Comparative metabolomics analysis reveals secondary cell wall thickening as a barrier to resist Aspergillus flavus infection in groundnut
Aflatoxin contamination caused by Aspergillus flavus significantly threatens food safety and human health. Resistance to aflatoxin is a highly complex and quantitative trait, but the underlying molecular and biochemical mechanisms are poorly understood. The present study aims to identify the resista...
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| Veröffentlicht in: | Physiologia plantarum 2024-01, Vol.176 (1), p.n/a |
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| creator | Avuthu, Tejaswi Sanivarapu, Hemalatha Prasad, Kalyani Sharma, Niharika Sudini, Hari Kishan Yogendra, Kalenahalli |
| description | Aflatoxin contamination caused by Aspergillus flavus significantly threatens food safety and human health. Resistance to aflatoxin is a highly complex and quantitative trait, but the underlying molecular and biochemical mechanisms are poorly understood. The present study aims to identify the resistance‐related metabolites in groundnut that influence the defense mechanism against aflatoxin. Here, metabolite profiling of resistant (55–437) and susceptible (TMV‐2) groundnut genotypes, which exhibited contrasting levels of resistance to A. flavus growth and aflatoxin accumulation under pathogen‐ or mock‐inoculated treatments, was undertaken using liquid chromatography and high‐resolution mass spectrometry (LC‐HRMS). Non‐targeted metabolomic analysis revealed key resistance‐related metabolites belonging to phenylpropanoids, flavonoids, fatty acids, alkaloids, and terpenoid biosynthetic pathways. The phenylpropanoids ‐ hydroxycinnamic acid amides (HCAAs) and lignins were among the most abundantly accumulated metabolites in the resistant genotype compared to the susceptible genotype. HCAAs and lignins are deposited as polymers and conjugated metabolites to strengthen the secondary cell wall, which acts as a barrier to pathogen entry. Further, histochemical staining confirmed the secondary cell wall thickening due to HCAAs and lignin depositions. Quantitative real‐time PCR studies revealed higher expressions of phenylalanine ammonia‐lyase (PAL), 4‐coumarate: CoA ligase (4CL), cinnamoyl CoA reductase (CCR2), cinnamoyl alcohol dehydrogenase (CAD1), agmatine hydroxycinnamoyl transferase (ACT), chalcone synthase (CHS), dihydroflavonol 4‐reductase (DFR) and flavonol synthase (FLS) in the pathogen‐inoculated resistant genotype than in the susceptible genotype. This study reveals that the resistance to aflatoxin contamination in groundnut genotypes is associated with secondary cell wall thickening due to the deposition of HCAAs and lignins. |
| doi_str_mv | 10.1111/ppl.14169 |
| format | Article |
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Resistance to aflatoxin is a highly complex and quantitative trait, but the underlying molecular and biochemical mechanisms are poorly understood. The present study aims to identify the resistance‐related metabolites in groundnut that influence the defense mechanism against aflatoxin. Here, metabolite profiling of resistant (55–437) and susceptible (TMV‐2) groundnut genotypes, which exhibited contrasting levels of resistance to A. flavus growth and aflatoxin accumulation under pathogen‐ or mock‐inoculated treatments, was undertaken using liquid chromatography and high‐resolution mass spectrometry (LC‐HRMS). Non‐targeted metabolomic analysis revealed key resistance‐related metabolites belonging to phenylpropanoids, flavonoids, fatty acids, alkaloids, and terpenoid biosynthetic pathways. The phenylpropanoids ‐ hydroxycinnamic acid amides (HCAAs) and lignins were among the most abundantly accumulated metabolites in the resistant genotype compared to the susceptible genotype. HCAAs and lignins are deposited as polymers and conjugated metabolites to strengthen the secondary cell wall, which acts as a barrier to pathogen entry. Further, histochemical staining confirmed the secondary cell wall thickening due to HCAAs and lignin depositions. Quantitative real‐time PCR studies revealed higher expressions of phenylalanine ammonia‐lyase (PAL), 4‐coumarate: CoA ligase (4CL), cinnamoyl CoA reductase (CCR2), cinnamoyl alcohol dehydrogenase (CAD1), agmatine hydroxycinnamoyl transferase (ACT), chalcone synthase (CHS), dihydroflavonol 4‐reductase (DFR) and flavonol synthase (FLS) in the pathogen‐inoculated resistant genotype than in the susceptible genotype. This study reveals that the resistance to aflatoxin contamination in groundnut genotypes is associated with secondary cell wall thickening due to the deposition of HCAAs and lignins.