Cell Wall Invertase and Sugar Transporters Are Differentially Activated in Tomato Styles and Ovaries During Pollination and Fertilization
Flowering plants depend on pollination and fertilization to activate the transition from ovule to seed and ovary to fruit, namely seed and fruit set, which are key for completing the plant life cycle and realizing crop yield potential. These processes are highly energy consuming and rely on the effi...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-04-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2019.00506/full |
| _version_ | 1811210916805476352 |
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| author | Si Shen Si Shen Si Ma Si Ma Yonghua Liu Yonghua Liu Shengjin Liao Jun Li Limin Wu Dewi Kartika Hans-Peter Mock Yong-Ling Ruan |
| author_facet | Si Shen Si Shen Si Ma Si Ma Yonghua Liu Yonghua Liu Shengjin Liao Jun Li Limin Wu Dewi Kartika Hans-Peter Mock Yong-Ling Ruan |
| author_sort | Si Shen |
| collection | DOAJ |
| description | Flowering plants depend on pollination and fertilization to activate the transition from ovule to seed and ovary to fruit, namely seed and fruit set, which are key for completing the plant life cycle and realizing crop yield potential. These processes are highly energy consuming and rely on the efficient use of sucrose as the major nutrient and energy source. However, it remains elusive as how sucrose imported into and utilizated within the female reproductive organ is regulated in response to pollination and fertilization. Here, we explored this issue in tomato by focusing on genes encoding cell wall invertase (CWIN) and sugar transporters, which are major players in sucrose phloem unloading, and sink development. The transcript level of a major CWIN gene, LIN5, and CWIN activity were significantly increased in style at 4 h after pollination (HAP) in comparison with that in the non-pollination control, and this was sustained at 2 days after pollination (DAP). In the ovaries, however, CWIN activity and LIN5 expression did not increase until 2 DAP when fertilization occurred. Interestingly, a CWIN inhibitor gene INVINH1 was repressed in the pollinated style at 2 DAP. In response to pollination, the style exhibited increased expressions of genes encoding hexose transporters, SlHT1, 2, SlSWEET5b, and sucrose transporters SlSUT1, 2, and 4 from 4 HAP to 2 DAP. Upon fertilization, SlSUT1 and SlHT1 and 2, but not SlSWEETs, were also stimulated in fruitlets at 2 DAP. Together, the findings reveal that styles respond promptly and more broadly to pollination for activation of CWIN and sugar transporters to fuel pollen tube elongation, whereas the ovaries do not exhibit activation for some of these genes until fertilization occurs.HighlightsExpression of genes encoding cell wall invertases and sugar transporters was stimulated in pollinated style and fertilized ovaries in tomato. |
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| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-12T05:04:05Z |
| publishDate | 2019-04-01 |
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| series | Frontiers in Plant Science |
| spelling | doaj.art-bf78f8194a414ba48ce87ddc0d1f38be2022-12-22T03:46:55ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-04-011010.3389/fpls.2019.00506436390Cell Wall Invertase and Sugar Transporters Are Differentially Activated in Tomato Styles and Ovaries During Pollination and FertilizationSi Shen0Si Shen1Si Ma2Si Ma3Yonghua Liu4Yonghua Liu5Shengjin Liao6Jun Li7Limin Wu8Dewi Kartika9Hans-Peter Mock10Yong-Ling Ruan11School of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW, AustraliaCollege of Agronomy and Biotechnology, China Agricultural University, Beijing, ChinaSchool of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW, AustraliaBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural University, Beijing, ChinaSchool of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW, AustraliaInstitute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaSchool of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW, AustraliaSchool of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW, AustraliaCSIRO Agriculture and Food, Canberra, ACT, AustraliaSchool of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW, AustraliaLeibniz Institute of Plant Genetics and Crop Plant Research, Gatersleben, GermanySchool of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW, AustraliaFlowering plants depend on pollination and fertilization to activate the transition from ovule to seed and ovary to fruit, namely seed and fruit set, which are key for completing the plant life cycle and realizing crop yield potential. These processes are highly energy consuming and rely on the efficient use of sucrose as the major nutrient and energy source. However, it remains elusive as how sucrose imported into and utilizated within the female reproductive organ is regulated in response to pollination and fertilization. Here, we explored this issue in tomato by focusing on genes encoding cell wall invertase (CWIN) and sugar transporters, which are major players in sucrose phloem unloading, and sink development. The transcript level of a major CWIN gene, LIN5, and CWIN activity were significantly increased in style at 4 h after pollination (HAP) in comparison with that in the non-pollination control, and this was sustained at 2 days after pollination (DAP). In the ovaries, however, CWIN activity and LIN5 expression did not increase until 2 DAP when fertilization occurred. Interestingly, a CWIN inhibitor gene INVINH1 was repressed in the pollinated style at 2 DAP. In response to pollination, the style exhibited increased expressions of genes encoding hexose transporters, SlHT1, 2, SlSWEET5b, and sucrose transporters SlSUT1, 2, and 4 from 4 HAP to 2 DAP. Upon fertilization, SlSUT1 and SlHT1 and 2, but not SlSWEETs, were also stimulated in fruitlets at 2 DAP. Together, the findings reveal that styles respond promptly and more broadly to pollination for activation of CWIN and sugar transporters to fuel pollen tube elongation, whereas the ovaries do not exhibit activation for some of these genes until fertilization occurs.HighlightsExpression of genes encoding cell wall invertases and sugar transporters was stimulated in pollinated style and fertilized ovaries in tomato.https://www.frontiersin.org/article/10.3389/fpls.2019.00506/fullcell wall invertasefertilizationfruit setpollinationpollen tube elongationsugar transporter |
| spellingShingle | Si Shen Si Shen Si Ma Si Ma Yonghua Liu Yonghua Liu Shengjin Liao Jun Li Limin Wu Dewi Kartika Hans-Peter Mock Yong-Ling Ruan Cell Wall Invertase and Sugar Transporters Are Differentially Activated in Tomato Styles and Ovaries During Pollination and Fertilization Frontiers in Plant Science cell wall invertase fertilization fruit set pollination pollen tube elongation sugar transporter |
| title | Cell Wall Invertase and Sugar Transporters Are Differentially Activated in Tomato Styles and Ovaries During Pollination and Fertilization |
| title_full | Cell Wall Invertase and Sugar Transporters Are Differentially Activated in Tomato Styles and Ovaries During Pollination and Fertilization |
| title_fullStr | Cell Wall Invertase and Sugar Transporters Are Differentially Activated in Tomato Styles and Ovaries During Pollination and Fertilization |
| title_full_unstemmed | Cell Wall Invertase and Sugar Transporters Are Differentially Activated in Tomato Styles and Ovaries During Pollination and Fertilization |
| title_short | Cell Wall Invertase and Sugar Transporters Are Differentially Activated in Tomato Styles and Ovaries During Pollination and Fertilization |
| title_sort | cell wall invertase and sugar transporters are differentially activated in tomato styles and ovaries during pollination and fertilization |
| topic | cell wall invertase fertilization fruit set pollination pollen tube elongation sugar transporter |
| url | https://www.frontiersin.org/article/10.3389/fpls.2019.00506/full |
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