Regulatory Roles of Small Non-coding RNAs in Sugar Beet Resistance Against Beet curly top virus
Beet curly top virus (BCTV) mediated yield loss in sugar beets is a major problem worldwide. The circular single-stranded DNA virus is transmitted by the beet leafhopper. Genetic sources of BCTV resistance in sugar beet are limited and commercial cultivars rely on chemical treatments versus durable...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-01-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2021.780877/full |
| _version_ | 1798034394832699392 |
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| author | Rajtilak Majumdar Paul J. Galewski Imad Eujayl Rakesh Minocha Eric Vincill Carl A. Strausbaugh |
| author_facet | Rajtilak Majumdar Paul J. Galewski Imad Eujayl Rakesh Minocha Eric Vincill Carl A. Strausbaugh |
| author_sort | Rajtilak Majumdar |
| collection | DOAJ |
| description | Beet curly top virus (BCTV) mediated yield loss in sugar beets is a major problem worldwide. The circular single-stranded DNA virus is transmitted by the beet leafhopper. Genetic sources of BCTV resistance in sugar beet are limited and commercial cultivars rely on chemical treatments versus durable genetic resistance. Phenotypic selection and double haploid production have resulted in sugar beet germplasm (KDH13; 13 and KDH4-9; 4) that are highly resistant to BCTV. The molecular mechanism of resistance to the virus is unknown, especially the role of small non-coding RNAs (sncRNAs) during early plant–viral interaction. Using the resistant lines along with a susceptible line (KDH19-17; 19), we demonstrate the role of sugar beet microRNAs (miRNAs) in BCTV resistance during early infection stages when symptoms are not yet visible. The differentially expressed miRNAs altered the expression of their corresponding target genes such as pyruvate dehydrogenase (EL10Ac1g02046), carboxylesterase (EL10Ac1g01087), serine/threonine protein phosphatase (EL10Ac1g01374), and leucine-rich repeats (LRR) receptor-like (EL10Ac7g17778), that were highly expressed in the resistant lines versus susceptible lines. Pathway enrichment analysis of the miRNA target genes showed an enrichment of genes involved in glycolysis/gluconeogenesis, galactose metabolism, starch, and sucrose metabolism to name a few. Carbohydrate analysis revealed altered glucose, galactose, fructose, and sucrose concentrations in the infected leaves of resistant versus susceptible lines. We also demonstrate differential regulation of BCTV derived sncRNAs in the resistant versus susceptible lines that target sugar beet genes such as LRR (EL10Ac1g01206), 7-deoxyloganetic acid glucosyltransferase (EL10Ac5g12605), and transmembrane emp24 domain containing (EL10Ac6g14074) and altered their expression. In response to viral infection, we found that plant derived miRNAs targeted BCTV capsid protein/replication related genes and showed differences in expression among resistant and susceptible lines. The data presented here demonstrate the contribution of miRNA mediated regulation of metabolic pathways and cross-kingdom RNA interference (RNAi) in sugar beet BCTV resistance. |
| first_indexed | 2024-04-11T20:43:46Z |
| format | Article |
| id | doaj.art-b272e76b881940f9a1738a4a01773e21 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-11T20:43:46Z |
| publishDate | 2022-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-b272e76b881940f9a1738a4a01773e212022-12-22T04:04:07ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-01-011210.3389/fpls.2021.780877780877Regulatory Roles of Small Non-coding RNAs in Sugar Beet Resistance Against Beet curly top virusRajtilak Majumdar0Paul J. Galewski1Imad Eujayl2Rakesh Minocha3Eric Vincill4Carl A. Strausbaugh5Northwest Irrigation and Soils Research, United States Department of Agriculture-Agricultural Research Service, Kimberly, ID, United StatesNorthwest Irrigation and Soils Research, United States Department of Agriculture-Agricultural Research Service, Kimberly, ID, United StatesNorthwest Irrigation and Soils