</description><identifier>ISSN: 0031-9317</identifier><identifier>EISSN: 1399-3054</identifier><identifier>DOI: 10.1111/ppl.14169</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Aflatoxins ; Agmatine ; Alcohol dehydrogenase ; Amides ; Ammonia ; Aspergillus flavus ; biosynthesis ; Cell walls ; Chalcone synthase ; Contamination ; coumaric acids ; Flavonoids ; Flavonols ; Food contamination ; Food safety ; genotype ; Genotype & phenotype ; Genotypes ; Groundnuts ; human health ; Hydroxycinnamic acid ; hydroxycinnamoyltransferase ; ligases ; Lignin ; Liquid chromatography ; Mass spectrometry ; Mass spectroscopy ; Metabolites ; Metabolomics ; naringenin-chalcone synthase ; Pathogens ; peanuts ; Phenylalanine ; phenylalanine ammonia-lyase ; Phenylpropanoids ; Polymers ; quantitative polymerase chain reaction ; quantitative traits ; Reductases ; terpenoids ; Thickening</subject><ispartof>Physiologia plantarum, 2024-01, Vol.176 (1), p.n/a</ispartof><rights>2024 Scandinavian Plant Physiology Society.</rights><rights>2024 Scandinavian Plant Physiology Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3259-f163c4d20fb53210a2a5403b38928fbd7204d7e1e6135394c4bf420fdccb0ddf3</cites><orcidid>0000-0003-3546-7367 ; 0000-0002-2110-1308 ; 0000-0002-9032-5102 ; 0000-0001-6707-4467 ; 0000-0001-7200-6215</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fppl.14169$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fppl.14169$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids></links><search><creatorcontrib>Avuthu, Tejaswi</creatorcontrib><creatorcontrib>Sanivarapu, Hemalatha</creatorcontrib><creatorcontrib>Prasad, Kalyani</creatorcontrib><creatorcontrib>Sharma, Niharika</creatorcontrib><creatorcontrib>Sudini, Hari Kishan</creatorcontrib><creatorcontrib>Yogendra, Kalenahalli</creatorcontrib><title>Comparative metabolomics analysis reveals secondary cell wall thickening as a barrier to resist Aspergillus flavus infection in groundnut</title><title>Physiologia plantarum</title><description>Aflatoxin contamination caused by Aspergillus flavus significantly threatens food safety and human health. Resistance to aflatoxin is a highly complex and quantitative trait, but the underlying molecular and biochemical mechanisms are poorly understood. The present study aims to identify the resistance‐related metabolites in groundnut that influence the defense mechanism against aflatoxin. Here, metabolite profiling of resistant (55–437) and susceptible (TMV‐2) groundnut genotypes, which exhibited contrasting levels of resistance to A. flavus growth and aflatoxin accumulation under pathogen‐ or mock‐inoculated treatments, was undertaken using liquid chromatography and high‐resolution mass spectrometry (LC‐HRMS). Non‐targeted metabolomic analysis revealed key resistance‐related metabolites belonging to phenylpropanoids, flavonoids, fatty acids, alkaloids, and terpenoid biosynthetic pathways. The phenylpropanoids ‐ hydroxycinnamic acid amides (HCAAs) and lignins were among the most abundantly accumulated metabolites in the resistant genotype compared to the susceptible genotype. HCAAs and lignins are deposited as polymers and conjugated metabolites to strengthen the secondary cell wall, which acts as a barrier to pathogen entry. Further, histochemical staining confirmed the secondary cell wall thickening due to HCAAs and lignin depositions. Quantitative real‐time PCR studies revealed higher expressions of phenylalanine ammonia‐lyase (PAL), 4‐coumarate: CoA ligase (4CL), cinnamoyl CoA reductase (CCR2), cinnamoyl alcohol dehydrogenase (CAD1), agmatine hydroxycinnamoyl transferase (ACT), chalcone synthase (CHS), dihydroflavonol 4‐reductase (DFR) and flavonol synthase (FLS) in the pathogen‐inoculated resistant genotype than in the susceptible genotype. This study reveals that the resistance to aflatoxin contamination in groundnut genotypes is associated with secondary cell wall thickening due to the deposition of HCAAs and lignins.