The Intergenic Interplay between Aldose 1-Epimerase-Like Protein and Pectin Methylesterase in Abiotic and Biotic Stress Control
The mechanical damage that often precedes the penetration of a leaf by a pathogen promotes the activation of pectin methylesterase (PME); the activation of PME leads to the emission of methanol, resulting in a “priming” effect on intact leaves, which is accompanied by an increased sensitivity to Tob...
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| Format: | Article |
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Frontiers Media S.A.
2017-09-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fpls.2017.01646/full |
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| author | Ekaterina V. Sheshukova Tatiana V. Komarova Tatiana V. Komarova Denis V. Pozdyshev Natalia M. Ershova Natalia M. Ershova Anastasia V. Shindyapina Anastasia V. Shindyapina Vadim N. Tashlitsky Eugene V. Sheval Yuri L. Dorokhov Yuri L. Dorokhov |
| author_facet | Ekaterina V. Sheshukova Tatiana V. Komarova Tatiana V. Komarova Denis V. Pozdyshev Natalia M. Ershova Natalia M. Ershova Anastasia V. Shindyapina Anastasia V. Shindyapina Vadim N. Tashlitsky Eugene V. Sheval Yuri L. Dorokhov Yuri L. Dorokhov |
| author_sort | Ekaterina V. Sheshukova |
| collection | DOAJ |
| description | The mechanical damage that often precedes the penetration of a leaf by a pathogen promotes the activation of pectin methylesterase (PME); the activation of PME leads to the emission of methanol, resulting in a “priming” effect on intact leaves, which is accompanied by an increased sensitivity to Tobacco mosaic virus (TMV) and resistance to bacteria. In this study, we revealed that mRNA levels of the methanol-inducible gene encoding Nicotiana benthamiana aldose 1-epimerase-like protein (NbAELP) in the leaves of intact plants are very low compared with roots. However, stress and pathogen attack increased the accumulation of the NbAELP mRNA in the leaves. Using transiently transformed plants, we obtained data to support the mechanism underlying AELP/PME-related negative feedback The insertion of the NbAELP promoter sequence (proNbAELP) into the N. benthamiana genome resulted in the co-suppression of the natural NbAELP gene expression, accompanied by a reduction in the NbAELP mRNA content and increased PME synthesis. Knockdown of NbAELP resulted in high activity of PME in the cell wall and a decrease in the leaf glucose level, creating unfavorable conditions for Agrobacterium tumefaciens reproduction in injected leaves. Our results showed that NbAELP is capable of binding the TMV movement protein (MPTMV) in vitro and is likely to affect the cellular nucleocytoplasmic transport, which may explain the sensitivity of NbAELP knockdown plants to TMV. Although NbAELP was primarily detected in the cell wall, the influence of this protein on cellular PME mRNA levels might be associated with reduced transcriptional activity of the PME gene in the nucleus. To confirm this hypothesis, we isolated the N. tabacum PME gene promoter (proNtPME) and showed the inhibition of proNtPME-directed GFP and GUS expression in leaves when co-agroinjected with the NbAELP-encoding plasmid. We hypothesized that plant wounding and/or pathogen attack lead to PME activation and increased methanol emission, followed by increased NbAELP expression, which results in reversion of PME mRNA level and methanol emission to levels found in the intact plant. |
| first_indexed | 2024-12-24T05:33:38Z |
| format | Article |
| id | doaj.art-c33b0356328a40df863c14570d9ddfad |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-24T05:33:38Z |
| publishDate | 2017-09-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Plant Science |
| spelling | doaj.art-c33b0356328a40df863c14570d9ddfad2022-12-21T17:13:06ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2017-09-01810.3389/fpls.2017.01646289170The Intergenic Interplay between Aldose 1-Epimerase-Like Protein and Pectin Methylesterase in Abiotic and Biotic Stress ControlEkaterina V. Sheshukova0Tatiana V. Komarova1Tatiana V. Komarova2Denis V. Pozdyshev3Natalia M. Ershova4Natalia M. Ershova5Anastasia V. Shindyapina6Anastasia V. Shindyapina7Vadim N. Tashlitsky8Eugene V. Sheval9Yuri L. Dorokhov10Yuri L. Dorokhov11Vavilov Institute of General Genetics (RAS)Moscow, RussiaVavilov Institute of General Genetics (RAS)Moscow, RussiaA.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State UniversityMoscow, RussiaVavilov Institute of General Genetics (RAS)Moscow, RussiaVavilov Institute of General Genetics (RAS)Moscow, RussiaA.