Identification and characterization of lettuce cultivars with high inhibitory activity against the human pathogen Escherichia coli O157:H7: Toward a plant-intrinsic hurdle approach to microbial safety

Foodborne illness linked to fruit and vegetables poses a major challenge to public health and horticulture production. Processed lettuce has been implicated in recurrent outbreaks of pathogenic Shiga toxin-producing Escherichia coli (STEC) infection. We hypothesized that plant defenses elicited by m...

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Veröffentlicht in:Postharvest biology and technology 2024-05, Vol.211, p.112816, Article 112816
Hauptverfasser: George, Andree S., Simko, Ivan, Brandl, Maria T.
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description Foodborne illness linked to fruit and vegetables poses a major challenge to public health and horticulture production. Processed lettuce has been implicated in recurrent outbreaks of pathogenic Shiga toxin-producing Escherichia coli (STEC) infection. We hypothesized that plant defenses elicited by mechanical injury may effect STEC inhibition in cut leaves. Intact and cut leaves of 31 lettuce cultivars (Lactuca spp.) selected from >500 accessions based on their resistance to common insect pests and the necrotrophic lettuce drop pathogen were assessed for STEC serovar O157:H7 (EcO157) survival under cold storage conditions. The cultivars were previously ranked also for phenotypes such as resistance to other phytopathogens and physiological traits. Total leaf phenolic compounds, anthocyanins, and reactive oxygen species (ROS); and phenylalanine lyase (PAL), peroxidase (POD), and polyphenol oxidase (PPO) activity were quantified in each cultivar. Principal Component Analysis (PCA) and K-means cluster analysis were applied to group phenotypes and EcO157 population decline on lettuce. In five cultivars, high resistance to herbivorous insects (aphids, leaf miners and thrips), diseases (lettuce drop, downy mildew, and Impatiens Necrotic Spot Virus), and the disorder tipburn was associated with up to 42-fold EcO157 population decline on cold-stored cut (shredded) leaves, and with up to 11-fold difference in decline on cold-stored intact vs cut leaves (ΔD). The decline on these cold-stored cut cultivars also was up to 24-fold greater than on the cultivar with the lowest decline, and up to 8-fold greater than the mean decline for all 31 cultivars (P 
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Processed lettuce has been implicated in recurrent outbreaks of pathogenic Shiga toxin-producing Escherichia coli (STEC) infection. We hypothesized that plant defenses elicited by mechanical injury may effect STEC inhibition in cut leaves. Intact and cut leaves of 31 lettuce cultivars (Lactuca spp.) selected from &gt;500 accessions based on their resistance to common insect pests and the necrotrophic lettuce drop pathogen were assessed for STEC serovar O157:H7 (EcO157) survival under cold storage conditions. The cultivars were previously ranked also for phenotypes such as resistance to other phytopathogens and physiological traits. Total leaf phenolic compounds, anthocyanins, and reactive oxygen species (ROS); and phenylalanine lyase (PAL), peroxidase (POD), and polyphenol oxidase (PPO) activity were quantified in each cultivar. Principal Component Analysis (PCA) and K-means cluster analysis were applied to group phenotypes and EcO157 population decline on lettuce. In five cultivars, high resistance to herbivorous insects (aphids, leaf miners and thrips), diseases (lettuce drop, downy mildew, and Impatiens Necrotic Spot Virus), and the disorder tipburn was associated with up to 42-fold EcO157 population decline on cold-stored cut (shredded) leaves, and with up to 11-fold difference in decline on cold-stored intact vs cut leaves (ΔD). The decline on these cold-stored cut cultivars also was up to 24-fold greater than on the cultivar with the lowest decline, and up to 8-fold greater than the mean decline for all 31 cultivars (P &lt; 0.01). Resistance to the hemibiotrophic pathogen causing lettuce bacterial leaf spot, Xanthomonas hortorum pv. vitians, was not indicative of high EcO157 inhibition in this system. High PAL activity, and phenolic and anthocyanin content (PPA); and high PAL and POD activity, were associated with high EcO157 population decline (P &lt; 0.05). One cultivar with high susceptibility to herbivorous insects and phytopathogens, and low levels of defense metabolism nevertheless showed high EcO157 inhibition, suggesting other plant inhibitory characteristics at play. Basal plant immunity and pathways associated with a strong wound response may inform about enteric pathogen survival on minimally processed postharvest lettuce. The related traits identified in this study may serve to breed new genotypes with intrinsically enhanced microbial safety. •Lettuce cultivars selected from &gt;500 accessions for jasmonic acid-linked immunity.•Selected cultivars varied in pathogenic E. coli survival on cold-stored cut lettuce.•Lettuce resistance to insects and pathogens associated with high E. coli inhibition.•High PAL, POD, and phenolics contribute to E. coli inhibition on cut lettuce at 5°C.•Breeding and genotype selection may enhance safety of postharvest fresh-cut lettuce.</description><identifier>ISSN: 0925-5214</identifier><identifier>EISSN: 1873-2356</identifier><identifier>DOI: 10.1016/j.postharvbio.2024.112816</identifier><language>eng</language><publisher>Elsevier B.V</publisher><subject>animal pathogens ; anthocyanins ; catechol oxidase ; cluster analysis ; cold storage ; cultivars ; decline ; downy mildew ; enteropathogens ; Escherichia coli O157 ; foodborne illness ; Foodborne pathogen ; Genotype ; herbivores ; horticulture ; immunity ; Impatiens necrotic spot tospovirus ; insects ; Lactuca ; leaf spot ; leaves ; lettuce ; metabolism ; pathogen survival ; peroxidase ; phenylalanine ; plant pathogens ; population dynamics ; Postharvest ; principal component analysis ; Produce ; public health ; reactive oxygen species ; serotypes ; Shiga toxin ; Wound response ; Xanthomonas hortorum</subject><ispartof>Postharvest biology and technology, 2024-05, Vol.211, p.112816, Article 112816</ispartof><rights>2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c349t-77474b293eb4e04c0879d93edf73990adf3f2bbdc2d918bd1a87fabc8de0cbb93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0925521424000619$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids></links><search><creatorcontrib>George, Andree S.</creatorcontrib><creatorcontrib>Simko, Ivan</creatorcontrib><creatorcontrib>Brandl, Maria T.</creatorcontrib><title>Identification and characterization of lettuce cultivars with high inhibitory activity against the human pathogen Escherichia coli O157:H7: Toward a plant-intrinsic hurdle approach to microbial safety</title><title>Postharvest biology and technology</title><description>Foodborne illness linked to fruit and vegetables poses a major challenge to public health and horticulture production. Processed lettuce has been implicated in recurrent outbreaks of pathogenic Shiga toxin-producing Escherichia coli (STEC) infection. We hypothesized that plant defenses elicited by mechanical injury may effect STEC inhibition in cut leaves. Intact and cut leaves of 31 lettuce cultivars (Lactuca spp.) selected from &gt;500 accessions based on their resistance to common insect pests and the necrotrophic lettuce drop pathogen were assessed for STEC serovar O157:H7 (EcO157) survival under cold storage conditions. The cultivars were previously ranked also for phenotypes such as resistance to other phytopathogens and physiological traits. Total leaf phenolic compounds, anthocyanins, and reactive oxygen species (ROS); and phenylalanine lyase (PAL), peroxidase (POD), and polyphenol oxidase (PPO) activity were quantified in each cultivar. Principal Component Analysis (PCA) and K-means cluster analysis were applied to group phenotypes and EcO157 population decline on lettuce. In five cultivars, high