</description><subject>Aflatoxins</subject><subject>Agmatine</subject><subject>Alcohol dehydrogenase</subject><subject>Amides</subject><subject>Ammonia</subject><subject>Aspergillus flavus</subject><subject>biosynthesis</subject><subject>Cell walls</subject><subject>Chalcone synthase</subject><subject>Contamination</subject><subject>coumaric acids</subject><subject>Flavonoids</subject><subject>Flavonols</subject><subject>Food contamination</subject><subject>Food safety</subject><subject>genotype</subject><subject>Genotype & phenotype</subject><subject>Genotypes</subject><subject>Groundnuts</subject><subject>human health</subject><subject>Hydroxycinnamic acid</subject><subject>hydroxycinnamoyltransferase</subject><subject>ligases</subject><subject>Lignin</subject><subject>Liquid chromatography</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Metabolites</subject><subject>Metabolomics</subject><subject>naringenin-chalcone synthase</subject><subject>Pathogens</subject><subject>peanuts</subject><subject>Phenylalanine</subject><subject>phenylalanine ammonia-lyase</subject><subject>Phenylpropanoids</subject><subject>Polymers</subject><subject>quantitative polymerase chain reaction</subject><subject>quantitative traits</subject><subject>Reductases</subject><subject>terpenoids</subject><subject>Thickening</subject><issn>0031-9317</issn><issn>1399-3054</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp1kctOwzAQRS0EEuWx4A8ssYFFWjtO0maJKl5SJVjA2nKccTE4drCTon4Cf81AWSExixkvzp2R7yXkjLMpx5r1vZvyglf1HplwUdeZYGWxTyaMCZ7Vgs8PyVFKr4zxquL5hHwuQ9erqAa7AdrBoJrgQmd1osort0020QgbUC7RBDr4VsUt1eAc_VDYhher38Bbv6YKJbRRMVqIdAgoQ_FAr1IPcW2dGxM1Tm1wWG9ADzZ4fNF1DKNv_TickAODZ-D0dx6T55vrp-Vdtnq4vV9erTIt8rLODK-ELtqcmaYUOWcqV2XBRCMWdb4wTTvPWdHOgUPFRSnqQheNKZButW5Y2xpxTC52e_sY3kdIg-xs-v6R8hDGJAXDdYtFXc4RPf-DvoYxoi9J5uglnkRDkbrcUTqGlCIY2UfboU-SM_kdisRQ5E8oyM527Id1sP0flI-Pq53iC528kPQ</recordid><startdate>202401</startdate><enddate>202401</enddate><creator>Avuthu, Tejaswi</creator><creator>Sanivarapu, Hemalatha</creator><creator>Prasad, Kalyani</creator><creator>Sharma, Niharika</creator><creator>Sudini, Hari Kishan</creator><creator>Yogendra, Kalenahalli</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7ST</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-3546-7367</orcidid><orcidid>https://orcid.org/0000-0002-2110-1308</orcidid><orcidid>https://orcid.org/0000-0002-9032-5102</orcidid><orcidid>https://orcid.org/0000-0001-6707-4467</orcidid><orcidid>https://orcid.org/0000-0001-7200-6215</orcidid></search><sort><creationdate>202401</creationdate><title>Comparative metabolomics analysis reveals secondary cell wall thickening as a barrier to resist Aspergillus flavus infection in groundnut</title><author>Avuthu, Tejaswi ; Sanivarapu, Hemalatha ; Prasad, Kalyani ; Sharma, Niharika ; Sudini, Hari Kishan ; Yogendra, Kalenahalli</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3259-f163c4d20fb53210a2a5403b38928fbd7204d7e1e6135394c4bf420fdccb0ddf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Aflatoxins</topic><topic>Agmatine</topic><topic>Alcohol dehydrogenase</topic><topic>Amides</topic><topic>Ammonia</topic><topic>Aspergillus flavus</topic><topic>biosynthesis</topic><topic>Cell walls</topic><topic>Chalcone synthase</topic><topic>Contamination</topic><topic>coumaric acids</topic><topic>Flavonoids</topic><topic>Flavonols</topic><topic>Food contamination</topic><topic>Food safety</topic><topic>genotype</topic><topic>Genotype & phenotype</topic><topic>Genotypes</topic><topic>Groundnuts</topic><topic>human health</topic><topic>Hydroxycinnamic acid</topic><topic>hydroxycinnamoyltransferase</topic><topic>ligases</topic><topic>Lignin</topic><topic>Liquid chromatography</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>Metabolites</topic><topic>Metabolomics</topic><topic>naringenin-chalcone synthase</topic><topic>Pathogens</topic><topic>peanuts</topic><topic>Phenylalanine</topic><topic>phenylalanine ammonia-lyase</topic><topic>Phenylpropanoids</topic><topic>Polymers</topic><topic>quantitative polymerase chain reaction</topic><topic>quantitative