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State UniversityMoscow, RussiaVavilov Institute of General Genetics (RAS)Moscow, RussiaA.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State UniversityMoscow, RussiaFaculty of Chemistry, Lomonosov Moscow State UniversityMoscow, RussiaA.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State UniversityMoscow, RussiaVavilov Institute of General Genetics (RAS)Moscow, RussiaA.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State UniversityMoscow, RussiaThe mechanical damage that often precedes the penetration of a leaf by a pathogen promotes the activation of pectin methylesterase (PME); the activation of PME leads to the emission of methanol, resulting in a “priming” effect on intact leaves, which is accompanied by an increased sensitivity to Tobacco mosaic virus (TMV) and resistance to bacteria. In this study, we revealed that mRNA levels of the methanol-inducible gene encoding Nicotiana benthamiana aldose 1-epimerase-like protein (NbAELP) in the leaves of intact plants are very low compared with roots. However, stress and pathogen attack increased the accumulation of the NbAELP mRNA in the leaves. Using transiently transformed plants, we obtained data to support the mechanism underlying AELP/PME-related negative feedback The insertion of the NbAELP promoter sequence (proNbAELP) into the N. benthamiana genome resulted in the co-suppression of the natural NbAELP gene expression, accompanied by a reduction in the NbAELP mRNA content and increased PME synthesis. Knockdown of NbAELP resulted in high activity of PME in the cell wall and a decrease in the leaf glucose level, creating unfavorable conditions for Agrobacterium tumefaciens reproduction in injected leaves. Our results showed that NbAELP is capable of binding the TMV movement protein (MPTMV) in vitro and is likely to affect the cellular nucleocytoplasmic transport, which may explain the sensitivity of NbAELP knockdown plants to TMV. Although NbAELP was primarily detected in the cell wall, the influence of this protein on cellular PME mRNA levels might be associated with reduced transcriptional activity of the PME gene in the nucleus. To confirm this hypothesis, we isolated the N. tabacum PME gene promoter (proNtPME) and showed the inhibition of proNtPME-directed GFP and GUS expression in leaves when co-agroinjected with the NbAELP-encoding plasmid. We hypothesized that plant wounding and/or pathogen attack lead to PME activation and increased methanol emission, followed by increased NbAELP expression, which results in reversion of PME mRNA level and methanol emission to levels found in the intact plant.http://journal.frontiersin.org/article/10.3389/fpls.2017.01646/fullaldose 1-epimerase-like proteinpectin methylesteraseabiotic and biotic stressvirusbacteriagene |
| spellingShingle | Ekaterina V. Sheshukova Tatiana V. Komarova Tatiana V. Komarova Denis V. Pozdyshev Natalia M. Ershova Natalia M. Ershova Anastasia V. Shindyapina Anastasia V. Shindyapina Vadim N. Tashlitsky Eugene V. Sheval Yuri L. Dorokhov Yuri L. Dorokhov The Intergenic Interplay between Aldose 1-Epimerase-Like Protein and Pectin Methylesterase in Abiotic and Biotic Stress Control Frontiers in Plant Science aldose 1-epimerase-like protein pectin methylesterase abiotic and biotic stress virus bacteria gene |
| title | The Intergenic Interplay between Aldose 1-Epimerase-Like Protein and Pectin Methylesterase in Abiotic and Biotic Stress Control |
| title_full | The Intergenic Interplay between Aldose 1-Epimerase-Like Protein and Pectin Methylesterase in Abiotic and Biotic Stress Control |
| title_fullStr | The Intergenic Interplay between Aldose 1-Epimerase-Like Protein and Pectin Methylesterase in Abiotic and Biotic Stress Control |
| title_full_unstemmed | The Intergenic Interplay between Aldose 1-Epimerase-Like Protein and Pectin Methylesterase in Abiotic and Biotic Stress Control |
| title_short | The Intergenic Interplay between Aldose 1-Epimerase-Like Protein and Pectin Methylesterase in Abiotic and Biotic Stress Control |
| title_sort | intergenic interplay between aldose 1 epimerase like protein and pectin methylesterase in abiotic and biotic stress control |
| topic | aldose 1-epimerase-like protein pectin methylesterase abiotic and biotic stress virus bacteria gene |
| url | http://journal.frontiersin.org/article/10.3389/fpls.2017.01646/full |
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