Research, United States Department of Agriculture-Agricultural Research Service, Kimberly, ID, United StatesNorthern Research Station, United States Department of Agriculture Forest Service, Durham, NH, United StatesNorthwest Irrigation and Soils Research, United States Department of Agriculture-Agricultural Research Service, Kimberly, ID, United StatesNorthwest Irrigation and Soils Research, United States Department of Agriculture-Agricultural Research Service, Kimberly, ID, United StatesBeet curly top virus (BCTV) mediated yield loss in sugar beets is a major problem worldwide. The circular single-stranded DNA virus is transmitted by the beet leafhopper. Genetic sources of BCTV resistance in sugar beet are limited and commercial cultivars rely on chemical treatments versus durable genetic resistance. Phenotypic selection and double haploid production have resulted in sugar beet germplasm (KDH13; 13 and KDH4-9; 4) that are highly resistant to BCTV. The molecular mechanism of resistance to the virus is unknown, especially the role of small non-coding RNAs (sncRNAs) during early plant–viral interaction. Using the resistant lines along with a susceptible line (KDH19-17; 19), we demonstrate the role of sugar beet microRNAs (miRNAs) in BCTV resistance during early infection stages when symptoms are not yet visible. The differentially expressed miRNAs altered the expression of their corresponding target genes such as pyruvate dehydrogenase (EL10Ac1g02046), carboxylesterase (EL10Ac1g01087), serine/threonine protein phosphatase (EL10Ac1g01374), and leucine-rich repeats (LRR) receptor-like (EL10Ac7g17778), that were highly expressed in the resistant lines versus susceptible lines. Pathway enrichment analysis of the miRNA target genes showed an enrichment of genes involved in glycolysis/gluconeogenesis, galactose metabolism, starch, and sucrose metabolism to name a few. Carbohydrate analysis revealed altered glucose, galactose, fructose, and sucrose concentrations in the infected leaves of resistant versus susceptible lines. We also demonstrate differential regulation of BCTV derived sncRNAs in the resistant versus susceptible lines that target sugar beet genes such as LRR (EL10Ac1g01206), 7-deoxyloganetic acid glucosyltransferase (EL10Ac5g12605), and transmembrane emp24 domain containing (EL10Ac6g14074) and altered their expression. In response to viral infection, we found that plant derived miRNAs targeted BCTV capsid protein/replication related genes and showed differences in expression among resistant and susceptible lines. The data presented here demonstrate the contribution of miRNA mediated regulation of metabolic pathways and cross-kingdom RNA interference (RNAi) in sugar beet BCTV resistance.https://www.frontiersin.org/articles/10.3389/fpls.2021.780877/fullBCTV (Beet curly top virus)sugar beetRNAiKDH13KDH4-9virus |
| spellingShingle | Rajtilak Majumdar Paul J. Galewski Imad Eujayl Rakesh Minocha Eric Vincill Carl A. Strausbaugh Regulatory Roles of Small Non-coding RNAs in Sugar Beet Resistance Against Beet curly top virus Frontiers in Plant Science BCTV (Beet curly top virus) sugar beet RNAi KDH13 KDH4-9 virus |
| title | Regulatory Roles of Small Non-coding RNAs in Sugar Beet Resistance Against Beet curly top virus |
| title_full | Regulatory Roles of Small Non-coding RNAs in Sugar Beet Resistance Against Beet curly top virus |
| title_fullStr | Regulatory Roles of Small Non-coding RNAs in Sugar Beet Resistance Against Beet curly top virus |
| title_full_unstemmed | Regulatory Roles of Small Non-coding RNAs in Sugar Beet Resistance Against Beet curly top virus |
| title_short | Regulatory Roles of Small Non-coding RNAs in Sugar Beet Resistance Against Beet curly top virus |
| title_sort | regulatory roles of small non coding rnas in sugar beet resistance against beet curly top virus |
| topic | BCTV (Beet curly top virus) sugar beet RNAi KDH13 KDH4-9 virus |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2021.780877/full |
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