al. 2022. Fruit phenolic and triterpenic composition of progenies of Olea europaea subsp. cuspidata, an interesting phytochemical source to be included in olive breeding programs. Plants. 11:1791. doi:10.3390/plants11141791.
   Google Scholar
• Skodra C, Michailidis M, Dasenaki M, Ganopoulos I, Thomaidis NS, Tanou G, et al. 2021. Unraveling salt-responsive tissue-specific metabolic pathways in olive tree. Physiol Plant. 173:1643–1656.
   PubMed Web of Science ®Google Scholar
• Sumner LW, Amberg A, Barrett D, Beale MH, Beger R, Daykin CA, et al. 2007. Proposed minimum reporting standards for chemical analysis: chemical analysis working group (CAWG) metabolomics standards initiative (MSI). Metabolomics. 3:211–221. doi:10.1007/s11306-007-0082-2.
   PubMed Web of Science ®Google Scholar
• Tassou CC, Nychas GJE. 1994. Inhibition of Staphylococcus aureus by olive phenolics in broth and in a model food system. J Food Prot. 57:120–124. doi:10.4315/0362-028x-57.2.120.
   PubMed Web of Science ®Google Scholar
• Termentzi A, Halabalaki M, Skaltsounis AL. 2015. From drupes to olive oil: an exploration of olive key metabolites. In: Olive and olive oil bioactive constituents. AOCS Press; p. 147–177. doi:10.1016/B978-1-63067-041-2.50012-4.
   Google Scholar
• Thatcher LF, Anderson JP, Singh KB. 2005. Plant defence responses: what have we learnt from Arabidopsis? Funct Plant Biol. 32:1–19. doi:10.1071/FP04135.
   PubMed Web of Science ®Google Scholar
• Torres-Vega J, Gómez-Alonso S, Pérez-Navarro J, Alarcón-Enos J, Pastene-Navarrete E. 2021. Polyphenolic compounds extracted and purified from Buddleja globosa hope (Buddlejaceae) leaves using natural deep eutectic solvents and centrifugal partition chromatography. Molecules. 26:2192. doi:10.3390/molecules26082192.
   PubMed Web of Science ®Google Scholar
• Trapero C, Alcántara E, Jiménez J, Amaro-Ventura MC, Romero J, Koopmann B, et al. 2018. Starch hydrolysis and vessel occlusion related to wilt symptoms in olive stems of susceptible cultivars infected by Verticillium dahliae. Front Plant Sci. 9:1–8. doi:10.3389/fpls.2018.00072.
   PubMed Web of Science ®Google Scholar
• Trapero C, Rallo L, López-Escudero FJ, Barranco D, Díez CM. 2015. Variability and selection of Verticillium wilt resistant genotypes in cultivated olive and in the Olea genus. Plant Pathol. 64:890–900. doi:10.1111/ppa.12330.
   Web of Science ®Google Scholar
• Trapero C, Serrano N, Arquero O, Del Río C, Trapero A, López-Escudero FJ. 2012. Field resistance to Verticillium wilt in selected olive cultivars grown in two naturally infested soils. Plant Dis. 97:668–674. doi:10.1094/PDIS-07-12-0654-RE.
   Web of Science ®Google Scholar
• Tsror LL. 2011. Review: epidemiology and control of Verticillium wilt on olive. Isr J Plant Sci. 59:59–69. doi:10.1560/IJPS.59.1.59.
   Web of Science ®Google Scholar
• Uccella N. 2000. Olive biophenols: biomolecular characterization, distribution and phytoalexin histochemical localization in the drupes. Trends Food Sci Technol. 11:9–10. doi: 10.1016/S0924-2244(01)00029-2
   Web of Science ®Google Scholar
• Valverde P, Barranco D, López-Escudero FJ, Díez CM, Trapero C. 2023. Efficiency of breeding olives for resistance to Verticillium wilt. Front Plant Sci. 14:566.
   Web of Science ®Google Scholar
• Valverde P, Trapero C, Arquero O, Serrano N, Barranco D, Muñoz Díez C, et al. 2021. Highly infested soils undermine the use of resistant olive rootstocks as a control method of Verticillium wilt. Plant Pathol. 70:144–153. doi:10.1111/ppa.13264.
   Web of Science ®Google Scholar
• Wen JH, Zhao HF, Hong JH, He Y, Guang ZZ, Chang JJ, et al. 2011. Benzoic acid allopyranosides and lignan glycosides from the twigs of Keteleeria evelyniana. Zeitschrift fur Naturforsch. Sect B J Chem Sci. 66:733–739. doi:10.1515/znb-2011-0715.
   Google Scholar
• Zarco-Tejada PJ, Poblete T, Camino C, González-Dugo V, Calderón R, Hornero A, et al. 2021. Divergent abiotic spectral pathways unravel pathogen stress signals across species. Nat Commun. 12:1–11. doi:10.1038/s41467-021-26335-3.
   PubMed Web of Science ®Google Scholar