traits</topic><topic>Reductases</topic><topic>terpenoids</topic><topic>Thickening</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Avuthu, Tejaswi</creatorcontrib><creatorcontrib>Sanivarapu, Hemalatha</creatorcontrib><creatorcontrib>Prasad, Kalyani</creatorcontrib><creatorcontrib>Sharma, Niharika</creatorcontrib><creatorcontrib>Sudini, Hari Kishan</creatorcontrib><creatorcontrib>Yogendra, Kalenahalli</creatorcontrib><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Environment Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Physiologia plantarum</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Avuthu, Tejaswi</au><au>Sanivarapu, Hemalatha</au><au>Prasad, Kalyani</au><au>Sharma, Niharika</au><au>Sudini, Hari Kishan</au><au>Yogendra, Kalenahalli</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comparative metabolomics analysis reveals secondary cell wall thickening as a barrier to resist Aspergillus flavus infection in groundnut</atitle><jtitle>Physiologia plantarum</jtitle><date>2024-01</date><risdate>2024</risdate><volume>176</volume><issue>1</issue><epage>n/a</epage><issn>0031-9317</issn><eissn>1399-3054</eissn><abstract>Aflatoxin contamination caused by Aspergillus flavus significantly threatens food safety and human health. Resistance to aflatoxin is a highly complex and quantitative trait, but the underlying molecular and biochemical mechanisms are poorly understood. The present study aims to identify the resistance‐related metabolites in groundnut that influence the defense mechanism against aflatoxin. Here, metabolite profiling of resistant (55–437) and susceptible (TMV‐2) groundnut genotypes, which exhibited contrasting levels of resistance to A. flavus growth and aflatoxin accumulation under pathogen‐ or mock‐inoculated treatments, was undertaken using liquid chromatography and high‐resolution mass spectrometry (LC‐HRMS). Non‐targeted metabolomic analysis revealed key resistance‐related metabolites belonging to phenylpropanoids, flavonoids, fatty acids, alkaloids, and terpenoid biosynthetic pathways. The phenylpropanoids ‐ hydroxycinnamic acid amides (HCAAs) and lignins were among the most abundantly accumulated metabolites in the resistant genotype compared to the susceptible genotype. HCAAs and lignins are deposited as polymers and conjugated metabolites to strengthen the secondary cell wall, which acts as a barrier to pathogen entry. Further, histochemical staining confirmed the secondary cell wall thickening due to HCAAs and lignin depositions. Quantitative real‐time PCR studies revealed higher expressions of phenylalanine ammonia‐lyase (PAL), 4‐coumarate: CoA ligase (4CL), cinnamoyl CoA reductase (CCR2), cinnamoyl alcohol dehydrogenase (CAD1), agmatine hydroxycinnamoyl transferase (ACT), chalcone synthase (CHS), dihydroflavonol 4‐reductase (DFR) and flavonol synthase (FLS) in the pathogen‐inoculated resistant genotype than in the susceptible genotype. This study reveals that the resistance to aflatoxin contamination in groundnut genotypes is associated with secondary cell wall thickening due to the deposition of HCAAs and lignins.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><doi>10.1111/ppl.14169</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-3546-7367</orcidid><orcidid>https://orcid.org/0000-0002-2110-1308</orcidid><orcidid>https://orcid.org/0000-0002-9032-5102</orcidid><orcidid>https://orcid.org/0000-0001-6707-4467</orcidid><orcidid>https://orcid.org/0000-0001-7200-6215</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Aflatoxins Agmatine Alcohol dehydrogenase Amides Ammonia Aspergillus flavus biosynthesis Cell walls Chalcone synthase Contamination coumaric acids Flavonoids Flavonols Food contamination Food safety genotype Genotype & phenotype Genotypes Groundnuts human health Hydroxycinnamic acid hydroxycinnamoyltransferase ligases Lignin Liquid chromatography Mass spectrometry Mass spectroscopy Metabolites Metabolomics naringenin-chalcone synthase Pathogens peanuts Phenylalanine phenylalanine ammonia-lyase Phenylpropanoids Polymers quantitative polymerase chain reaction quantitative traits Reductases terpenoids Thickening |
| title | Comparative metabolomics analysis reveals secondary cell wall thickening as a barrier to resist Aspergillus flavus infection in groundnut |
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