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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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Autores principales: Shen, Si, Ma, Si, Liu, Yonghua, Liao, Shengjin, Li, Jun, Wu, Limin, Kartika, Dewi, Mock, Hans-Peter, Ruan, Yong-Ling
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6482350/
https://www.ncbi.nlm.nih.gov/pubmed/31057596
http://dx.doi.org/10.3389/fpls.2019.00506
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author Shen, Si
Ma, Si
Liu, Yonghua
Liao, Shengjin
Li, Jun
Wu, Limin
Kartika, Dewi
Mock, Hans-Peter
Ruan, Yong-Ling
author_facet Shen, Si
Ma, Si
Liu, Yonghua
Liao, Shengjin
Li, Jun
Wu, Limin
Kartika, Dewi
Mock, Hans-Peter
Ruan, Yong-Ling
author_sort Shen, Si
collection PubMed
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. HIGHLIGHTS: Expression of genes encoding cell wall invertases and sugar transporters was stimulated in pollinated style and fertilized ovaries in tomato.
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spelling pubmed-64823502019-05-03 Cell Wall Invertase and Sugar Transporters Are Differentially Activated in Tomato Styles and Ovaries During Pollination and Fertilization Shen, Si Ma, Si Liu, Yonghua Liao, Shengjin Li, Jun Wu, Limin Kartika, Dewi Mock, Hans-Peter Ruan, Yong-Ling Front Plant Sci Plant Science 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. HIGHLIGHTS: Expression of genes encoding cell wall invertases and sugar transporters was stimulated in pollinated style and fertilized ovaries in tomato. Frontiers Media S.A. 2019-04-18 /pmc/articles/PMC6482350/ /pubmed/31057596 http://dx.doi.org/10.3389/fpls.2019.00506 Text en Copyright © 2019 Shen, Ma, Liu, Liao, Li, Wu, Kartika, Mock and Ruan. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Shen, Si
Ma, Si
Liu, Yonghua
Liao, Shengjin
Li, Jun
Wu, Limin
Kartika, Dewi
Mock, Hans-Peter
Ruan, Yong-Ling
Cell Wall Invertase and Sugar Transporters Are Differentially Activated in Tomato Styles and Ovaries During Pollination and Fertilization
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 Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6482350/
https://www.ncbi.nlm.nih.gov/pubmed/31057596
http://dx.doi.org/10.3389/fpls.2019.00506
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