Production of Biopharmaceuticals in Nicotiana benthamiana—Axillary Stem Growth as a Key Determinant of Total Protein Yield
Data are scarce about the influence of basic cultural conditions on growth patterns and overall performance of plants used as heterologous production hosts for protein pharmaceuticals. Higher plants are complex organisms with young, mature, and senescing organs that show distinct metabolic backgroun...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-06-01
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| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2019.00735/full |
| _version_ | 1818201550679441408 |
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| author | Marie-Claire Goulet Linda Gaudreau Marielle Gagné Anne-Marie Maltais Ann-Catherine Laliberté Gilbert Éthier Nicole Bechtold Michèle Martel Marc-André D’Aoust André Gosselin Steeve Pepin Dominique Michaud |
| author_facet | Marie-Claire Goulet Linda Gaudreau Marielle Gagné Anne-Marie Maltais Ann-Catherine Laliberté Gilbert Éthier Nicole Bechtold Michèle Martel Marc-André D’Aoust André Gosselin Steeve Pepin Dominique Michaud |
| author_sort | Marie-Claire Goulet |
| collection | DOAJ |
| description | Data are scarce about the influence of basic cultural conditions on growth patterns and overall performance of plants used as heterologous production hosts for protein pharmaceuticals. Higher plants are complex organisms with young, mature, and senescing organs that show distinct metabolic backgrounds and differ in their ability to sustain foreign protein expression and accumulation. Here, we used the transient protein expression host Nicotiana benthamiana as a model to map the accumulation profile of influenza virus hemagglutinin H1, a clinically promising vaccine antigen, at the whole plant scale. Greenhouse-grown plants submitted to different light regimes, submitted to apical bud pruning, or treated with the axillary growth-promoting cytokinin 6-benzylaminopurine were vacuum-infiltrated with agrobacteria harboring a DNA sequence for H1 and allowed to express the viral antigen for 7 days in growth chamber under similar environmental conditions. Our data highlight the importance of young leaves on H1 yield per plant, unlike older leaves which account for a significant part of the plant biomass but contribute little to total antigen titer. Our data also highlight the key contribution of axillary stem leaves, which contribute more than 50% of total yield under certain conditions despite representing only one-third of the total biomass. These findings underline the relevance of both considering main stem leaves and axillary stem leaves while modeling heterologous protein production in N. benthamiana. They also demonstrate the potential of exogenously applied growth-promoting hormones to modulate host plant architecture for improvement of protein yields. |
| first_indexed | 2024-12-12T02:55:20Z |
| format | Article |
| id | doaj.art-104a8b7d304c4ca48f75afa96cc25230 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-12T02:55:20Z |
| publishDate | 2019-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-104a8b7d304c4ca48f75afa96cc252302022-12-22T00:40:47ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-06-011010.3389/fpls.2019.00735455375Production of Biopharmaceuticals in Nicotiana benthamiana—Axillary Stem Growth as a Key Determinant of Total Protein YieldMarie-Claire Goulet0Linda Gaudreau1Marielle Gagné2Anne-Marie Maltais3Ann-Catherine Laliberté4Gilbert Éthier5Nicole Bechtold6Michèle Martel7Marc-André D’Aoust8André Gosselin9Steeve Pepin10Dominique Michaud11Centre de recherche et d’innovation sur les végétaux, Faculté des Sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, CanadaCentre de recherche et d’innovation sur les végétaux, Faculté des Sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, CanadaCentre de recherche et d’innovation sur les végétaux, Faculté des Sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, CanadaCentre de recherche et d’innovation sur les végétaux, Faculté des Sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, CanadaCentre de recherche et d’innovation sur les végétaux, Faculté des Sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, CanadaCentre de recherche et d’innovation sur les végétaux, Faculté des Sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, CanadaMedicago Inc., Québec, QC, CanadaMedicago Inc., Québec, QC, CanadaMedicago Inc., Québec, QC, CanadaCentre de recherche et d’innovation sur les végétaux, Faculté des Sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, CanadaCentre de recherche et d’innovation sur les végétaux, Faculté des Sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, CanadaCentre de recherche et d’innovation sur les végétaux, Faculté des Sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, CanadaData are scarce about the influence of basic cultural conditions on growth patterns and overall performance of plants used as heterologous production hosts for protein pharmaceuticals. Higher plants are complex organisms with young, mature, and senescing organs that show distinct metabolic backgrounds and differ in their ability to sustain foreign protein expression and accumulation. Here, we used the transient protein expression host Nicotiana benthamiana as a model to map the accumulation profile of influenza virus hemagglutinin H1, a clinically promising vaccine antigen, at the whole plant scale. Greenhouse-grown plants submitted to different light regimes, submitted to apical bud pruning, or treated with the axillary growth-promoting cytokinin 6-benzylaminopurine were vacuum-infiltrated with agrobacteria harboring a DNA sequence for H1 and allowed to express the viral antigen for 7 days in growth chamber under similar environmental conditions. Our data highlight the importance of young leaves on H1 yield per plant, unlike older leaves which account for a significant part of the plant biomass but contribute little to total antigen titer. Our data also highlight the key contribution of axillary stem leaves, which contribute more than 50% of total yield under certain conditions despite representing only one-third of the total biomass. These findings underline the relevance of both considering main stem leaves and axillary stem leaves while modeling heterologous protein production in N. benthamiana. They also demonstrate the potential of exogenously applied growth-promoting hormones to modulate host plant architecture for improvement of protein yields.https://www.frontiersin.org/article/10.3389/fpls.2019.00735/fullplant molecular farmingNicotiana benthamianainfluenza virus hemagglutinin H1light regimeapical pruninghormone treatment |
| spellingShingle | Marie-Claire Goulet Linda Gaudreau Marielle Gagné Anne-Marie Maltais Ann-Catherine Laliberté Gilbert Éthier Nicole Bechtold Michèle Martel Marc-André D’Aoust André Gosselin Steeve Pepin Dominique Michaud Production of Biopharmaceuticals in Nicotiana benthamiana—Axillary Stem Growth as a Key Determinant of Total Protein Yield Frontiers in Plant Science plant molecular farming Nicotiana benthamiana influenza virus hemagglutinin H1 light regime apical pruning hormone treatment |
| title | Production of Biopharmaceuticals in Nicotiana benthamiana—Axillary Stem Growth as a Key Determinant of Total Protein Yield |
| title_full | Production of Biopharmaceuticals in Nicotiana benthamiana—Axillary Stem Growth as a Key Determinant of Total Protein Yield |
| title_fullStr | Production of Biopharmaceuticals in Nicotiana benthamiana—Axillary Stem Growth as a Key Determinant of Total Protein Yield |
| title_full_unstemmed | Production of Biopharmaceuticals in Nicotiana benthamiana—Axillary Stem Growth as a Key Determinant of Total Protein Yield |
| title_short | Production of Biopharmaceuticals in Nicotiana benthamiana—Axillary Stem Growth as a Key Determinant of Total Protein Yield |
| title_sort | production of biopharmaceuticals in nicotiana benthamiana axillary stem growth as a key determinant of total protein yield |
| topic | plant molecular farming Nicotiana benthamiana influenza virus hemagglutinin H1 light regime apical pruning hormone treatment |
| url | https://www.frontiersin.org/article/10.3389/fpls.2019.00735/full |
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