resistance to herbivorous insects (aphids, leaf miners and thrips), diseases (lettuce drop, downy mildew, and Impatiens Necrotic Spot Virus), and the disorder tipburn was associated with up to 42-fold EcO157 population decline on cold-stored cut (shredded) leaves, and with up to 11-fold difference in decline on cold-stored intact vs cut leaves (ΔD). The decline on these cold-stored cut cultivars also was up to 24-fold greater than on the cultivar with the lowest decline, and up to 8-fold greater than the mean decline for all 31 cultivars (P &lt; 0.01). Resistance to the hemibiotrophic pathogen causing lettuce bacterial leaf spot, Xanthomonas hortorum pv. vitians, was not indicative of high EcO157 inhibition in this system. High PAL activity, and phenolic and anthocyanin content (PPA); and high PAL and POD activity, were associated with high EcO157 population decline (P &lt; 0.05). One cultivar with high susceptibility to herbivorous insects and phytopathogens, and low levels of defense metabolism nevertheless showed high EcO157 inhibition, suggesting other plant inhibitory characteristics at play. Basal plant immunity and pathways associated with a strong wound response may inform about enteric pathogen survival on minimally processed postharvest lettuce. The related traits identified in this study may serve to breed new genotypes with intrinsically enhanced microbial safety. •Lettuce cultivars selected from &gt;500 accessions for jasmonic acid-linked immunity.•Selected cultivars varied in pathogenic E. coli survival on cold-stored cut lettuce.•Lettuce resistance to insects and pathogens associated with high E. coli inhibition.•High PAL, POD, and phenolics contribute to E. coli inhibition on cut lettuce at 5°C.•Breeding and genotype selection may enhance safety of postharvest fresh-cut lettuce.</description><subject>animal pathogens</subject><subject>anthocyanins</subject><subject>catechol oxidase</subject><subject>cluster analysis</subject><subject>cold storage</subject><subject>cultivars</subject><subject>decline</subject><subject>downy mildew</subject><subject>enteropathogens</subject><subject>Escherichia coli O157</subject><subject>foodborne illness</subject><subject>Foodborne pathogen</subject><subject>Genotype</subject><subject>herbivores</subject><subject>horticulture</subject><subject>immunity</subject><subject>Impatiens necrotic spot tospovirus</subject><subject>insects</subject><subject>Lactuca</subject><subject>leaf spot</subject><subject>leaves</subject><subject>lettuce</subject><subject>metabolism</subject><subject>pathogen survival</subject><subject>peroxidase</subject><subject>phenylalanine</subject><subject>plant pathogens</subject><subject>population dynamics</subject><subject>Postharvest</subject><subject>principal component analysis</subject><subject>Produce</subject><subject>public health</subject><subject>reactive oxygen species</subject><subject>serotypes</subject><subject>Shiga toxin</subject><subject>Wound response</subject><subject>Xanthomonas hortorum</subject><issn>0925-5214</issn><issn>1873-2356</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqNkctu2zAQRYWiBeqm_Yfprhu5pB6WlF1hpEmAANkka2JIjswxZFElaQfuF-azysBddNnVPDD34A5uUXyVYi2F3Hzfrxcfk8Nw0uzXlaiatZRVLzfvipXsu7qs6nbzvliJoWrLtpLNx-JTjHshRNu2_ap4vbc0Jx7ZYGI_A84WTMahSRT492XpR5gopaMhMMcp8QlDhBdODhzvHPDsWHPy4QxZxidOudkhzzFBcgTueMAZFkzO72iGm2hcZhvHCMZPDI-y7a7vumt48i8YLCAsE86p5DmFDGGTCcFOBLgswaNxkDwc2ASvGSeIOFI6fy4-jDhF-vK3XhXPP2-etnflw-Pt_fbHQ2nqZkhl1zVdo6uhJt2QaIzou8HmyY5dPQwC7ViPldbWVHaQvbYS-25EbXpLwmg91FfFtws3W_l1pJjUgaOhKTsmf4yqlm29qVohNvl0uJxmpzEGGtUS-IDhrKRQb-mpvfonPfWWnrqkl7Xbi5byLyemoKJhmg1ZDmSSsp7_g_IHAEawSg</recordid><startdate>202405</startdate><enddate>202405</enddate><creator>George, Andree S.</creator><creator>Simko, Ivan</creator><creator>Brandl, Maria T.</creator><general>Elsevier B.V</general><scope>6I.</scope><scope>AAFTH</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>202405</creationdate><title>Identification and characterization of lettuce cultivars with high inhibitory activity against the human pathogen Escherichia coli O157:H7: Toward a plant-intrinsic hurdle approach to microbial safety</title><author>George, Andree S. ; 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Processed lettuce has been implicated in recurrent outbreaks of pathogenic Shiga toxin-producing Escherichia coli (STEC) infection. We hypothesized that plant defenses elicited by mechanical injury may effect STEC inhibition in cut leaves. Intact and cut leaves of 31 lettuce cultivars (Lactuca spp.) selected from &gt;500 accessions based on their resistance to common insect pests and the necrotrophic lettuce drop pathogen were assessed for STEC serovar O157:H7 (EcO157) survival under cold storage conditions. The cultivars were previously ranked also for phenotypes such as resistance to other phytopathogens and physiological traits. Total leaf phenolic compounds, anthocyanins, and reactive oxygen species (ROS); and phenylalanine lyase (PAL), peroxidase (POD), and polyphenol oxidase (PPO) activity were quantified in each cultivar. Principal Component Analysis (PCA) and K-means cluster analysis were applied to group phenotypes and EcO157 population decline on lettuce. In five cultivars, high resistance to herbivorous insects (aphids, leaf miners and thrips), diseases (lettuce drop, downy mildew, and Impatiens Necrotic Spot Virus), and the disorder tipburn was associated with up to 42-fold EcO157 population decline on cold-stored cut (shredded) leaves, and with up to 11-fold difference in decline on cold-stored intact vs cut leaves (ΔD). The decline on these cold-stored cut cultivars also was up to 24-fold greater than on the cultivar with the lowest decline, and up to 8-fold greater than the mean decline for all 31 cultivars (P &lt; 0.01). Resistance to the hemibiotrophic pathogen causing lettuce bacterial leaf spot, Xanthomonas hortorum pv. vitians, was not indicative of high EcO157 inhibition in this system. High PAL activity, and phenolic and anthocyanin content (PPA); and high PAL and POD activity, were associated with high EcO157 population decline (P &lt; 0.05). One cultivar with high susceptibility to herbivorous insects and phytopathogens, and low levels of defense metabolism nevertheless showed high EcO157 inhibition, suggesting other plant inhibitory characteristics at play. Basal plant immunity and pathways associated with a strong wound response may inform about enteric pathogen survival on minimally processed postharvest lettuce. The related traits identified in this study may serve to breed new genotypes with intrinsically enhanced microbial safety. •Lettuce cultivars selected from &gt;500 accessions for jasmonic acid-linked immunity.•Selected cultivars varied in pathogenic E. coli survival on cold-stored cut lettuce.•Lettuce resistance to insects and pathogens associated with high E. coli inhibition.•High PAL, POD, and phenolics contribute to E. coli inhibition on cut lettuce at 5°C.•Breeding and genotype selection may enhance safety of postharvest fresh-cut lettuce.</abstract><pub>Elsevier B.V</pub><doi>10.1016/j.postharvbio.2024.112816</doi><oa>free_for_read</oa></addata></record>
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source Elsevier ScienceDirect Journals
subjects animal pathogens
anthocyanins
catechol oxidase
cluster analysis
cold storage
cultivars
decline
downy mildew
enteropathogens
Escherichia coli O157
foodborne illness
Foodborne pathogen
Genotype
herbivores
horticulture
immunity
Impatiens necrotic spot tospovirus
insects
Lactuca
leaf spot
leaves
lettuce
metabolism
pathogen survival
peroxidase
phenylalanine
plant pathogens
population dynamics
Postharvest
principal component analysis
Produce
public health
reactive oxygen species
serotypes
Shiga toxin
Wound response
Xanthomonas hortorum
title Identification and characterization of lettuce cultivars with high inhibitory activity against the human pathogen Escherichia coli O157:H7: Toward a plant-intrinsic hurdle approach to microbial safety
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